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Appendix E
Changes in the Zooplankton of
the San Francisco Estuary1
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 popu-
lation 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.
231
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232 SUSTAINABLE WATER MANAGEMENT IN THE DELTA
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 subse-
quent 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, al-
though 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 inva-
sions. 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 advan-
tages over the previously abundant species. First, anchovies abandoned this
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APPENDIX E 233
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, Pseudo-
diaptomus 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 competi-
tion 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 reproduc-
tive 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 salin-
ity, but still less so than in many other estuaries.
One component of the zooplankton that has only recently been exam-
ined 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,
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234 SUSTAINABLE WATER MANAGEMENT IN THE DELTA
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 lim-
ited, 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 opportuni-
ties 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
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APPENDIX E 235
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.
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