LESS WELL-KNOWN INDIVIDUAL FORMS OF LIFE
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Microbial Diversity and the Biosphere
Microorganisms occupy a peculiar place in the human view of life. They receive little attention in our general texts of biology. They are largely ignored by most professional biologists and are virtually unknown to the public except in the contexts of disease and rot. Yet the workings of the biosphere depend absolutely on the activities of the microbial world (Madigan and others 1996). And a large bulk of global biomass is microbial (Whitman and others 1998). Our texts articulate biodiversity in terms of large organisms: insects usually top the count of species. Yet if we squeeze out any insect and examine its contents under the microscope, we find hundreds or thousands of distinct and unidentified microbial species. A handful of soil contains billions of microorganisms, of so many types that accurate numbers remain unknown. At most only a few of these microorganisms would be known to us; only about 5,000 noneukaryotic organisms have been formally described (Bull and others 1992) in contrast with the half-million described insect species. We know little about microbial biology, a part of biology that looms large in the sustenance of life on this planet.
The reason for our poor understanding of the microbial world lies in the fact that microorganisms are tiny, individually invisible to the eye. The mere existence of microbial life was recognized only relatively recently in history, about 300 years ago, with Leeuwenhoek's invention of the microscope. Even under the microscope, however, the simple structures of most microorganisms, usually nondescript rods and spheres, prevented their classification by morphology, through
which large organisms had always been related to one another. It was not until the late 19th century and the development of pure-culture techniques that microorganisms could be studied as individual types and characterized to some extent, mainly by nutritional criteria. However, the pure-culture approach to the study of the microbial world seriously constrained the view of microbial diversity because most microorganisms defy cultivation by standard methods. Moreover, the morphological and nutritional criteria used to describe microorganisms failed to provide a natural taxonomy, ordered according to evolutionary relationships. Molecular tools and a perspective based on gene sequences are now alleviating these constraints to some extent. Even the early results are changing our perception of microbial diversity.
A Sequence-Based Map of Biodiversity
Before the development of sequence-based methods, it was impossible to know the evolutionary relationships connecting all of life and thereby to draw a universal evolutionary tree. Whittaker, in 1969, just as the molecular methods began to develop, summarized evolutionary thought in the context of the “five kingdoms” of life: animals, plants, fungi, protists (“protozoa”), and monera (bacteria) (Whittaker 1969). There also was thought to be a higher, seemingly more fundamental taxonomic distinction between eukaryotes, organisms that contain nuclear membranes, and prokaryotes, predecessors of eukaryotes that lack nuclear membranes (Chatton 1937). Those two categories were considered independent and coherent groups. The main evolutionary diversity of life on Earth, four of the five traditional taxonomic kingdoms, was believed to lie among the eukaryotes, particularly the multicellular forms. These still-pervasive notions had never been tested, however, and they proved to be incorrect.
The breakthrough that called previous beliefs into question and brought order to microbial, indeed biological, diversity emerged with the determination of molecular sequences and the concept that sequences could be used to relate organisms (Schwartz and Dayhoff 1978; Zuckerkandl and Pauling 1965). The incisive formulation was reached by Carl Woese, who, by comparing ribosomal RNA (rRNA) sequences, established a molecular sequence-based phylogenetic tree that could be used to relate all organisms and reconstruct the history of life (Woese 1987; Woese and Fox 1977). Woese articulated the now-recognized three primary lines of evolutionary descent, termed “urkingdoms” or “domains”: Eucarya (eukaryotes), Bacteria (initially called eubacteria), and Archaea (initially called archaebacteria) (Woese and others 1990).
Figure 1 is a current phylogenetic tree based on small-subunit (SSU) rRNA sequences of the organisms represented. The construction of such a tree is conceptually simple (Swofford and others 1996). Pairs of rRNA sequences from different organisms are aligned, and the differences are counted and considered to be some measure of “evolutionary distance” between the organisms. There is no consideration of the passage of time, only of change in nucleotide sequence. Pairwise differences between many organisms can be used to infer phylogenetic trees, maps that represent the evolutionary paths leading to the modern-day sequences.
The tree in figure 1 is largely congruent with trees made by using any molecule in the nucleic acid-based, information-processing system of cells. But phylogenetic trees based on metabolic genes, those involved in manipulation of small molecules and in interaction with the environment, commonly do not concur with the rRNA-based version; see Doolittle and Brown (1994), Palmer (1997), and Woese (1998) for reviews and discussions of phylogenetic results with different molecules. Incongruities in phylogenetic trees made with different molecules can reflect lateral transfers or even the intermixing of genomes in the course of evolution. Some metabolic archaeal genes, for instance, appear much more highly related to specific bacterial versions than to their eucaryal homologues; other archaeal genes seem decidedly eukaryotic; still others are unique. Nonetheless, recently determined sequences of archaeal genomes show clearly that the evolutionary lineage of Archaea is independent of both Eucarya and Bacteria (Bult and others 1996; Smith and others 1997).
Interpreting the Molecular Tree of Life.
“Evolutionary distance” in the type of phylogenetic tree shown in figure 1, the extent of sequence change, is read along line segments. The tree can be considered a rough map of the evolution of the genetic core of the cellular lineages that led to the modern organisms (sequences) included in the tree. The time of occurrence of evolutionary events cannot be extracted reliably from phylogenetic trees, despite common attempts to do so. Time cannot be accurately correlated with sequence change, because the evolutionary clock is not constant in different lineages (Woese 1987). This disparity is evidenced in figure 1 by the fact that lines leading to the different reference organisms are not all the same length; these different lineages have experienced different extents of sequence change. Nonetheless, the order of occurrence of branchings in the trees can be interpreted as a genealogy, and intriguing insights into the evolution of cells are emerging.
A sobering aspect of large-scale phylogenetic trees like that shown in figure 1 is the graphic recognition that most of our legacy in biological science, historically based on large organisms, has focused on a narrow slice of biological diversity. Thus, we see that animals (represented in figure 1 by Homo), plants (Zea), and fungi (Coprinus) constitute small and peripheral branches of even eukaryotic cellular diversity. If the animals, plants, and fungi are taken to make up taxonomic “kingdoms”, we must recognize as kingdoms at least a dozen other eukaryotic groups, all microbial, with at least as much independent evolutionary history as that which separates the three traditional eukaryotic kingdoms. The taxonomic termkingdom has no molecular definition. I use it to indicate main lines of radiation in the particular domain; 14 such “kingdom-level” lines are associated with the eucaryal line of descent in figure 1 (see also Sogin 1994).
The rRNA and other molecular data solidly confirm the notion stemming from the last century that the major organelles of eukaryotesmitochondria and chloroplastsare derived from bacterial symbionts that have undergone specialization through coevolution with the host cell. Sequence comparisons establish mitochondria as representatives of Proteobacteria (the group in figure 1 including Es-
cherichia and Agrobacterium) and chloroplasts as derived from cyanobacteria (Synechococcus and Gloeobacter in figure 1) (Sapp 1994). Thus, all respiratory and photosynthetic capacity of eukaryotic cells was obtained from bacterial symbionts;the “endosymbiont hypothesis” for the origin of organelles is no longer hypothesis but well-grounded fact. The nuclear component of the modern eukaroytic cell did not derive from one of the other two lineages, however. The rRNA and other molecular trees show decisively that the eukaryotic nuclearline of descent extends as deeply into the history of life as do the bacterial and archaeal lineages. The mitochondrion and chloroplast came in relatively late. This late evolution is evidenced by the fact that mitochondria and chloroplasts diverged from free-living organisms that branched peripherally in molecular trees. Moreover, the most deeply divergent eukaryotes lack even mitochondria (Cavalier-Smith 1993). These latter organisms, little studied but sometimes troublesome creaturessuch as Giardia, Trichomonas, and Vairimorphanonetheless contain at least a few bacterium-type genes (Bui and others 1996; Germot and others 1996; Roger and others 1996). That might be evidence of an earlier mitochondrial symbiosis with' Eucarya that was lost (Palmer 1997) or perhaps other symbiotic or gene-transfer events between the evolutionary domains.
The root of the universal tree in figure 1, the point of origin of the modern lineages, cannot be established by using sequences of only one type of molecule. However, recent phylogenetic studies of gene families that originated before the last common ancestor of the three domains have positioned the root of the universal tree deep on the bacterial line (Doolittle and Brown 1994). Therefore, Eucarya and Archaea had a common history that excluded the descendants of the bacterial line. The period of evolutionary history shared by Eucarya and Archaea was an important time in the evolution of cells during which the refinement of the primordial information-processing mechanisms occurred. Thus, modern representatives of Eucarya and Archaea share many properties that differ from bacterial cells in fundamental ways. One example of similarities and differences is in the nature of the transcription machinery. The RNA polymerases of Eucarya and Archaea resemble each other in subunit composition and sequence far more than either resembles the bacterial type of polymerase. Moreover, whereas all bacterial cells use sigma factors to regulate the initiation of transcription, eucaryal and archaeal cells use TATA-binding proteins (Marsh and others 1994; Rowlands and others 1994).
The Metabolic Diversity of Life
The molecular-phylogenetic perspective, as depicted in figure 1, is a reference framework within which to describe microbial diversity; the sequences of genes can be used to identify organisms. That is an important concept for microbial biology. It is not possible to describe microorganisms as is traditional with large organisms, through their morphological properties. To be sure, some microorganisms are intricate and beautiful under the microscope, but mainly they are relatively unfeatured at the resolution of routine microscopy. Therefore, to distinguish different types of microorganisms, early microbiologists turned to
metabolic properties of the organisms, such as their sources of carbon, nitrogen, and energy. Microbial taxonomy accumulated as anecdotal descriptions of metabolically and morphologically distinct types of organisms that were essentially unrelatable. Molecular phylogeny now provides a framework within which we can relate organisms objectively and through which we can interpret the evolutionary flow of the metabolic machineries that constitute microbial diversity.
Laboratory studies of microbial metabolism have focused mainly on such organisms as Escherichia coli and Bacillus subtilis. In the broad sense, such organisms metabolize much as animals do; we are all “organotrophs,” using reduced organic compounds for energy and carbon. Organotrophy is not the prevalent form of metabolism in the environment, however. Autotrophic metabolismfixation of CO2 to reduced organic compoundsmust necessarily contribute to a greater biomass than the organotrophic metabolism that it supports (a principle long appreciated by ecologists). Energy for fixing CO2 is gathered in two ways: “phototrophy” (photosynthesis) and “lithotrophy” (coupling the oxidation of reduced inorganic compoundssuch as H2, H2S, and ferrous ironto the reduction of a chemical oxidant, a terminal electron acceptor, such as oxygen, nitrate, sulfate, sulfur, and CO2). Thus, metabolic diversity can be generalized in terms of organ otroph or autotroph, phototroph or lithotroph, and the nature of the electron donor and acceptor.
The phylogenetic patterns of types of carbon and energy metabolism among different organisms do not necessarily follow the evolutionary pattern of rRNA (figure 1). Presumably, that is because of past lateral transfers of metabolic genes and larger-scale symbiotic fusions. Nonetheless, domain-level tendencies might speak to the ancestral nature of the three domains of life (Kandler 1993). The perspective, here, is limited mainly to Archaea and Bacteria. Such broad generalities cannot yet be assessed for the Eucarya, because so little is known about the metabolic breadth of the domain and the properties of the most deeply divergent lineages. There is considerable information about one pole of eukaryotic diversitythat represented by animals, plants, and fungi. We know little about the other polethe amitochondriate organisms that spun off the main eucaryal line early in evolution (Sogin 1994). The known instances of such lineagesrepresented by Trichomonas, Giardia, and Vairimorpha in figure 1are primarily pathogens. Pathogenicity in humans is a rare trait among the rest of eukaryotes and bacteria, and no archaeal pathogen is known. That correlation might indicate that nonpathogenic, deeply divergent eukaryotes are abundant in the environment but not yet detected. They should be sought in anaerobic ecosystems, possibly coupled metabolically to other organisms. A driving theme of the eucaryal line seems to be the establishment of physical symbiosis with other organisms. Beyond that, the general metabolism of the rudimentary eukaryotic cell seems simple and based on fermentative organotrophy. By virtue of symbiotic partners, however, eukaryotes are able to take on phototrophic or lithotrophic lifestyles and to respire using the electron-acceptor oxygen (Smith and Douglas 1987).
Symbiotic microorganisms commonly confer the lithotrophic way of life even on animals, although this was only recently recognized. The 2-m-long submarine vent tubeworm Riftia pachyptila, for instance, lives in the vicinity of sea-floor hy-
drothermal vents and metabolizes H2S and CO2 by means of sulfide-oxidizing, CO2-fixing, bacterial symbionts (Tunnicliffe 1992). This invertebrate and metabolically similar ones might contribute substantially to primary productivity in the ocean (Kates and others 1993; Lutz and others 1994). It is not necessary to go to (from our perspective) unusual places, such as ocean-floor vents, to encounter equally fascinating H2S-dependent eukaryotes (Fenchel and Finlay 1995). Under foot at the ocean beach, for example, microbial respiration of seawater sulfate creates an H2S-rich ecosystem populated by little-known creatures, such as Kentrophoros, a flat, gulletless ciliate that under the microscope appears fuzzy because it cultivates a crop of sulfide-oxidizing bacteria on its outer surface (Fenchel and Finlay 1989); the bacteria are ingested by endocytosis and thereby provide nutrition for Kentrophoros. In other anaerobic environments, methanogens, members of Archaea, live intracellularly with eukaryotes and serve as metabolic hydrogen sinks (Embley and Finlay 1994). Still other symbioses based on inorganic energy sources are all around us and are little explored for their diversity of microbial life (Fenchel and Finlay 1995).
Many lithotrophic but comparatively few organotrophic representatives of Archaea have been obtained in pure culture (Kates and others 1993). There are primarily two metabolic themes, both relying on the use of hydrogen as a main energy source. Among the known members of Euryarchaeota, one of the two archaeal kingdoms known through cultivated organisms, the main electron acceptors are CO2 and the product CH4, “natural gas.” Most of the CH4 encountered in the outer few kilometers of Earth's crust or on the surface is determined by isotopic analysis to be the product of methanogenic archaea communities, past and present. Such organisms probably constitute a huge component of global biomass. They certainly offer an inexhaustible source of renewable energy to humankind.
The general metabolic theme of the other established kingdom of Archaea, Crenarchaeota, also is the oxidation of H2, but with a sulfur compound as the terminal electron acceptor. All the cultivated representatives of Crenarchaeota also are thermophiles. Consequently, such organisms have been referred to as thermoacidophilic or hyperthermophilic archaeons; some grow at the highest known temperatures for life, up to 113°C in the case of Pyrolobus fumaris (Stetter 1995). These crenarchaeotes might seem bizarre to us, capable as they are of thriving at temperatures sometimes above the usual boiling point of water on a diet of H2, CO2, and S and exhaling H2S. Yet, in terms of the molecular structures of the basic cellular machineries, these creatures resemble eukaryotes far more closely than either resembles our gut bacterium E. coli (Marsh and others 1994).
The metabolic diversity of microorganisms is usually couched in terms of the use of complex organic compounds. From that standpoint and on the basis of cultivated organisms, metabolic diversity seems to have flowered mainly among the Bacteria. Even here, however, reliance on organic nutrients probably was not ancestral. The most deeply branching of the cultured bacterial lineages, represented by Aquifex and Thermotoga in figure 1, are basically lithotrophs that use H2 as an energy source and such electron acceptors as sulfur compounds (Ther-
motoga) or low concentrations of O2 (Aquifex) (Pitulle and others 1994). Cultivated organisms from these deeply branching bacterial lineages also are all thermophilic and thus share two important physiological attributes with the deeply branching and slowly evolving Archaea; a H2-based energy source and growth at high temperatures. That coincidence suggests that the last common ancestor of all life also metabolized H2 for energy at high temperatures; this inference is consistent with current notions regarding the origin of lifethat it came to be in the geothermal setting at high temperature (Pace 1991).
Chlorophyll-based photosynthesis was a bacterial invention. It seems to have appeared well after the establishment of the bacterial line of descent at or before the divergence of the line in figure 1 leading to Chloroflexus, a photosynthetic genus (Pierson 1993), and after the deeper divergences, such as those leading to Aquifex, and Thermotoga, which are not known to have photosynthetic representatives. Most bacterial photosynthesis is anaerobic, however. Oxygenic photosynthesis, the water-based photosynthetic mechanism that produces the powerful electron acceptor O2, arose only in the kingdom-level lineage of cyanobacteria. This invention changed the surface of Earth profoundly and is conventionally thought to be the basis, directly or indirectly, of most present-day biomass.
Anaerobic photosynthesis is widely distributed in the late-branching bacterial kingdoms. The more ancient theme of lithotrophy, metabolism of inorganic compounds, is also widely distributed phylogenetically, intermixed with organotrophic organisms. The pattern suggests that organotrophy arose many times from otherwise photosynthetic or lithotrophic organisms. Indeed, many instances of bacteria can switch between these modes of nutrition, carrying out photosynthesis in the light and lithotrophy or organotrophy in the dark. Particularly among bacteria, the type of energy metabolism seems highly volatile in evolution; bacteria that are closely related by molecular criteria can display strikingly different phenotypes when assessed in the laboratory through the nature of their carbon and energy metabolism. In the relatively closely related “gamma subgroup” of the kingdom of Proteobacteria (delineated by the genus Escherichia in figure 1), for instance, we find the phenotypically disparate organisms E. coli (organotroph), Chromatium vinosum (H2S-based phototroph), and the symbiont of the tubeworm R. pachyptila (H2S-based symbiont). The superficial metabolic diversity of these types of bacteria belies their underlying close evolutionary relatedness, giving no hint of the close similarities of their basic machineries. The versatility of Bacteria makes the metabolic machineries of Archaea and Eucarya seem comparatively monotonous. As the sequences of diverse genomes are compared, it will be possible to map the flow of metabolic genes onto the rRNA-based tree and see how metabolic diversity has been molded through evolution.
The molecular perspective gives us more than just a glimpse of the evolutionary past; it also brings a new future to the discipline of microbial biology. Because the molecular-phylogenetic identifications are based on sequence, not metabolic properties, microorganisms can be identified without the requirement for cultivation. Consequently, all the sequence-based techniques of molecular biology can be applied to the study of natural microbial ecosystems, heretofore little known with regard to organismal makeup.
A Sequence-Based Glimpse of Biodiversity in the Environment
Knowledge of microorganisms in the environment has depended mainly on studies of pure cultures in the laboratory. Rarely are microorganisms so captured, however. Studies of several types of environments estimate that more than 99% of organisms seen microscopically are not cultivated with routine techniques (Amann and others 1995). With the sequence-based taxonomic framework of molecular trees, only a gene sequence, not a functioning cell, is required to identify an organism in terms of its phylogenetic type. The occurrence of phylogenetic types of organisms, “phylotypes,” and their distributions in natural communities can be surveyed by sequencing rRNA genes obtained from DNA isolated directly from the environment. A molecular-phylogenetic assessment of an uncultivated organism can provide insight into many of its properties through comparison with its relatives. Analysis of microbial ecosystems in this way is more than a taxonomic exercise in that the sequences provide experimental tools, such as molecular hybridization probes, that can be used to identify, monitor, and study the microbial inhabitants of natural ecosystems (Amann and others 1995; Hugenholtz and Pace 1996; Pace and others 1985).
Every nucleic acid-based study of natural microbial ecosystems so far performed has uncovered novel types of rRNA sequences, often representing major new lineages only distantly related to known ones. The discovery of rRNA sequences in the environment that diverge more deeply in phylogenetic trees than those of cultivated organisms is particularly noteworthy. It means that the divergent organisms recognized by rRNA sequence are potentially more different from known organisms in the lineage than the known organisms are from one another. The deepest divergences in both Bacteria and Archaea were first discovered in rRNAbased surveys of communities associated with hot springs in Yellowstone National Park (See Hugenholtz and others 1998, for review).
The gene-based studies of organisms in the environment have substantially expanded our view of the extent of microbial diversity, reflected in new branches in phylogenetic trees. Figure 2 shows a diagrammatic tree of known bacterial diversity. When Woese first summarized the phylogeny of the phylogenetic domain Bacteria, he could articulate about 12 main phylogenetic groups. These groups have been called “phyla,” “kingdoms,” or “phylogenetic divisions”; I use the latter term. The number of recognized bacterial phylogenetic divisions has expanded now to about 36 (figure 2). About one-third of these divisions, indicated by the outlined wedges in figure 2, have no known cultivated representative and were detected only by rRNA gene-based studies of environmental organisms. Some of the most abundant organisms in the biosphere fall into these divisions with no cultured examples. Their abundance identifies such organisms as worthy of future study (Hugenholtz and others 1998). Environmental surveys of rRNA genes also have expanded the known diversity of Archaea and revealed that such organisms, previously thought restricted to “extreme” environments (from the human standpoint), in fact are ubiquitous. Crenarchaeota, for instance, all of whose cultured representatives are thermophiles, is revealed by the
molecular studies to be abundant in the marine environment and in soils (see Pace 1997, for review).
Microbial Diversity and the Limits of the Biosphere
Textbooks generally portray only a part of the global distribution of lifethe part that is immediately dependent on either the harvesting of sunlight or the
metabolism of the decay products of photosynthesis. The molecular phylogenetic record shows, however, that lithotrophic metabolism preceded and is more widespread phylogenetically and geographically than either phototrophy or organotrophy. The lithotrophic biosphere potentially extends kilometers into the Earth's crust, an essentially unknown realm (Ghiorse 1997). These considerations suggest that lithotrophy contributes far more to the biomass of Earth than currently thought. If so, where is it?
Part of the lithotrophic biomass is in microhabitats all around us, usually away from light and O2. It is not necessary to look far to find such environments: the rumens of cattle and the guts of termites and humans, for example, are important sources of CH4, a signature of hydrogen metabolism. Most life that depends on inorganic energy metabolism, however, probably is in little-known environments, according to poorly understood geochemistry. The oceans, for instance, cover 70% of Earth's surface to an average depth of 4 km. Most life in the ocean is microbial, and the metabolic patterns of such organisms are not understood. Does the occurrence of a large standing crop of low-temperature crenarchaeotes, potentially H2 oxidizers, indicate an unsuspected, lithotrophy-based food chain in the oceans? Another little-studied environment with global importance is the deep subsurface (Fredrickson and Onstott 1996; Gold 1992; Lovely 1995). There is increasing evidence that the Earth's crust is shot through with biomass wherever the physical conditions permit. Metabolism of H2 is a dominant theme among organisms isolated from geothermal settings or deep aquifers (Pedersen 1993; Stevens 1997). H2 is generated readily by abiotic mechanisms, such as interaction of water with iron-bearing basalt, the main stuff of Earth's crust. Consequently, a food source is unlikely to be limiting in most subterranean environments; it is likely to be the oxidant, the terminal electron acceptor, that limits growth. Nonetheless, it seems possible that much, perhaps most, of the biomass on Earth is subterranean, a biological world based on lithotrophy. Although the metabolic rate of this subterranean biosphere is likely to be far lower than in the more dynamic, photic environment, life is likely to be as pervasive in occurrence, and perhaps in cellular diversity, as we experience on the surface.
The opportunities for discovery of new organisms and development of resources based on microbial diversity are greater than ever before. Molecular sequences have finally given microbial biologists a way to define their subjectsthrough molecular phytogeny. The sequences also are the basis of the tools that will allow microbial biologists to explore the distribution and roles of the organisms in the environment. Microbial biology can now be a whole science and can study the organism in the ecosystem.
I thank Sydney Kustu, Gary Olsen, and Carl Woese for helpful comments on the manuscript and Sue Barns and Phil Hugenholtz for assistance with figures. Research in my laboratory is supported by grants from the National Science Foundation and the National Institutes of Health. This article is based on an earlier one (Pace 1997).
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Biodiversity, Classification, and Numbers of Species of Protists
Clear recognition of the great evolutionary gulf between the prokaryotes (essentially bacteria) and the eukaryotes (all other organisms) nearly four decades ago led to numerous studies that preoccupied research biologists' time for some years. But in the 1970s, attention began to refocus on the equally important specific fields of eukaryogenesis (the evolutionary appearance of cells above the bacterial level) and the phylogenetic origin of multicellular-multitissued organisms themselves, with the recognition that filling the gap between bacteria and animals/ plants seemed to require some intermediate level of organismic organization. The hypothetical “gap-fillers”to the surprise, perhaps, of many experimental biologists but not of field and taxonomic protozoologists and phycologiststurned out to be represented by the largely unicellular eukaryotic microorganisms, a huge assemblage (tens of thousands of species) of widespread but often poorly known forms that now can collectively be called the protists. Thus dawned the interdisciplinary field of protistology, arbitrarily said to have reached a recognizable state in about 1975 (Corliss 1986, 1987). Vast improvements in cytological techniques, including kinds of electron microscopy (Patterson 1994) and the advent of molecular methods (Cavalier-Smith 1995), have since aided greatly in the expansion of such investigations exploiting what may be termed the protist perspective.
Biodiversity, quite new itself as a term and concept in biology, is often linked with conservation in people's minds, and the organisms involved are typically the highly visible plants and animals now living on Earth. The protiststhat is, the generally unicellular and microscopic algae and protozoa and the lower fungiare, like the bacteria, cosmopolitan and ubiquitous; but the healthy abundance
of many of these microorganisms is absolutely necessary for maintenance of a sustainable world. Their roles at the base of the food chain and in nutrient recycling are known to be of the highest importance, and their potential in treating diseases is under study. Their roles in the preservation, not to mention the (past) evolution, of other organisms have been and are indeed indispensable. In contrast, some of the parasitic species are highly virulent to their hosts and thus can have disastrous effects on human populations, food crops, and domesticated animals. Today's unpredicted increase in appearance of opportunistic protistan parasites in AIDS patients is an example of our need to understand these organisms better. Only recently have all the points such as those mentioned above begun to become appreciated (Andersen 1992, 1998; Colwell 1997; Corliss 1989b, 1991, 1998a; Finlay 1998; Finlay and Esteban 1998; Hawksworth and Colwell 1992; John 1994; Norton and others 1996; Patterson and Sogin 1993; Sogin and Hinkle 1997; Vickerman 1992, 1998). But it is increasingly clear that much further work is required to assess the multiple roles of protists in natural ecosystems.
To speak quantitatively about the numbers of known protistan species, a main aim of this paper, we must first have some idea of the qualitative nature of protists: what are they, and how can they be defined and classified? A further questionwhat are the probable evolutionary and phylogenetic interrelationships of what to most people is the rather large number of separate high-level taxa commonly recognized as containing protists?is mostly well beyond discussion in the present brief essay, although it obviously affects the classification of the organisms concerned. For often detailed treatments of major aspects of the last question, the reader is referred to Coombs and others (1998), Hausmann and Hülsman (1996), Hülsmann and Hausmann (1994), Karpov (1990), Katz (1998), Knoll (1992), Ku´znicki and Walne (1993), Lipscomb and others (1998), Patterson (1994), Schlegel (1998), Sleigh (1995), Sogin and others (1996) and the many pertinent references within those works.
What is a Protist?
Even defining the term protist is somewhat controversial, so I shall offer only a broad and general description here, attempting to make clear their essential uniquenesses, in combination, as a great and diverse assemblage of organisms on Earth. Recent comments on this difficult question have appeared in works by Andersen (1998), Cavalier-Smith (1993b, 1998a), Corliss (1994a, 1998b), Hausmann and Hülsmann (1996), Margulis (1996), Patterson (1994), Vickerman (1998).
Protists, typically and mostly, are single-celled, microscopic eukaryotic organisms, occasionally forming a single tissue that can lead to large body size (for example, in some multicellular brown algae). As cells, they may have one to several nuclei; and various other organelles are always present in their cytoplasm. They represent, in general, a structural grade between the bacteria or prokaryotes and the so-called higher eukaryotes. Although eukaryotic themselves, protists do not have multicelled organs or true vascular systems, and ordinarily they do not show complex developmental or embryonic stages in their life cycles (ontogeny). Whereas the ancestors of some contemporary protistan groups very likely gave rise
to lines leading to such recognized kingdoms as Fungi, Animalia, and Plantae, othersas far as we can surmise at this timehave retained their protistan nature, evolutionarily speaking. It is reasonable to assume that extinction of protistan groups occurred often during past millennia, although the fossil record to date has not been very helpful in this respect (Lipps 1993; Tappan 1980). Sexuality is not recognized in species of many taxa; asexual division is the most common mode of reproduction and allows stability of an adapted genotype.
Overall distribution today of these lower eukaryotes is cosmopolitan; nutritional and locomotive modes are many, and there are amazing structural and functional adaptations (Hausmann and Hülsmann 1996). The single-celled species are wholly independent organisms: the two termscell and organismare thus not mutually exclusive descriptors (Corliss 1989a; Hausmann and Bradbury 1996). Major habitats of free-living forms include soils and bodies of freshwater and salt water; and ectosymbiotic and endosymbiotic species are found in association with numerous animal and some plant species and even other protists. Some parasitic forms are highly pathogenic (some malarial species of the genus Plasmodium are most notable), with hosts that include humans. Useful species (from the human perspective) include the many involved in essential food chains, in nutrient turnover in lakes and seas, in functioning as bioindicators or biomonitors of pollution and potentially as biocontrol agents, in serving as ideal cells in a multitude of biomedical and medical research projects, and in their direct roles in the petroleum, food, medicinal, agricultural, aquacultural, and other commercial industries. It has been said that 40% of global photosynthesis (carbon fixation and oxygen production) is contributed by algae, and the abundant diatoms alone are responsible for nearly half that (Andersen 1992, 1998).
Historical Background on Protistan Taxonomy
We need to understand background informationhowever briefon the overall classification of species now known as protists to appreciate their present status. More than a century ago, Ernst Haeckel (1866, 1878; and see Aescht 1998) and a few others proposed that these “lower forms” on the ladder of life should be considered as members of a distinct third kingdom, alongside the established kingdoms of Animalia and Plantae. To shorten a lengthy tale (Corliss 1998c; Lipscomb 1991; Ragan 1997; Rothschild 1989), such ideas, for various involved reasons, did not succeed for a long time, although refined and resurrected by such notable workers as Copeland (1956) and Whittaker (1969).
When the evolutionist-geneticist-microbiologist Margulis (1974, 1988; Margulis and Schwartz 1982; Margulis and others 1990) came on the scene, her forceful arguments stimulated a great deal of research in cell and evolutionary biology. Her undiluted enthusiasm convinced many a formerly reluctant biologist to appreciate the wisdom and particularly the convenience and pedagogical usefulness of a five-kingdom arrangement for all living organisms: Monera (or Bacteria), Protista (or Protoctista), Fungi, Plantae, and Animalia. A neo-Haeckelian system seemed to have become established for all time, although battles were (and are) incessantly waged over the internal composition of the “new” kingdom: what
and how many algal divisions and protozoan phyla, for example, are to be subsumed under that heading? What was definitely and irrevocably clear was that protozoa should no longer be treated as “mini-animals” and that most algae must no longer be considered to be merely “mini-plants” (Corliss 1983).
In recent years, considerable evidence has indicated that some major lines of protists share closer relationships with other kingdoms (an outstanding example is green algae with land plants) than they do with formerly neighboring protistan taxa. Such revelations threaten the stability of the whole five-kingdom conceptbut this is a complex subject largely beyond further consideration here. However, it is still often convenient and appropriate (as in this paper) to treat the many protistan groups as a single great assemblage, although using a lowercase “p” and writing of “the protists” rather than of “a kingdom Protista”. Incidentally, another problem, not due extended discussion here but deserving mention, is the nomenclatural matter of Protista and Protoctista (the latter is properly pronounced “proto-tista”, in that the “c” is silent in this combination). Arguments for both names exist in the literature, but I believe that today the consensus among research protistologists favors the shorter name; and there is no rule of nomenclature that obliges one to treat the longer word as having any official priority (Corliss 1990, 1994a).
Alternatives to accepting a single formal kingdom Protista have recently been reviewed (Corliss 1994a,b, 1998c; see also Cavalier-Smith 1998a); listing them should suffice here to give the reader an appreciation of possible choices that exist. One is to recognize no separate high-level taxon for the protists, considering them overall to represent but an evolutionary grade or level of cellular organization (between bacteria and the higher eukaryotes) and thus sidestepping a number of high-level taxonomic problems. A second is to view groups of protists as simply mostly independent evolutionary lines or lineages, again leaving aside attempts to define high-level taxonomic interrelationships among such lines; cladistically derived phylogenetic trees (such as those constructed from collected molecular biological data) often support such a choice. Finally, to avoid a single, perhaps highly artificial kingdom for the diverse protist assemblages, some workers have proposed the assignment of these organisms to multiple kingdoms of eukaryotes. Such kingdoms can number from five or six to 18–20 or even more. Some might be composed solely of protists; others might contain various protistan taxa but comprise predominantly taxa of existing major kingdoms of multicellular organisms (such as the Plantae, Animalia, or Fungi).
Classificational Framework for Major Groups of Protists
Although discussion of the evolutionary or phylogenetic relationships of the diverse high-level protistan groups is beyond the scope of the present paper, a taxonomic framework of some sort is necessary for clarity in the treatment of their nature or composition, including numbers and inventories of species. Only naming or identifying major assemblages will make possible our recognizing, comparing, and retrieving information about the different groups (Mayr 1997, 1998),
many of which, in the case of the protists, have been known (under a variety of names) for scores of years.
Adopting Cavalier-Smith's (1998a) five eukaryotic kingdoms and their names, and using a constellation-of-characters (Corliss 1976) approach as a basis for their taxonomic separateness, I have assigned some 14 phyla of protists to PROTOZOA, 11 to CHROMISTA, six to PLANTAE, and two each to FUNGI and ANIMALIA; see table 1. Thus, I am suggesting that some 35 eukaryotic phyla are required to contain the protists overalla welcome reduction from the 45 of 15 years ago (Corliss 1984). A very brief description of the taxonomic composition of the kingdoms involved is appropriate here because even the better-known ones might no longer embrace the same phyletic taxa as in years past. A link with the classical systems, at both nomenclatural and taxonomic levels, is needed if we are to understand the present locations and interrelationships of the diverse protistan forms implicated.
PROTOZOA (literally meaning “first animals”) traditionally has embraced species belonging not only to the phyla listed in Protozoa in table 1 but also to other major taxa no longer included there, most notably Cryptomonada, Haptomonada, Labyrinthomorpha, Opalinata, and some lower taxa of Bicosoecae, Chrysophyta, and Dictyochae; I consider these seven phyla to belong to the kingdom Chromista. The phyla Choanozoa, Myxozoa, and Microspora were also treated as protozoan taxa in the past. The first two of these are now assigned to Animalia, and the third to Fungi (see table 1). Even a few well-studied genera of Chlorophyta and Prasinophyta, phyla now both in Plantae in table 1, have been steadfastly embraced by protozoologists in their classification schemes. So, interestingly, the present kingdom Protozoa is considerably more restricted, more refined, and thus more meaningful than the former phylum Protozoa of the literature (see discussions in Cavalier-Smith 1993b; Corliss 1994a).
CHROMISTA never existed in former times as such, before Cavalier-Smith's (1981) proposal of this particular name (see also Cavalier-Smith 1986, 1989,
1997b, 1998a). Despite its containing some former protozoan groups (see above), it is now largely “algal” in composition, including such major well- and long-known, mainly photosynthetic groups as Chrysophyta, Diatomae, Phaeophyta, and Raphidophyta (with their many well-known classes). Furthermore, botanists have generally claimed Bicosoecae and Dictyochae at the same time that zoologists were considering them to be “first animals”. In much of its composition, the kingdom Chromista of table 1 resembles the rather similar assemblage widely known today as the stramenopiles (Patterson 1989, 1994; Sogin and Hinkle 1997). Both circumscribed groups, chromists and stramenopiles, contain predominantly species of the old and large heterokont algal assemblage of the past botanical and phycological literature (see historical reviews in Corliss 1984, 1994a).
PLANTAE, a kingdom for scores of years, has conventionally been composed not only of the bryophytes, pteridophytes, and higher aquatic and terrestrial species (gymnosperms, angiosperms, and so on), but also traditionally of all the so-called algae, ranging from the prokaryotic cyanobacteria (blue-green algae) through the algal classes and divisions (or phyla) listed in this paper under various kingdoms, not to mention all fungal and even bacterial taxa. Here (see Corliss 1994a, 1998c), I have restricted the plant kingdom to the vascular (multicellular) photosynthetic eukaryotes plus four phyla of green algae, one of red algae, and one for the enigmatic glaucophytes (table 1).
FUNGI, separated from Plantae by various workers during the last 40–50 years (recently more vigorously; see Barr 1992), is sometimes persistently considered basically as a “plant” group. It has long included phyla of the so-called higher fungi (Ascomycota, Zygomycota, and Basidiomycota), but it has conventionally also laid claim to various lower fungi, including diverse kinds of slime molds (now under Protozoa or Chromista; see table 1) and the water molds or so-called motile zoosporic fungi (the chytrids, which are true fungi, and members of the Pseudofungi, which are quite different in many taxonomic characteristics and now assignable as heterokontic algae to Chromista). Very recent molecular studies add the curious and possibly ancient “protozoan” group of Microspora (the microsporidians), minute intracellular parasites with unique spores, to the Fungi (Canning 1998; Edlind 1998; Keeling and McFadden 1998).
ANIMALIA, long recognized as the haven for numerous invertebrate and vertebrate phyla, is little affected by protistan studies and reclassifications. However, the always-enigmatic Myxozoa (protozoan myxosporidians of the literature) are now thought to be animals of some sort (Anderson 1998; Cavalier-Smith 1998a; Corliss 1998b; Schlegel and others 1996; Siddall and others 1995; Smothers and others 1994). One might add to the kingdom, as I have controversially done (Corliss 1998c), the choanoflagellates, definitely considered a link to the sponges of Animalia and now to the Fungi as well (Cavalier-Smith 1998a,b).
Obstacles to Deriving Reliable Estimates of Numbers of Protists.
There are many reasons why our knowledge of the kinds and numbers of protistan species generally lags far behind that for numerous other groups of organ-
isms; these deserve brief mention here. In general, and above all, their tremendous diversitycombined with their often microscopic size, cosmopolitan nature, lack of overt sexual processes, and no helpful fossil recordrenders precise study of the morphology, taxonomy, and evolution of most of them very difficult. Furthermore, protists for scores of years have been described by a motley array of naturalists, zoologists, botanists, mycologists, cell biologists, ecologists, limnologists, microscopists, parasitologists, and, more recently, geneticists and evolutionary and molecular biologistspersons with highly diverse backgrounds and conceptual outlooks and, in many cases, without rigorous taxonomic training or even proper awareness of the relevant systematic literature in protistology. Other, more specific reasons for our continuing ignorance and uncertainty about numbers of protists in existence include the following (sometimes overlapping) factors:
• The lack of a universal definition of a species among largely asexual eukaryotic microorganisms. There are few guidelines to assist taxonomic protistologists in their choice from a veritable smorgasbord of kinds (some overlapping) of species in the biological literature: morphological, phenetic, nominal, ecological, cryptic, endemic, taxonomic, parataxonomic, biological, asexual, sexual, genetic (sibling or syngenic), molecular, and chimaeric. The morphospecies concept seems reliable for numerous protists (Finlay and others 1996). But what are the criteria for recognition of the separateness of presumably closely related species? And to what extent does polymorphism (common and often striking in many groups of protists) complicate the problem, not to mention the historical acquisition of some endocytoplasmic inclusions or organelles by engulfment of (or invasion by) “foreign” microorganisms in eons past (Bardele 1997; Cavalier-Smith and Lee 1985; Gray 1992; Margulis 1993, 1996; Sapp 1994; Taylor 1987a)?
• An abundance of nomenclatural problems, exacerbated by lack of clarity in recognizing boundaries at the species and much higher taxonomic levels (Corliss 1993). Different protists have inadvertently been given identical names, and the same protist might have been described independently under different names: this has happened especially in cases of the so-called ambiregnal protists (Corliss 1984, 1986, 1995; Patterson 1986b; Taylor and others 1986). Names of species not accepted by later revisers (for example, of a genus or family) fall into synonymy with the oldest name available (rule of priority); but the senior synonym itself could be associated with an inadequately described organism. Problems are compounded by lumpers and splitters (Corliss 1976) in taxonomic protistology. And, in recent years, with the seemingly constant shifting about in the assignment of various groups to individual higher taxa, anyone tabulating species must be careful not to count the same organism twice under different headings in the ever-changing scheme of higher protistan classification (Corliss 1998b).
• The justification of new species continually being described in the literature on practically all protistan taxonomic groups (see the Zoological Record and relevant botanical and algal lists and monographs). The lack of appropriate techniques of study in the past might often have been the cause of proliferation of what are now deemed unnecessary or unacceptable species; but, today, is it the availability of improved cytological, biochemical, and molecular methods that fuels
the persistent description of new forms? Yet, as habitats and niches in diverse geographic and ecological areas (including new host species for symbiotic forms) are more thoroughly explored (perhaps even for the first time), is it not reasonable to anticipate the finding of at least some novel species of algae and protozoa? In general, taxonomic protistologists are in widespread agreement that this is inevitably the case, while they understandably bewail the shortage of trained students and funds to investigate such habitats (Andersen 1992; Vickerman 1992). For the large protozoan phylum Ciliophora, in particular, Finlay and others (1996) argue that the great majority of the free-living, free-swimming, phagotrophic forms from freshwater and salt water habitats probably have been discovered and described already and that the number of these considered acceptable reaches only a few thousand. Foissner (1998), in contrast, claims that hundreds of additional species of ciliates inhabiting such edaphic habitats as diverse soils, with perhaps as many as 75% of them not living elsewhere, have been largely and unfairly neglected.
• The different ways in which different workers categorize the areas covered in their own studies or reviews. For example, members of most protistan high-level taxa might be thought of, by some, as falling into only three major groupings, with scant attention to overlappings: free-living species, symbiotic-parasitic forms, and fossilized species (of extinct or contemporary taxa). But the extent to which “symbiotic” and “free-living” forms can coincide is often blurred; consider the cases of mutualistic and commensalistic forms versus “true” endoparasites and ectoparasites, or even those of symphorionts (basically independent organisms merely carried about by nonspecific “hosts”). Other investigators might divide protistan groups on the basis of their being found in different major ecosystems: freshwater, marine, estuarine, or terrestrial habitats. Numerous workers emphasize what seems to be the preference of their organisms for specific geographic areas, raising the problem of endemism versus cosmopolitanism in recognition of “new” species. Still another popular general categorization highlights modes of nutrition: autotrophs (via photosynthetic pigments) versus heterotrophs (phagotrophs and osmotrophs or saprotrophs), with bacteria and algal protists serving as the most commonly engulfed prey organisms. Unfortunately, authors have sometimes not specified the limits or boundaries used in arriving at their particular “total numbers” of species assignable to a given higher taxon.
Is it any wonder that few published works make reliable overall estimates of the total numbers of species of protists? Keeping in mind the difficulties mentioned above, I am attempting here to overcome most such obstacles and arrive as objectively as possible at reasonably accurate figures of known protists as of 1998.
Numbers of Protists in Major Groups
In the following sections, I purposely arrange major taxa of protists under widely known “tried and true” top-level conventional headings, using vernacular titles for such broad categories“protozoa,” “algae,” “fungi,” “plants,” and “animals.” In each section, the formal names of protistan phyla acceptable to me (see table 1)
are given in boldface, often with an indication of synonymous names and with cross-references, as needed, to the kingdom (names are in all capital letters for easy recognition) in which a given phylum, in my opinion, seems best assigned today. The final location of a phylum might not match the title of the section; and for some groups, the reader is referred to fuller treatment under one of the other sections.
Sources of data leading to my estimated numbers have been many, beginning with those cited, directly or indirectly, in my own first publications on the subject (Corliss 1982, 1984). All such figures have naturally required considerable updating to take into account new species descriptions and to accommodate revisions in which former species might have been rejected. Too numerous to list here have been the useful taxonomic monographs, books, compendia, and authoritative individual papers that I have consulted. But I should mention the most helpful single modern source of information, the volume edited by Margulis and others (1990), a prodigious work that contains 36 scholarly chapters contributed by some 60 specialists on the diverse high-level taxa of protists.. For some groups, our knowledge of numbers is still frustratingly fragmentary. Also distressful is the continuing instability of the exact composition of various higher taxa involved in overall protistan megasystematics, which makes exact placement of some implicated genera and their species difficult. Generic names that are representative of particular taxa, incidentally, are generally not included in the present paper, because of space limitations, illustrative of diversity though they would be. For the interested reader some 1,100 of them have recently appeared elsewhere (Corliss 1994a; and see many more in specialized phycological and protozoological textbooks and in Lee and others 1985, Margulis and others 1990, Margulis and Schwarz 1998, Parker 1982, and Tappan 1980, although genera might be quite differently classified at the highest levels in such works).
Conventional Protozoan Phyla
The taxa below follow the usual arrangement commonly found in well-known biological and more-specialized protozoological textbooks. That is, forms mostly amoeboid, although also including some amoeboflagellates, with pseudopodia of various kinds (the old rhizopod and actinopod “sarcodinids”) make up the first grouping; the numerous taxa whose species are predominantly biflagellated or multiflagellated (both pigmented and nonpigmented arrays, roughly the “phytoflagellates” and “zooflagellates,” respectively, of old) come next; spore-forming parasitic taxa (sporozoa and the former “cnidosporidian” groups) are then treated; and finally the ciliates, a large collection of species that represents one of the most circumscribed and noncontroversial protistan taxa of all, are mentioned.
Names given first (and in boldface type) follow those used in table 1; but explanations and brief descriptions plus major synonymous names are supplied when deemed helpful. Note that, although some two dozen phyletically named taxa are considered below as, in effect, conventionally known “protozoan-like groups,” nearly half have been reassigned to kingdoms other than the PROTOZOA of the present paper, as pointed out in appropriate places.
Archamoebae (synonym Karyoblastea): The pelobionts (such as Pelomyxa, a free-living, freshwater, benthic “giant amoeba” reaching 5 mm in diameter), embracing some five or six genera if the parasitic Entamoeba is also accepted here. Not long ago, these amitochondriate protists were placed in a separate kingdom, the “ARCHEZOA,” along with the Metamonada and the Parabasala (see below). Although descriptions of quite a few species have appeared in the literature, there is now wide agreement that the number of acceptable ones is probably less than 12. The conservative figure that I am using as a total here is 10.
Neomonada: A group of often small, free-living, marine heterotrophic flagellates and amoeboflagellates (Cavalier-Smith 1998b), still ill-defined, many formerly in Cavalier-Smith's (1993a, 1997a) phylum “Opalozoa”. Depending on the workers involved, the number can range from a dozen or two to several score (including some of the “unassignable” forms of Patterson and Zölffel 1991); many genera are monotypic (that is, they have only a single species). At this time, I estimate 30 as a possible total number of valid species here.
Rhizopoda (synonym Amoebozoa, in part, of Corliss 1984): Predominantly typical amoeboid forms, including ones with tests, shells, or thecae, but some small heterotrophic flagellates here as well (see Patterson and Zölffel 1991). Some workers put the enigmatic algal Chlorarachnion here; others, 40 or more species of plasmodiophorans (endoparasitic slime molds). Separation from the following phyletic group is not always clear. There are at least 5,000 species, with some to be dropped (for example, hundreds of poorly described testaceous amoebae might be rejected by future workers), but predictably with many new “small naked amoebae” awaiting discovery (Vickerman 1992). A few fossil formsand possibly 250 symbiotic specieshave been described.
Mycetozoa (synonyms Eumycetozoa and Myxomycetes): A “lower fungal” plasmodial slime mold group containing both cellular and “acellular” species. Some plasmodia can be longer than 3 m. Exact boundaries are uncertain (see remark under Rhizopoda, above). Some 800–900 species are assigned here, with probably more to be moved in from other taxa and still others to be found and described as new. Possibly a few fossils and a number of symbiotic forms belong here as well (for example, the necrotrophic plasmodiophorans, the soil protists infecting cabbage and other plants).
Foraminifera (synonym Granuloreticulosea): The foraminifers in the broadest sense (Lee and Anderson 1991). Perhaps as many as 45,000 species have been described, with nearly 40,000 as fossilized forms (many represent extinct lines and make up the “globigerine ooze” on ocean floors and are invaluable in dating strata for the petroleum industry). The diameter of some extinct fossil shells or tests may reach 15 cm; of living extant species, up to 6.5 cm. No end of new forams is in sight, although some workers question the taxonomic significance of some minor differences in morphology of the calcareous test. A few taxonomists include 15 genera of xenophyophorans (body diameters, up to 25 cm) and 12 genera of komokiaceans here.
Labyrinthomorpha: Net slime molds of mycologists; unique parasitic forms (for example, on eelgrass); also some saprotrophic on dead tissues. These are now better placed in the kingdom CHROMISTA than in PROTOZOA or FUNGI (Cavalier-Smith 1998a). The group includes labyrinthuleans proper plus thraustochytriaceans. It totals about 50 species.
Heliozoa: Mostly a freshwater group of the classical “actinopod sarcodinids”. The amazing marine Sticholonche zanclea, a single species formerly considered to make up the separate heliozoan class Taxopoda, is perhaps better assigned to membership in the next phylum (Radiozoa, below). Some 180 species have been described as heliozoa, but only about 100 might be acceptable to today's specialists on the group, which itself could still be a polyphyletic taxon (Smith and Patterson 1986).
Radiozoa (synonym Radiolaria): Spherical marine planktonic “actinopods”, producers of great depths of “radiolarian ooze” on ocean floors. There are three major subgroups, of which the first two are closer taxonomically to each other than to the third (all are sometimes treated as separate phyla): Acantharia, 500 species (possibly only half valid), of which no fossils have been described; Polycystina, 10,000 species (possibly only half valid), nearly 75% of which are found as fossils; Phaeodaria, without the endosymbionts found in preceding groups, 1,150 species (possibly only 60% valid), few of which have been found as fossils.
Percolozoa: Small heterotrophic flagellates or amoeboflagellates; a considerably smaller group than when originally circumscribed (Cavalier-Smith 1993b). Some former heterolobosean genera are here, some “unassignable” forms of Patterson and Zölffel (1991), and, controversially, the ciliate-turned-flagellate (Lipscomb and Corliss 1982; Patterson and Brugerolle 1988) Stephanopogon. There are more than 100 species.
Bicosoecae: Small nonpigmented heterotrophic flagellates, some colonial. This group has long been claimed by protozoologists, but see the treatment under “Algae,” below. It is assigned to the kingdom CHROMISTA.
Dictyochae: Silicoflagellates, some known from the fossil record; long claimed by protozoologists; but see the treatment under “Algae,” below. It is assigned to the kingdom CHROMISTA.
Cryptomonada: Mostly pigmented species, although many are heterotrophic. The group has long been claimed by protozoologists, but see the treatment under “Algae,” below. It is assigned to the kingdom CHROMISTA.
Haptomonada: Pigmented, but claimed also by protozoologists. It is treated here under “Algae,” below. It is assigned to the kingdom CHROMISTA.
Opalinata (synonyms Protociliata, Paraflagellata): Protozoologists' well-known opalinid parasites (in the strictest sense) plus Karotomorpha and Proteromonas (Delvinquier and Patterson 1992; Patterson 1986a). More than 400 species are
reported in the literature, but many of the opalinids described are from ill-fixed material; perhaps only 200 are acceptable as valid today. The group was in PROTOZOA and is now assigned to the kingdom CHROMISTA (Cavalier-Smith 1998a,b).
Euglenozoa: Two principal subgroups (Triemer and Farmer 1991; Vickerman and others 1991): The Euglenophyta of the algal literature, more than 1000 species, mainly free-living, freshwater, and photosynthetic, although also phagotrophic, colorless, and some symbiotic-parasitic (and rare fossil) forms are known; and the Kinetoplastidea of the protozoological-parasitological literature, more than 600 species, ranging from pathogenic blood and tissue parasites of human beings (trypanosomatids) to free-living, freshwater or salt-water biflagellated species (bodonids).
Dinozoa (synonyms Dinoflagellata, Pyrrhophyta, and Peridinea + Syndinea): A major group of unique biflagellated protists, the dinoflagellates, long claimed by both phycologists and protozoologists. The pigmented species, some also heterotrophic, are a major component of marine plankton, but 10% occur in fresh-water habitats; about 50% of the species are nonpigmented; some dinos are thecate and some colonial. About half the described species have been found as fossils, exclusive of 400 genera of acritarchs (a fossil group also assigned here by some workers) but including the small taxa of ebriideans and ellobiophyceans. Some species are important symbionts of other organisms; others exhibit toxic blooms (for example, red tides) with direct and indirect effect on humans. There is a distinct taxonomic subdivision of osmotrophic, endosymbiotic forms in diverse marine hosts. A primitive group might now include the nonpigmented former apicomplexan (see below) parasite Perkinsus (Siddall and others 1997). There are some 4,500 species, with perhaps nearly 2,500 as fossils of some extant but mostly extinct forms (Fensome and others 1993; Taylor 1987b).
Metamonada (synonym “polymastigotes,” in part): Biflagellated to multiflagellated forms, typically gut parasites of diverse hosts (from insects to humans), allegedly (with the following phylum) primitive protists (Vickerman and others 1991). They have no mitochondria but hydrogenosomes (latest review, Müller 1998). There are about 300 species, but some are in need of restudy.
Parabasala (synonym “polymastigotes,” in part): Mostly parasitic multiflagellated forms (called trichomonads and hypermastigotes), amitochondriate, and with striking parabasal (Golgi) apparatus. They share enough characteristics with the above phylum (Metamonada) to be joined with it (and the Archamoebae) under the one-time kingdom “ARCHEZOA” of Cavalier-Smith (1993b, 1998a, and references therein). The group has more than 400 species, some in need of restudy; doubtless more will be found, especially in the inadequately explored insect (woodroach) digestive tract.
Choanozoa (synonyms Choanoflagellata, Craspedophyceae): Planktonic (mostly marine) nonpigmented “collar-flagellates” with a single smooth anterior flagellum, often stalked or loricate. The group was placed in the protozoan phy-
lum Neomonada by Cavalier-Smith (1998b) and tentatively transferred to the kingdom ANIMALIA by Corliss (1998c) and here. There are about 150 species.
Apicomplexa: Popular name for what is essentially the still-valid “Sporozoa” of old (Ellis and others 1998). An “apical complex” is made visible only by electron microscopy. The species are all symbiotic in a great variety of hosts, many as harmful endoparasites (Levine 1988; Perkins 1991). They include some of the smallest protists (intracellular forms with diameters less than 1mm), although others can be up to 10 mm long. The major subgroups are gregarines (some large), coccidians (Toxoplasma and others in humans), and haematozoeans (malarial organisms and others). Perkinsus has been transferred to the phylum Dinozoa (see above). The “Ascetospora” of the literature is tentatively placed here. There are more than 5,000 species, some questionable today because of inadequate past accounts; but parasitologists predict numerous yet-to-be-described species. Levine (1973) once estimated, on the basis of potential combinations of numbers of sporocysts and sporozoites in the oocyst (which represent important differentiating taxonomic characters), that there could be, hypothetically, more than a million species in the second sporozoan subgroup (the coccidians) alone!
Microspora (synonym Microsporidia): A highly unusual group, with very small spores (diameters less than 1 mm) containing a complex extrusome and with a chitinous cell wall. The group consists of obligate intracellular parasites found in other protists, insects, fishes, and, opportunistically, human AIDS patients. Unicellular forms long considered as protozoa, they are here placed in the kingdom FUNGI on the basis of recent molecular findings (see citations in a preceding section of this paper). There are more than 800 species.
Myxozoa (synonyms Myxosporidia and Myxospora): Formerly grouped with Microspora as “cnidosporidians”. These are histozoic or coelozoic parasites, mainly of cold-blooded vertebrates (the cause of great economic losses in the commercial fish industry). They have valved multicellular spores with polar capsules that include extrusible filaments. They were long considered as protozoa but here are placed in the kingdom ANIMALIA mainly on the basis of molecular data (see citations in a preceding section of this paper). There are more than 1,200 species. Some species in invertebrates, formerly assigned to independent status in a (second) major class, Actinomyxidea, are now being identified as simply stages in the life cycle of well-known myxosporidian fish parasites (Kent and others 1994).
Ciliophora (synonym Heterokaryota): Multiciliated (usually), colorless (with exceptions), relatively large cilioprotists (general range, 10–500 mm; a few up to 5,000 mm; and some colonies up to 15 cm in diameter). They exhibit nuclear dualism (the heterokaryotic conditiontwo kinds of nuclei, macronuclei and micronuclei; see Raikov 1996 for latest review), and are often phagotrophs, freeliving in widely diverse habitats, although many groups are symbiotic-parasitic (including Balantidium in humans) or symphoriontic (the latter usually stalked). This is a large phylum (ranking fifth among all protists, behind diatoms, forams, charophytes, and radiolarians), with 8–10 classes and many orders. The total
number of species is often said to be at least 8,000, including about 200 fossil forms (all of tintinnids) and an estimated 2,600 symbiotic species, with many more presumably awaiting discovery (Corliss 1979; Lynn and Corliss 1991; Small and Lynn 1985). But more conservative figures have recently been offered by Finlay and others (1996), who estimate a maximum of 4,300 for their pragmatic “morphospecies” of cosmopolitan free-living, phagotrophic forms primarily from major freshwater and salt-water habitats (calculating this to be 70% of all ciliates, including symbiotic species) and who suggest that careful taxonomic revisions might reduce their number to about 3,000. The matter is controversial (there might be many more valid soil-dwelling species than is often appreciated: see Foissner 1998).
Additional “protozoan” groups: Treated in the following section as conventional green or golden-brown “algal”taxa, are three phyla from within which selected (mostly motile) subgroups have long been of interest to protozoologists: the Chlorophyta (the volvocine line) and the Prasinophyta (both assigned here to the kingdom PLANTAE) and the Chrysophyta, assigned to the kingdom CHROMISTA. Treated in the later section on conventional “fungal” phyla are members of the Chytridiomycota, a number of species of which have been routinely included in protozoological textbooks. But that phylum, in its entirety, is placed in the kingdom FUNGI in this paper. Finally, the “Ascetospora” or “Haplosporidea” of both old and more recent literature (for example, CavalierSmith 1993b; Corliss 1994a) is tentatively placed within the Apicomplexa (above) here, on the basis of reasoning found in Cavalier-Smith (1998a).
Conventional Algal Phyla
Deliberately omitted here is further mention of the prokaryotic (cyanobacterial) divisions or classes of algae, the “Cyanophyta” or blue-green algae, with some 2,000 species, and the “Prochlorophyta” with fewer than six. Many botanists and phycologists recognize three “true” major broad algal assemblages, the red algae, the green algae, and the chromophyte algae. The latter vast group (containing numerous classes, depending on the author) has been known by a variety of names, including Chromobionta, Heterokontae, Heterokontophyta, and even Chrysophyta (in its broadest usage). Andersen (1992), whose summarizing table on numbers of algal species overall has been especially helpful to me (see also John 1994; Norton and others 1996), considered those three diverse assemblages to be taxonomically and phylogenetically “the major algal lineages,” with four additional “minor lineages” (dinoflagellates, euglenophytes, cryptophytes, and glaucophytes) listed in his table below his classes of chromophytes.
Here I recognize some 16 eukaryotic algal groups, at phylum (division) rank, eight of which I assign to the kingdom CHROMISTA, six to PLANTAE, and two to PROTOZOA (Euglenozoa, Dinozoa: see above). The chromistan phyla contain the majority of the species broadly classified as “chromophyte algae” by botanists, and most of their species are pigmented (that is, carry out photosynthesis). My order of presentation below more or less follows the conventional arrangement used by many phycologists. Space does not permit specific mention of the names
of many often traditionally well-recognized algal taxa usually treated (and here generally so retained) at the level of class or below, not as divisions or phyla. Their numbers of species have not been left out of my overall count but are included, as appropriate, in totals given for such large, all-embracing phyla or divisions as the Chlorophyta and the Chrysophyta. Some former classes have been elevated to phyletic status, or their names have here been considered more or less synonymous with preferred different names for the higher rank of phylum. “Taxonomic inflation”, bringing about a concomitant increase in names, has been as inevitably rampant, in recent years, among the “algal” protists as among their “protozoan” and “fungal” counterpartsperhaps a consequence of our increasingly precise methods of study and analysis of the systematics and phylogeny of these highly diverse eukaryotic microorganisms (Corliss 1998b).
Rhodophyta: Nonflagellated, mostly marine, macroalgae (red seaweeds), but some minute unicells as well, and some parasitic species. Meter-long multicellular parenchymatous forms appear along rocky shores. The two principal classes or subgroups, Bangiophyceae and Florideophyceae, each have several or many orders. Species encrusted with CaCO3 fossilize well. Red algae are a source of commercially valuable agar and of maerl, widely used as a fertilizer. This taxon (containing some of the oldest fossil algae known) has been given very high independent ranking taxonomically or, as here, has been assigned a unique place in the kingdom PLANTAE. There are well over 5,000 species (about 750 as fossils), and more than 100 species have been described as parasites of other red algae.
Glaucophyta (synonym Glaucocystophyta): A small algal group, all with cyanelles, all freshwater, and most biflagellated. They are placed in or near Rhodophyta by many workers; here, they are tentatively assigned to separate phyletic status in the kingdom PLANTAE. Depending on the number of accepted genera, the species counts range from a few to about 15.
Prasinophyta (synonym Micromonadophyceae): Grass-green scaly algae, freshwater, mostly small (and possibly primitive) biflagellated unicells. One of the tiniest free-living protists belongs to the picoplanktonic genus Micromonas (diameter, 1 mm). These species are assigned to the kingdom PLANTAE with other green algae. Some 400 species have been described (but perhaps only half that number are fully acceptable). About 100 have been found as fossils (some of which were originally identified as acritarchs; see the comment under Dinozoa, above).
Chlorophyta: The green algae of the botanical literature, mostly unicells or colonial in freshwater, many nonmotile. The celebrated “zoochlorellae” (symbionts of many ciliates) of the classical protozoological literature (and see Reisser 1992) belong here. There are many separate classes or orders; some phycologists conservatively include here members of some of the other phyla described below (such as Ulvophyta). This evolutionarily important and ecologically widespread group is assigned to the kingdom PLANTAE. It contains perhaps more than
3,500 species, depending on the inclusiveness of the phylum and thus on the workers making the counts.
Ulvophyta: Includes macroscopic seaweeds from tropical marine waters. They are sessile, with coenocytic or multicellular thalli. The group is assigned to the kingdom PLANTAE and contains at least 300 species, a few of which are fossils.
Charophyta (synonyms Conjugatophyceae, Gamophyceae, and Zygonematophyceae, and others): Mostly (including the ubiquitous desmids) unicellular or filamentous in freshwater, vegetative stage nonflagellated, and with conjugation often involving amoeboid gametes. Larger formsfar fewer in speciesare placed in a separate class, which includes the well-known stoneworts, with macroscopic thalli typically scale-covered. Several charophyte characteristics are clearly reminiscent of land plants, their evolutionary descendants. This group of green algae is assigned to the kingdom PLANTAE. It has some 12,000 species, but about 9,000 are desmids alone (of which half are of uncertain validity); stoneworts number fewer than 400 species, about 300 of which have been found only as fossils.
Dinozoa: Long (and still) claimed as algae, but treated in this paper as PROTOZOA (see preceding section).
Euglenozoa: Long (and still) claimed as algae, but treated in this paper as PROTOZOA (see preceding section).
Bicosoecae: Freshwater and marine nonpigmented flagellates, some with loricae. These were formerly placed within Chrysophyta. The group is assigned to the kingdom CHROMISTA and contains about 40 species.
Dictyochae (synonym Dictyochophyceae): Silicoflagellates, formerly in Chrysophyta, with a number of fossil marine forms. Dictyocha is the only genus with extant species (as the phylum is restricted here). The group is assigned to the kingdom CHROMISTA. It has fewer than 12 species (excluding Actinomonas and Pedinella and close relatives that are placed here by some phycologists).
Cryptomonada (synonym Cryptophyta): Well-known freshwater and marine mostly pigmented biflagellated protists, some phagotrophic, some endosymbiotic. The group is controversially assigned to the kingdom CHROMISTA but not within the large heterokontic moiety. There are about 200 species.
Haptomonada (synonyms Coccolithophora, Haptophyta, and Prymnesiophyta): Yellow-brown algae, typically marine flagellates with unique haptonema arising between a pair of polar flagella and a body usually covered with layers of scales, some known as coccoliths. The group is controversially assigned to the kingdom CHROMISTA but not within the large heterokontic moiety. Some 500 living and 1,200 fossil species have been described; the celebrated white cliffs of Dover are composed mostly of coccoliths.
Chrysophyta: The golden-brown algae, numerous freshwater species, some with delicate loricae, and many producing a unique statospore as a resting stage. The group is assigned to the kingdom CHROMISTA as a major phylum of the heterokontic moiety there. There are perhaps more than 1,500 species, several classes of which are given independent phyletic status by some workers. The total includes about 250 fossil forms.
Diatomae (synonyms Bacillariophyta, Diatomea, and Diatomophyceae): The diatoms. “Bacillariophyceae” is the most popular name used for this taxonomic group. They are yellow-brown unicells, widespread planktonic and benthic forms in salt-water amd today especially freshwater habitats and are also found in moist soil; a few are endosymbionts of the protozoan foraminifers (Lee 1992). They are nonflagellated in the vegetative stage. Diatoms have the characteristic two-valved siliceous test or frustule, which is readily fossilizable and the main component of commercially useful diatomite (“diatomaceous earth”). The group is assigned to the kingdom CHROMISTA. The number of recorded forms has apparently reached 100,000, including fossils of both extinct and extant forms, according to Round and others (1990), or even 200,000 according to Mann and Droop (1996). But some conservative phycologists have estimated that only about 25% (or less) might be acceptable as truly separate extant species. The ratio of living to fossil forms has been given as 2:3. Some diatom specialists (personal communications acknowledged in Andersen 1992 and Norton and others 1996; see also John 1994) predict that the “real” (potentially describable) number of species of these highly abundant and very important autotrophic protists might reach an amazing total of 10,000,000!
Raphidophyta (synonym Chloromonadophyceae and inappropriately known as “the chloromonads”, but Chloromonas is a genus of the green algal phylum Chlorophyta in the kingdom PLANTAE): Small group of yellow-green algae, from freshwater and salt-water habitats, formerly placed in Chrysophyta by some workers. The group is assigned to the kingdom CHROMISTA. It has fewer than three dozen species.
Phaeophyta (synonyms Fucophyceae and Melanophyceae): The brown heterokont algae, with multicellular filaments or thalli. These are large seaweeds (kelp) of intertidal or subtidal habitats, gigantic protists reaching lengths of up to 60 m. Many are of commercial value, directly as food or as sources of alginates, fertilizers, vitamins, and minerals. The group, sometimes closely linked to the Chrysophyta, is assigned to the kingdom CHROMISTA. It has more than 1,600 species, a few described as fossils and a few as symbionts on other algae or seagrass.
Conventional Fungal Phyla
Under consideration in this paper are only the basically unicellular “fungus-like” protists, not the long-accepted “higher” fungal taxa. As implied in earlier sections, botanists (that is, mycologists) formerly claimed many protozoan-protistan groups as “lower” fungi, particularly the slime molds (including the labyrinthulids and plasmodiophorans) and the zoosporic taxa. In recent years, there has been
growing acceptance of removal from the kingdom FUNGI not only of the various slime molds but also of two of the three flagellated (independently motile) groups (see Pseudofungi, below), leaving only the chytrids as true (although unicellular and flagellated) fungi.
Myxomycetes (synonym Myxomycota): See account under the “protozoan” phylum Mycetozoa, above. The group is assigned to the kingdom PROTOZOA.
Labyrinthomorpha: See the group, by the same name, above (with other “protozoan” phyla). But the group is assigned in this paper to the kingdom CHROMISTA.
Pseudofungi (synonyms, at least in part, Mastigomycetes, Oomycota, Phycomycetes, and Pseudomycota): Zoosporic protists separable into two subphyletic zoosporic taxa, the Oomycetes (synonym Oomycota) and the Hyphochytriomycetes (synonyms Hyphochytrea and Hyphochytridiomycota) of the literature. Both groups are assigned to the kingdom CHROMISTA. These small but numerous freshwater “water molds,” whose zoospores have an anteriorly projecting flagellum bearing mastigonemes, parasitize hosts ranging from other protists and aquatic plants to fishes and, via the soil, grapes and potatoes. Many species are also saprotrophic on detritus and dead tissues in aqueous and terrestrial habitats. More than 800 species of oomycetes have been described, although some are now considered doubtful; about two dozen species are known from the second taxon.
Chytridiomycota: A third taxon of zoosporic protists, but with posteriorly projecting smooth flagellum (no mastigonemes) and taxonomically remaining in the kingdom FUNGI. They have several fungal characteristics, including chitinous cell walls in their hyphal stage, although they are basically unicellular. They are symbionts or saprobes in soil and freshwater habitats (Powell 1993); a few, treated as protozoa in past years, are found in the digestive tract of horses and ruminants. Some 900 species have been described.
Microspora: As pointed out above (under conventional “protozoan” phyla), only very recently have true fungal affinities been discovered for these tiny intracellular parasites presumably of ancient phylogenetic origin. See the protozoan section (above) for data on the group; but recall that it now properly belongs here in the kingdom FUNGI as the second phylum of fungal protists (the first being the Chytridiomycota, see immediately above).
Conventional Plant Phyla
Considering here only the basically unicellular (or multicellular but not truly multitissued) “lower” plants, I hardly need to point out that formerly all “algal” taxa, including some claimed also by protozoologists, were treated as members of the kingdom PLANTAE. Because all fungi were under this banner, too, it follows that the “lower” fungi, most groups of which are now considered to be members of the totally protistan kingdoms PROTOZOA and CHROMISTA, were also formerly claimed by botanists as plants. Today, I assign or retain essentially only
the red and (some of) the green algal groups as protistan assemblages in the kingdom PLANTAE (see conventional “algal” section, above).
Conventional Animal Phyla
Considering the protozoa as basically unicellular organisms, it is common knowledge that they were long treated as animals, as a single phylum (or eventually at best a subkingdom) of the kingdom ANIMALIA. It follows that all subtaxa of such protozoan protists were considered taxonomically as microscopic “first” animals. Some algal groups were also included, mostly under the title of “Phytomastigina” or “Phytomastigophora”, as well as two phyla (the chytrids and microsporidianssee above) now treated as true fungi. In this paper, I append only two protistan phyla to the kingdom ANIMALIA (see above, under conventional “protozoan” phyla), namely the Choanozoa (controversially) and the Myxozoa.
Some Summarizing Observations
Using (with appropriate caution) data given on the preceding pages, we can draw several conclusions concerning total numbers of species of protists (see also table 2). A grand total of at least 213,000 species, distributed among the 35 phyla recognized in this paper, have been described in the literature to date. Interestingly enough, about 113,000 of these are fossil forms. Five of the 18 phyla known to have any fossils at all contain 98% of the known fossil protists; these groups, in order of richness in fossil species, are the diatoms, foraminifers, radiozoa, dinoflagellates, and haptomonads. In fact, the diatoms and forams alone are responsible for 90% of them. Still, fossil forms also represent an important percentage of the species of some of the smaller phyla (for example, 15–25% of chrysophytes, prasinophytes, and rhodophytes).
Among the extant contemporary forms, numbering some 100,000 species, only about 14% can be labeled as symbionts in the broadest sense, ranging from symphoriontic, commensalistic, and mutualistic forms to obligate ectoparasites and endoparasites (with the latter including some highly pathogenic microorganisms) on and in all kinds of protistan, plant, fungal, and animal hosts. Free-living species would thus seem to outnumber greatly the symbiotic forms. The percentage figure given above, however, is somewhat misleading. If, in addition to fossils, we also leave to one side the huge number (40,000) of nonfossil diatoms (many controversial anyway?), the roughly 14,000 symbiotic species become nearly one-fourth (23%) of all other extant protists.
Incidentally, 95% of the 14,000 symbiotic species are members solely of the 10 following phyla: Apicomplexa (all), Ciliophora (one-third), Myxozoa (all), Chytridiomycota (all), Pseudofungi (all), Microspora (all), Metamonada plus Parabasala (essentially all), Euglenozoa (some euglenids plus essentially all trypanosomatids), and Opalinata (all). But the remaining 5% include scattered important species found among dinoflagellates, cryptophytes, chlorophytes, and rhodophytes, with the majority pigmented; among amoebae, mycetozoa, and amoeboflagellates; and among members of various other usually smaller protistan groups.
Additional calculable totals and other comments can be found in table 2, where the phyla of the five kingdoms are in a different arrangement from that found in table 1, in keeping more closely with the order of their presentation on the preceding pages.
Briefly, the totals (here rounded off) per kingdom of all species of protists contained therein (be they fossilized; free-living or symbiotic; autotrophic, heterotrophic, or mixotrophic; benthic or planktonic; from aquatic or terrestrial habitats; and so on) are as follows: PROTOZOA (as restricted in this paper), 82,700 species; CHROMISTA (with its mixture of many traditional algal phyla and some others), 106,400 (but 94% of these are diatoms); PLANTAE (six algal phyla), 21,200; FUNGI (two phyla), 1,700; and ANIMALIA (two phyla), 1,350.
With respect to described species versus putatively valid or acceptable species, I have despaired of solving all such problems here. In my calculations (and in table 2), I have generally used numbers from the first categorythat of described formson the basis of the original literature (or reliable second-hand sources). For the great majority of protistan phyla, there has seldom been to date a significant difference between the two sets of figures, so I have not cited the latter numbers in this paper. However, there are two striking examples of disparity or discrepancy between the numbersdescribed versus acceptable speciesin the cases of Diatomae and Radiozoa. Of the 100,000 (or more!) diatom species (extant and extinct) allegedly established in the literature, are as few as 10,000–12,000 the maximal number acceptable to many phycologists today? Or are authors of the lower figure excluding fossil (and some other) forms from their estimates without clearly informing their readers of the fact? For the radiozoa, are about half the 11,650 described species now to be considered by protozoologists to be invalid or uncertain? Or do some papers on the subject seem confusing only to the unsophisticated reader? I suggest that specialists, not generalists like me, should discuss and eventually solve or at least clarify such serious problems to everyone's satisfaction.
Whereas there is little doubt that many species of protists have not been carefully enough described in a comparative way (and thus really are “lumpable”) and that endemism has been overused as a basis for newness (including that old parasitological dictum, “A new host means a new species”), is it possible that only a relatively few truly new species remain undetected in the largely unexplored biomes of eukaryotic microorganisms?
On the basis of personal communication with many protistologists, I am obliged to draw the conclusion that, for numerous groups, vast numbers of unique protists do await description. Perhaps we have only scratched the surface regarding the biodiversity of these organisms. Thus, with rare exception, I have not attempted to include estimates of the probable numbers of species assignable to the phyla described to date.
Outlook and Goals for the Future
The roles of protists in natural ecosystems are, in a general way, beginning to be appreciated, but they are hardly yet understood to a very helpful degree, one
applicable to humankind's many environmental challenges. Awareness of their potential is only the first step in the process of getting to know them better. Several major needs are becoming clear, as exposed very briefly below:
• The biodiversity of protistan groups must be studied in greater depth. That is, we need to understand their distributionand functionson a global scale to focus on their diverse interactions with other organisms in a wide variety of habitats. To investigate their ecology, we must improve our knowledge of their taxonomy (and vice versa: Corliss 1992). More-thorough comparative studies need to be carried out, with use of the most precise sampling and cytological techniques now available.
• Reaching widespread agreement on the nature of a protistan species is imperative. If we do not understand the dimensions of a species definition, taxonomic and nomenclatural problems will continue to plague our progress. And we can hardly prepare inventories without knowing the identity of our material in considerable depth.
• More-extensive work on the phylogeny of the prorists will throw light on their evolutionary relationships with the prokaryotic bacteria and with the other eukaryotes, the latter assemblages all supposedly having had protistan origins. An interdisciplinary approach thus needs to continue to be taken in studying protists because of the value of viewing major problems from different points of view. Cladistic trees and taxonomic classification systems must be refined and become more supportive of one another.
• Practical reasons for studying many protistan groups more intensely are related to their direct and indirect effects on human welfare, ranging from their basic food-chain involvement (nutrient and mineral recycling), their roles in agriculture and aquaculture, and their commercial, medicinal, and biomonitoring uses to their being causative agents of major diseases.
• Clearly, more financial support is needed for protistological research, for teaching and training more students and technicians, for maintenance and expansion of culture collections and gene banks, and for preparing appropriate inventories or censuses of species numbers. All these activities are necessary for determining future avenues worthy of exploration in the vast field of protistan biodiversity.
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Estimating the Extent of Fungal Diversity in the Tropics.
With the rapid global destruction of tropical habitats, many peopleincluding conservationists, research scientists, and those wishing to use biodiversityare beginning to recognize that we should find out what we are destroying before it is too late. Tropical deforestation has become the crucible of today's extinction crisis (Wildman 1997), but we should not forget that many other habitats are under threat.
But why in particular do we need to measure fungal diversity? Why do we even want to know which fungi are present in an ecosystem? Why not just measure their isozyme activity or use molecular techniques to indicate fungal presence? Mycologists have robust answers to such probing questions (Hawksworth 1991, 1993, 1998; Hyde 1996a,b; Lodge and others 1996), but conservationists and ecologists, let alone the broader public and politicians, are rarely appropriately briefed. Fungi are important in biological control, in medicine, in biotechnology, in bioactive novel compounds, in decomposition, in nutrient cycling, as actual and potential food resources, in enzyme and organic compound production, and in pollution monitoring. Few other organisms can boast such a successful record of usefulness to humanity! Four of the most important classes of life-saving pharmaceuticals known are produced by fungi: penicillin from Penicillium chrysogenum, cephalosporins from Acremonium chrysogenum, cyclosporin from Tolypocladium niveum, and lovastatin from Asperigillus terreus (Rossman 1997). Fungi are used in biotechnological processes or in the production of novel compounds, and they
have a huge potential for use in the pharmaceutical and health-care industries (Fox 1993; Nisbet and Fox 1991; Rossman 1997; Wildman 1997).
Fungi can also cause huge losses of food in storage and substantial disease in crop plants in the field. Furthermore, because of their integral role in ecosystem processesfor example, in nutrient cycling, plant growth, as a food source, and in their sensitivity to air pollution and perturbationfungi (including lichen-forming species) are ideal organisms for measuring and monitoring biodiversity (Rossman 1994). Fungi have proved to be important, and it is up to mycologists to raise awareness of them among the wider public and politicians. Each mycologist has been challenged to devote a part of his or her working time to this task (Hawksworth 1995).
Numbers of Fungi
There are several estimates of the numbers of fungi (Cannon 1997a; Hawksworth 1991, 1993), and a working figure of 1–1.5 million species is now generally accepted (Hammond 1992; Heywood 1995; Rossman 1997). Several lines of evidence point to a similar figure, but it can be derived by comparing the number of fungi known in all habitats in a single geographical area (the British Isles) with the number of native and naturalized plant species in the same area (Hawksworth 1991). The resulting ratio of six fungi to each plant in an area, extrapolation to a conservative 270,000 global vascular plants, and the use of some allowances yielded a global total of about 1.5 million species of fungi. That figure contrasts markedly with the 72,000–100,000 species known (Hawksworth 1995; Hawksworth and Rossman 1997), and a few authors have argued that 1.5 million is too high (Aptroot 1997; May 1994); however, skepticism is based largely on a lack of familiarity with fungal distributions and host specificity and on the lack of detailed studies in the tropics. Recent studies in the tropics have found a magnitude of novelty that tends to support the figure of 1.5 million (Fröhlich and Hyde 1999; Hawksworth 1998; Hawksworth and Rossman 1997).
The extent to which new species are found varies among different systematic and ecological groups. For example, on the basis of the results of a monographic treatment of the saprobic ascomycete genus Didymosphaeria, Aptroot (1997) estimated that there were only 20,000–40,000 nonlichenized ascomycetes in the world. However, his estimate was based on the assumption that only seven of the 550 taxa classified in Didymosphaeria, actually belong to that genus (Aptroot 1995). He considered this a general trend in ascomycete systematics; although it might be for many long unrevised genera, a realistic figure has been used in totaling the world's described fungi (Hawksworth and others 1983, 1995). In other genera, the opposite trend is occurring. Oxydothis previously had 27 species names, but the number was increased to 42-after publication of the monograph of Hyde (1994), and a further 23 species have since been found on palms in Australia, Brunei, Ecuador, and Hong Kong (Fröhlich 1997). Aptroot's assumptions are also based on wide species concepts. How can we be sure that fungi with a wide host
and biogeographical range and with varied structure are of the same species in the absence of inoculation experiments, incompatibility tests, and molecular data?
There are many potential pitfalls in endeavoring to extrapolate from limited datasets. For instance, a study of phyllachoraceous taxa in Australia and later extensive collecting across the continent increased the number of species known in the country only from 103 to 109 (Pearce and others 1997); extrapolation would provide lower estimates of fungi. But a study of palms in north Queensland identified 202 ascomycete taxa, of which eight genera and 95 species were new to science (Fröhlich and others 1997); extrapolation of these figures would provide much higher estimates of fungi. The original estimate of 1.5 million fungi (Hawksworth 1991) endeavored to account for numerous variables, and recent data from various sources (Cannon 1997; Fröhlich and others 1997a; Hawksworth 1993, 1998; Hyde 1995, 1996a) all point to the figure of 1.5 million as, if anything, conservative.
The number of vascular plants in the United Kingdom is about 2,089, and the number of fungi (including lichen-forming species) is estimated at 12,000 (Hawksworth 1991). Hong Kong, an island smaller than the Isle of Wight or Vancouver Island, has more than 1,700 vascular plants; if the ratio of six fungi to each plant species holds, there are more than 10,000 fungi in Hong Kong. We know of fewer than 500 species (or 5% of 10,000) of fungi in Hong Kong, but some plants have already been shown to support a large number of fungi, many of which are host-specific or family-specific (Fröhlich 1997; Fröhlich and Hyde 1999; Taylor 1997). Those findings indicate that a ratio of 1:6 for vascular plants to fungi might be low, at least in the tropics.
Measuring Fungal Biodiversity
Why should We Measure Fungal Diversity Rapidly?
The necessity for immediate assessments, new research, and rapid monitoring methods for measuring biodiversity is undisputed, and many of the general recommendations made also apply to fungi and other microorganisms (Burley and Gauld 1997). The ideal way to measure fungal diversity would be an all-taxa biodiversity inventory (Janzen and Hallwachs 1993) for fungian all-mycota biodiversity inventory (AMBI), as discussed further below. Because of the difficulty in detecting many fungi and because of their diverse nature, there is an urgent need for all fungi in one geographical region to be identified (Rossman 1994). This would provide basic data against which the results of other external and internal studies could be measured. However, because of the diverse ecologies, seasonality, sporadic findings, and so on, such a survey would take teams of specialists decades. There are at least 31 separate fungal niches in a tropical forest, almost all of which need different techniques and specialists to inventory (Hawksworth and others 1997).
Inasmuch as total inventories will always be impractical (except for a few sites), alternative methods for estimating fungal biodiversity and preparing environmental impact assessments are essential. If they can be developed, there will no longer
be any reason for fungi not to be used widely in environmental monitoring, impact assessments, and ecological research. Indeed, because of their sheer diversity and niche specificity, fungi could prove to be especially valuable as indicators of different kinds of environmental changes and ecological processes.
An All-Mycota Biodiversity Inventory?
The need for an AMBI is undeniable. The scientific benefits would be immense with respect to providing a dataset against which to test hypotheses on species richness and host specificity. Permanent plots or otherwise circumscribed sites need to be established to initiate such an inventory. The most intensively inventoried sites for fungi in the world are two in the United Kingdom: Esher Common in Surrey and Slapton Key National Nature Reserve in Devon. Each has around 2,500 species recorded after several decades of work, but neither has been completely surveyedspecies are still being added, some niches have not been sampled, and the two sites have only about one-third of the recorded species in common despite many similarities in the plants of the two sites. The true number of fungi in the two UK sites, both of which have been intensively affected by human influences, could well be around 3,000. Whatever the total in those disturbed temperate sites, the richness in pristine tropical forests can be expected to be much greater because of the much larger numbers of potential host plants and insects. No sites in the tropics have yet been studied to a comparable depth; one was contemplated in Costa Rica but has since been abandoned, and some are now being planned in Brunei and Taiwan.
Biodiversity measurement in one plot or site is complicated by the need to sample large numbers of habitats and by the diversity of the fungi encountered. Most of the fungi collected can be predicted to be new to science, and their identification only to genus or family level might be possible (Hawksworth and others 1997; Hyde and Hawksworth 1997). In the case of the Guanacaste project, an estimated 50,000 fungi were probably present, of which around 35,000 could be expected to be new to science (Cannon 1996a). Once some site inventories are complete, protocols for accurate measurement of fungal diversity can be developed and tested in them. However, because of the problems mentioned above, it is unlikely that such results will be available within the next 20 years. In the interim, we must develop the best protocols we can on the basis of existing knowledge.
Alternative Approaches to Inventorying and Monitoring
What is our best way forward? The problems associated with selecting target genera or families or specific habitats as a measure of biodiversity have been discussed (Burley and Gauld 1996). The best approach is thought to be to integrate target groups and specific habitats. Carefully selected permanent plots (selected to incorporate a high degree of plant and habitat diversity) would be established under the auspices of local scientists. The plant species within a plot would be identified and labeled if possible. Mycological inventory could then be carried out over a period of years with input from appropriate specialists. The larger basidiomycetes (for example, polypores), ascomycetes (for example, Xylaria), and some biological groups of fungi (for example, entomophagous fungi, freshwater fungi,
and lichen-forming fungi) could be collected and identified (spatially and temporally) over the whole plot, inasmuch as their numbers would be manageable. The microfungi could be investigated in smaller plots or individual host trees (Hyde and Hawksworth 1997).
Because of the difficulties likely to be encountered if we choose to use predictor sets of fungi as a measure of species richness, another approach could be to select microhabitat predictors. Specific microhabitats in an area would be chosen, and a measure of the diversity of microfungi in those microhabitats would be made according to standard protocols. Random collections of leaf litter followed by isolation according to standard techniques might give us a good measure of overall diversity. If this were used with standardized isolations from random soil samples, estimation of fungal endophyte numbers in an endemic tree species, estimation of aerofungi and lichenized fungi on bark or leaves, and collections of Xylaria species, we might have a tangible, albeit qualitative, estimate of the actual diversity in a given region.
The microhabitat components chosen for such an approach to the estimation of biodiversity could vary from habitat to habitat, at this stage; we have no data on which microhabitats would be most representative of microfungal species richness. In the absence of an AMBI, a specific research effort on selected microhabitats is needed to assess which ones would yield the best indications of species richness, to prepare standard protocols for these, and to test the protocols for effectiveness, reproducibility, and ease of application. Five to eight years of coordinated effort across forest regions would be required to allow the identification of suitable predictor microhabitats and then to provide methods for rapid evaluations of fungal diversity in different regions.
Rapid Biodiversity Assessment
In rapid biodiversity assessment or RBA (Beattie and others 1993), numbers of fungi would be estimated without identification as to named species but by sorting them into recognizable, similar species units based on morphological similarities (Cannon 1997b; Hyde 1997; Hyde and Hawksworth 1997). Trained biodiversity technicians (“paratechnicians”) are required to sort specimens into recognizable taxonomic units (RTUs). It has been demonstrated that RTU estimates of spiders, ants, polychaetes, and mosses made by biodiversity technicians can be close enough to formal taxonomic estimates of species richness to be useful for RBA (Oliver and Beattie 1993), and we see no reason why this should not be tried with fungi.
The idea of applying RBA in mycology has been viewed optimistically by several authors (Cannon 1997b; Hyde 1997; Hyde and Hawksworth 1997), but it is not clear that workable reproducible protocols can be developed. High priority is now attached to the production of protocols, which can be tested by paratechnicians, revised, and widely promulgated, as addressed in more detail elsewhere (Will-Wolf and others 1999).
Assessment with Molecular Techniques
The use of molecular techniques in estimating fungal biodiversity has been mentioned as a possibility (Cannon 1997b, 1999; Liew and others 1998) but not used. These techniques have been used to estimate bacterial species, including species that cannot be grown in culture (Tiedje and Zhou 1996), and theoretically they can be applied to fungi, although within-species genotype variation and the low proportion of fungi on which any sequence data are available, they pose particular problems in interpretation. Molecular techniques can be used to access litter and soil samples; although they are still tedious at the cloning stage, the rapid development of automated sequencing machines and computer generation of phylogenetic trees is making them increasingly feasible (Liew and others 1998).
Diversity Assessment with Image Analysis.
Computerized image analysis has been successfully developed to identify high-profile groups of fungi, such as airborne species, that might cause allergic responses in humans and trigger asthma (Benyon and others 1997). It could be feasible to develop identification by computerized image analysis for other groups of fungi, such as soil, litter, or mosaics of lichen-forming fungi on leaves or bark. However, computerized analysis is expensive to develop, and the method is unlikely to provide an alternative for wide-scale fungal assessments soon.
Selected Groups for Rapid Biodiversity Assessment
Recognizing the problems of inventorying all the fungi present in an area and the limitations of various other approaches as reviewed above, we discuss here some candidate groups for use in RBA.
The large basidiomycetes are probably the easiest group of fungi to record in biodiversity surveys because they are conspicuous, easy to collect, and generally easily identified as to genus. Further separation at the species level can be carried out on site even if the fungi cannot be given an existing species name; they can be given numbers (for example, Coprinus sp.) (Hyde 1997). After a spell of rain, the fruiting bodies of macromycetes will flourish in most habitats, but it must be remembered that this is only a representative sample of those actually present; long-term studies over many years are needed to approach a full survey of larger fungi in a site, as demonstrated by studies in Malaysia and Puerto Rico in particular (Hawksworth 1993). Over a period of 7 weeks, sites in Tai Po Kau Nature Reserve and on the University of Hong Kong campus were visited during the wet season. Representative collections of all macromycetes were made on each visit and sorted into recognizable species units. The cumulative numbers of basidiomycetes at both sites indicated that the total numbers of recognizable species units had not been established. Numerous visits to each site are therefore required to obtain best estimates of species numbers.
The Xylariaceae are a large family of ascomycetes, most of which are relatively conspicuous. They are particularly well represented in the tropics, although their identification at the species level might require good access to the literature, and some genera are rich in undescribed species in the tropics. They can easily be spotted in the field, occur on the forest floor, or sprout from dead stumps, logs, and branches; because of the robust nature of most species, they require minimal care in handling. A short visit to a site can generate large numbers of xylariaceous taxa. Identification to genus, species, or other recognizable units is relatively easy for paratechnicians. Because the fruiting bodies of these fungi are tough and persistent, they can provide a better comparative measure of fungal diversity than is the case with the more ephemeral, larger basidiomycetes.
The lichen-forming fungi in tropical regions are confined mainly to the bark of trees and leaves. Their development depends heavily on light penetration, and in dense tropical forests most will be in the canopy layers. If they can be assessed, lichens can be especially attractive for RBA because of their perennial nature and variations in shape and color. In numerous cases, lichens have been surveyed by schoolchildren as a part of studies of air-pollution patterns, including one in Hong Kong (Thrower 1980). In tropical forests, some groups whose spores or other propagules are large or that for other reasons can be dispersed over only short distances (for example, Thelotremataceae) act as indicators of forests with long histories of ecological continuity; in Thailand, lichens on bark have been related to fire histories (Wolseley and others 1995).
The value of lichens living on leaves in the tropics as indicators of habitat disturbance has been demonstrated by a series of elegant studies in Costa Rica (Lücking 1997). The species forming mosaics on leaf surfaces lend themselves to being counted by eye and with a 10x hand lens by nonspecialists, so they can generate comparable data if similar trees and canopy-sampling strategies are used.
Lichens are now widely used in site assessments in temperate forests (Rose 1992) and merit parallel attention in the tropics. Lichens not only act as indicators of air pollutants and habitat disturbance themselves. Because a wide range of invertebrates feed on or are camouflaged to resemble lichens and provide hiding and breeding places for insects sought by insectivorous birds, sites with a high lichen diversity will also be rich in other dependent organism groups.
Endophytes are fungi or bacteria that for all or part of their life cycle live in tissues of living plants and cause unapparent and asymptomatic infections entirely in the plant tissues but cause no disease symptoms (Wilson 1995). There have been many papers on endophyte associations, mainly from temperate countries, but with some attention paid to tropical habitats (Dreyfuss and Petrini 1984; Fisher and others 1993; Rodrigues 1994; Rodrigues and Petrini 1997; Rodrigues and Samuels 1990). It is now believed that all plants have associated endophytes
and that their foliage holds a reservoir of fungi, which can be easily recovered and isolated into culture. Isolation materials are widely available and inexpensive, and plant material is easily sampled and transported. Simple standardized protocols can be constructed to ensure comparability between samples, although allowances must be made for host specificity, and sampling is ideally restricted to particular kinds of trees.
Some endophytes have been shown to be organ- or tissue-specific, so sampling different parts of the plant (Fisher and Petrini 1988, 1990; Petrini and Fisher 1988) and varying the preparations and media used for their recovery yield different assemblages (Chapela and Boddy 1988; Fisher and others 1993; Petrini and others 1992; Pfenning 1997). With the exception of some fungi, such as xylariaceous anamorphs and some species of coprophilous fungi, endophytes are seldom recovered from soil or decaying vegetation (Bills and Polishook 1992).
J.E. Taylor has studied the endophytes and saprobes associated with the Chinese palm Trachycarpus fortunei, saprobes associated with Australian endemic Archontophoenix alexandrae, and the pantropical Cocos nuciferain and outside the natural biogeographic range of the former two species. Standardized sampling is needed at all the sites, and several sites at each location were investigated. Sampling was undertaken at the same time of the year (depending on seasonably and precipitation) to obtain comparable results. The results generated by both the endophytic and saprobic studies indicate a decrease in species numbers on palms when they are outside their natural range, unless they are in equivalent habitats within the case of palms, for instancea source of fungi from other palm hosts.
Selected Habitats for Rapid Biodiversity Assessment
As a complement to selecting particular groups of fungi to subject to RBA, we suggest that particular habitats be examined in addition to selected groups.
Palms are an integral part of most tropical forests and so are a valuable host group for comparisons of the fungi present. The fronds and stems of palms are robust, long-lived, and available for colonization by fungi over a relatively long period.
Investigations of palm pathogens, saprobes, and endophytes have revealed a high diversity of palm microfungi, mainly ascomycetes and related mitosporic fungi (Fröhlich 1992; Hyde 1992, 1993, 1994; Hyde and others 1997; Rodrigues 1994; Rodrigues and Petrini 1997). Fröhlich was intrigued by the seemingly limitless microfungal species that could be found on a single palm species in a given patch of forest and investigated the number of species that could be supported by a single host tree. An individual palm tree contains many distinct microhabitats: trunks, stems, roots, frond blades, petioles, inflorescences, fruits, seeds, and assorted appendages such as flagella and spines; these tissues vary in attractiveness to different fungi with age and health. To sample the mycota completely, it would be necessary to examine the following habitats separately:
• all the living palm surfaces, especially the frond blade (phylloplane), for lichens;
• any diseased areas, such as leafspots or frond tips, for pathogens;
• the surfaces and interior of all the senescing and dead tissues for saprobes;
• living tissue collected in the field and incubated in the laboratory for latent pathogens and saprobes;
• the interior of all the healthy, fleshy organs, including the roots, for endophytes; and
• the root surfaces and interior for mycorrhiza.
Studies of the fungal saprobe numbers by Fröhlich and Hyde (1999) indicate that 172 species of saprobes occurred on three fan palms (Licuala sp.) in Brunei Darussalam (sampled three times over 1½ years), and 100 species of saprobes occurred on three fan palms (Licuala ramsayi) in Australia (sampled once). Palm saprobes could be a useful target group for biodiversity assessment; substantial data can be collected with minimal fieldwork.
Bamboo is also a good substrate for biodiversity assessment in the tropics because it is relatively common. In a preliminary study, a Bambusa sp. and Dendrocalamus sp. were collected in Tai Po Kau Country Park, Hong Kong, and on Mt. Makiling, Los Baños, in the Philippines. One decaying culm in each of three replicated clumps was cut down and chopped into pieces measuring about 25 × 3 cm. Twenty pieces were randomly selected and taken to the laboratory, where they were incubated and kept moist for 1–2 weeks. Each piece was microscopically examined, fungi were recorded, and the number of species on each host at each site was recorded.
The bamboo on Mt. Makiling was found to support 114 species, and that in Tai Po Kau Park 101 species. The hosts had different mycota, and the use of bamboo in RBA therefore seems likely to be effective.
Pandanus leaves are another good substrate for microfungi, particularly hyphomycetes. Collection is relatively simple and involves a pair of secateurs and thick protective gloves. Material can be collected dry or after rain. It should be returned to the laboratory and incubated for a few days. The hyphomycetes present on the material should sporulate quickly and can be identified to provide a measure of fungal diversity. Ascomycetes on Pandanus, bamboo, and palms can deteriorate after several days of incubation. If the material is allowed to air dry after a week of incubation, however, this arrests the deterioration of the ascomycetes and allows storage for long periods if necessary.
Fungi flourish on submerged decaying plant material in freshwater; over 300 species of hyphomycetes (Goh and Hyde 1996) and about 300 species of ascomycetes (Shearer 1993) have been recorded. The number of new taxa is
increasing (Goh and Hyde 1996). Thomas (1996) defines freshwater fungi as any species that rely on free freshwater for all or part of their life cycle. The richest fungal assemblages occur in average-size, more or less clean, well-aerated forest streams and rivulets with fairly turbulent water (Subramanian 1983).
The common sampling techniques involve collecting substratessuch as foam, water, and submerged plant debrisand examining them microscopically either directly or after incubation in moist or water aeration chambers. Plating is also common but is more labor-intensive and time-consuming and is not appropriate for rapid assessment. Foam filtration and water filtration are convenient and widely adopted. Foam and water samples usually contain conidia of numerous “Ingoldian fungi” with branched or coiled conidia that are separable microscopically without special training.
In contrast with the above methods, which yield mostly freshwater hyphomycetes, the incubation of wood samples from freshwater in moist chambers reveals diverse ascomycetes. Wong (1997) listed 363 species of freshwater ascomycetes, among which 303 were recorded on submerged wood, 18 on submerged bamboo, 40 on submerged leaves and two in foam samples. Hyde, Ho, Tsui, and Ranghoo, University of Hong Kong (pers. comm.), also noted that an extremely rich ascomycete biota occurred in tropical lakes and rivers. Examination of a good collection of wood samples by a mycologist takes about a month, in contrast with 3–5 days needed for a foam or water sample. However, it does reveal another important group of freshwater fungi, and it is therefore recommended for biodiversity assessment in freshwater habitats.
Plant pathogens might prove useful for estimating biodiversity. Collection will involve wandering around a site and collecting diseased leaves, which can be taken to the laboratory and examined. It is important that the collectors have a trained eye, but if this is the case it is possible to estimate diversity of plant pathogens in the field without laboratory examination. Many diseases are host-specific, and different fungal pathogens on a given plant usually differ in the symptoms that they cause.
It is rare to find leafspots on rain-forest plants, particularly palms and Pandanus species, and tar spots of phyllachoraceous taxa are also rare. However, large numbers of pathogens occur in gardens, nurseries, or monocultured crops.
Other Habitats for Rapid Biodiversity Assessment
The habitats suggested above are those we have worked on, and they have proved to be excellent sources of fungal diversity. Many others could perform equally as surrogates for biodiversity measurement of, for example, entomophagous fungi in the rain forests of Thailand (Hywel-Jones 1997) or leaf-litter fungi in Costa Rica (Bills and Polishook 1995). There are also ways of standardizing techniques for isolating soil fungi (Cannon 1996b). Disturbed forests harbor fewer rare species in the soil than undisturbed forest and so might be a good indicator of fungal diversity (Pfenning 1997). A concerted effort by mycologists is now needed to try to develop these target groups and microhabitat predictors. A given
subset of target groups or microhabitat predictors is unlikely to work for all habitats, so a folio of basic methods must be selected to match local needs. However, until an all-mycota biodiversity inventory can be carried out, we would be wise to develop these methods to obtain estimates of fungal diversity.
It is unlikely that trained mycologists will always be available for or have the time to devote to measuring fungal diversity in a given habitat, but it can be possible to use mycodiversity technicians (Hyde 1997; Hyde and Hawksworth 1997). Mycodiversity technicians (a kind of “parataxonomist”) are not formally trained, but rather undergo minimal training to help in the task of biodiversity assessment. Their value can be exemplified by the use of students to measure endophyte diversity in one species of Pandanus and one of Livistona in Hong Kong and of summer students to measure larger basidiomycetes in two plots in Hong Kong.
In an experiment carried out with 54 students in Hong Kong, Livistona chinensis (a nonnative naturalized palm) and Pandanus furcatus were sampled for endophytes from the same piece of secondary woodland. The sampling and time-tabling were carried out as follows: Livistona chinensis (27 students divided into eight groups), eight plants sampled with 32 sampling units per individual (mature and immature leaves only); Pandanus furcatus (27 students divided into eight groups), eight plants sampled with 16 sampling units per individual (mature and immature leaves only). Far more fungi were recovered from P. furcatus in the pilot studies, so the number of sampling units had to be limited to a manageable amount. An alternative method would be to sample more individuals of a single host.
The general process was as follows:
Although some fungi would sporulate after 7 weeks, for the purposes of this practical class it was necessary to limit the number of weeks devoted to the study.
Several skilled demonstrators were necessary to assist with running the practical work, especially sorting the isolates into morphospecies and identifying them. In addition, the results were entered onto a database for the students, and the results were presented in a form suitable for statistical analysis. Assistance for 2 hours per week was also necessary for the intervening weeks when the students carried out subculturing. Recording of data was performed accurately, and there were few errors in the final dataset. The only technical problem was in numbering the individual isolates recovered by each group of students; this problem can
be circumvented by allotting each group a series of numbers1–60, 61–120, and so onor different prefixes, such as A1–A60.
The study was labor-intensive and required considerable effort and input by the assisting demonstrators and technicians. However, the advantages were that this applied approach enabled students to investigate a fairly difficult concept and to carry out real scientific investigation on previously unstudied hosts. The students became proficient in sterile techniques, recording of results, and data analysis. The practical class can be carried out in later years on a variety of hosts, giving each group the chance to undertake a first study of endophytes from a specific host plant. Alternatively, technicians familiar with surface sterilization techniques and recording of data could undertake the labor-intensive parts of the work, leaving the identification to the trained mycologists.
In a separate experiment, we used four students over the summer break to compare basidiomycete diversity in a plot at Tai Po Kau Nature reserve with that in one on the Hong Kong University campus. The group first measured out a 1-ha plot and visited the site weekly for 7 weeks. During each visit, the students would walk through the plots, along paths parallel to one side of the plot; the paths were about 10 m apart. The mycodiversity technicians collected representatives of any macromycetes visible from the paths, placed them in suitable containers, and took them to the laboratory. The specimens were identified, isolated, photographed, and dried. Species that could not be identified were placed in recognizable taxonomic units and treated as above. Slide preparations were also made for future reference, and materials and slides are held in the herbarium (HKU) at the University of Hong Kong. Collections from later visits could be compared with photographs and slides from previous visits; in this way, it was possible to identify newly collected species.
Fifty-seven fungi were collected at Tai Po Kau Nature Reserve and 51 at the site at the University of Hong Kong. This indicates that the diversity of fungi was similar in the two sites. However, not all the macromycetes present would have been detected, so the cumulative number had not leveled off. It is interesting to note that more fungi were found at Tai Po Kau during the first visit (25 taxa) than at the other site (13 taxa). Although inconclusive, this pilot experiment indicates that
• mycodiversity technicians can be used in fungal diversity assessment;
• further studies are required to establish whether a single visit to a site to assess fungal diversity is representative; and
• further studies are required to establish how many visits to a site are required to collect an adequate representation of the macromycete species present.
Toward a Set of Protocols for the Rapid Assessment of Fungal Diversity
Here we propose protocols for several target groups and predictor habitats that should provide tangible estimates of fungal biodiversity in the tropics. We propose that at least six of these protocols be chosen to obtain a reasonable estimate
of biodiversity and remove bias from any individual protocol. This set of procedures is proposed to provide a starting point for diversity assessment of fungi. The set can be tested, procedures can be added, and others can be removed, until we establish a robust mechanism for estimating fungal diversity across a range of global habitats. For the purposes of this exercise, we assume that appropriate human resources are not available and that specialized help will be provided by mycodiversity technicians. Most of the studies should be carried out during wet spells.
The easily visible, larger fungi are an ideal target group on which to base biodiversity estimates, as long as they are integrated with other estimates to eliminate bias. We have found that a plot of 50–100 m2 can be thoroughly investigated in 2–3 hours, when all the larger fungi can be collected. This will require walking throughout the plot along lines 10 m apart, from where most fungi can be seen. Compartmentalized plastic fishing-tackle boxes or egg boxes are suitable and can be used to take the samples to the laboratory. It must be wet during the period under study, and at least 10 weekly visits should be made to each plot under investigation. It might be necessary to estimate the diversity of the longer-living polyspores on only one visit.
In the laboratory, untrained technicians can visually sort the material into morphospecies by using form and color. Slides and spore prints can be prepared, fresh specimens photographed, and single-spore isolations attempted. The specimens can then be freeze-dried or air-dried and placed in a reference collection for future study. Total diversity must exclude duplications of the same species collected on each visit. Over a 10-week period, it should be possible to obtain an indicative estimate of macromycete diversity by using mycodiversity technicians (mostly for unnamed specimens) or trained mycologists (for named specimens).
Lichens are especially attractive for use in rapid biodiversity assessment because they are perennial and generally can be sorted into morphospecies first by eye and then with a hand lens. Although microscopic and chemical studies might be needed for critical determinations, they are not necessary when comparative assessments of species numbers are required. Experience with previously untrained students has shown that 1–2 days of training is sufficient to train a mycodiversity technician to survey these fungi. Lichens are long-lived, so only a single site visit is necessary, although ideally it should last for 2–4 days. The same sample plot as used for macromycetes could be surveyed, and it would be valuable to collect data on morphospecies distinguishable on tree bark and leaves separately. Where possible, canopy samples should be obtained from recently fallen or felled trees, although it is often the understory rather than the exposed crowns that are richest in leaf-inhabiting species. As many as possible should be examined because there can be variations due to light regimes and other microclimatic factors, which will affect the development of different species.
The numbers of morphospecies can be compared directly by pooling or considering separately the datasets on bark and leaf-inhabiting species. The numbers of species to be found can be considerable. For example, studies of the crowns of 14 trees in a semideciduous tropical forest in Guyana yielded 100 lichen-forming fungi on leaves alone (Sipman 1997).
For those wishing to go further, the literature on the collection and identification of lichen-forming fungi is immense, but we recommend particularly a recent well-illustrated guide to New Zealand lichens (Malcolm and Galloway 1997). A detailed overview of lichen collection and identification is in press (Will-Wolf and others 1999).
The Xylariaceae constitute a tangible target group for biodiversity assessments because only a short period of training is needed to enable mycodiversity technicians to recognize them in the field. We have found that a plot of 50–100 m2 can be thoroughly investigated in 2–3 hours, when all the visible xylariaceous fungi can be collected. This requires walking throughout the plot along lines 10 m apart and closely examining potential substrates, especially logs on the ground. Most of these fungi are robust and require no special handling. It is often not possible to separate them in the field; therefore, all specimens will need to be returned to the laboratory for microscopic examination. It must be wet during the period under study, and we suggest that at least five visits, 2 weeks apart, be made to each plot under investigation.
In the laboratory, mycodiversity technicians can visually sort the fungi into groups (genera) according to form and to a lesser extent color. Further separations can be made with a hand lens or a dissecting microscope. Slide preparations of spores and asci are, however, essential for species-richness assessments, and the mycodiversity technicians will need to draw and measure these structures. Gross structure, asci, and spores could be photographed from fresh specimens, and isolations into culture from single ascospores can be attempted. The specimens can then be air-dried and placed in a reference collection for possible future study. Total diversity must exclude overlap of the same species collected on each visit. Over five visits, comparative estimates of the diversity of the Xylariaceae present can be obtained by mycodiversity technicians.
Logs and Branches
Numerous dead branches occur on the floor in most tropical habitats and can provide components for rapid fungal-diversity assessments. A short period of training provides mycodiversity technicians with the skill to collect logs and examine them for fungi in the laboratory. The plot of 50–100 m2 can be used, but in this case 20 logs can be randomly collected during a wet period and then incubated in moist chambers.
In the laboratory, mycodiversity technicians visually examine the logs with a dissecting microscope and make slides of fungi encountered. They can then sort the fungi into different groups on the basis of a minimum of taxonomic knowledge, that is, morphology, spore size, shape, septation, and color. In this way,
fungi can be sorted into morphospecies. Photographs can be taken and specimens preserved or cultures attempted as for macromycetes. Total-diversity assessments must exclude overlap of the same species collected on each visit. We suggest that 20 samples is sufficient for mycodiversity technicians to provide a reasonably comparative estimate of the diversity of fungi on logs.
It is relatively easy for mycodiversity technicians to carry out standard procedures to recover endophytic fungi. The methods will depend on the host plant, and pilot studies need to be undertaken to develop optimal sampling and surface sterilization techniques. Surface sterilization techniques are outlined in the methodology of every paper dealing with the recovery of these fungi (Petrini 1986; Petrini and others 1992; Schulz and others 1994). The number of samples necessary to yield at least 80% of all the endophyte taxa at a single site has been estimated (Petrini and others 1992) at a maximum of 40 individuals per species and 30–40 sampling units per individual.
Although fairly labor-intensive, most of the techniques can be used by relatively unskilled technicians, or students, and results can be obtained in less than 3 months. The equipment necessary is inexpensive and widely available. Mycodiversity technicians will need to learn isolation techniques and spend some time at the microscope to separate fungi into “species units” or “morphospecies”. The same or allied hosts should be chosen to eliminate differences due to host diversity. Suggested species for which we already have results are palms (Fröhlich 1997; Taylor 1997), bamboo (Umali, unpublished), and mangroves (Rodrigues and Petrini 1997). Sporulation was promoted in many of these cultures with 43–52 species identified within 32 genera; however, different strains of the same species often exhibited different cultural characteristics.
Palm rachids or petioles probably support the highest diversity of palm fungi, so we suggest these for biodiversity assessment. Numerous dead rachids can be found on the floor or attached to living palms in most tropical habitats and so are considered an ideal component of a suite of fungal-diversity assessment protocols. A short period of training will provide mycodiversity technicians with the skill to collect samples and examine them for fungi in the laboratory. The same plot of 50–100 m1 can be used, but in this case 20 rachid samples can be “selectively” randomly collected during a wet period or a dry period. They can be examined after air drying.
In the laboratory, mycodiversity technicians examine the samples with a dissecting microscope and make slides of fungi encountered. Fungi are sorted into different groups on the basis of minimal taxonomic knowledgespore type, spore size, shape, septation, and color. In this way fungi can be sorted into morphospecies. Photographs can be taken and specimens preserved or cultures attempted as for macromycetes. Total diversity must exclude overlap of the same species collected on each visit. We suggest that 20 samples are sufficient for microdiversity technicians to provide a comparative estimate of fungi on palms.
Dead bamboo culms support a high diversity of fungi, and we suggest these for biodiversity assessment. Numerous dead culms can be found on the floor or standing, and two species of bamboo can be selected and sampled. Training, sampling, examination, and interpretation are similar to those for palms, and the same plot of 50–100 m2 can be used. Samples should first be examined for ascomycetes and basidiomycetes and then incubated for 14 days, after which they can be examined for other fungi.
Fungi on Pandanus
Dead Pandanus leaves support a high diversity of fungi, and we suggest these for biodiversity assessment. Numerous dead leaves can be found on the floor or attached to the plants, and these can be randomly collected. The type of training required and procedures to be followed are similar to those for palms and bamboos. The same plot of 50–100 m2 can be used, but in this case 20 leaves can be “selectively” randomly collected during a wet period or a dry period. Leaves should first be examined for ascomycetes and basidiomycetes and then incubated for 3 days, after which they can be examined for other fungi.
Comparative-biodiversity studies of fungi in freshwater habitats require the use of standard methods for foam and water examination. Examination of 10 foam collections and the filtrates from two membrane-filtered (pore size, 5–8 mm) 5-L water samples from three locations in the freshwater habitat should be carried out. Foam samples are collected in separated, clean, sterilized vials and preserved with the addition of formal-acet-alcohol or stored in an icebox. In the water-filtration method, the membrane filter is stained and fixed with lactic acid cotton blue or lactic acid fuchsin. This preserves and stains the spores and renders the membrane filter semitransparent. Samples should be examined until the number of new morphospecies recorded declines to a minimum; this can be assessed by plotting a cumulative graph of the number of new taxa recorded versus the number of slides examined in foam samples or the number of filter papers from the waterfiltration method examined. The direct examination of random wood samples for surface fungi could also provide a good estimate of fungal diversity.
Observation of conidia on semitransparent filter membranes might be difficult, especially with respect to the minute characters of fungal spores. The difficulty can be overcome with the use of a high-power dissecting microscope or a compound microscope with an upper light source. Conidia might also be covered by particles filtered in the filtration process; these can occlude important features.
Fungi are ideal organisms to work with in the field and in the laboratory. Collection requires a visit to the area under investigation and either collection of the visible fungi concerned or collection of small parts of the habitat under
investigation. In the laboratory, the fungi are easy to handle and can be photographed and dried. Alternatively, isolations can be made with established techniques. Most fungi grow rapidly in culture and require no complicated procedures for their study.
We have endeavored to indicate the richness of tropical fungi and comparative approaches to the assessment of fungal diversity between different tropical sites. The several-protocol approach that we recommend is essential to capture some representation of the microfungi present. This is critical because the microfungi make up the highest proportion of fungi in any ecosystem. However, if time is short, we recognize that there could be advantages in paying particular attention to macromycetes and lichen-forming fungi in preliminary assessments.
In the exploration of fungal diversity, much attention has been focused on obtaining data on species richness in different systematic groups or in particular niches or substrates. Such studies have been important in vindicating hypotheses regarding the richness of the world's mycota, but we believe that it is now time to focus on securing comparative data on the richness of fungi in different sites. The approaches to rapid assessment of biodiversity in fungi described here are intended both to further discussion as to the best suite of protocols to recommend and more important to stimulate more work in tropical sites, even in the absence of experienced mycologists.
We are grateful to P.H. Raven for encouraging us to prepare this contribution for these proceedings. Helen Leung is thanked for technical assistance.
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Pervading the Earth and Linking All Life
Abundance of Nematodes
The phylum Nematoda (Nemata), known commonly as roundworms, contains the most abundant, common, and genetically diverse multicellular organisms (Lambshead 1993; Platt and Warwick 1983). Usually, these organisms are invisible to all but a few specialized scientists because most are essentially microscopic and transparent. More than 85 years ago, Cobb (1914) eloquently noted that “if all the matter in the universe except the nematodes were swept away, our world would still be dimly recognizable, and if, as disembodied spirits, we could then investigate it, we should find its mountains, hills, vales, rivers, lakes, and oceans represented by a film of nematodes.” “So little do we know of this vast multitude of soil-inhabiting nematodes that the first spadeful of earth we lift is practically certain to contain kinds never seen before”, and 'There exists . . .a greater disproportion between the known and the unknown than exists in almost any other class of organisms.” With respect to Cobb's characterization of our knowledge of nematode diversity, relatively little has changed during the last 85 years. Somewhere between 500,000 and more than 100,000,000 nematode species are believed to exist on Earth (Lambshead 1993), but habitats certain to be richest in new species are mostly unexplored, and fewer than 25,000 species have been described (Andrássy 1992; Platt and Warwick 1983).
Diverse morphological, physiological, and behavioral adaptations allow nematodes to pervade nearly every habitat, but most habitat adaptations cross formal taxonomic boundaries, which arguably include two classes and 18 orders
(figure 1). Most nematodes are nothing like the vertebrate parasite Ascaris (figure 2J), which represents the phylum in introductory biology texts and laboratory dissections; rather, most are microscopic nonparasites designated microbivorous because they feed on small organisms, such as bacteria, fungi, and algae. A few are parasites of plants, vertebrates, or invertebrates; others browse on plants as herbivores or are predators of small organisms. Most microbivorous nematodes are of unnamed species, but these poorly characterized taxa play an important role in decomposition of organic matter and nutrient cycling in all ecosystems (Freckman 1988; Peterson and Luxton 1982). Nonparasitic nematodes are commonly the most abundant microinvertebrates of terrestrial (Nielsen 1949), marine-estuary sediment (Warwick and Rice 1979), and freshwater ecosystems; they are also taxonomically heterogeneous, transcending 12 orders (figure 1). Seabeds, ranging from the tropics to the Arctic, are the habitats by far richest in nematode species diversity (Boucher 1990; Lambshead 1993). Although 4,000–5,000 marine nematode species have been named and described, full surveys of marine habitats probably will reveal many millions of previously unknown species (Andrássy 1992; Hope and Murphy 1972). The natural histories of these marine nematodes are diverse and sometimes astounding. Consider for example, marine nematodes that are symbiotic with chemotropic sulfur bacteria, a nematode that
attaches its eggs to itself and guards them until they hatch, and a moderate-size nematode (4 mm long) that lacks a mouth and digestive system but is packed with symbiotic organisms (Bernard 1994). It is impossible to anticipate the richness of lifestyles that will be discovered among such underexplored habitats. Nematodes of soil and freshwater sediment are only somewhat better known; about 6,000 species in these habitats have been named, but the rate of discovery of new species in some habitats suggests that that is only a small fraction of extant species (Andrássy 1992). Although nonparasitic nematodes have great diversity in tropical and temperate soils, they characterize the biota of all soils and are even present in dry Antarctic ones (Freckman and Virginia 1997; Lawton and others 1996; Sohlenius 1980; Yeates 1980).
Many of the most thoroughly studied human parasites, being macroscopic, have been recognized since ancient times (Thorne 1961). However, parasitic taxa of economic importance, such as those of plants and vertebrates, probably include fewer than 5% of all nematode species. Nearly 2,000 species in three orders are herbivores or known to parasitize plants (figure 2A-E); a few hundred principal species are responsible for billions of dollars of crop losses annually (Barker 1994). Even in nonagricultural habitats, the impact of plant parasites can be impressive; pinewood nematodes introduced from North America are capable of killing a large pine tree in Japan in less than six weeks (Mamiya 1983; Rutherford and others 1990). Similarly, roughly 12,000 species in six major orders are known to parasitize vertebrates, but among these, only about 36 are considered to have a direct impact on human health and 300 are of veterinary importance. Most invertebratesmainly insectsalso host nematodes, the associations ranging from phoresis to obligate parasitism. Although hundreds of named nematode species in four orders are known to be associated with insects, they probably represent a small fraction of the existing species, considering insect diversity and nematode specialization on such hosts. It is very likely that this pool of largely unexplored parasites is rich in potential biocontrol agents and management tools for medical, veterinary, and agricultural insect pests.
The inadequately developed state of systematic surveys has been a major limitation in the development of a phylogenetic taxonomic system for phylum Nematoda, but such a framework is fundamental to the predictability and repeatability of all other research on the group. The problem is not unlike assembling a 1,000-piece jigsaw puzzle with 975 missing pieces! Another limitation in developing this taxonomic framework has been the historical fragmentation of nematologists into groups that study vertebrate parasites, invertebrate parasites, herbivore and plant parasites, or free-living forms in such disciplines as agriculture, parasitology, veterinary science, medicine, and ecology. As a consequence, taxonomic classifications often reflect academic specializations, rather than broad-scale nematode phylogenetic relationships. This fragmented approach is like grouping puzzle pieces by their similar shapes; in some cases (as it is with edge pieces) it might be useful; but in most cases, there is little predictive power or congruence with historical relationships. These “discipline-specific taxonomies” are now being tested and for some groups revealed as artificial by robust DNA-based phylogenetic hypotheses (Blaxter and others 1998). Fragmentation by discipline also has resulted
in overemphasis on parasitic groups of obvious economic importance but with no contextual connection to the grossly understudied nonparasitic groups, which make up the majority of nematodes. Broad-based biotic inventories will transcend these previous boundaries as taxonomists with diverse specializations collaborate to investigate nematode diversity through the application of varied methods.
Most recognized nematode species have been described on the basis of a morphotype that is presumed to be unique. Such species can be synonymized if it is demonstrated that the morphotype either is not unique or representative for the taxon. Andrássy (1992) estimated that 18% of named species of terrestrial and freshwater nonparasitic nematodes are invalid because they are synonyms or because information on the species is inadequate for assessing validity; it is unclear, however, whether this estimate of “invalid species” is generally applicable to the entire phylum. A potential source of error that has been more difficult to assess is the degree to which morphotypic uniqueness is a good estimator for ontologically real species; the integration of molecular data in nematode systematics provides an independent line of evidence to help address this problem (Adams 1998; Szalanski and others 1997; Thomas and others 1997).
Current systematics practice emphasizes that discovery and description of new nematode species requires phylogenetic context for many taxonomic decisions, including reevaluation of previously described species and their relationships. Errors in estimating evolutionary history can have critical implications for over-estimating or underestimating species numbers (Adams 1998). But one advantage of phylogenetic approaches to studying species-level questions is that thorough integrated approaches to gathering character data (for example, structural, molecular, genetic, and developmental data) can promote discovery of new taxa.
Geographic Distribution of Species
A measure of the distribution or degree of localization of nematode species is crucial to developing sampling strategies for estimating worldwide species richness. For example, is species abundance in the North American deserts similar to abundance in African deserts, and to what extent do the same species occur in both habitats? Because lifestyles and feeding habits of nematodes (figure 1) cover the biological spectrum, it is not surprising that species are varied in their patterns of distribution. A high degree of localization might be expected among the majority of nematodes that have low mobility and a life history that lacks a dispersal phase; these are determinants for high speciation rates (Castillo-Fernandez and Lambshead 1990). In some habitats, limited dispersal is by mechanisms that move sediment or soil, including wind or flowing water. Other species are globally distributed, because of a deep evolutionary history predating dispersal of continents (Baldwin 1992; Ferris 1979). In still other cases, nematode distribution is determined by the habitats of organisms with which they are closely associated. Many nematodes are dispersed through phoretic associations with mobile insects or birds, by anthropogenic effects (such as agriculture), or by congruence with a specific host. Such mechanisms determining geographic pattern cannot be separated
from issues of isolation and speciation. Highly localized species or species restricted to a narrow habitat regime or a single host include a majority of nematodes, and these are most vulnerable to annihilation. The resources to measure the rate at which nematode species, including beneficial ones, are lost to anthropogenic effects are unavailable, but we can expect that the rate of loss is huge.
We have noted arguments that most nematodes are nonparasitic marine species (Lambshead 1993). However, in the marine environment, abundance and perhaps species geographic pattern vary somewhat with concentrations of organic matter, vertical distribution, latitude, and depth (Boucher 1990; Lambshead and others 1995). In deep seabeds and undisturbed soil systems, regardless of overall abundance, individuals of a particular species often are rare (Lambshead 1993; Grassle and Maciolek 1992; Hessler and Sanders 1967). For example, a deep-sea sample yielding 148 nematode species included only 216 individuals (Hope 1987).
Considering terrestrial and freshwater nematodes, Nicholas (1975)citing examples from the orders Dorylaimida, Araeolaimida, and Tylenchidaargued that to a striking degree, particular genera and species occur in all parts of the world and in a variety of habitats, irrespective (within wide limits) of soil's physical and chemical factors, climate, or vegetation. We would add a range of microbivorous Rhabditida, such as Acrobeloides nanus and Panagrolaimus rigidus, which, regardless of limited sampling, are known to have distributions that include all of Europe, Australia, Asia, Africa, and North and South America (Andrássy 1984). Often such wide distribution is difficult to explain. For example, a survey of nematodes in a freshwater lake in the Galápagos, colonized during its recent history of 15,000 years, included 18 species in five orders; 16 of the species were known in other parts of the world (Abebe and Coomans 1995). Thus, mechanisms of dispersal and colonization are not fully understood. In some cases, supposed geographic limits of species are an aberration of inadequate testing. For example, recent sampling in a California desert led to the discovery of microbivorous nematodes, including species previously known only in South Africa. Such geographic limits would be difficult to explain through introductions or biogeography; it is much more likely that more-extensive surveys will demonstrate a broad distribution of these species beyond California and South Africa.
Some parasitic nematodes have broad host ranges and are distributed nearly worldwide; an example is the root knot nematode, Meloidogyne incognita, one of the most destructive plant pathogens of agriculture and widespread in relatively undisturbed habitats (Eisenback and Triantaphyllou 1991). Other parasitic nematodes often are highly regionalized by specific requirements of their host and habitat. For example, the citrus pathogenic variant of Radopholus citrophilus, which at one time nearly destroyed the Florida citrus industry, is known only in that region. This nematode's requirement for a habitat of deep sandy soils might limit its distribution (O'Bannon 1977). A closely related species, Radopholus similis, is distributed globally throughout the tropics, whereas most other Radopholus species seem to be restricted to Australia, Asia, or Africa (Huettel and Dickson 1984; O'Bannon 1977; Sher 1968). To some extent, the wide distribution of Radopholus similis might be affected by anthropogenic effects of agriculture, including the spread on infected corms from Asia via propagation of bananas throughout the tropics.
The cyst nematodes include a group of about six genera and 70 species, many of which have great economic importance to agriculture and diverse patterns of species distribution, determined by host specificity and coevolution, biogeography, and anthropogenic effects (Baldwin 1992; Baldwin and Mundo-Ocampo 1991). For example, the cyst nematode Punctodera chalcoensis is restricted to Mexico and clearly coevolved with its only host, Zea, including Z. mays (cultivated maize) and uncultivated species endemic to Mexico. The potato cyst nematodes, Globodera rostochiensis and G. pallida, were thought to be restricted to potatoes in Europe until the 1950s, when they were discovered on a shipment of potatoes from Peru. Later surveys in South America revealed that the potato cyst nematodes occur on wild plants throughout a region of the Andes, where they probably coevolved with potatoes. It is commonly believed that they were introduced to Europe with potatoes in the 1600s and later throughout many of the potato-growing regions of the world, despite rigorous regulation of shipments (Baldwin and Mundo-Ocampo 1991). Whereas a number of species of Globodera parasitize Solanaceae in the new world, another group of Globodera species seem to have coevolved with Compositae in Europe (Baldwin and Mundo-Ocampo 1991). The distribution of a wide range of cyst species can be traced from particular hosts and regions to biogeographic patterns and more recently movement of these nematodes with soil and roots associated with shipments of agricultural products (Baldwin and Mundo-Ocampo 1991; Ferris 1983, 1985; Stone 1977).
We have noted that distribution of parasites is a function of the distribution of the hosts. One general precept of animal parasitology is the expectation that a host species harbors several parasite species, some of which are probably restricted to that species of host. By extension, many nematologists who study animal parasites are not surprised when a new nematode species is described from a host species that has not been the subject of exhaustive examination. In fact, this generalization is frequently confirmed; most thoroughly investigated vertebrate hosts are likely to yield one or more novel nematode species.
The nematode parasites of domesticated hosts have been intensively studied because of their importance to agriculture. Host-parasite lists (for example, Soulsby 1982) provide some insight into the diversity of nematodes from domesticated hosts and other vertebrates. For example, bovine species have been reported to harbor more than 60 nominal nematode species representing 28 genera; these nematodes include specialists for many “habitats” within the hosts, including the digestive tract, circulatory system, respiratory system, muscles, urogenital system, skin, eyes, and body cavities. Similarly, pigs are reported to serve as hosts for 37 nominal species representing 24 genera, and equids host at least 43 nominal species representing 29 genera. It is unclear how many of the congeners reported from a single vertebrate host species are synonyms. This problem is no doubt more acute for some nematode groups than others, but recent molecular investigations show promise for investigating potential synonymies. For example, a study of nucleotide sequences indicated that three described species of vertebrate parasites (Teladorsagia spp.) had no detectable nucleotide differences in a rapidly evolving region of ribosomal DNA; this result was interpreted as evidence that the previously described morphotypes represented a single species (Stevenson and others
1996). Similarly, sequence-based results (Newton and others 1998) were consistent with the inference of one species in the case of two nominal (and controversial) taxa of nematode parasites (Cooperia oncophora and C. surnabada) that were previously diagnosed on the basis of structural differences; this molecular finding was also consistent with the results of cross-breeding studies (Isenstein 1971). Conversely, it is unclear how many of the taxa assigned to a single morphological taxon represent cryptic species, but again genetic methods are beginning to shed light on the nature of species complexes in nematodes (Chilton and others 1992; Chilton and others 1995).
For many nematodes of vertebrate hosts, the extent to which nominal species are regionalized is often unknown because of the absence of systematic survey data. In addition, assessing geographic distributions of nematode parasites of vertebrates is made more difficult by the fact that nematodes are typically not uniformly distributed among individuals of a host species; instead many hosts remain uninfected while a few individuals harbor many nematodes (overdispersion). Predictably, the nematode parasites of domesticated vertebrates are geographically widespread because of transport of these hosts. Exceptions to that prediction might involve vector-transmitted nematode parasites, inasmuch as hosts could be moved to regions where required vectors are not codistributed. In the case of human-mediated movement of domesticated animals, the effect on their parasites is also evident from studies of nematode population genetic structure. For example, studies of four trichostrongylid nematode species (Ostertagia ostertagi, Haemonchus placei, H. contortus, and Teladorsagia circumcinta) occurring in three domesticated hosts revealed very little genetic differentiation among geographic regions of North America; this suggests that human transport of domesticated hosts has resulted in high nematode gene flow (Blouin and others 1992; Blouin and others 1995). In contrast, the genetic structure of a trichostrongylid nematode of deer (Mazamastrongylus odocoilei) was much more regionalized and showed a pattern of genetic isolation by distance (Blouin and others 1995).
Number of Species Per Habitat.
The vast numbers of nematode species, the diversity of their habitats (from soils and sediments to animals and plants), the paucity of surveys, and the inadequately developed state of nematode taxonomy make a global estimate of nematode species daunting. Nematodes can live in the bark of trees (pinewood nematode); as parasites of bees, lizards, and tomato plants; and even in mushrooms and earthworms. Even the smallest samples of habitat can contain hundreds of nematode species, including many unknown species. For example, Tietjen (1984) found in sampling marine sediments of the Venezuela basin that only two of 196 nematode species had been previously described. Lawton and others (1996) found over 200 nematode species in moist tropical Cameroon soils, but because of the expertise needed and the cost of identifying species, had to leave twice that many undescribed. For these reasons, the number of descriptions of nematode species is still in its infancy, and nematologists and ecologists rely on descriptions of functional groups or become specialists in the identification of particular groups of species.
Nevertheless, there is some information that we can use with caution to examine global geographic and latitudinal patterns of nematode species diversity (table 1). The few studies in tropical forest soils (Coleman 1970; Hodda and
Wanless 1994) before Lawton's study did not indicate that the tropics were foci of nematode diversity or abundance, as was found for nematode species associated with plants and animals. Temperate forests had much higher species diversity. Although table 1 shows that the number of species is similar in Indiana agroecosystems and in the Cameroon forest, species were still being identified in the Cameroon when the study ended. The results seem to support Hammond (1992), who suggested that the well-documented floristic richness of areas that are seasonally dry might not be paralleled by the richness of terrestrial invertebrates, fungi, or microorganisms. At the other extreme of diversity are the soils of the Antarctic Dry Valleys (78°S), which have only three endemic speciesperhaps the lowest nematode diversity on Earth (Freckman and Virginia 1997). Surprisingly, agroecosystems, which we think of as being disturbed ecosystems, can have over 100 nematode taxa (Freckman and Ettema 1993; Yeates 1980). Yet we also know that different agronomic practices have different effects on nematode diversity, including the loss of some species. Those examples indicate the need for a more strategic effort in identifying these speciose animals.
The lack of knowledge about the total numbers of nematode species present on even the smallest scalessay, in 10 g of soilmakes estimates of total species in different habitats or even globally a monumental task. There is considerable variability in estimates that have been attempted (table 1), with estimates of total nematode species globally as low as 100,000 (GBA 1995); in contrast, Lambshead and others (1993) estimated the highest number of marine nematode species alone to be 100,000,000.
A fundamental problem encountered in estimating regional or global nematode species diversity is that many of the traditional diversity methods might not be applicable to such a group as poorly described and as varied as nematodes. For the near future, estimates of global nematode biodiversity will remain speculative. Methods often used to estimate species numbers for poorly known but speciose groups do not seem particularly appropriate for nematodes. For example, one traditional method is to extrapolate from reliable available data with ratios that are established for better-known groups, such as birds or vascular plants. For nematodes, reliable data on species numbers on even the smallest scale are available for only a small number of habitats. Furthermore, by definition, groups that are well described can be very different from such poorly described groups, so it cannot be assumed that patterns are similar in both. Other methods, such as relating first principles and processes of ecology to species number (such as body size, food web structures, trophic links, and parasite-host relationships) are similarly compromised because the data behind the relationships are based on groups that are easy to access and might not be representative of nematodes. Methods that base estimates of total species numbers on patterns in the number of species that have already been detected are likely to be uninformative because rates of discovery probably are biased by our interests and resources rather than reflecting a true insight into the ratio of discovered to undiscovered species (Hammond 1992; May 1988, 1998).
Until a major effort is launched by the scientific community, we will continue to guess at this most abundant and important group of invertebrates. One approach
that shows promise in estimating nematode species numbers in different habitats, and ultimately globally, is to develop theoretical estimates based on energetics. A model is being developed to estimate the total nematode biomass that can be supported in different habitats, on the basis of the carbon available in those habitats. This information might be used to estimate maximal viable nematode population sizes and species number at each trophic level (Freckman and Moore 1998).
Gaps in Knowledge?
Although nematodes are the most species-rich phylum of metazoa, most of the world's habitats are undersampled, and we can only begin to envision the numbers of species. Worldwide, wherever habitat is destroyed, microscopic nematode species with highly localized distribution are likely to be lost at a high rate with a cost to humankind that includes loss of biological control agents and unique natural compounds. The compounds, largely unexplored, might include anticoagulants, plant-growth regulators, and antimicrobials in bacteria dependent on nematodes (Jarosz 1996). Loss of nematode species also results in loss of opportunities to measure anthropogenic disturbance; the latter has implications for understanding and managing ecosystems. Inadequate knowledge of nematode diversity has led to introduction of destructive nematode species. Most recent surveys are biased toward the regions most accessible to the world's small and shrinking supply of nematode taxonomists, and development of a taxonomic system is biased to parasites that have obvious economic and medical effects. The greatest need is for data from representative habitats that will provide a predictive framework for testing hypotheses of global species diversity and targeting areas of strategic importance for the conservation and use of nematode species. Whereas it would be difficult to identify any region, even Europe or North America, as adequately sampled, the most undersampled habitats, relative to suspected diversity, are deep ocean sediments, wetlands, and tropical nematode-invertebrate associations. Data from expanded nematode surveys in Asia and Africa are particularly needed.
Assessment and conservation of nematode species diversity are confounded by an inadequate taxonomic and phylogenetic framework. The situation is exacerbated by the need for a new generation of nematode taxonomists with broad training in a range of classical and molecular tools in a rigorous phylogenetic context (Barker 1994; Ferris 1994; Hyman and Powers 1991; Systematics Agenda 2000 1994). Taxonomists can broaden their reach by working closely with parataxonomists, specialists trained to work with taxonomists for field collecting, processing material, and routine identifications. Furthermore, substantial financial resources are needed to support research in nematode biodiversity in general and to facilitate greater integration of nematode taxonomists throughout the world via readily accessible and well-supported taxonomic collections and electronic databases.
Number of Trained People Available
There is little argument that the number of persons trained to identify and describe new species of nematodes is woefully inadequate in light of the enormous
size of the phylum and its largely underexplored state. No group of nematodes is as species-rich as marine forms. Lambshead (1993), predicting 100,000,000 species of marine nematodes, notes that even if there were only 1,000,000 species of nematodes, the task would be overwhelming; if 20 active marine nematode taxonomists worldwide were collectively describing about 200 species per year (an optimistic set of assumptions), it would take 5,000 years to describe the species! Considering broader groups of nematodes, about 30 taxonomists worldwide have the experience necessary to describe species in one or more orders of nonparasitic nematodes, including some marine taxa (SON Systematics Resources Committee 1994). The availability of taxonomists is only slightly greater for more specialized nematodes of economic importance. About 60 taxonomists worldwide work on one or more families of the orders Tylenchida, Dorylaimida, and Triplonchida, which include herbivores and plant parasites (figure 1). Taxonomy is a small portion of the overall responsibilities of these scientists; each might describe one or two species per year. For the six major orders of vertebrate parasites (figure 1), there are about 45 taxonomists worldwide. Species belonging to the four orders that include parasites or associates of other invertebrates (figure 1) have received expanded attention in recent years because of their potential as biological control agents of insect pests; but only about 25 specialists worldwide work on these nematodes. From the perspective of advancing knowledge of nematode biodiversity, more taxonomic emphasis should be placed on understanding nonparasitic taxa, particularly aquatic species.
Problem-Solving and Approaches for Greater Awareness
Increasing public value of ecology and the environmental sciences presents nematologists with opportunities to respond to a public receptive to understanding food webs, nutrient cycling, regulation of microbial populations, natural history, and biogeography. Bernard (1994) suggests that ocean-dwelling nematodes, because of their remarkable structural and biological variation, are potential magnets for programs that illustrate their natural history. Research on the nematode model Caenorhabditis elegans has already been featured in PBS programs on genetics, reproduction, and developmental biology. Internet sites, such as the Tree of Life Project (D.R. Madison and W.P. Madison; http://phylogeny.arizona.edu/tree/phylogeny.html), should not be underestimated in their effect on increasing public awareness of nematodes. The cost associated with such increased public awareness is that nematologists must be willing to set aside other responsibilities to accept outreach opportunities.
Understanding of nematode biodiversity will advance most efficiently when there is a global program harnessing the world's nematology expertise for coordinated sampling and database development; the first step in such a program will be to develop a sampling strategy designed to yield maximal information on global diversity with minimal expenditure of time and human and economic resources. Because nematodes are so pervasive and integrated with all of life, a global sampling program must be integrated with appropriate complementary
expertise, including soils, marine biology, entomology, botany, and vertebrate zoology.
Development of the taxonomic infrastructure in nematology requires a commitment to programs for strengthening taxonomic expertise; these include international programs for training new taxonomists and support for systematic museum collections. Specimen-based collections provide basic tools for taxonomic work as repositories of preserved specimens, preserved DNA, and supporting databases and Web sites to aid inventory and access for specialists. Among the most promising new approaches for taxonomists are molecular tools refined to increase the efficiency and accuracy of surveys through databases that link morphological and molecular species diagnostics (NSF Workshop on Systematics and Inventory of Soil Nematodes, http://www.nrel.colostate.edu/soil/home.html) (Szanlanski and others 1997; Thomas and others 1997). Surveys and species identification are inseparable from the task of reconstructing a phylogenetic framework for nematodes (Adams 1998), but the tools for developing such a framework are more powerful and promising than ever before (Blaxter and others 1998).
The sciences that support advances in our understanding of nematode biodiversity are at an important crossroads. Nematology's base of classical taxonomistswith their wealth of information on nematode structure, diagnoses, and natural historyhas been seriously eroded over the last 15 years. Although molecular systematists are applying modern approaches that offer much promise to advance the discipline, the most fruitful outcomes will come from collaborative efforts of classically trained nematologists, molecular systematists, and other scientists who can apply novel tools that enhance our ability to address complex problems in biodiversity. There is a very narrow window of opportunity to train the next generation of nematode biosystematists schooled in both classical and new approaches, given that many universities have hired scientists who use reductionist approaches in preference to those who use the entire organism as the unit of study. With the reduction and dispersion of the remaining expertise, training of broad-based nematode biosystematists is more expensive because it often requires on-site work at several laboratories. Given our lack of data on the full extent of nematode diversity, it is not practical to estimate how many additional scientists are required to develop a thorough understanding of the phylum. But doubling the number of nematode biosystematists during the next two decades seems to be a conservative and necessary first step. Clearly, more emphasis should be placed on taxa that are not of direct economic importance, such as nonparasitic soil and aquatic species.
Those scientific imperatives cannot be accomplished without addressing some serious practical considerations. What agencies will provide the funding for this important research? How will the current pecking order among scientists be altered so that organismal biologists are considered to be as essential to university research programs as scientists who study fundamental processes at the molecular level? Documents like this cannot serve science if such practical problems remain unresolved or if scientists themselves do not adopt a more panoramic perspective of biology and, in the process, see fit to set priorities in research support for groups of organisms that are poorly understood and rapidly disappearing.
We acknowledge support of National Science Foundation grants PEET 97-12355, DEB-93-18249, OPP 91-20123, and DEB 96-26813 and the help of Gina Adams. This work is a contribution to OPP 92-11773, the MCM LTER.
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Global Diversity of Mites
The mites and ticks make up the order Acari (or Acarina) within the class Arachnida. They differ from other arachnids in that, in virtually all cases, all traces of body segmentation have disappeared. The body of a mite is divided into the gnathosoma (mouthparts) and the idiosoma. There is no recognizable head, and the structures normally associated with the head, such as eyes and brain, are incorporated into the idiosoma. There are no antennae, but in many groups the first pair of legs is long and slender and serves a sensory function. Their ancestral arachnid relatives were predatory, but the mites have diversified from this origin to the extent that they now occupy an extraordinarily diverse range of niches. Many have remained predatory, but other groups have adapted to plant feeding and scavenging on dead plant matter and, alone among the arachnids, have developed into parasites of vertebrate and invertebrate animals. They have developed a wide range of associations with other organisms, including phoretic relationships, some of which have produced morphological and behavioral adaptations in both the mites themselves and the animals that they use for transportation.
The acari are usually subdivided into seven suborders. Astigmata includes forms that occur in patchy habitats, such as dung, carrion, decaying wood, fungi, and the nests of mammals and birds; the latter have evolved into many families of vertebrate parasites, the common pests of stored products that occur in the
home and in food storage, and the dust mites that are implicated in allergy and asthma. Oribatida contains essentially feeders on dead plant material and fungi; these mites play an important part in litter decomposition and soil formation, and a few are important as intermediate hosts of cestode parasites. Prostigmata is a diverse assemblage of predators, plant parasites, algal feeders, and parasites of vertebrate and invertebrate animals. Mesostigmata also includes parasites, but most of its members are predators in soil and decomposing organic material. Ixodida contains the ticks, which are exclusively parasites of vertebrates that feed by drawing blood from their hosts with specially adapted mouthparts. The members of the remaining suborders, Opilioacarida and Holothyrida, are less diverse and less well known; they occur in damp habitats, such as forest leaf litter, and are believed to be predators.
Mites are small. The smallest adults are plant parasites about 80 mm long; the largest are predators about 13 mm long. Most are 400–800 mm long. Their small size has contributed to the diversity of their life cycles and basic biology and has allowed them to exploit an extraordinary variety of niches. The taxonomic and ecological diversity of mites is accompanied by structural diversity. Some exhibit specialized adaptations of the mouthparts, from elongated attenuated chelicerae for sucking plant or animal fluids in parasitic groups to very heavy robust chewing mouthparts in families that feed on fungi or dead plant material. Associations with other organisms have produced specialized structures and organ systems used for grasping and holdingsuch as hypertrophied claw-like setae, modified mouthparts, and adhesive sucker platesand modifications of the life cycle to synchronize with other species on which they depend for feeding and dispersal.
Mites are equally diverse in their modes of reproduction. Some copulate with direct sperm transfer from the male to the primary or a secondary genital aperture of the female. In others, males transfer sperm to the female with their chelicerae or deposit a spermatophore on the substrate for females to pick up. Each of those systems is associated with specific structural and behavioral adaptations, some of which are highly complex.
In the face of the tremendous diversity of this group of organisms, generalizations about taxonomic and ecological diversity are difficult. We do not attempt a comprehensive overview of all these varied phenomena here. Instead, we attempt the more modest objective of assessing the evidence of how many species of mites exist. It would be easy to make sweeping generalizations about the existence of millions of species on the basis of our acknowledged ignorance of most mite groups, but we have resisted that temptation. Instead, we present an analysis of the state of knowledge of the mite faunas of Great Britain, Australia, and North America based on the results of recent taxonomic studies of selected taxa. We use these data as the basis of an extrapolation to an estimate of the number of species that remain to be described in these regions and then, more speculatively, to an estimate of the total world fauna of mite species. Previous estimates of the number of described mite species are summarized in table 1, and our current estimate is 48,200 described species.
Mite Fauna of Australia
We have conducted a comprehensive survey of the literature associated with the Australian mite fauna. By August 1997, about 2,700 described species of mites in Australia were knownAstigmata, 330; Oribatida, 330; Prostigmata, 1,270; Ixodida, 80; Holothyrida, 3; and Mesostigmata, 675 (Halliday 1998). We may then ask ourselves how to extrapolate this figure to derive an estimate of the size of the total fauna. One approach is suggested by the figures presented in table 2. The table lists a series of mite groups in which the Australian fauna has been the subject of modern revision and shows the numbers of species before and after revision. The totals show that the previously known fauna was multiplied by a factor of about 2.9 as a result of revision. That might lead to an expectation that the total Australian mite fauna could include about 7,800 species if the same trend is repeated in other groups.
However, we believe for several reasons that a multiplying factor of 2.9 is a serious underestimate. The water-mite survey published by Cook (1986) essentially reported the results of a single collecting expedition by a single person, and many
other species of water mites have been reported in Australia since then (for example, Harvey, 1987, 1989, 1990a,b,c,d, 1996). Schicha's (1987) revision of Phytoseiidae included mainly species associated with economic crop plants. The fauna associated with native plants, such as those occurring in rain forests, has only recently been studied (for example, Schicha and O'Dowd 1993) and is likely to be a rich source of new species. The study of the Ascidae reported by Halliday and others (1998) deliberately excluded many undescribed species and documented only enough species to record the presence of each genus in Australia.
It is also informative to examine the state of knowledge of some groups that are not in table 2. The known Australian fauna of Eriophyoidea includes only 53 described species of a world total of 2,884 (Armine and Stasny 1994). The United States has 635 described species of Eriophyoidea (Baker and others 1996), described from 579 host plant species. The Australian flora is very likely to include over 25,000 species of plants (George 1981), so if the same relationship between plant species and mite species numbers exists in Australia, the eriophyoid fauna of Australia might exceed 5,000 or even 10,000 species. A total of 64 species of described feather mites has been recorded from Australia. The number of bird species in Australia is about 700 (Slater 1970), and the feather mites demonstrate a high degree of host specificity (Gaud and Atyeo 1996), so the number of feather mite species might exceed 1,000. Hirschmann and Wisniewski (1993) listed some 2,000 described Uropodina species worldwide, but only 67 from Australia are known. The uropodine fauna of Australian rain forests is extremely rich and is likely to yield hundreds of species. Until the 1980s, the Australian fauna of Halacaridae had been very little studied and included fewer than 20 described species. However, a single collecting trip to a small island (Rottnest Island, WA; area, 1,900 ha) in 1991 yielded over 80 species (Bartsch 1996), most of which remain undescribed. The Australian fauna now comprises 80 described species, almost all of which were first described in the last five years. The Australian coastline of over 36,000 km is certain to yield hundreds of species of Halacaridae. About 300 described species of Tarsonemidae are known worldwide (Lindquist 1986), but only eight from Australia are recorded. Bearing all those factors in mind, we conservatively estimate that the Australian mite fauna is likely to exceed 20,000 species, more than seven times as many as the known described species.
Mite Fauna of Great Britain and Ireland
On the basis of the checklists of Turk (1953) and Luxton (1996), the recent monograph by Hillyard (1996), and a search of the Zoological Record, we obtained a total of 1,740 species for the mite fauna of Great Britain and IrelandAstigmata, 265; Oribatida, 303; Prostigmata, 675; Ixodida, 22; and Mesostigmata, 475. However, the regularity with which acari new to science or newly recorded are still being found (for example, Luxton 1996; Skorupski and Luxton 1996) is evidence that the fauna is incompletely known.
A multiplying factor of 1.49 was obtained with the method described above (table 3), and this gives a projected total fauna of 2,590 species. Examination of the taxonomic attention that the various mite taxa have received in Great Britain
and Ireland, however, suggests that far more are likely to occur there. The Ixodida have been extensively studied, and it is unlikely that additional native species will be discovered (Arthur 1963; Hillyard 1996). The Oribatida have also been the subject of much taxonomic work over many years (for example, Michael 1884, 1888; Luxton 1996), but new records are still being uncovered (Luxton 1996). Some families of Mesostigmata, such as the Macrochelidae, have been reviewed more than once in the last 50 years (Evans and Browning 1956; Hyatt and Emberson 1988), but most families have not been studied in great detail. Of all the orders, the Astigmata and Prostigmata have been the least studied; apart from Green and Macquitty (1987) and Gledhill and Viets (1976), there are no modern taxonomic monographs or reviews of the British members of either taxa. More often, descriptions or records appear in studies of particular habitats, such as human dwellings and food stores (Hughes 1976) or hosts (Hyatt 1990).
Many localities and habitats remain to be comprehensively sampled. Green and Macquitty (1987) acknowledged that their monograph on the marine mites could not be regarded as a complete account of the British fauna, because so much of the coastline was unexplored for halacarids. Similarly, Gledhill (1979) anticipated additional records of freshwater mites when the hyporheic zone of superficial riverine gravels and sands was more exhaustively sampled. Surveys of terrestrial mitessuch as the Eupodidae, Rhagidiidae, and Phytoseiidae (table 3)have concentrated on the faunas of woodland soils and plants, but even such a narrow range of situations has yielded many new species and records. Such habitats as tree-hole litter, fungi, mosses, and intertidal areas are still to be thoroughly examined.
It can be expected, therefore, that surveys of the majority of mite taxa will result in large numbers of species being added to the fauna of Great Britain and Ireland, as will a close examination of the many habitats for which the mite fauna is not known in any detail.
Mite Fauna of North America.
OConnor (1990) reviewed the status of the mite fauna of North America north of Mexico by using data derived from species lists maintained by systematists working with each major taxonomic group. At that time, 5,106 described species had been recorded for the regionOpilioacarida, 1; Ixodida, 83: Mesostigmata, 869; Prostigmata, 2,803; Oribatida + “Endeostigmata”, 930; and Astigmata, 420. Contributors to that dataset were asked to estimate the total number of species expected in the North American fauna. The estimates were Opilioacarida, 1; Ixodida, 84; Mesostigmata, 2,827; Prostigmata, 7,977; Oribatida + “Endeostigmata”, 15,300; and Astigmata, 3,611. That is a total estimated fauna of 29,800 species, which means a multiplying factor of almost six. Since those data were reported, several revisionary works and compilations have added to the fauna. Farrier and Hennessey (1993) cataloged the free-living Mesostigmata, recording over 1,300 species in “North America”, including Mexico and parts of Central America. Baker and Tuttle (1994) revised the spider-mites (Tetranychidae) of the United States, and Baker and others (1996) revised the Eriophyoidea of the United States. Numerous smaller-scale revisions of families and genera have also been published, most notably for several groups of Oribatida (for example, Behan-Pelletier 1986, 1989, 1990, 1993, 1994; Norton and others 1996) and water mites (for example, Smith 1989a,b, 1990a,b, 1991a,b, 1994). The latter data provide something of a test of the earlier estimates of faunal diversity. With the method described above (see table 4), an increase factor of 3.24 was obtained for the oribatid groups recently revised and 2.65 for the water mites. The prior published estimates would predict increase factors of 16.5 for the oribatids and 1.79 for the water mites. The much lower observed increase factor for the oribatids might be explained by the fact that the recent revisions dealt primarily with faunas occurring in boreal Canada, where species diversity might be expected to be lower than
in North America as a whole. The larger than predicted increase for the water-mite taxa might reflect the fact that many of the included groups specialize in stream and hyporheic environments, which have received much less attention than lotic environments. The data again point out the danger in extrapolating too much from limited observations.
As has been the case for other regions, North American taxa of economic and medical importance have received more attention. For example, in the first compilation of North American Phytoseiidae, Cunliffe and Baker (1953) reported 26 species. Farrier and Hennessey's 1993 catalog lists 150, for an increase factor of 5.77. Baker and Tuttle's 1994 review of the thoroughly studied North American Tetranychidae lists 218 species, of which only 12 were newly reported. The fauna of Ixodida is essentially completely known. However, many other taxa have received scant attention in North America; relatively little information is available on such major faunal elements as the free-living Prostigmata and Mesostigmata and the arthropod-associated Mesostigmata and Astigmata. Evidence of the latter includes OConnor's (1991) report of 57 species of insect-associated Astigmata collected at a single forested site in northern Michigan; of those, only four were previously described. Later collecting at the same site has yielded an additional 25 undescribed species (OConnor, unpublished data). Most taxa that have received some taxonomic treatment have not been thoroughly surveyed over the entire continent; most published treatments are at best regional. Major areas of endemismsuch as California, the Pacific Northwest, the arid Southwest, and subtropical Floridaremain poorly collected for most free-living taxa.
How Many Species of Mites have been Described?
Various figures have been quoted for the number of mite species described worldwide (table 1). We now present a total of 48,200 nominate species (to June 1997). This figure was obtained from three main sources: an index of species at The Natural History Museum, London, which was maintained until 1977; the Zoological Record from 1978 on, which showed that an average of 788 new species were being described each year during that period (table 5); and, for Ixodida, Keirans (1992). The search of the Zoological Record from 1978 to 1996 also showed that mite species names were being synonymized at the rate of about 40 per year during that period, so this figure should be moderated slightly. Nevertheless, the figure of 48,200 should be regarded as a realistic assessment of the total number of valid mite species known worldwide.
It is evident from the estimates of biodiversity in the geographic regions considered above that the true number of mite species in the world fauna is much higher than 48,200. New species of Ixodida are now found only infrequently. The groups in which there are likely to be the greatest increases are the Astigmata, Mesostigmata, Oribatida, and Prostigmata (table 6). Many parts of the world have no active specialists in mite taxonomy or have not been the subject
of faunal surveys. Similarly, the mites in many habitats and associations are poorly known, such as the soils of tropical rain forests and species associated with other arthropods (Welbourn 1983). Taxonomic attention is sometimes focused on a group when its economic importance is recognized, with the resulting description of huge numbers of new species. For mites, perhaps the best example is seen in the family Phytoseiidae. In the 1950s, when the potential of some phytoseiid species as biological control agents was first noticed, 165 species were listed in the world fauna (Chant 1959). By 1994, no fewer than 1,745 species had been described (Kostiainen and Hoy 1996), and another 55 new species have been found since then. That represents an increase factor of more than 10; if applied to our figure for valid species in other groups, the factor would yield a total of over a half-million.
We can suggest several strategies that will help to increase our knowledge of the world's mite fauna. It would be useful to document and publicize the existence of collections of unsorted material, such as Berlese funnel samples, so that material collected incidentally by nonacarologists and samples of no immediate interest to acarologists is not lost but is available for later study. It would also be useful if entomologists, mammologists, and ornithologists were encouraged to retain the parasitic and phoretic mites that they find, rather than discarding them, and to draw them to the attention of acarologists. The specimens should either be kept with the host or have collection data included with them if separation is necessary. But the availability of specimens is not likely to be the most important limiting factor in the progress of systematic acarology. Serious assessment of mite biodiversity will continue to be inhibited by the shortage of trained taxonomists, especially in tropical areas, where species diversity is likely to be much greater than in the areas we have examined here.
We thank Emma de Boise, Department of Entomology, The Natural History Museum, London, for help in the assessment of numbers of valid mite species and Dave Walter for generously providing access to unpublished information.
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Biodiversity of Terrestrial Invertebrates in Tropical Africa:
Assessing the needs and Plan of Action
Biological resources are the basis of the prosperity of the developed world, yet the biologically rich underdeveloped nations of Africa are the economically poorest in the world. Africa's biodiversity, if conserved and developed sustainably, can be used to relieve poverty and achieve economic stability. The challenge lies in rapidly acquiring the required knowledge of the biodiversity resource: knowing what the critical species are and where they occur, obtaining information about their natural history, and establishing sustainable patterns of resource use.
Although the continent of Africa is most renowned for its highly charismatic megafauna, the greatest contributions to its biodiversity (as elsewhere) in fact lie in its other taxa, which ultimately facilitate the existence of these flagship species. Insects and other arthropods compose more than 70% of the world's fauna. Insects contribute the largest number of taxa by far to biological diversity in both Africa and the world (figure 1). Many major effects on human welfarehuman and animal diseases carried by insect vectors; outbreaks of migrant pests, such as locusts and armyworms; destruction of food by plant pests; toxic residues from pesticides; and overuse and depletion of agricultural lands and adjoining forestsare problems whose answers lie well within the field of biodiversity and, more specifically, insect diversity (Hill 1997). By performing critical “service” functions within ecosystems, insects are key to the stability of ecosystems. Many insects provide a direct economic return (for example, silkworms and bees); others produce chemicals for medicinal use. Some constitute an important source of pro-
tein in the diet of rural peoples; others play predatory and parasitic roles that regulate pests (Odindo 1995). Arthropods are key in providing pollination services to both natural and human-made ecosystems.
No African invertebrate species have been documented yet as becoming extinct either directly or indirectly because of human activities during historical times, although several butterflies and lacewings might have become extinct in South Africa (Siegfried and Brooke 1995). However, invertebrates are generally so poorly known that even probable extinction is difficult to detect. With insects more than with any other taxa, we risk losing aspects of biodiversity without ever knowing their value.
This paper outlines an approach to putting terrestrial invertebrates on the agenda for conservation of biodiversity in Africa. We seek to fill two key gaps in the understanding and use of the positive aspects of insects in African biodiversity. First, almost all research on insects in tropical Africa focuses on the negative aspects of insectsfor example, the problems in agriculture, forestry, livestock, and human health that are caused by less than 1% of the species of insectsand ignores the remaining 99% of insect species. Of the more than 100,000 described
species of insects in the Afrotropical region, fewer than 500 species were mentioned between 1990 and 1995 in the journal Insect Science and its Application, one of the major African entomology journals, and 97% of the articles over this time focused on pest or other economically important species.
Most programs of biodiversity studies and conservation currently operating in tropical Africa focus on vertebrates or, secondarily, flowering plants and ignore insects, which E.O. Wilson (1987) has called “the little things that run the world” because of their key roles in ecosystem function. For example, in 1994, a survey of sets of biodiversity data available for East Africa included only 12 for insects, whereas mammals and plants had more than 50 each and birds and fish had more than 40 each (World Conservation Monitoring Centre 1994).
Through extensive consultation, we have reviewed many programs around the world that have dealt, successfully or unsuccessfully, with similar challenges (for example, Hawksworth and Ritchie 1993; Miller 1994). By this process, we have identified some basic premises that have guided the development of our program.
First, if we are to protect biodiversity, it must have utility for human societies, and if it is to be used sustainably, it must be understood. This premise is the basis for several conservation initiatives in Costa Rica and Africa (see Janzen paper in this volume; see also Ramberg 1993 and Noss 1997). The developed-country model of protecting biodiversity in national parks is not sustainable in developing countries. Long-term protection of biodiversity depends on making it useful and valuable to the people who live amid and around it. This means that some of the biodiversity must be used to provide the means for supporting and managing the rest. Sustainable use of biodiversity requires knowing how to find what you need, understanding the implications of that use, and learning how to encourage the regeneration or recovery of the resource to support its continued use.
A second premise is that systematics provides the framework for organizing and communicating basic information about biodiversity (Janzen 1993). Thus, the involvement of the taxasphere, the international infrastructure for biological systematics, including the natural-history museums that hold most of the collections of specimens, is vital. We also expect to integrate our activities with those at smaller (for example, national or local) and larger (for example, international) levels, including BioNet International, Systematics Agenda 2000 International, and Species 2000 (Hawksworth 1997).
Finally, it is more cost-effective to use what we already know than it is to recreate basic information on biodiversity (Nielsen and West 1994; Soberon and others, 1996). An enormous body of information is theoretically available, but it is highly dispersed, extraordinarily varied in form, uncoordinated, and largely unavailable in most of Africa. Much of this information is in museum collections (Cotterill 1997). Recent developments in information technology have provided the means to achieve a coordinated information base on African insect fauna and an efficient means of disseminating that information. The task requires effective collaboration of experts and stakeholders from all aspects of the process, from the
discovery through the management and use of biodiversity (World Conservation Monitoring Centre 1996).
An Organizational Structure for a Continentwide Biodiversity Initiative
One irony of current biodiversity-conservation initiatives is that while we continually are refining our skills to document the value of the ecosystem services that biodiversity provides, few governments or legal entities are prepared to pay for the conservation of these services, which, until now, have been exploited freely by human societies. An example that is specific to our program is that no country in Africa has the resources to initiate a program of conserving insect biodiversity; the task is formidable, and the benefits are so basic and diffuse that they become lost in a sea of competing priorities. Only a highly-targeted, cost-effective program that can coordinate the resources and disseminate the benefits on a wide scale (regional or continental) can return the expected outcomes.
The leadership for such a program has been assumed by the International Centre for Insect Physiology and Ecology (ICIPE), an international institute that is situated centrally on the continent in Kenya. ICIPE is a major international institution that has more than 27 years of experience in research and monitoring of arthropods. It has developed integrated pest and vector-management techniques and biological-control strategies for insects that are disease vectors and plant pests. The institution combines research with interactive training of scientists, technicians, and farmers and herders at both national and subregional levels, and it provides training programs for graduate students from universities throughout Africa. ICIPE has memorandums of understanding with more than 20 sub-Saharan countries, and more than 30 countries worldwide have signed its charter. With an established structure in place for joint training and research with the major taxonomic and biodiversity institutions of Europe and the United States, implementation of a collaborative program would be possible without untimely delays.
We have identified a mixture of projects that provide a cost-effective foundation for understanding the diversity of insects, the roles they play in natural systems, and ways to manage those interactions more effectively. Our initiative includes three main components. First, an information-management program will organize and make available a large volume of information that already exists but is not readily accessible to users. This will be coordinated with other activities that are already under way in the museum, systematics, and conservation communities and will be targeted carefully to fill key gaps. Second, a series of field projects will evaluate the use of insects as indicator organisms and will quantify their roles in ecosystem processes. In many cases, these projects will take approaches that have been successful in South Africa and the Northern Hemisphere and will apply them, with appropriate modifications, to tropical Africa. Third,
training and participatory technology transfer will build on ICIPE's existing training programs, including the African Regional Postgraduate Programme in Insect Science (ARPPIS).
An initiative for reviewing the literature and creating a database of specimens will repatriate 200 years' worth of information collected in sub-Saharan Africa and now housed in museums in the United Kingdom, France, Belgium, Germany, elsewhere in Europe, South Africa, Kenya, elsewhere in Africa, and the United States and Canada. This initiative will support individual projects and applications within the ICIPE program and will provide relevant information to a wide audience in Africa. One of the first and most important steps in managing the biodiversity of African insects is to find and organize what we already know. As we have stated, a tremendous amount of information is available but not in a cohesive and accessible form; recent developments in information technology will allow us to compile an information base on African insects; they will also allow efficient dissemination of this information (Vane-Wright 1998). Note the continuing growth of the technology from, for example, the discussion of early Internet tools in Miller (1993) to those in Helly and others (1996). As a result, gaps in our knowledge will become apparent, allowing us to establish priorities for further work. Our checklist of insects known from Africa is in progress, and an interim product is on the World Wide Web (www.icipe.org/environment/biodiversity_index.html).
Pilot Projects and Applications of Conservation Biology that Focus on Insects
A series of experiments, surveys, and applications will be designed to investigate the role of key groups of insects in the function and management of ecosystems and to provide information on the conservation and sustainable management of the insect resource. The major foci will include identification of high-priority areas for conserving biodiversity, using butterflies, fruit flies, dragonflies, and termites; impact assessments, using insects as “indicators”; and identification of the roles of insects in pollination, soil processes, and the organization of tropical-forest ecosystems.
Training and Participatory Technology Transfer
An important element in the overall program is capacity-building: producing trained technicians and scientists who will be able to implement the information-management and research tasks. In the multidisciplinary field that is inherent to conservation of biodiversityfrom taxonomy to database management to field techniquesindividual and institutional capacity spans every activity. This feat will be achieved through partnerships with universities, museums, advanced-research laboratories, and national institutions throughout the world. Developing an African and overseas reciprocal research exchange within Africa will ensure a permanent conduit for technology transfer. Many of the students trained through this program will become interns in museums and research centers throughout
Europe and North America, thus effecting the transfer of skills, as well as information.
Formal university training will be conducted through the ARPPIS PhD program at ICIPE, in which students undergo three years of research training. The ICIPE provides a thesis project, research facilities and supervision, and a training fellowship to support the students' maintenance, university fees, and research costs, for a total of US$30,000 per student per year. Students are registered at participating African universities, which examine the students and award them their degrees. The program has, at any one time, 20–40 students at various stages of their thesis work at ICIPE. To date, 131 scholars from 25 African countries have enrolled in the program, and 91 have graduated. The success of the ARPPIS program has stimulated the interest of universities; 18 universities have renewed their agreements with ICIPE. ICIPE is proud that after they have graduated, almost all former ARPPIS scholars have stayed in Africa to work toward solving the continent's insect-related problems. Most graduates are employed by national research systems, universities, or science-based international organizations.
Training means more than formal university training, however. Two other major activities are the enhancement of national capacities for the diffusion, adoption, and use of technology and the facilitation of the dissemination and exchange of information.
Examples of Research on Insect Biodiversity in Africa in Support of Sustainable Development
Recent research initiatives undertaken in Kenya have shown that basic research on the biodiversity of arthropods can contribute in substantial ways to sustainable agricultural development.
The Role of Habitat in the Agroecosystem of Maize
Losses of maize, sorghum, and other cereals caused by stemborers remains one of the biggest threats to the security of the food supply in eastern and southern Africa. Maize yields in Africa are less than half the average yield worldwide. Especially damaging is the moth Chilo partellus (Lepidoptera: Crambidae), an intruder from Asia that was introduced accidentally into Africa in the 1930s and has now displaced indigenous pests. This exotic species soon became infamous for causing losses of 20–80% of crops.
Native predators may play an important role in suppressing stemborer populations. Studies conducted in Kenya's Coast Province revealed that ants are the most abundant predator. The abundance and diversity of predators increased with the age of the plants and was highest at the tasseling stage of maize. An even broaderand very promisingview is being taken by looking not just at the farmer's field, but also at the surrounding environment (Khan and others 1997).
ICIPE's project on the role of wild habitat in the invasion of gramineous crops by stemborers already is yielding hard data on the benefits of preserving and managing biodiversity in small and medium-size farms. The project is developing a novel approach to pest management that uses a stimulus-deterrent (“push-pull”)
diversionary strategy. A better understanding of the relationship between diversity of habitat and resilience to pest challenge is being developed, as are ideas for modifying the habitat to contain this challenge.
Several plants that lower the density of stemborers by the “push-pull” strategy have been identified, resulting in higher crop yields. Especially promising in this respect are Napier grass (Pennisetum purpureum), Sudan grass (Sorghum vulgare sudanens), and molasses grass (Melinis minutiflora). These three important fodder grasses act as traps by “pulling” or attracting the borers and serving as reservoirs for the natural enemies of the stemborers. Furthermore, Sudan grass increases the efficiency of the natural enemies. The rate of parasitism on larvae of the spotted stemborer, Chilo partellus, more than tripled, from 4.8% to 18.9%, when Sudan grass was planted around maize in a field. Napier grass has its own defense mechanism against crop borers: When the larvae enter the stem, the plant produces a gum-like substance that kills the pest. Molasses grass releases volatiles that not only repel (or “push”) stemborers, but also attract parasitoids. Both whole live plants of M. minutiflora and its volatiles were shown to attract the natural enemy of the wasp, Cotesia sesamiae (Hymenoptera: Braconidae). Intercropping with M. minutiflora increases parasitism, particularly by the larval parasitoid wasp and the pupal parasitoid Dentichamis busseolae (Hymenoptera: Ichneumonidae). Analysis of the volatile oils from molasses grass shows that they contain several physiologically active compounds. Two of these inhibit egg-laying in Chilo, even at low concentrations. In contrast, Chilo's host plants (maize, sorghum, and Napier grass) have been found to contain volatile compounds, such as eugenol, that attract Chilo and stimulate egg-laying. Molasses grass also emits a chemical that summons the borers' natural enemies. This same substance is released by whole plants as a distress signal when they are being damaged by pests. The results of this study have opened up the new and intriguing possibility of using intact plants that have an inherent ability to release these stimuli. Such plants will be useful in ecologically based crop-protection strategies.4
Commercial and Sustainable Production of Wild Insects
Wild insects long have been part of the diet of humans in Africa; termites and locusts are two highly valued food items among the arthropods. Wild insects also are husbanded for the products they create. If harvesting and use of wild insects are to be sustained with increasing population, however, they will need to be studied carefully and rationally. ICIPE currently undertakes studies of African honeybee culture and wild silk production (ICIPE 1997).
Apiculture is a traditional occupation in most African communities, but centuries-old practices of harvesting honey are inefficient and often cause the death of the colony; the aggressiveness of African honeybees has been attributed to these management practices. ICIPE is introducing improved methods of beekeeping to farmers and to women's groups, supported by research to solve the problems of queen-rearing and African honeybee aggressiveness and to improve the production of honey and other valuable hive products. Linking honey production to floral calendars can help local producers understand the direct benefit of habitat conservation.
Similarly, production of wild silk moths can provide a strong economic incentive for rural communities to adopt sound wild-land management practices as an adjunct to subsistence agriculture. Currently, silk moth larvae and pupae are harvested in bulk as a source of dietary protein, but no mechanisms exist to replenish the silkworms (the moth larvae). Techniques of sericulture (the deliberate rearing of silk moths for harvesting of the pupal cases) are unknown at the village level, yet at least three species of moth that yield high-quality wild silk have been identified. ICIPE has undertaken a project to develop methods of sericulture that are appropriate for Africa and that also will assist in conserving the valuable wild species of moths. The interest shown by authorities from national parks and by communities in East Africa is proof of the timeliness of this project and augurs well for the future of a strong conservation industry built around wild silk moths.
We expect that the foundation of knowledge and trained personnel that will be generated by this new initiative will enable sophisticated strategies of ecological monitoring and applications of sustainable development that draw on the strengths of the resource base of African arthropods. In a continent that until now has been remarkable for the coexistence of a rich and varied wildlife with human societies, we are challenged to direct development along lines that also foster the coexistence with the ubiquitous but less-noticed aspects of biodiversity, such as arthropods. Because these aspects most directly impinge on human welfare, the success of biodiversity conservation may depend on how well we meet this challenge. In the largely intact, undeveloped landscapes of Africa, we still have a tremendous chance to conserve the fine fabric and delicate linkages of nature in and with human development if only we can document its existence and importance before we have lost it.
We thank all the colleagues and institutions, too numerous to name here, who have helped in the development of our ideas and plans. The government of Norway provided seed funding for the development phase of this initiative. We also acknowledge the seminal role played by biological-survey and information-management activities in Australia (ERIN), Costa Rica (INBio), and Mexico (CONABIO) in developing and testing many of the ideas that we and others have been able to build from.
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Global Diversity of Insects:
The Problems of Estimating Numbers.
The class Insecta is the most species-rich of all major groups of living multicellular organisms. Any meaningful assessment of the diversity of life on earth depends on estimates of both the number of named insect species and the number of insect species that are living but are yet unnamed or even undiscovered.
Common sense might suggest that the number of described species would be a statistic that science would have available. However, no single compilation exists of the names of described insect species, so the total number remains a matter of conjecture. Indeed, for most groups of insects, apart from the Diptera (Evenhuis 1989), published lists of species names are not readily available, despite a recent surge of interest in computer listings. The production of lists of described taxa should have high priority for insect taxonomic science, whether for a local fauna, such as the Lepidoptera of Australia (Nielsen and others 1996), or for the worldwide fauna of a particular group, such as Geometridae (Scoble 1999). Such lists provide some measure of what has been achieved at a given time. More important, they can be a means of stimulating further studies and of attracting research funding in other aspects of biology (Mound 1998). However, within the taxonomic community, tradition remains biased toward the production of scholarly nomenclatural catalogs, with details of type material that are useful only to other specialist taxonomists. Our use of the term checklist implies a product that can be used as the starting point for investigations into biological diversity by the biological and conservation community in general.
As a result of the lack of checklists, available estimates of the numbers of described species often differ widely. Indeed, at times it is difficult to understand
precisely what an author means by a figure for the number of species in an insect group. The numbers may represent all published species-group names; only technically available species-group names (excluding, for example, nomina nuda); currently accepted valid species, excluding synonyms but with or without names of subspecies; or the estimated currently extant species, including undescribed or even undiscovered species. In recent accounts, the estimated number of named species varies from 751,000 to 950,000, and the estimated number of living species ranges from 1 million to 100 million (Hammond 1994). The numbers we quote in table 1 presumably suffer from similar problems, but we have attempted to clarify the situation whenever possible.
A further problem is that “species” are not comparable units throughout the Insecta, thus at times rendering comparisons potentially misleading (Vane-Wright 1992). Although the “species” is the most commonly used unit of biodiversity, organismal diversity cannot be measured objectively solely by differences in the number of species (Hawksworth and Kalin-Arroyo 1995). It is widely agreed that the species number is the most important measure that we have, but we cannot regard it as a standard unit in any statistical sense. The existence of sibling species of Diptera that are distinguishable only through examination of their chromosomes has been well known for many years. In other groups of insects, DNA methods are increasingly demonstrating genetic differences that many authors interpret as evidence of different species. In some ways, we face the same problem that plagued Alfred Russel Wallace and Charles Darwin, in attempting to distinguish units within biological systems that sometimes appear to exhibit almost continuous variation. The peaks of ecological and evolutionary adaptation that we call species can modulate and move in space and time in response to varying pressures of selection. In conservation, it is this ability to change and adapt that we need to protect, not merely the units that we use to measure diversity.
The estimates we give of the number of named species, particularly the total diversity within each order of insects, clearly depend heavily on the bibliographic efficiency and practical experience of individual taxonomic specialists. May (1990) expressed concern that no full published list exists of all described taxa of insects. However, no individual working taxonomist has a particular requirement for such a list. Moreover, most taxonomists who work on insects in the major orders study only a small subset of any major group and thus have little requirement for even a checklist of all the available names within an order or major family. Given that some genera of insects, for example within the Ichneumonidae and Staphylinidae, include more than 1,000 species each, it is scarcely surprising that individual taxonomists have not had the resources to produce or maintain such massive checklists.
Estimates of the possible number of living insect species originate essentially from two sources. One source is the few taxonomists who have experience with very large collections, usually coupled with field experience in areas of high biological diversity. In this case, the data will have been produced haphazardly and over a long time, albeit on a wide front, and the estimate is based on the frequency with which novelties appear in collections. The second source is ecologists who are interested in estimates of species richness. In this case, the data come from intensive sampling of restricted areas over a restricted period followed by extrapolation of these numbers into unsampled areas. Not surprisingly, these techniques yield rather different estimates. The first, which is essentially a species-accumulation curve, is related to the acquisition policy of institutes and the distribution patterns of species. This method will underestimate the total number of species through any failure to score fully the many species in large genera that are difficult to distinguish because they are represented only by single individuals. The second method is concerned with the numbers of species that can be found at a single point, and any assumptions of local endemicity or host specificity when extrapolating from these data will tend to overestimate the total number.
Gaston (1991a) pointed out that few of his taxonomic colleagues who had experience with tropical diversity considered it likely that the group in which they specialized would prove to be larger than the currently described subset by orders of magnitude. Similarly, Hodkinson and Casson (1991) produced a figure for the total worldwide insect fauna of 1.87–2.49 million species on the basis of large collections of Hemiptera made in Sulawesi. In contrast, ecological estimatessuch as those by Erwin (1982), Stork (1988, 1993), Kitching (1990), and Recher and Majer (1996)imply that the world's insect fauna is 30 or more times that of the currently described subset. Current evidence from the major museum collections of sorted and labeled insect species, whether described or undescribed, does not support these larger estimates. Insect taxonomists generally concur that, although there may be as many as 5 million species of insects in the world, there are probably fewer than 10 million.
The suggestion that urgent efforts be made to describe all the world's species of insects leads us to a further series of issues. Even an estimate of 5 million species implies logistical demands that far exceed available resources. Mound (1998) pointed out that the practical problems involved in describing such very large numbers of species have never been considered seriously. These problems include communicating the information to other scientists, the effect on library budgets of a further 8 million pages of descriptions for the minimum of 4 million new species, and the effect of all the new insect material on museum budgets. Wilson (1985) expressed a more positive viewpoint by saying that describing a large proportion of the world's fauna is feasible but with the caveat that this possibility exists only if the priorities of human society change substantially from producing armaments to protecting the biosphere.
Some biologists assert that the study of highly diverse biological systems must be preceded by description of the many species that make up such systems. This is not entirely true, as indicated by the extensive karyotypic studies by M. J. D. White (1982) on species of Australian morabine grasshoppers that even now are undescribed. Similarly, Robinson and Nielsen (1989) gave an account of the Australian fauna of tineid moths, despite the fact that half the 380 known species remain formally unnamed. In both those instances, the species are sorted, labeled, and available for study in the Australian National Insect Collection. The importance of a major collection is the quantity and quality of information that it can contain, including distribution patterns in time and space and biological details, such as host plants and parasites. This information can be made available to biologists and conservation workers, even if not all the taxa are formally named. We certainly are not suggesting a moratorium on describing species of insects, but we suggest that greater thought be given to the question of what benefits will be obtained by describing a much larger fraction of the world's insect fauna.
The question of how science should respond to the problem of such a vast number of undescribed insect species is complex. Gaston (1994) pointed out that although most insect species are tropical, most taxonomic effort continues to be applied to temperate faunas. Mound (1998) indicated that science budgets in tropical countries will need to take a greater share of this burden of description
in the future, but emphasized that more appropriate responses need to be considered than the ad hoc description of large numbers of species. The interesting scientific problem lies not in the description of all the species, but in why so many species exist. We need to describe formally only the species that we require for our analyses of biologically diverse systems, whether these analyses are ecological or systematic. The activity of describing species is sometimes advocated as providing the building blocks for the rest of biology. However, ad hoc description of new taxa is like the unplanned production of building blocks in the hope that one day they may find a place in our biological building. Can we not find a more rational and effective use of our resources for such a gigantic task?
Gaston (1991b) made the point that better data on the total numbers of species could be obtained by conducting detailed studies of the numbers of both described and undescribed species from a number of specified sites; that is, data should be collected purposefully, with particular objectives. Similarly, Longino (1994) has pointed out the advantages to be gained from a sampling program that has specific long-term objectives. Again, Mound (1998) pointed out that when descriptive taxonomy is incorporated into focused interdisciplinary projects on particular systems or groups, then the whole subject is enriched by data from other biological disciplines. Detailed sampling and interdisciplinary studies then have the objective of facilitating comparisons between sites, seasons, and habitats and thus are relevant to a wider community of scientists. More important, such an approach is based on the view of faunas as dynamic systems, in which processes can be studied, rather than as static systems, in which units need to be described.
As taxonomists ourselves, we find that the absence of an accurate figure for the total number of living insect species does not limit our studies of patterns in structural, behavioral, and geographic diversity. We continue to describe new species when this is relevant to our exploration of interesting patterns in nature, not as part of any program to provide names for the entire insect fauna. Far more important to us are the problems of the origin of insect diversity and of how to maintain this diversity in a rapidly changing world. In this context, we emphasize again the importance of well-curated museum collections and effective access to the information they contain (Nielsen and West 1994), because these tangible and available records of biodiversity facilitate the comparisons between sites and seasons that are valuable to the rest of society.
Table 1 summarizes the number of named species and the estimated total number of species that we consider valid, and table 1 is a brief discussion of each order according to various authors. Our estimated numbers are those we believe to be most accurate, given our current knowledge.
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We are grateful to our many colleagues in Canberra, at the Australian National Insect Collection and Australian Biological Resources Study, for their frequent advice, help, and criticism. C.W. Schaefer, of the University of Connecticut, Storrs, kindly gave us his opinion on numbers of Heteroptera species.
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