Page 115

PART 2—
LESS WELL-KNOWN INDIVIDUAL FORMS OF LIFE



The National Academies | 500 Fifth St. N.W. | Washington, D.C. 20001
Copyright © National Academy of Sciences. All rights reserved.
Terms of Use and Privacy Statement



Below are the first 10 and last 10 pages of uncorrected machine-read text (when available) of this chapter, followed by the top 30 algorithmically extracted key phrases from the chapter as a whole.
Intended to provide our own search engines and external engines with highly rich, chapter-representative searchable text on the opening pages of each chapter. Because it is UNCORRECTED material, please consider the following text as a useful but insufficient proxy for the authoritative book pages.

Do not use for reproduction, copying, pasting, or reading; exclusively for search engines.

OCR for page 115
Page 115 PART 2— LESS WELL-KNOWN INDIVIDUAL FORMS OF LIFE

OCR for page 115

OCR for page 115
Page 117 Microbial Diversity and the Biosphere Norman R. Pace Departments of Plant and Microbial Biology and Molecular and Cell Biology, University of California, Berkeley, CA (Current address: Department of Molecular, Cellular, and Developmental Biology, University of Colorado, Boulder, CO 80309-0347) Introduction 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

OCR for page 115
Page 118 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.

OCR for page 115
Page 119 Figure 1 Universal phylogenetic tree based on small-subunit ribosomal RNA sequences. Sixty-four rRNA sequences representative of all known phylogenetic domains were aligned, and a tree was produced with FASTDNAML (Barns and others 1996; Maidak and others 1997). That tree was modified to the composite one shown by trimming lineages and adjusting branchpoints to incorporate results of other analyses. The scale bar corresponds to 0.1 change per nucleotide. (From Pace 1997, reprinted with permission.)

OCR for page 115
Page 120 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 eukaryotes—mitochondria and chloroplasts—are 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-

OCR for page 115
Page 121 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 creatures—such as Giardia, Trichomonas, and Vairimorpha—nonetheless 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

OCR for page 115
Page 122 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 metabolism—fixation of CO2 to reduced organic compounds—must 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 compounds—such as H2, H2S, and ferrous iron—to 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 diversity—that represented by animals, plants, and fungi. We know little about the other pole—the amitochondriate organisms that spun off the main eucaryal line early in evolution (Sogin 1994). The known instances of such lineages—represented by Trichomonas, Giardia, and Vairimorpha in figure 1—are 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-

OCR for page 115
Page 123 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-

OCR for page 115
Page 124 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 life—that 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.

OCR for page 115
Page 125 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

OCR for page 115
Page 212 Cole FR, Reeder DM, Wilson DE. 1994. A synopsis of distribution patterns and the conservation of mammal species. J Mammalogy 75:266–76. Cotterill FPD. 1997. The second Alexandrian tragedy, and the fundamental relationship between biological collections and scientific knowledge. In: Nudds JR, Pettitt CW (eds). The value and valuation of natural science collections: proceedings of the international conference, Manchester 1995. London UK: Geological Soc. p 227–41. Duellman WE. 1993. Amphibians in Africa and South America: evolutionary history and ecological comparisons. In: Goldblatt P (ed). Biological relationships between Africa and South America. New Haven CT and London UK: Yale Univ Pr. p 200–43. Eldredge LG, Miller SE. 1998. Numbers of Hawaiian species: supplement 3, with notes on fossil species. Bishop Museum Occasional Papers 55:3–15. Groombridge B (ed). 1992. Global biodiversity: status of the Earth's living resources. London UK: Chapman & Hall. Hawksworth DL. 1997. Biosystematics: meeting the demand. Biol Internat 35:21–4. Hawksworth DL, Ritchie JM. 1993. Biodiversity and biosystematic priorities: microorganisms and invertebrates. Wallingford UK: CAB International. 120p. Helly J, Case T, Davis F, Levin S, Michener W (eds). 1996. The state of computational ecology. San Diego Supercomputer Center, San Diego. 20p. [also at http://www.sdsc.edu/compeco_workshop/report/helly_publication.html. Hill DS. 1997. The economic importance of insects. London UK: Chapman & Hall. ICIPE [International Centre for Insect Physiology and Ecology]. 1997. 1996/1997 annual report. Nairobi Kenya: ICIPE. Janzen DH. 1993. Taxonomy: universal and essential infrastructure for development and management of tropical wildland biodiversity. In: Sandlund OT, Schei PJ (eds). Proceedings of the Norway/UNEP expert conference on biodiversity. Trondheim Norway: Directorate for Nature Management and Norwegian Institute for Nature Research. p 100–13. Khan ZR, Ampong-Nyarko K, Chiliswa P, Hassanali A, Kimani S, Lwande W, Overholt WA, Pickett JA, Smart LE, Wadhams LJ, Woodcock CM. 1997. Intercropping increases parasitism of pests. Nature 388:631–2. Miller SE. 1993. The information age and agricultural entomology. Bull Entomol Res 83:471–4. [Also at http://www.bishop.hawaii.org/bishop/HBS/BER.html Miller SE. 1994. Development of world identification services. In: Hawksworth DL (ed). The identification and characterization of pest organisms. Wallingford UK: CAB International. p 69–80. Nielsen ES, West JG. 1994. Biodiversity research and biological collections: transfer of information. In: Forey PL, Humphries CJ, Vane-Wright RI (eds). Systematics and conservation evaluation. Oxford UK: Clarendon Pr. p 101–21. Noss AJ. 1997. Challenges to nature conservation with community development in central African forests. Oryx 31:180–8. Odindo MO (ed). 1995. Beneficial African insects: a renewable natural resource: Proceedings of the 10th meeting and scientific conference of the African Association of Insect Scientists. Nairobi Kenya: African Association of Insect Scientists. iii + 251p. Ramberg L. 1993. African communities in conservation: a humanistic perspective. J Afr Zool 107:5–18. Siegfried WR, Brooke RK. 1995. Anthropogenic extinctions in the terrestrial biota of the Afrotropical region in the last 500,000 years. J Afr Zool 109:5–14. Soberon J, Llorente J, Benitz H. 1996. An international view of national biological surveys. Ann Missouri Bot Gard 83:562–73. Vane-Wright RI. 1997. African lepidopterology at the millennium. Metamorph Suppl 3:11–27. Vuilleumier F, Andors AV. 1993. Avian biological relationships between Africa and South America. In: Goldblatt P (ed). Biological relationships between Africa and South America. New Haven CT and London UK: Yale Univ Pr. p 289–328. Wheeler Q. 1990. Insect diversity and cladistic constraints. Ann Ent Soc Amer 83:1031–47. Wilson EO. 1987. The little things that run the world (the importance and conservation of invertebrates). Cons Biol 1:344–6. World Conservation Monitoring Centre. 1994. Availability of biodiversity information for East Africa, [computer disk]. Dar es Salaam Tanzania: FAO. World Conservation Monitoring Centre. 1996. Guide to information management in the context of the Convention on Biological Diversity. Nairobi Kenya: UNEP.

OCR for page 115
Page 213 Global Diversity of Insects: The Problems of Estimating Numbers. Ebbe S. Nielsen Laurence A. Mound Australian National Insect Collection, CSIRO Entomology, GPO Box 1700, Canberra ACT 2601, Australia 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

OCR for page 115
Page 214 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. TABLE 1 Our Estimates of Numbers of Named and Living Species of Insects Order Estimated Total Named Estimated Total Species Collembola 7,213 50,000+ Protura 300 1,000 Diplura 659 1,500 Archaeognatha 300 1,000 Thysanura 370 500 Ephemeroptera 2,000 4,000 Odonata 4,870 5,500 Plecoptera 2,000 3,000 Blattodea 4,000 5,000 Isoptera 1,900 2,300 Mantodea 1,600 2,000 Grylloblattodea 20 30 Dermaptera 1,300 3,000 Orthoptera 12,500 20,000 Phasmatodea 2,500 3,000 Embioptera 200 2,000 Zoraptera 30 50 Psocoptera 3,500 5,000 Phthiraptera 3,000 5,000 Hemiptera 85,600 190,000 Thysanoptera 5,000 10,000 Megaloptera 300 500 Raphidioptera 200 200 Neuroptera 5,000 7,000 Coleoptera 350,000 850,000 Strepsiptera 530 700 Mecoptera 500 700 Siphonaptera 2,200 2,500 Diptera 99,000 150,000+ Trichoptera 7,000 12,000 Lepidoptera 146,500 400,000 Hymenoptera 115,000 230,000+ TOTALS ca 865,000 ca 2,000,000+

OCR for page 115
Page 215 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.

OCR for page 115
Page 216 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 estimates—such 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

OCR for page 115
Page 217 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.

OCR for page 115
Page 218 TABLE 2 Various Authors' Inventories of the Insect Orders Order Reference Comments Collembola Hopkins 1996 Janssens 1997 Estimated more than 50,000 species worldwide. Number of currently described species is considered to be 7,213. Protura Imadate 1991 Tuxen 1964 About 500 species have been described worldwide. Only 260 were included in Tuxen's catalog. No estimate is available of the possible worldwide total. Diplura Conde and Pages 1991 Arnett 1993 Estimated that this group has about 800 species worldwide. Arnett estimated 659 described species. Archaeognatha Watson and Smith 1991 Arnett 1993 Stated that this order includes about 350 species. Arnett estimated about 250 species but indicated that many more probably remain to be discovered. Thysanura Smith and Watson 1991 About 370 species are known; this figure presumably does not included any estimate of undescribed species. Ephemeroptera Arnett 1993 Approximately 2,000 species have been described; no estimate of potential fauna worldwide is available. Odonata Arnett 1993 This order has 4,870 known species. Because of the intensity with which they have been collected, the group is not likely to be much larger. Plecoptera Arnett 1993 Theischinger 1991 Estimated the number of described species to be about 1,550. Theischinger estimates the number to be slightly more than 2,000. No estimate of the potential extent worldwide is available. Blattodea Roth 1991 About 4,000 species of cockroaches are known worldwide. Isotera Arnett 1993 Watson and Gay 1991 About 1,900 species of termites are cataloged. Estimated 2,300 worldwide; this presumably includes an estimate of undescribed species known then. Mantodea Arnett 1993 Balderson 1991 Estimated 1,500 known mantid species. Estimated 1,800 known species. Grylloblattodea Storozhenko 1986 About 20 known species in this curious Northern-hemispheric group. Dermaptera Arnett 1993 Rentz 1991 Estimated about 1,100 known species of earwigs. Said that 1,800 species had been described. Orthoptera Rentz 1991 Arnett 1993 More than 20,000 known species in this major group. Estimated 12,500 species. Phasmatodea Key 1991 Estimated of 2,500 species is possibly an underestimate of worldwide fauna.     continues (table continued on next page)

OCR for page 115
Page 219 TABLE 2 Continued Order Reference Comments Embioptera Ross 1991 Ross 1995 Fewer than 200 species have been described, but estimates are that as many as 2,000 species exist. Provides a worldwide list of described species on a web site. Zoraptera Smithers 1991 About 30 species have been described. Psocoptera Smithers 1996 About 3,000 species worldwide have been described. Phthiraptera Palma and Barker 1996 More than 3,000 species have been described, but a considerable number of species probably remain undescribed. Heteroptera C.W. Schaefer (pers. comm.). Estimated about 37,000 described and 24,500 undescribed species of Hemiptera-Heteroptera exist. Homoptera Hodkinson and Casson 1991 Estimated grand total of 48,660 described species. Extrapolated estimate of total worldwide fauna in Hemiptera and Homoptera combined is about 190,000 species. Thysanoptera Mound manuscript catalog About 6,880 species are named, but this is reduced by known and suspected synonymy to about 5,000 valid species. Total fauna worldwide is possibly twice this, but sampling in tropical areas of high diversity remains inadequate for any serious estimate. Megaloptera Theischinger 1991 About 300 species have been described worldwide. Raphidioptera Aspöck and Aspöck 1991 Number of species does not exceed 200, most of which have been described. Neuroptera New 1991 Includes slightly more than 5,000 described species. Coleoptera Arnett 1993 Lawrence and Britton 1994 Lawrence 1991 Stated that approximately 290,000 species of beetles had been described. Estimated 350,000 named species. Stated that Australian fauna includes 20,000 described species of beetles; another 10,000 species likely exist. If this ratio between named and total known species is extrapolated worldwide, this would include more than 500,000 species.   Hammond 1992, Hammond 1994 Hammond (1992) estimated about 400,000 described species and a total fauna of 2.3 million and 866,667 species (Hammond 1994). We consider 850,000 species to be a reasonable estimated, because we believe that the proportion of described species in Australia is possibly higher than it is in parts of the wet tropics.     continues (table continued on next page)

OCR for page 115
Page 220 TABLE 2 Continued Order Reference Comments Strepsiptera Kathirithamby 1991 532 species have been described. Mecoptera Byers 1991 Penny 1995 About 500 species have been described. Maintains a worldwide list on the web. Siphonaptera Dunnet and Mardon 1991 By 1985, a total of 2,380 species and subspecies of fleas had been described. Diptera Arnett 1993 Colless and McAlpine 1991 98,500 species of flies have been described. Indicated that if undescribed species are included, this order is likely to include at least 150,000 species. Trichoptera Neboiss 1991 Morse 1997 More than 7,000 species have been described but since tropical faunas generally have been sampled poorly, the worldwide total is likely to be considerably larger. Maintains a searchable list of worldwide species on a web site. Lepidoptera Heppner 1991, Hammond 1992 N.P. Kristensen (1992, unpubl. ms., “Lepidoptera of the World. Status and Perspectives on the Inventory of a Major Insect Order.” Concluded that 146,277 species have been named; this is close to Hammond's estimate of 150,000 species. Estimated that the total fauna ranges from more than 250,000 to fewer than 1 million species. A number of published estimates fall within the range of 360,000 to 500,000 species. Hymenoptera Gaston 1993 Estimated 115,000 described species after personal contact with many of the world's most experienced specialists. The number of living species is unlikely to be less than 2 times this number and, given the relatively low effort in taxonomy in tropical countries, could be considerably more than 2 times this number. Acknowledgments 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. References Arnett RH. 1993. American Insects. A handbook of the insects of America north of Mexico. Gainesville: Sandhill Crane Pr. 850 p. Aspöck H. Aspöck U. 1991. Raphidioptera (Snake-flies, camelneck-flies). In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ. 1991. (eds). The insects of Australia. 2nd ed. Carlton: Melbourne Univ Pr. Balderson J. 1991. Mantodea (praying mantids). In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ. 1991. (eds). The insects of Australia. 2nd ed. Carlton: Melbourne Univ Pr.

OCR for page 115
Page 221 Bayers GW. 1991. Mecoptera (scorpion-flies, hanging-flies). In: Naumann ID, Carne, PB, Lawrence, JF, Nielsen, ES, Spradbery, JP, Taylor, RW, Whitten, MJ, Littlehohn, MJ.1991. (eds.). The Insects of Australia. 2nd ed. Carlton: Melbourne University Press. Colless DH, McAlpine DK, 1991. Diptera (flies). In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ. 1991. (eds). The insects of Australia. 2nd ed. Carlton; Melbourne Univ Pr. Condé B, Pagés J. 1991. Diplura. In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ. 1991. (eds). The insects of Australia. 2nd ed. Carlton: Melbourne Univ Pr. Erwin TL. 1982. Tropical forests: their richness in Coleoptera and other arthropod species. Coleopt Bull 36:74—5. Evenhuis NL (ed) 1989. Catalog of the Diptera of the Australian and Oceanian regions. Honolulu: Bishop Museum. Dunnet GM, Mardon DK. 1991. Siphonaptera (fleas). In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ. 1991. (eds). The insects of Australia. 2nd ed. Carlton: Melbourne Univ Pr. Gaston KJ. 1991a. The magnitude of global insect species richness. Cons Biol 5:283–96. Gaston KJ. 1991b. Estimates of the near-imponderable: a reply to Erwin. Cons Biol 5:564–6. Gaston KJ. 1993. Spatial patterns in the description and richness of the Hymenoptera. In: LaSalle J, Gauld ID (eds). Hymenoptera and biodiversity. Wallingford UK:CAB International, p 277–93. Gaston KJ. 1994. Spatial patterns of species description: how is our knowledge of the global insect fauna growing? Biolog Conserv 67:37–40. Hammond P. 1992. Species inventory. In: Groombridge B (ed). Global biodiversity, status of the earth's living resources New York NY: Chapman & Hall. p 17–39. Hammond P. 1994. Practical approaches to the estimation of the extent of biodiversity in species groups. Philos Trans Roy Soc London B 345:119–36. Hawksworth DL, Kalin-Arroyo MT. 1995. Magnitude and distribution of biodiversity. In: Heywood VH (ed). Global biodiversity assessment. Cambridge UK: Cambridge Univ Pr. p 107–91. Heppner JB. 1991. Faunal regions and their diversity of Lepidoptera. Tropical Lepidoptera 2, Supplement 1. Hodkinson ID, Casson D. 1991. A lesser predilection for bugs: Hemiptera (Insecta) diversity in tropical rain forests. Bio J Linnean Soc 43:101–9. Hopkins SP. 1996. Biology of the springtails. Insects: Collembola. Cambridge UK: Cambridge Univ Pr. Imadaté G. 1991. Protura. In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ. 1991. (eds). The insects of Australia. 2nd edition. Carlton: Melbourne Univ Pr. Janssens Fl. 1997. Web site address: http://www.geocities.com/CapeCanaveral/Lab/1300/2 Kathirithamby J. 1991. Strepsiptera. In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ. 1991. (eds). The insects of Australia. 2nd ed. Carlton: Melbourne Univ Pr. Key KHL. 1991. Phasmatodea (stick-insects). In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ. 1991. (eds). The insects of Australia. 2nd ed. Carlton: Melbourne Univ Pr. Kitching R. 1990. The science show. Australian Broadcasting Corporation (28 July 1990). Kristensen NP. unpublished. Lepidoptera of the world. Status and perspectives on the inventory of a major insect order. Lawrence JF, Britton EB. 1991. Coleoptera (beetles). In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ. 1991. (eds). The insects of Australia. 2nd ed. Carlton: Melbourne Univ Pr. Lawrence JF, Britton EB. 1994. Australian beetles. Melbourne Univ Pr. Longino JT. 1994. How to measure arthropod diversity in a tropical rainforest. Bio Intl 28:3–13. May RM. 1990. How many species? Philos Trans Roy Soc Lond (B) 330:293–304. Morse JC. 1997. http://biowww.clemson.edu/ento/databases/trichoptera/trichintro.html. Mound LA. 1998. Insect taxonomy in species-rich countries: the way forward? An Soci Entomol Brasil 27:l–8. Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ. 1991. (eds). The insects of Australia. 2nd ed. Carlton: Melbourne Univ Pr.

OCR for page 115
Page 222 New TR. 1991. Neuroptera (lacewings). In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ. 1991. (eds). The insects of Australia. 2nd ed. Carlton: Melbourne Univ Pr. Nielsen ES, Edwards ED, Rangsi TV (eds). 1996. Checklist of the Lepidoptera of Australia. Monogr Austral Lepidop 4:1–529. Nielsen EB, West JG. 1994. Biodiversity research and biological collections: transfer of information. Syste Asso Spec Vol 50:101–21. Palma RL, Barker SC. 1996. Phthiraptera. In: Wells A (ed). Zoological catalogue of Australia. Vol 26, Psocoptera, Phthiraptera, Thysanoptera. Melbourne: CSIRO Publishing, p 81–247, 333–61 (App. I–IV), 373–96 (Index). Penny ND. 1995. gopher://CAS.calacademy.org:70/00/depts/ent/mecolist Recher HF, Majer J. 1996. One humble gum tree; home to 1000 species. Geo Austral 18:20–9. Rentz DCF. 1991. Orthoptera (grasshoppers, locusts, katydids, crickets). In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ. 1991. (eds). The insects of Australia. 2nd ed. Carlton: Melbourne Univ Pr. Rentz DCF, Kevan DKM. 1991. Dermaptera (earwigs). In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ. 1991. (eds). The insects of Australia. 2nd ed. Carlton: Melbourne Univ Pr. Robinson GS, Nielsen ES. 1989. Tineid genera of Australia. Monogr on Austral Lepidop 2:1–344. Ross ES. 1991. Embiotera, Embiidina (Embiids, web-spinners, foot-spinners). In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ. 1991. (eds). The insects of Australia. 2nd ed. Carlton: Melbourne Univ Pr. Ross ES. 1995. gopher://CAS.calacademy.org:70/00/depts/ent/embilist Roth LM. 1991. Blattodea blattaria (cockroaches). In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ. 1991. (eds). The insects of Australia. 2nd ed. Carlton: Melbourne Univ Pr. Scoble MJ (ed). 1999. Geometrid moths of the world: a catalogue (Lepidoptera, Geometridae). Melbourne: CSIRO Publishing. Smith GB, Watson JAL. 1991. Thysanura Zygentoma (Silverfish). In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ. 1991. (eds). The insects of Australia. 2nd ed. Carlton: Melbourne Univ Pr. Smithers CN. 1991. Zoraptera. In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ. 1991. (eds). The insects of Australia. 2nd edition. Carlton: Melbourne Univ Pr. Smithers CN. 1996. Psocoptera. In: Wells A (ed). Zoological catalogue of Australia. Vol 26, Psocoptera, Phthiraptera, Thysanoptera. Melbourne: CSIRO Publishing, Australia, p 1–79, 363–72 (index). Stork NE. 1988. Insect diversity: fact, fiction and speculation. Bio J Linnaean Soc 35:321–37. Stork NE. 1993. How many species are there? Biod Cons 2:215–32. Storozhenko S. 1986. The annotated catalogue of living Grylloblattida (Insecta). Articulata 2:279–92. Theischinger G. 1991a. Plectopetra (stoneflies). In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ. 1991. (eds). The insects of Australia. 2nd ed. Carlton: Melbourne Univ Pr. Theischinger G. 1991b. Megaloptera (alderflies, dobsonflies). In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ. 1991. (eds). The insects of Australia. 2nd ed. Carlton: Melbourne Univ Pr. Tuxen SL. 1964. The Protura. A revision of the species of the world, with keys for determination. Paris: Hermann. 360 p. Vane-Wright RI. 1992. Species concepts. In: Groombridge B (ed). Global biodiversity: status of the Earth's living resources. New York NY: Chapman & Hall. p.13–6 Watson JAL, Gay FJ. 1991. Isoptera (termites). In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ. 1991. (eds). The insects of Australia. 2nd ed. Carlton: Melbourne Univ Pr. Watson JAL, Smith GB. 1991. Archaeognatha microcoryphia (bristletails). In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ. 1991. (eds). The insects of Australia. 2nd ed. Carlton: Melbourne Univ Pr. Wilson EO. 1985. The biological diversity crisis: a challenge to science. Iss Sci Tech 2:20–9. White MJD. 1982. Karyotypes and meiosis of the morabine grasshoppers. IV. The genus Gecomima. Aust J Zool 30:1027–34.