By Wim Kimmerer, San Francisco State University,
22 November 2011
This section discusses changes in the zooplankton that have occurred over the past four decades and how these changes may influence the population status of delta smelt, listed anadromous fishes, and other species of concern. Of these species only delta smelt feeds mainly on zooplankton and remains within the upper estuary throughout its life cycle. Therefore this section addresses zooplankton as a key element of the food web throughout the estuary, while focusing on details in delta smelt habitat, particularly brackish water (the “low-salinity zone”), during summer and fall.
Considerable data are available to support this summary. The long-term monitoring program run by the Interagency Ecological Program (IEP) has sampled and identified zooplankton regularly since 1972 in the delta and Suisun Bay (“upper estuary”) and in most of those years in San Pablo Bay (Winder and Jassby 2011). Additional sampling has occurred since 1995 as part of a spring survey of young delta smelt, and recently zoo-plankton sampling has been added to other fish surveys. Numerous research projects have examined zooplankton, including several investigations of zooplankton abundance and species composition in San Pablo to South Bay (Ambler et al. 1985, Bollens et al. 2011, Kimmerer et al. in preparation) and studies of processes such as tidally oriented vertical migration, feeding, predation by fish and clams, and population dynamics (e.g., Kimmerer et al. 1994, 1998, 2005, Hooff and Bollens 2004, Kimmerer 2006, Bouley and Kimmerer 2006, Gould and Kimmerer 2010, Bollens et al. 2011).
Zooplankton live in a moving frame of reference. Their swimming
1 The committee thanks Professor Wim Kimmerer for providing this material.
ability is limited by their small size; while they can migrate vertically on a diurnal or tidal cycle, they cannot swim against tidal currents, but rather they move passively with horizontal movements of water. Therefore it is often better to sample zooplankton and characterize their habitat according to salinity rather than location (Laprise and Dodson 1993). This way of looking at zooplankton is helpful when analyzing the food supply of delta smelt, which also move with the water.
The long-term data show several periods of substantial change in the last 38 years. Many species or groups of species are now at much lower population levels than they were when monitoring started. Declines have occurred throughout the estuary, except possibly Central Bay, but have been most severe in the freshwater delta and the low-salinity zone.
From 1972 through 1986 the zooplankton species composition of the upper estuary was stable except for the introductions of three species of copepod from Asia (Orsi and Mecum 1986). The introduction and subsequent spread of the overbite clam in 1987 caused an immense disruption of the food web in brackish to saline waters between San Pablo Bay and the west-central delta, and several zooplankton species declined sharply (Kimmerer et al. 1994, Kimmerer and Orsi 1996, Orsi and Mecum 1996). Between 1988 and 1994 a series of additional introductions essentially filled in the gap in the summer food web left by the earlier declines (Kimmerer and Orsi 1996, Orsi and Ohtsuka 1999). Since 1994 the food web has seen no further major introductions, yet some declines continue, and most of the species in the low-salinity zone are introduced (Orsi and Ohtsuka 1999, Winder and Jassby 2011).
Most of the introduced species probably arrived in ballast water, although Winder et al. (2011) reported that droughts may have facilitated the spread of some introduced species. Regulations requiring exchange of ballast water at sea since 2000 seem to have reduced the frequency of invasions. A study conducted in 2002-2003 found some potential invaders in ballast water of ships entering the estuary, but their numbers were low and in some cases their condition was poor, suggesting that they were unlikely to overcome the rigors of their new habitat to establish new populations (Choi et al. 2005). The lack of invasions could also be a matter of chance, since a successful invasion requires several coincident conditions that may be met only infrequently (Choi and Kimmerer 2009).
Many of the changes discussed above occurred within the low-salinity habitat of juvenile delta smelt (Bennett 2005). The overbite clam clearly had a substantial effect through grazing on phytoplankton, resulting in poor feeding conditions for some zooplankton. The clam also consumes larval stages of some zooplankton (Kimmerer et al. 1994). The zooplankton species introduced after the clam became abundant have had several advantages over the previously abundant species. First, anchovies abandoned this
region of the estuary, probably because of poor food conditions compared to higher salinity, which removed a significant consumer of plankton from this region (Kimmerer 2006). Second, each of these species has mechanisms for counteracting the effects of clam grazing; for example, one species (Limnoithona tetraspina) is very small, making it less vulnerable than other species to predation by fish, and it eats ciliates and other microzooplankton rather than phytoplankton (Bouley and Kimmerer 2006). Notably, Pseudodiaptomus forbesi is most abundant in freshwater, where the overbite clam is absent, and its population in brackish water is subsidized by movement from the freshwater population center, offsetting losses to clams and other consumers (Durand, 2010).
Causes of the declines in abundance likely differ by region within the estuary, and some may never be identified. However, the abrupt changes in the zooplankton in brackish water in the mid- to late 1980s was very likely due to the establishment of the overbite clam (Kimmerer et al. 1994). A more recent decline in Pseudodiaptomus forbesi may be due to competition with the highly abundant but small Limnoithona tetraspina. This is worrisome because the latter does not provide as valuable a food resource to small fish as does Pseudodiaptomus forbesi (L. Sullivan, SFSU, personal communication). The long-term decline in phytoplankton biomass and changes in size and species composition (Lehman 2000, Kimmerer 2005, Kimmerer et al. (2012) have also limited the food supply for zooplankton.
Today, growth of delta smelt in their summer-fall low-salinity habitat is probably limited by the low abundance of suitable zooplankton species there (Bennett 2005, Kimmerer 2008). Zooplankton growth and reproductive rates are also low, indicating that their food supply is limited (Kimmerer et al. 2005, unpublished). At such a low level of growth and reproduction, these populations can support only a very low level of consumption by fish such as delta smelt.
The situation in the freshwater delta is somewhat similar to that in the low-salinity zone. Although the food available to zooplankton is more abundant in freshwater, some species have declined over the years and are now much less abundant than formerly. Some species may be harmed by blooms of freshwater cyanobacteria (“blue-green algae”), which have become prominent in the past decade (Lehman et al. 2005), or by various toxic substances. In areas of higher salinity including San Pablo and San Francisco bays, zooplankton appear to be more abundant than in low salinity, but still less so than in many other estuaries.
One component of the zooplankton that has only recently been examined is microzooplankton such as ciliate protozoa. These organisms are the second most important consumers of phytoplankton after clams, and the most important food for many larger zooplankton (Murrell and Hollibaugh 1998, Bouley and Kimmerer 2006, Gifford et al. 2007, York et al. 2010,
Rollwagen-Bollens et al. 2011). All of the copepods consumed by delta smelt rely on microzooplankton for most of their food. The abundance and species composition of microzooplankton is highly variable, so monitoring of their abundance is essential for interpreting changes in the larger zoo-plankton fed on by fish.
Opportunities to reverse the declines in zooplankton are severely limited, at least with our current knowledge of their ecology. Producing more food for them is impracticable because adding more phytoplankton to the system would probably just produce more clams. There may be opportunities to enhance populations of some zooplankton through manipulations of freshwater flow, and control of nutrient inputs to the delta may improve growth conditions for phytoplankton and reduce the frequency of harmful algal blooms. These are active areas of research which will help to clarify the potential responses to these changes.
Significant gaps in the available information limit our understanding of zooplankton. First, most of the sampling by the zooplankton monitoring program has focused on the delta and Suisun Bay, with limited sampling in San Pablo Bay and none in San Francisco Bay. Because zooplankton move with the water, during high freshwater flows their populations move seaward, and the monitoring misses the bulk of these populations. Thus, the potentially important influence of freshwater flow on the zooplankton is known only from low to moderate flows.
Another gap is the lack of information on important changes in the more seaward reaches of the estuary, such as the potential response of zoo-plankton in South San Francisco Bay to a recent upsurge in production of algal food. We also lack a system for detecting new and potentially harmful introductions, and neither the rate of arrival of organisms in ballast nor the efficacy of ballast exchange in removing organisms is being monitored.
The third gap is a complete lack of routine monitoring for microzoo-plankton and bacteria. The current monitoring program was begun in the late 1960s under a conceptual model for planktonic food webs that is now outdated. The key role of microzooplankton in the planktonic food web, well known from other marine and estuarine locations, has been established for the San Francisco Estuary by several researchers. Bacteria are sometimes as important in the food web as phytoplankton, but only a few short-term studies have examined the roles of bacteria in the estuary. An expansion of the monitoring program to include these key components is long overdue.
The existing zooplankton monitoring program is very well run and, after a great deal of work, the database is in excellent condition. However, the other programs that monitor zooplankton are not well coordinated with the core program, and none of the data from any of these programs is readily available online. Thus, there are several opportunities to update
and improve the existing programs to make them more useful and relevant to our current understanding.
Despite the gaps discussed above, the knowledge of zooplankton in this estuary is considerable. This body of knowledge has benefited from the valuable data from the consistent, long-term monitoring program, put in place 40 years ago by agency scientists who clearly had an ecosystem-level perspective.
Ambler, J. W., J. E. Cloern, and A. Hutchinson. 1985. Seasonal cycles of zooplankton from San Francisco Bay. Hydrobiologia 129:177-197.
Bennett, W. A. 2005. Critical assessment of the delta smelt population in the San Francisco Estuary, California. San Francisco Estuary and Watershed Science 3(2):Article 1.
Bollens, S. M., G. Rollwagen-Bollens, J. A. Quenette, and A. B. Bochdansky. 2011. Cascading migrations and implications for vertical fluxes in pelagic ecosystems. Journal of Plankton Research 33:349-355.
Bouley, P., and W. J. Kimmerer. 2006. Ecology of a highly abundant, introduced cyclopoid copepod in a temperate estuary. Marine Ecology Progress Series 324:219-228.
Choi, K.-H., and W. J. Kimmerer. 2009. Mating success and its consequences for population growth of an estuarine copepod. Marine Ecology Progress Series 377:183-191.
Choi, K. H., W. Kimmerer, G. Smith, G. M. Ruiz, and K. Lion. 2005. Post-exchange zooplankton in ballast water of ships entering the San Francisco Estuary. Journal of Plankton Research 27:707-714.
Durand, J.R. 2010. Determinants of seasonal abundance in key zooplankton of the San Francisco Estuary. MS Thesis, San Francisco State University. 55 pp.
Gifford, S. M., G. C. Rollwagen-Bollens, and S. M. Bollens. 2007. Mesozooplankton omnivory in the upper San Francisco Estuary. Marine Ecology Progress Series 348:33-46.
Gould, A. L., and W. J. Kimmerer. 2010. Development, growth, and reproduction of the cyclopoid copepod Limnoithona tetraspina in the upper San Francisco Estuary. Marine Ecology Progress Series 412:163-177.
Hooff, R. C., and S. M. Bollens. 2004. Functional response and potential predatory impact of Tortanus dextrilobatus, a carnivorous copepod recently introduced to the San Francisco Estuary. Marine Ecology Progress Series 277:167-179.
Kimmerer, W. J. 2005. Long-term changes in apparent uptake of silica in the San Francisco estuary. Limnology and Oceanography 50:793-798.
Kimmerer, W. J. 2006. Response of anchovies dampens effects of the invasive bivalve Corbula amurensis on the San Francisco Estuary foodweb. Marine Ecology Progress Series 324:207-218.
Kimmerer, W. J. 2008. Losses of Sacramento River Chinook salmon and delta smelt to entrainment in water diversions in the Sacramento-San Joaquin Delta. San Francisco Estuary and Watershed Science 6(2):Article 2.
Kimmerer, W. J., J. R. Burau, and W. A. Bennett. 1998. Tidally-oriented vertical migration and position maintenance of zooplankton in a temperate estuary. Limnology and Oceanography 43: 1697-1709.
Kimmerer, W. J., E. Gartside, and J. J. Orsi. 1994. Predation by an introduced clam as the probable cause of substantial declines in zooplankton in San Francisco Bay. Marine Ecology Progress Series 113:81-93.
Kimmerer, W. J., M. H. Nicolini, N. Ferm, and C. Peñalva. 2005. Chronic food limitation of egg production in populations of copepods of the genus Acartia in the San Francisco Estuary. Estuaries 28:541-550.
Kimmerer, W. J., and J. J. Orsi. 1996. Causes of long-term declines in zooplankton in the San Francisco Bay estuary since 1987, p. 403-424. In J. T. Hollibaugh [ed.], San Francisco Bay: The Ecosystem. AAAS.
Kimmerer, W. J., A. E. Parker, U. Lidström, and E. J. Carpenter. 2012. Short-term and interannual variability in primary production in the low-salinity zone of the San Francisco Estuary. Estuaries and Coasts 35:913-929.
Laprise, R., and J. J. Dodson. 1993. Nature of environmental variability experienced by benthic and pelagic animals in the St. Lawrence Estuary, Canada. Marine Ecology Progress Series 94:129-139.
Lehman, P. W. 2000. The influence of climate on phytoplankton community biomass in San Francisco Bay Estuary. Limnology and Oceanography 45:580-590.
Lehman, P. W., G. Boyer, C. Hall, S. Waller, and K. Gehrts. 2005. Distribution and toxicity of a new colonial Microcystis aeruginosa bloom in the San Francisco Bay Estuary, California. Hydrobiologia 541:87-99.
Murrell, M. C., and J. T. Hollibaugh. 1998. Microzooplankton grazing in northern San Francisco Bay measured by the dilution method. Aquatic Microbial Ecology 15:53-63.
Orsi, J., and W. Mecum. 1986. Zooplankton distribution and abundance in the Sacramento-San Joaquin Delta in relation to certain environmental factors. Estuaries 9:326-339.
Orsi, J. J., and W. L. Mecum. 1996. Food limitation as the probable cause of a long-term decline in the abundance of Neomysis mercedis the opossum shrimp in the Sacramento-San Joaquin estuary. Pp. 375-401 in San Francisco Bay: The Ecosystem, edited by J. T. Hollibaugh. AAAS.
Orsi, J. J., and S. Ohtsuka. 1999. Introduction of the Asian copepods Acartiella sinensis, Tortanus dextrilobatus (Copepoda: Calanoida), and Limnoithona tetraspina (Copepoda: Cyclopoida) to the San Francisco Estuary, California, USA. Plankton Biology and Ecology 46:128-131.
Rollwagen-Bollens, G., S. Gifford, and S. M. Bollens. 2011. The role of protistan microzooplankton in the Upper San Francisco Estuary planktonic food web: Source or sink? Estuaries and Coasts 34:1026-1038.
Winder, M., and A. D. Jassby. 2011. Shifts in zooplankton community structure: Implications for food web processes in the upper San Francisco Estuary. Estuaries and Coasts 34:675-690.
Winder, M., A. D. Jassby, and R. Mac Nally. 2011. Synergies between climate anomalies and hydrological modifications facilitate estuarine biotic invasions. Ecology Letters 14(8):749-757.
York, J., B. Costas, and G. Mcmanus. 2010. Microzooplankton grazing in green water—results from two contrasting estuaries. Estuaries and Coasts 34:373-385.