Estuaries are highly dynamic aquatic systems in boththe horizontal and vertical dimensions, where salinityand current speed may vary substantially on an hourly,daily, annual and interannual basis. Moreover, temper-ate estuaries experience a wide range of precipitationand riverine inputs, leading to significant seasonal
variability in the vertical salinity gradient. A key ques-tion for estuarine ecology is therefore the degree towhich variability in the physical environment, in addi-tion to biological factors, may affect the vertical distri-bution of planktonic organisms.
Changes in plankton vertical distribution inresponse to environmental stimuli have primarily beenexamined among meso- and macrozooplankton (or-
Vertical distribution of micro- and nanoplanktonin the San Francisco Estuary in relation to
hydrography and predators
Gretchen C. Rollwagen-Bollens1,*, Stephen M. Bollens1, Deborah L. Penry2
1School of Biological Sciences, Washington State University Vancouver, 14204 NE Salmon Creek Avenue, Vancouver,Washington 98686, USA
2Department of Integrative Biology, University of California at Berkeley, Berkeley, California 94720, USA
ABSTRACT: Temperate estuaries are characterized by significant seasonal variability in the verticalsalinity gradient, which, along with biological factors, may play a role in determining plankton ver-tical distribution. We examined the vertical distribution of microplankton (20 to 200 µm) andnanoplankton (~5 to 20 µm) in the San Francisco Estuary (SFE) over diel, seasonal and interannualtime scales, and assessed the degree to which abiotic (hydrography) and biotic (predation) factorsinfluenced these patterns. We sampled 2 hydrographically-distinct locations within the SFE: SanPablo Bay, a partially-mixed estuary, and South Bay, a lagoonal estuary. We conducted replicateNiskin bottle casts during the day and night at each location on 6 occasions between 1998 and1999. We also conducted replicate day and night pump sampling for mesozooplankton (>153 µm)on 4 of these dates. The vertical distribution of micro- and nanoplankton was often homogeneouswith depth, even under substantially different hydrographic conditions. ANOVA testing ofweighted mean depths (WMD) of chlorophyll, major taxa of micro- and nanoplankton, and cope-pods (factors: location, year, season, time of day) revealed that only the microplankton taxa (specifi-cally ciliates) showed significant differences in vertical distribution over the sampling period. Themost significant differences in WMD were observed seasonally. Ciliates and copepods (Acartiaspp.) showed significant diel differences in WMD on several occasions, but diel differences wererarely observed among other micro- and nanoplankton. The degree of salinity stratification wasnever correlated to WMD of any micro- or nanoplankton group, however vertical distributions ofheterotrophic loricate and aloricate ciliates and dinoflagellates were often significantly correlatedwith distributions of chlorophyll and autotrophic nanoflagellates (presumed food), as well as withthe vertical distributions of Acartia spp (presumed predators). We conclude that micro- andnanoplankton are often relatively homogeneously distributed with respect to depth in the SFE.However, when micro- and nanoplankton distributions were more heterogeneous, biotic factors hada greater influence on vertical distribution than abiotic factors (stratification) in the SFE.
KEY WORDS: Vertical distribution · Microzooplankton · Ciliates · Flagellate · Nanoplankton ·Copepods · Estuaries · San Francisco Bay · Stratification
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Aquat Microb Ecol 44: 143–163, 2006
ganisms >200 µm in size), in particular copepods. Dielvertical migration behavior has been observed in manycopepod taxa, as a response to light (e.g. Stearns &Forward 1984), to avoid visual predators (e.g. Bollens &Frost 1989), to exploit food resources (e.g. Uchima &Hirano 1988), or to maintain position within a largeestuary (e.g. Laprise & Dodson 1994). However, muchless is known about the factors influencing the verticaldistribution of microplankton (20 to 200 µm) ornanoplankton (2 to 20 µm), especially in estuaries.
Ciliated protozoans dominate estuarine microplankton(Porter et al. 1985, Revelante & Gilmartin 1990, Pierce &Turner 1992, G. C. Rollwagen-Bollens & D. L. Penry un-publ.). Recent studies have demonstrated that somemarine ciliate species are capable of limited vertical mi-gration (Dale 1987, Jonsson 1989, Perez et al. 2000). Forexample, the swimming speed of the mixotrophic alori-cate ciliate Myrionecta rubra (= Mesodinium rubrum) isas high as 8.5 mm s–1 (Lindholm 1985, Jonsson & Tiselius1990), and this species also migrates vertically (Smith etal. 1979, Dale 1987, Figueroa et al. 1998). Motile flagel-lates are abundant nanoplankton taxa in estuaries(Porter et al. 1985, Dolan & Coats 1990, G. C. RollwagenBollens & D. L. Penry unpubl.). Thus, in addition to pas-sive shifts in vertical distribution due to mixing or otherphysical conditions, many estuarine micro- andnanoplankton taxa may have the ability to activelychange their position in the water column in response toabiotic and biotic factors.
The San Francisco Estuary (SFE) is one of the largesttemperate estuaries in North America and an impor-tant habitat for a wide range of fish and invertebratespecies. The SFE is also shallow (mean depth 6 m),such that benthic suspension feeders may consume asubstantial proportion of planktonic production (Clo-ern 1982, Jassby et al. 2002). Water column hydrogra-phy (e.g. stratification) is therefore an important phys-ical factor that affects both the abundance and verticaldistribution of plankton in the SFE. For example,during periods of strong density stratification, typicallylate winter and spring, plankton may be sequesteredinto the upper and lower water column. Those organ-isms in the upper layer have access to light and nutri-ents, and are isolated from benthic grazers, resulting atleast initially in a vertical distribution skewed towardthe surface (Cloern 1982, 1991, 1996). Biologicalfactors such as predation may also affect the verticaldistribution of micro- and nanoplankton in estuaries.In addition to benthic grazing, there is a robust community of zooplankton consumers in the SFE,most notably herbivorous and omnivorous copepods(Ambler et al. 1985, Kimmerer & Orsi 1996, Bollens etal. 2002, Purkerson et al. 2003).
Understanding the factors that influence the verticaldistribution of micro- and nanoplankton in estuaries,
and in marine systems more generally, is especiallyimportant given the significant role that these organ-isms play in the pelagic food web. Numerous fieldstudies have demonstrated that heterotrophic and/ormixotrophic ciliates, dinoflagellates and small flagel-lates <200 µm in size (i.e. ‘microzooplankton’) are themajor grazers of phytoplankton carbon in marinesystems (e.g. Landry et al. 1995, Tamigneaux et al.1997, Lessard & Murrell 1998, Suzuki et al. 2002,Landry & Calbet 2004), as well as significant bacteri-vores (Sherr & Sherr 1987, 1994, Vacqué et al. 1992,Strom 2000). Moreover, ciliates and flagellates maycomprise a significant proportion of copepod diets inboth marine and estuarine environments (Gifford &Dagg 1991, Kleppel 1992, Buskey et al. 1993, Fes-senden & Cowles 1994, Kleppel et al. 1996, Verity &Paffenhöfer 1996, Nejstgaard et al. 1997, Zeldis et al.2002, Rollwagen-Bollens & Penry 2003). Thus, micro-zooplankton often serve to connect microbial produc-tion to the larger metazoan food web.
Despite their importance in pelagic food webs, stud-ies of their distribution in estuarine systems has beenrelatively limited, particularly in the SFE. For example,a number of long term studies in the SFE have exam-ined fish populations (e.g. Stevens 1977, Armor &Herrgesell 1985, Meng et al. 1994, Gewant & Bollens2005), benthic invertebrates (e.g. Nichols 1985, Alpine& Cloern 1992), macro- and mesozooplankton (e.g.Ambler et al. 1985, Kimmerer & Orsi 1996, Bollens etal. 2002, Hooff & Bollens 2004, Gewant & Bollens2005), water quality (e.g. Smith et al. 1979, Thompsonet al. 2000), and particularly the rates of and limits onprimary productivity (e.g. Cloern et al. 1985, Cloern1987, Jassby et al. 2002). Prior to the present study andrelated projects, there had been no effort to measurethe contribution of heterotrophic protist plankton<200 µm (microzooplankton) to overall planktonicabundance and food web dynamics.
In order to address this gap, in 1997 we established a3 yr field and experimental program to assess theabundance, distribution and composition of micro-zooplankton in the saline reaches of the SFE, with themajor goal of characterizing the potential role of micro-zooplankton as trophic links between metazoans (i.e.copepods) and the microbial food web.
Our research program consisted of 3 elements. First,in order to assess the availability of potential protistprey for mesozooplankton, we measured the temporaland geographic variability in abundance, biomass andcomposition of microplankton (20 to 200 µm) andnanoplankton (~5 to 20 µm) in the lower estuary from1997 to 1999. This allowed seasonal comparisons aswell as comparisons between the strong 1997 to 1998El Niño and the 1999 La Niña event that followed. Wefound that the microplankton community was always
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dominated by heterotrophic/mixotrophic ciliate bio-mass (primarily the genera Strombidium, Tintinnopsis,Strobilidium, Codonellopsis), except during a brief, butextreme spring diatom bloom during the 1998 El Niño.In contrast, heterotrophic nanoplankton biomass(almost exclusively non-pigmented flagellates) wasconsistently much lower than the biomass of auto-trophic cells (small diatoms and pigmented flagellates)(G. C. Rollwagen-Bollens & D. L. Penry unpubl.).
Another important element of our overall researchprogram was to experimentally assess the role ofmicrozooplankton in the diet of Acartia spp. copepods,the dominant mesozooplankton consumers in thelower SFE. During incubations with Acartia spp. feed-ing upon the natural planktonic assemblage from theSFE in spring 2000, we observed that ciliates and large(15 to 20 µm) heterotrophic nanoflagellates were oftenpreferentially consumed compared to diatoms andother autotrophic prey (Rollwagen-Bollens & Penry2003). In a separate, later study Bollens & Sanders(2004) also found loricate ciliates to be a major compo-nent of the diet of larval herring in the SFE.
In this paper we present the results of the third compo-nent of the SFE field study, which had the followingobjectives: (1) to describe the vertical distribution of mi-croplankton and nanoplankton at 2 locations in the SFE,San Pablo Bay (a partially-mixed estuary) and South Bay(a lagoon-type estuary), over diel, seasonal, and interan-nual time scales, and (2) to seek possible explanations forthe observed vertical distribution patterns in relation toenvironmental conditions, both abiotic (e.g. hydro-graphy) and biotic (e.g. planktonic predators).
MATERIALS AND METHODS
Study site. The SFE is comprised of 2 hydrographi-cally distinct sub-estuaries, South Bay and San PabloBay, which connect via the Central Bay and dischargethrough the Golden Gate to the Pacific Ocean (seeFig. 1). Both bays are wide and shallow (mean depth =6 m) and are incised by a narrow, relatively deep(~12 to 15 m) channel (Conomos et al. 1985).
San Pablo Bay is the seaward embayment of thegreater North Bay/Delta system, through which theSacramento and San Joaquin rivers drain approxi-mately 40% of the land area of California. The SanFrancisco Bay area is characterized by a Mediter-ranean climate, with 2 seasons defined primarily bythe degree of precipitation: a cool, wet winter season(November through April) and a warm, occasionallyfoggy dry season (May through October). As a result,during winter and spring San Pablo Bay is a partially-mixed estuary, with high levels of freshwater inflow,along with short water residence times and high tur-
bidity. In contrast, South Bay is a lagoon-type estuarywith lower inputs of freshwater. The water column isrelatively homogeneous with respect to temperatureand salinity during much of the year, water residencetime is on the order of months and turbidity is rela-tively low (Cloern et al. 1985, Conomos et al. 1985).
In both bays, blooms of phytoplankton occur duringthe wet season, however the timing and mechanismsfor these blooms differ between the 2 locations. InSouth Bay an intense, but short-lived phytoplanktonbloom occurs each spring, when pulses of freshwater,reduced winds and neap tides combine to producestrong density stratification. Phytoplankton in the sur-face layer are isolated from benthic grazers, allowingan increase in biomass (Cloern 1982, 1987, 1991).
Prior to 1986, late spring/early summer phytoplank-ton blooms also occurred in San Pablo Bay as decreas-ing river flow into the Bay allowed algal doubling timeto exceed water residence time. Phytoplankton bio-mass decreased again in late summer due to light lim-itation, as turbidity increased during high winds andstrong tidal currents (Cloern et al. 1985). However, in1986 the Asian clam Potamocorbula amurensis wasintroduced into the SFE, and through its high filteringrate and wide salinity tolerance quickly eliminated anyphytoplankton blooms in the northern reaches of theestuary (Nichols et al. 1990). Hence, chlorophyll alevels in San Pablo Bay were consistently low throughthe 1990s (Lehman 2000). However, since 1998, ele-vated phytoplankton biomass (>5 to 10 µg chlorophylla l–1) in the San Pablo Bay channel has been observednearly every spring (Rollwagen Bollens & Penry 2003,US Geological Survey Menlo Park Water Quality web-site http://sfbay.wr.usgs.gov/access/wqdata/).
Field sampling. Micro- and nanoplankton: We sam-pled at 2 stations, 1 each in South Bay and San PabloBay (Fig. 1), using the 35-foot (11 m) RV ‘Questuary’.Both stations were located in the relatively deep (waterdepth ~12 m) channel that bisects the entire SFE.Duplicate casts, using 2.5 l Niskin bottles equippedwith external Teflon springs at 5 depths (2, 4, 6, 8,10 m), were conducted day and night at each station3 times per year between February 1998 and August1999, for a total of 6 day/night collections per station(Table 1). These collections spanned 2 yr, with 2 sets ofsamples obtained during each of 3 seasons: (1) wetseason, pre-phytoplankton bloom (December to Feb-ruary); (2) wet season, during phytoplankton bloom(March to May); and (3) dry season (June to Novem-ber). These time periods reflect the seasonality ofphytoplankton biomass in the SFE, which has beenextensively monitored and documented for >30 yr bythe Water Quality group at the US Geological SurveyMenlo Park, CA (http://sfbay.wr.usgs.gov/access/wqdata/).
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Subsamples to measure chlorophyll a concentration,and to characterize the microplankton (20 to 200 µm)and nanoplankton (~5 to 20 µm) components of theassemblage, were collected from each Niskin bottle.Subsamples (100 to 250 ml) for chlorophyll analysiswere immediately filtered onto Whatman GF/F filters.The filters were wrapped in foil, frozen, and returnedto the laboratory for fluorometric analysis (Strickland &Parsons 1972) within 2 to 4 d.
Subsamples for microplankton analysis weresiphoned from the Niskin bottles into amber Nalgenebottles pre-filled with acid Lugol’s solution (Throndsen1978) to a final concentration of 10% (Gifford 1993).Subsamples for nanoplankton analysis were similarlysiphoned into opaque Nalgene bottles pre-filled withcold gluteraldehyde, to a final concentration of 1%. Allsample bottles were kept chilled and returned to thelaboratory within 24 h of collection. Lugol’s preservedmicroplankton samples were then stored in the dark at10°C until analyzed. Duplicate 20 ml aliquots of
the gluteraldehyde-preserved nanoplankton sampleswere stained with fluorescein isothiocyanate (FITC),filtered onto 1.0 µm black polycarbonate filters, andmounted on glass slides (Sherr et al. 1993). The slideswere kept frozen at <0°C until analyzed.
Mesozooplankton: Mesozooplankton (>153 µm)were collected concurrently with micro- and nano-plankton during April and August 1998, and Marchand August 1999. Discrete mesozooplankton samplesfrom 5 depths (2, 4, 6, 8, 10 m) were obtained fromwater pumped through a 4” (10 cm) diameter hoseinto a 153 µm plankton net submerged in a 190 l con-tainer on deck. However, in August 1998 a 130 µmplankton net was used for pump sampling in SanPablo Bay. Mesozooplankton are traditionally definedas organisms >200 µm in size (Sieburth et al. 1978),however the nets available to use for this study were130 to 153 µm. This should not have affected ourresults since we excluded nauplii and specificallysorted the net samples only for copepodid and adultlife stages, which for the most abundant mesozoo-plankton taxa in the SFE were >200 µm in size. After5 min pumping at each depth, the mesozooplanktonwere rinsed into the net’s collecting bucket, trans-ferred to sample bottles, and preserved in 4%buffered formalin. Pump rates (l min–1) were mea-sured at the beginning and end of each cast andaveraged, in order to calculate the volume of waterfiltered for each sample from that cast. The volumeof water pumped during each cast averaged 0.86 ±0.02 l (data not shown).
Hydrography: Temperature and salinity profilesfrom the surface to near bottom (~10 to 11 m) wereobtained at the beginning of each Niskin bottle/pumpcast using a Seabird SBE19 CTD. The data werebinned into 0.25 m depth bins using SEASOFT soft-ware, and then averaged between the 2 replicate caststo produce mean day and night profiles of temperatureand salinity for each sampling period. Tidal stage (e.g.flood, slack, ebb) was also noted at the beginning ofeach cast.
Organism enumeration and identification. Micro-plankton: Aliquots of 25 to 50 ml from each Lugol sam-ple bottle were settled overnight in Utermöhl cham-bers, and the entire contents of the chamber between20 and 200 µm were enumerated using an invertedmicroscope at 200× magnification. In all samples, aminimum of 100 cells was counted, identified to genuswhere possible, and grouped into one of the followingmajor prey categories: loricate ciliates, Myrionectarubra (= Mesodinium rubrum) ciliates, aloricate non-Myrionecta ciliates, diatoms, or dinoflagellates.
It is difficult, and often impossible, to distinguishstrictly heterotrophic aloricate ciliates and dinoflagel-lates from mixotrophic forms in Lugol-preserved sam-
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Fig 1. San Francisco Estuary. (D) Locations where sampleswere collected in 1998 and 1999
Rollwagen-Bollens et al.: Microplankton vertical distribution in San Francisco Estuary
ples. However, in our samples the mixotrophic ciliateMyrionecta rubra was typically readily identifiable.Moreover, there exists a growing body of researchdescribing the unusual physiology and swimmingbehavior of M. rubra (e.g. Johnson & Stoecker 2005).Therefore, M. rubra were grouped into their own cate-gory, while all other naked ciliates were lumped intothe non-Myrionecta aloricate ciliate category and con-sidered heterotrophic/mixotrophic. Based on studies ofprotozoan feeding in Chesapeake Bay (Dolan 1991)and other work reviewed in Nejstgaard et al. (2001),the ciliate taxa present in the SFE are most likelyphagotrophic, ingesting bacterial, algal or flagellateprey, although some may also contain chloroplasts. Inaddition, large (>20 µm) individuals of the dinoflagel-late genera Protoperidinium and Gymnodinium(mostly G. breve) were categorized as heterotrophicsince they are documented phagotrophs (Hansen 1991and references therein).
Nanoplankton: A minimum of 100 cells between 5and 20 µm were counted from randomly selectedfields using an epifluorescence microscope at 400 to450× magnification. As the primary objective of thesecollections was to investigate protozoan–metazoan
(copepod) trophic interactions (Rollwagen-Bollens &Penry 2003, and unpubl.), only cells larger than 5 µmwere included. This is the threshold size for efficientcapture and ingestion by Acartia spp. (Nival & Nival1976), which are among the dominant copepod con-sumers in this part of the SFE (Ambler et al. 1985,Bollens et al. 2002, Purkerson et al. 2003). Nano-plankton are traditionally defined as cells 2 to 20 µmin size, and as such our analyses may have left out apotentially important component of small planktonbetween 2 and 5 µm (e.g. Kuuppo 1994). There areno published data quantifying the abundance of het-erotrophic nanoplankton <5 µm in the SFE. However,a long-term study of phytoplankton community com-position in the SFE showed that this nutrient-richestuary is dominated by large (>30 µm) cells, withcells <8 µm contributing only 4% of community bio-mass (Cloern & Dufford 2005). In addition, Cole et al.(1986) reported size fractioned chlorophyll a concen-trations that showed the <5 µm fraction to account for~30 to 40% of the chlorophyll <20 µm in both SouthBay and San Pablo Bay. Cole et al. (1986) alsoobserved that the chlorophyll biomass of phytoplank-ton cells <5 µm was low compared to that in other
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Season San Pablo Bay South BayDate Time (h) Tidal stage Date Time (h) Tidal stage
1998Wet, non-bloom Feb 20 Day 1, 14:30 Late ebb/slack Mar 2 Day 1, 15:15 Slack/early ebb
Day 2, 16:00 Slack/early flood Day 2, no castNight 1, 19:50 Late flood Night 1, 19:45 Late ebbNight 2, 21:40 Slack Night 2, 21:00 Slack
Wet, bloom Apr 13 Day 1, 15:45 Slack Apr 16 Day 1, 15:45 Late flood/slackDay 2, 16:55 Early ebb Day 2, 17:05 Slack/early ebb
Night 1, 21:20 Slack Night 1, 21:30 SlackNight 2, 22:35 Mid flood Night 2, 22:45 Early flood
Dry Aug 10 Day 1, 17:00 Slack/early ebb Aug 13 Day 1, 15:55 Late floodDay 2, 18:25 Mid ebb Day 2, 17:15 Slack
Night 1, 22:15 Slack Night 1, 21:40 Mid ebbNight 2, 23:25 Mid flood Night 2, 23:25 Late ebb
1999Wet, bloom Mar 31 Day 1, 13:50 Slack/early ebb Mar 26 Day 1, 13:30 Late ebb/slack
Day 2, 15:10 Mid ebb Day 2, 15:00 Slack/early floodNight 1, 21:00 Mid flood Night 1, 21:00 Late floodNight 2, 22:50 Mid/late flood Night 2, 21:50 Slack
Wet, non-bloom May 6 Night 1, 21:45 Mid ebb Apr 19 Day 1, 14:45 Late floodNight 2, 23:35 Late ebb Day 2, 16:20 Slack
May 7 Day 1, 13:15 Late ebb/slack Night 1, 21:00 SlackDay 2, 14:45 Early flood Night 2, 22:50 Early flood
Dry Aug 16 Night 1, 21:50 Mid ebb Aug 20 Day 1, 13:15 Late ebb/slackNight 2, 23:50 Late ebb Day 2, 14:40 Slack/early flood
Aug 17 Day 1, 13:15 Early flood Night 1, 21:20 Early ebbDay 2, 14:30 Mid flood Night 2, 22:50 Late ebb
Table 1. Dates, starting times and tidal stage of sampling in South Bay and San Pablo Bay, San Francisco Estuary, betweenFebruary 1998 and August 1999
Aquat Microb Ecol 44: 143–163, 2006
estuaries, such as the Hudson River estuary, Narra-gansett Bay and Chesapeake Bay. While this does notgive information about the heterotrophic nanoplank-ton <5 µm, it suggests that this component may alsobe low in the SFE relative to other estuaries. Cellswere grouped into 2 major categories: autotrophicnanoplankton or heterotrophic nanoplankton (basedon the presence or absence of chlorophyll autofluo-rescence within the cell).
Mesozooplankton: Preserved samples were sub-sampled with a Stempel pipette to a volume sufficientto allow enumeration of at least 300 organisms, andeach individual was identified to the most specific tax-onomic level and life history stage possible. In the caseof the genus Acartia, the SFE is characterized by agroup of subgenera and species, including Acartiurasp., Acartia tonsa, and A. californiensis. Individualswere identified as being a member of one of thesespecies. However, for the purposes of this study, allwere placed in the category Acartia spp.
Statistical analyses. In order to quantitativelydescribe the vertical distributions of chlorophyll a,micro- and nanoplankton, and mesozooplankton, wecalculated a weighted mean depth (WMD) for eachvertical profile using the following equation, modifiedfrom Bollens et al. (1993):
where i is each depth sampled, A is abundance(cells ml–1) or chlorophyll a concentration (µg l–1), andZ is the sampling depth (m). The WMDs from eachreplicate cast (n = 2) were then averaged to produce amean (+ SE) WMD for each time period. More sophis-ticated techniques for comparing 2 vertical distribu-tions, both with (Beet et al. 2003) and without (Solowet al. 2000) replication, have been recently described.However, the WMD approach allowed the calculationof a simple metric of vertical distribution that couldthen be analyzed across a number of different timeand space scales using standard analysis of variancetechniques.
We identified temporal and spatial patterns in thevertical distributions of micro- and nanoplankton byperforming multiple ANOVAs using JMP Version 5.1.2software for Macintosh on the WMD of all major taxo-nomic categories. The factors were year (levels: 1998,1999), season (levels: wet season–non-bloom, wet sea-son–bloom, dry season), time (levels: day, night) andlocation (levels: San Pablo Bay, South Bay). As an indi-cation of diel vertical migration, differences in daytimevs. nighttime WMD of the major categories of micro-and nanoplankton during each sampling period werefurther tested using Student’s t-tests, assumingunequal variance (Zar 1996).
Finally, to specifically compare the vertical distribu-tions of micro- and nanoplankton with water columnhydrography, as well as with potential predators, 2approaches were used.
First, a stratification index (ΔS) was calculated foreach cast as the difference between salinity at the sur-face and that at 10 m. Salinity stratification has beenshown to be a dominant factor affecting phytoplanktonproductivity in the SFE (e.g. Cloern et al. 1985, Jassbyet al. 2002) and the primary distinguishing physicalcharacteristic between San Pablo Bay and South Bay.Salinity stratification is also directly influenced by, e.g.tides, winds, and freshwater flow; thus, ΔS serves as aconvenient, easily measurable and statistically testablemetric of hydrography in general. The ΔS values werethen compared with the WMD of all micro- andnanoplankton categories using Pearson’s r correlationstatistic (Zar 1996) to assess the relationship of stratifi-cation and vertical distribution.
Second, we measured the potential effects of themost abundant mesozooplankton predators on micro-and nanoplankton vertical distribution, as well as thepotential of microplankton predators to influencenanoplankton distribution, by using Pearson’s r corre-lation statistic to compare the WMD of each potentialpredator population with each potential prey popula-tion.
RESULTS
The results of a 4-way ANOVA on stratification indexand weighted mean depths of chlorophyll a, micro- andnanoplankton for all sampling times and locations indi-cated that the most significant differences in hydrogra-phy and plankton vertical distribution occurred on aseasonal and to some extent diel basis, with yearly andregional differences of lesser importance (Table 2).Moreover, the ANOVA results showed differences be-tween the major categories of micro- and nanoplanktonwith respect to both time and location.
Therefore, in Figs. 2 to 5 we have presented the ver-tical distributions of each major micro- and nanoplank-ton taxonomic category by season and year in SanPablo Bay and South Bay, along with profiles of tem-perature and salinity to illustrate hydrography. Thesefigures also include profiles of Acartia spp., to illustratethe distributions of the most abundant potential meso-zooplankton predator at these sampling times andlocations. Not shown in the figures, but included in thecorrelations analyses described below, are 2 additionalcopepod taxa (Limnoithona tetraspina and Oithonadavisae) observed in these samples, but whose com-bined abundance was much lower and more variablethan that of Acartia spp.
WMD = ∑ ( )∑ ( )A Z
Ai i
i
·
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Rollwagen-Bollens et al.: Microplankton vertical distribution in San Francisco Estuary
Temporal variability in hydrography and planktonvertical distribution
Diel patterns
Hydrography. Statistically significant (p < 0.05) dif-ferences between daytime and nighttime stratificationindices (ΔS) were only occasionally observed. In SanPablo Bay, ΔS differed between day and night onlyonce, in August 1998 (Table 3). In South Bay, ΔSdiffered between day and night in April/May andAugust of both years, although in allcases except April 1998 the magnitudeof the diel difference was extremelysmall relative to the overall water col-umn salinity (Table 3).
Plankton distribution. In San PabloBay diel differences were more evi-dent in 1998 than in 1999 (Figs. 2 & 3).During all three 1998 sampling peri-ods, diatoms and/or Myrionecta rubraexhibited statistically significant dif-ferences in weighted mean depth dur-ing the day vs. night, although neitherday nor night mean depth was consis-tently shallower or deeper than theother (Fig. 2). In South Bay, significantdifferences in plankton mean depthsoccurred only once, in March 1999,and then only among heterotrophicnanoplankton and Acartia spp. (Figs. 4& 5).
The exception to the overall lack ofday–night differences in plankton verti-cal distribution was in August 1999 inboth South Bay and San Pablo Bay.Myrionecta rubra, heterotrophic dino-flagellates and heterotrophic/mixo-trophic aloricate ciliates were all distrib-uted higher in the water column duringthe day in San Pablo Bay (Fig. 3). Simi-larly M. rubra and autotrophic nano-plankton mean depths were shallowerduring the day than at night in SouthBay; however, Acartia spp. showed theopposite pattern, with a deeper meandepth during the day (Fig. 5).
Seasonal patterns
Hydrography. In both San Pablo Bayand South Bay, the stratification indexwas substantially higher (i.e. the watercolumn was more stratified) during the
winter/spring wet season than the summer dry seasonsin both 1998 and 1999 (Table 3).
Plankton distributions. In San Pablo Bay, naked cili-ates (both autotrophic Myrionecta rubra and other alor-icate ciliate species) were concentrated deeper in thewater column during the winter wet seasons than in thesummer dry seasons (Figs. 2 & 3, Table 4). However, inSouth Bay only the mean depths of diatoms and loricateciliates showed a seasonal pattern, with both groupsconcentrated at deeper depths during the wet seasonsthan during the dry seasons (Figs. 4 & 5, Table 4).
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Parameter Geographic Diel Seasonal Interannual(SPB vs. SB) (Day vs. Night) (Wet vs. dry) (1998 vs. 1999)
Table 2. p-values from 4-way ANOVA tests for geographic and temporalvariability in stratification index (ΔS), and weighted mean depths of microplank-ton (20 to 200 µm) and nanoplankton (5 to 20 µm) pooled for all sampling timesand locations in San Francisco Estuary between February 1998 and August1999. SPB: San Pablo Bay; SB: South Bay. Bold represents significant differences(*p < 0.05; **p < 0.01; ***p < 0.001). Spaces indicate insufficient data for analysis
Date San Pablo Bay South BayTime ΔS Time ΔS
Feb/Mar 1998 Day nd Day 4.33 (nr)Night 14.3 (2.52) Night 1.75 (0.02)
Apr 1998 Day 13.0 (0..57) Day 4.97 (0.30)Night 12.7 (1.33)*** Night 3.38 (0.50)*
Aug 1998 Day 2.7 (0.97) Day 0.08 (0.10)Night 5.57 (0.03) Night 0.44 (0.14)*
Mar 1999 Day 5.22 (3.59) Day 0.28 (0.23)Night 12.0 (4.43) Night 11.18 (0.69)
Apr/May 1999 Day 11.1 (7.45) Day 0.43 (0.11)Night 15.7 (0.43) Night 0.06 (0.08)*
Aug 1999 Day 6.93 (0.91) Day 0.15 (0.08)Night 4.81 (1.32) Night 0.29 (0.02)*
Table 3. Mean (±SE) stratification indices (ΔS, in ppt), calculated as differencebetween salinity at surface and at 10 m, for CTD casts in San Pablo Bay andSouth Bay in 1998 and 1999. Asterisks indicate statistically significant differ-ences between day and night ΔS, using Student’s t-test and assuming unequal
variance (*p < 0.05; ***p < 0.001). nd = no data; nr = no replicate
Aquat Microb Ecol 44: 143–163, 2006150
Lor
Cil
(cel
ls m
l-1 )
Myr
ione
cta
(cel
ls m
l-1 )
Dia
tom
s(c
ells
ml-
1 )D
inos
(cel
ls m
l-1 )
Aut
onan
o(1
02 c
ells
ml-
1 )H
eter
onan
o(1
02 c
ells
ml-
1 )
Mic
ropl
ankt
on (
20 t
o 20
0 µm
)N
anop
lank
ton
(5 t
o 20
µm
)
a b c
Cop
epod
s
Chl
a(µ
g l-
1 )L
or C
il(c
ells
ml-
1 )D
iato
ms
(cel
ls m
l-1 )
Din
os(c
ells
ml-
1 )A
uton
ano
(102
cel
ls m
l-1 )
Het
eron
ano
(102
cel
ls m
l-1 )
Aca
rtia
spp
.(i
nd. m
-3)
Chl
a(µ
g l-
1 )L
or C
il(c
ells
ml-
1 )D
iato
ms
(cel
ls m
l-1 )
Din
os(c
ells
ml-
1 )A
uton
ano
(102
cel
ls m
l-1 )
Het
eron
ano
(102
cel
ls m
l-1 )
Aca
rtia
spp
.(i
nd. m
-3)
35
0
3
52
0
2
4
0
412
0
12
0.2
0
0
.230
0
0
3
001.
8
0
1.8
8000
0
8
000
6
0
64
0
4
1.5
0
1
.540
0
40
1
0
15
0
5
1500
0
1
500
0.04
0
0.0
4
1.5
0
1
.51
0
1
2
0
20.
8
0
0.8
Chl
a(µ
g l-
1 )
0.04
0
0.0
4
Sal
init
y (P
SU
)0
15
0 2 4 6 8 10Depth (m)
Tem
pera
ture
(°C
)10
15
N
(No
day
tim
e C
TD
d
ata)
8
0
8
0 2 4 6 8 10
2
20
10
1
5
ND2
20
10
1
5
Sal
init
y (P
SU
)
Tem
pera
ture
(°C
)
Depth (m)
0 2 4 6 8 10
6
0
6
Het
Alo
r C
il(c
ells
ml-
1 )0.
03
0
0
.03
0 2 4 6 8 10
Het
Alo
r C
il(c
ells
ml-
1 )M
yrio
nect
a(c
ells
ml-
1 )
4
0
4
0 2 4 6 8 10
Myr
ione
cta
(cel
ls m
l-1 )
Het
Alo
r C
il(c
ells
ml-
1 )
1
0
1
***
*
***
***
*
***
***
0 2 4 6 8 1012
22
12
2
2
Sal
init
y (P
SU
)
Tem
pera
ture
(°C
)
Depth (m)
17
2
517
25
ND
Fig
. 2. S
an P
ablo
Bay
. (a)
Feb
ruar
y, (
b)
Ap
ril a
nd
(c)
Au
gu
st 1
998.
Ver
tica
l pro
file
s of
sal
init
y (t
hic
k li
nes
), t
emp
erat
ure
(th
in li
nes
), c
hlo
rop
hyl
l a(C
hl a
)co
nce
ntr
atio
n, a
nd
mea
n (
+S
E)
abu
nd
ance
of
maj
or t
axon
omic
cat
egor
ies
of m
icro
pla
nk
ton
, nan
opla
nk
ton
an
d c
opep
ods.
‘N’ o
r b
lack
bar
s: n
igh
ttim
e va
lues
; ‘D
’ or
gra
y b
ars:
day
tim
e va
lues
;A
uto
nan
o: a
uto
nan
ofla
gel
late
s; H
eter
onan
o: h
eter
onan
ofla
gel
late
s; M
yrio
nec
ta:
M.
rub
ra;
Din
os:
din
ofla
gel
late
s; L
or C
il:
lori
cate
cil
iate
s; H
et A
lor
Cil
: n
on-M
yrio
nec
taal
oric
ate
cili
ates
; (D
) n
igh
ttim
e w
eig
hte
d m
ean
dep
th; (
D)
day
tim
e w
eig
hte
d m
ean
dep
th; a
ster
isk
s in
dic
ate
sig
nif
ican
t d
iffe
ren
ces
bet
wee
n d
ay a
nd
nig
ht
wei
gh
ted
mea
nd
epth
(*p
< 0
.05;
***
p <
0.0
01)
Rollwagen-Bollens et al.: Microplankton vertical distribution in San Francisco Estuary 151
Chl
a(µ
g l-1
)L
or C
il(c
ells
ml-1
)M
yrio
nect
a(c
ells
ml-1
)D
iato
ms
(cel
ls m
l-1)
Din
os(c
ells
ml-1
)A
uton
ano
(102
cell
s m
l-1)
Het
eron
ano
(102
cell
s m
l-1)
Mic
ropl
ankt
on (
20 to
200
µm
)N
anop
lank
ton
(5 to
20
µm)
a b c
Cop
epod
s
Chl
a(µ
g l-1
)L
or C
il(c
ells
ml-1
)D
iato
ms
(cel
ls m
l-1)
Din
os(c
ells
ml-1
)A
uton
ano
(102
cell
s m
l-1)
Het
eron
ano
(102
cell
s m
l-1)
Aca
rtia
spp
.(i
nd. m
-3)
Chl
a(µ
g l-1
)L
or C
il(c
ells
ml-1
)D
iato
ms
(cel
ls m
l-1)
Din
os(c
ells
ml-1
)A
uton
ano
(102
cell
s m
l-1)
Het
eron
ano
(102
cell
s m
l-1)
Aca
rtia
spp
.(i
nd. m
-3)
1000
0 0
10
000
7
0
70.
5
0
0
.512
0
1
21.
2
0
1.2
20
0
20
0.25
0
0
.25
16
0
16
1.5
0
1.
50.
6
0
0.6
6
0
62
0
2
0.3
0
0.
360
0
6
0
3
0
33
0
3
4
0
41.
5
0
1.5
1.5
0
1
.51.
2
0
1.2
6000
0
6
000
0 2 4 6 8 109
14
9
1
4
Sal
init
y (P
SU
)
Tem
pera
ture
(°C
)
Depth (m)
2
2
12
21
ND
0 2 4 6 8 10
Het
Alo
r C
il(c
ells
ml-1
)
8
0
84
0
4
0 2 4 6 8 10
Myr
ione
cta
(cel
ls m
l-1)
Het
Alo
r C
il(c
ells
ml-1
)
2
0
2
0 2 4 6 8 10
Myr
ione
cta
(cel
ls m
l-1)
Het
Alo
r C
il(c
ells
ml-1
)2
0
2
0
0 2 4 6 8 10
Sal
init
y (P
SU
)
Tem
pera
ture
(°C
)
Depth (m)
12
1
7
11
2
311
23
12
1
7
***
***
***
***
Sal
init
y (P
SU
)
18
2
6
Depth (m)
0 2 4 6 8 10
Tem
pera
ture
(°C
)18
23
18
2
3
18
2
6
ND D
N
Fig
. 3.
San
Pab
lo B
ay.
(a)
Mar
ch,
(b)
May
an
d (
c) A
ug
ust
199
9. V
erti
cal
pro
file
s of
sal
init
y (t
hic
k l
ines
), t
emp
erat
ure
(th
in l
ines
), c
hlo
rop
hyl
l a
(Ch
l a)
con
cen
trat
ion
, an
dm
ean
(+
SE
) ab
un
dan
ce o
f m
ajor
tax
onom
ic c
ateg
orie
s of
mic
rop
lan
kto
n a
nd
cop
epod
s. F
urt
her
det
ails
as
in F
ig. 2
Aquat Microb Ecol 44: 143–163, 2006152
Chl
a(µ
g l-1
)L
or C
il(c
ells
ml-1
)M
yrio
nect
a(c
ells
ml-1
)D
iato
ms
(cel
ls m
l-1)
Din
os(c
ells
ml-1
)A
uton
ano
(102
cell
s m
l-1)
Het
eron
ano
(102
cell
s m
l-1)
Mic
ropl
ankt
on (
20 to
200
µm
)N
anop
lank
ton
(5 to
20
µm)
a b c
Cop
epod
s
Chl
a(µ
g l-1
)L
or C
il(c
ells
ml-1
)H
et A
lor
Cil
(cel
ls m
l-1)
Dia
tom
s(c
ells
ml-1
)D
inos
(cel
ls m
l-1)
Aut
onan
o(1
02 ce
lls
ml-1
)H
eter
onan
o(1
02 ce
lls
ml-1
)A
cart
ia s
pp.
(ind
. m-3
)
Chl
a(µ
g l-1
)L
or C
il(c
ells
ml-1
)H
et A
lor
Cil
(cel
ls m
l-1)
Dia
tom
s(c
ells
ml-1
)D
inos
(cel
ls m
l-1)
Aut
onan
o(1
02 ce
lls
ml-1
)H
eter
onan
o(1
02 ce
lls
ml-1
)A
cart
ia s
pp.
(ind
. m-3
)
12
0
12
1
0
11
0
1
0.3
0
0.3
12
0
12
5
0
5
60
0
60
1
0
12
0
2
40
0
40
2
0
212
0
0
12
03
0
3
1200
0 0
120
00
3
0
34
0
4
0.3
0
0.
33
0
3
0.4
0
0
.43
0
3
800
0
800
0.3
0
0
.3
0 2 4 6 8 10
Het
Alo
r C
il(c
ells
ml-1
)
0 2 4 6 8 10
3
0
30.
6
0
0
.6
Myr
ione
cta
(cel
ls m
l-1)
0.6
0
0.6
0 2 4 6 8 10
Myr
ione
cta
(cel
ls m
l-1)
5
0
5
Sal
init
y (P
SU
)9
15
Depth (m) Depth (m)
0 2 4 6 8 10
Tem
pera
ture
(°C
)10
15
9
15
10
1
5
ND
Sal
init
y (P
SU
)
Tem
pera
ture
(°C
)
0 2 4 6 8 10
15
2
1
10
1
5
15
2
1
10
1
5
ND
***
0 2 4 6 8 1015
20
15
2
0
Sal
init
y (P
SU
)
Tem
pera
ture
(°C
)
Depth (m)
22
2
822
28
ND
Fig
. 4. S
outh
Bay
. (a)
Mar
ch, (
b)
Ap
ril
and
(c)
Au
gu
st 1
998.
Ver
tica
l p
rofi
les
of s
alin
ity
(th
ick
lin
es),
tem
per
atu
re (
thin
lin
es),
ch
loro
ph
yll
a(C
hl
a)co
nce
ntr
atio
n, a
nd
mea
n(+
SE
) ab
un
dan
ce o
f m
ajor
tax
onom
ic c
ateg
orie
s of
mic
rop
lan
kto
n, n
anop
lan
kto
n a
nd
cop
epod
s. F
urt
her
det
ails
as
in F
ig. 2
Rollwagen-Bollens et al.: Microplankton vertical distribution in San Francisco Estuary 153
Chl
a(µ
g l-1
)L
or C
il(c
ells
ml-1
)M
yrio
nect
a(c
ells
ml-1
)D
iato
ms
(cel
ls m
l-1)
Din
os(c
ells
ml-1
)A
uton
ano
(102
cell
s m
l-1)
Het
eron
ano
(102
cell
s m
l-1)
Mic
ropl
ankt
on (
20 t
o 20
0 µm
)N
anop
lank
ton
(5 t
o 20
µm
)
a b c
Cop
epod
s
Chl
a(µ
g l-1
)L
or C
il(c
ells
ml-1
)H
et A
lor
Cil
(cel
ls m
l-1)
Dia
tom
s(c
ells
ml-1
)D
inos
(cel
ls m
l-1)
Aut
onan
o(1
02 ce
lls
ml-1
)H
eter
onan
o(1
02 ce
lls
ml-1
)
Aca
rtia
spp
.(i
nd. m
-3)
Chl
a(µ
g l-1
)L
or C
il(c
ells
ml-1
)H
et A
lor
Cil
(cel
ls m
l-1)
Dia
tom
s(c
ells
ml-1
)D
inos
(cel
ls m
l-1)
Aut
onan
o(1
02 ce
lls
ml-1
)H
eter
onan
o(1
02 ce
lls
ml-1
)A
cart
ia s
pp.
(ind
. m-3
)
1000
0 0
10
000
12
0
12
1
0
13
0
3
100
0
100
1.2
0
1.
260
0
6
01
0
1
10
0
10
0.2
0
0.
20.
6
0
0.6
30
0
30
5
0
520
0
2
00.
2
0
0.2
10
0
10
1.5
0
1.
55
0
5
1
0
10.
4
0
0.4
5
0
580
00
0
800
0
0
0 2 4 6 8 10 0 2 4 6 8 10
0 2 4 6 8 10
Het
Alo
r C
il(c
ells
ml-1
)
Myr
ione
cta
(cel
ls m
l-1)
Myr
ione
cta
(cel
ls m
l-1)
0.6
0
0.
6
2
0
2
0.6
0
0.
6
***
***
***
***
***
***
*
0 2 4 6 8 1015
20
15
2
0
22
2
622
26
Sal
init
y (P
SU
)
Tem
pera
ture
(°C
)
Depth (m)
ND
0 2 4 6 8 1010
15
10
1
5
Sal
init
y (P
SU
)
Tem
pera
ture
(°C
)
Depth (m)
20
2
620
26
ND
Sal
init
y (P
SU
)
29
3
5
Depth (m)
0 2 4 6 8 10
Tem
pera
ture
(°C
)15
20
15
2
0
29
3
5
ND
Fig
. 5. S
outh
Bay
. (a)
Mar
ch, (
b)
Ap
ril
and
(c)
Au
gu
st 1
999.
Ver
tica
l p
rofi
les
of s
alin
ity
(th
ick
lin
es),
tem
per
atu
re (
thin
lin
es),
ch
loro
ph
yll
a(C
hl
a)co
nce
ntr
atio
n, a
nd
mea
n(+
SE
) ab
un
dan
ce o
f m
ajor
tax
onom
ic c
ateg
orie
s of
mic
rop
lan
kto
n, n
anop
lan
kto
n a
nd
cop
epod
s. F
urt
her
det
ails
as
in F
ig. 2
Aquat Microb Ecol 44: 143–163, 2006
Interannual patterns
Hydrography. There was no significant difference inthe stratification index between 1998 and 1999 in SanPablo Bay; however, the stratification index was signif-icantly higher during 1998 than 1999 in South Bay(p << 0.001) (Table 3).
Plankton distributions. Several taxa showed signifi-cant interannual differences in weighted mean depthsin both San Pablo Bay and South Bay (Table 4), and inall cases these taxa were concentrated deeper in thewater column during 1999 and shallower during 1998(Figs. 2 to 5). This was especially true for hetero-trophic/mixotrophic aloricate ciliates, whose meandepths were deeper in 1999 in both bays. In addition,Myrionecta rubra and heterotrophic nanoflagellateswere found deeper only in San Pablo Bay (Figs. 2 & 3),and diatoms were observed deeper in South Bay in1999 (Figs. 4 & 5).
Correlation of plankton vertical distributions withabiotic and biotic factors
Abiotic factors
There was no significant correlation, either positiveor negative, between weighted mean depth of anymicro- or nanoplankton taxa and the stratificationindex (ΔS) in any comparison when the entire data setwas analyzed. However, there were rare instances ofsignificant correlation between the stratification indexand isolated taxa when the data were sorted by loca-tion. For instance, when weighted mean depths werecompared with the stratification index within SanPablo Bay, the only significant correlation observedwas for heterotrophic/mixotrophic aloricate ciliates,which were concentrated deeper when stratificationwas stronger, although the correlation was weak (r =0.47, p = 0.029; n = 22). Conversely, when the datawere sorted by season within San Pablo Bay, a strongcorrelation was observed between ΔS and loricate cili-ates (r = 0.90, p = 0.002, n = 8), which were deeper inthe water column when stratification was higher dur-ing the dry seasons of 1998 and 1999.
In South Bay, the water column was relatively well-mixed during nearly every sampling period, with ΔSrarely exceeding 1.0 ppt (Table 3). During the verywet spring of 1998, however, ΔS reached 5.0 ppt.However, despite the relatively strong stratification inspring 1998, there were no significant correlationsbetween the weighted mean depths of micro- ornanoplankton taxa and ΔS in South Bay, with the soleexception of large (>20 µm) dinoflagellates, whichclustered shallower in the water column when ΔS was
higher during wet season, non-bloom periods (March1998 and April 1999) (r = –0.84, p = 0.019, n = 8).
Biotic factors
In addition to abiotic factors such as water columnstratification, predation could also have influenced thevertical distributions of micro- and nanoplankton. Weidentified 2 potential classes of planktonic predators:(1) mesozooplankton (200 to 2000 µm), and (2) hetero-trophic microplankton (20 to 200 µm).
Mesozooplankton predators. The 3 most commonlyoccurring mesozooplankton taxa in our samples werecopepods, specifically the calanoid copepod groupAcartia spp. (most abundant), and 2 cyclopoid copepodtaxa, Oithona davisae and Limnoithona tetraspina(both present in relatively low abundance).
154
Seasonal Interannnual(wet vs. dry) (1998 vs. 1999)
San Pablo BayStratification (ΔΔS) 0.001*** 0.551Chlorophyll a 0.616 0.997MicroplanktonLoricate ciliates 0.180 0.663Aloricate ciliates 0.015* 0.013*Myrionecta rubra 0.027* 0.005**Diatoms 0.150 0.758Dinoflagellates 0.631 0.111
Table 4. p-values from 2-way ANOVA tests for temporalvariability in stratification index and weighted mean depthsof microplankton (20 to 200 µm) and nanoplankton (5 to20 µm) collected from San Pablo Bay and South Bay,San Francisco Estuary. Bold represents significant differences
(*p < 0.05; **p < 0.01; ***p < 0.001)
Rollwagen-Bollens et al.: Microplankton vertical distribution in San Francisco Estuary
Of the 3 copepod taxa, the vertical distribution ofAcartia spp. (weighted mean depth, WMD) showed thegreatest degree of correlation with that of micro- andnanoplankton. In particular, Acartia spp. distributionwas strongly (r between 0.6 and 0.8) positively corre-lated with that of loricate and aloricate ciliates and het-erotrophic flagellates during 1998 across both baysand all seasons. Correlations on a seasonal and dielbasis were less consistent, with a small number of neg-ative correlations observed in dry seasons and daytimesamples, and 1 positive correlation during wet season-bloom periods. On a regional basis, Acartia spp. distri-bution was relatively strongly (r ~ 0.5 to 0.6) positivelycorrelated with those of aloricate ciliates and <20 µmdinoflagellates in San Pablo Bay. However in SouthBay, Acartia spp. WMD was significantly correlatedonly with that of nanoflagellates, being negatively cor-related with pigment-containing nanoflagellates and
positively correlated with the distribution of non-pigment-containing nanoflagellates (Table 5).
The WMD of Oithona davisae was consistently nega-tively correlated with that of <20 µm diatoms (chieflySkeletonema spp.), particularly in San Pablo Bay duringthe daytime and during dry season periods in 1998. Con-versely, O. davisae WMD was strongly (r ~ 0.6 to 0.8)positively correlated with that of non-Myrionecta alori-cate ciliates in San Pablo Bay during 1998 (Table 5).
Finally, of the 3 copepod taxa, Limnoithona tetraspinadistribution showed the fewest significant correlationswith those of micro- or nanoplankton. However, in SouthBay, the WMD of L. tetraspina was very strongly (r ~ 0.9)correlated with that of aloricate ciliates (Table 5).
Microplankton predators. Our results revealed manysignificant correlations between the vertical distribu-tion of nanoplankton and 3 micro- plankton predatorgroups: (1) loricate ciliates, primarily the genera
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Predator Microplankton (20 to 200 µm) Nanoplankton (5 to 20 µm)Lor cil Het Alor Myrio Diat Dino Total Diat Dino Aflag Hflag Total
Table 5. Weighted mean depth (WMD) of copepod predators vs. WMD of prey. Pearson’s correlation coefficients for comparisonsbetween WMD of Acartia spp., Oithona davisae and Limnoithona tetraspina, and WMD of major categories of nano- andmicroplankton prey taxa. Lor cil: loricate ciliates; Het Alor: heterotrophic/mixotrophic aloricate ciliates; Myrio: Myrionecta rubra;Diat: diatoms; Dino: dinoflagellates; Aflag: autotrophic nanoflagellates; Hflag: heterotrophic nanoflagellates. *p < 0.05;
Tintinnopsis, Eutintinnus and Codonellopsis; (2)heterotrophic/mixotrophic aloricate ciliates, mostly thegenera Strombidium and Strobilidium; (3) heterotro-phic dinoflagellates, in particular the genera Protoperi-dinium and Gymnodinium.
The vertical distribution of all 3 groups of microplank-ton consumers showed significant positive correlationswith chlorophyll a distribution. In particular, each groupwas most closely correlated with chlorophyll during thedaytime, and only during 1999. In addition, both loricateciliate and heterotrophic/ mixotrophic aloricate ciliatedistributions were aligned with chloro-phyll concentration in South Bay, withaloricate ciliates further correlatedmost strongly during the dry season(Table 6).
With respect to correlations betweenmicroplankton consumers and potentialnanoplankton prey taxa, aloricate cili-ates and dinoflagellates exhibited thehighest frequency of significant correla-tion with nanoplankton distribution,with only weak and infrequent signifi-cant correlations between loricate cili-ates and nanoplankton. In particular,the vertical distribution of both aloricateciliates and dinoflagellates was consis-tently positively correlated with that ofautotrophic nanoflagellates on a diel,seasonal, interannual and regional ba-sis. Also, the distribution of heterotro-phic dinoflagellate distribution was of-ten positively correlated with that ofheterotrophic nanoflagellates, alternat-ing between positive correlation withthe autotrophic nanoflagellates duringthe dry season and heterotrophicnanoflagellates during the wet season,non-bloom periods. The vertical distrib-ution of heterotrophic dinoflagellatewas also negatively correlated with thatof <20 µm diatoms, especially in SouthBay during 1999 (Table 6).
DISCUSSION
The 4-way analysis of variance onthe WMD of micro- and nanoplanktontaxa produced several importantresults. First, the microplankton taxa,and more specifically the ciliates,showed the greatest variability in ver-tical distribution during the course ofthis study. The WMD of nanoplankton
taxa generally did not vary consistently according today vs. night, season, year or location within the SFE.Second, the most significant differences in the verticaldistribution of microplankton were observed on a sea-sonal basis, and to a lesser extent on the basis of timeof day and year. Location within the SFE appeared tohave much less effect on how microplankton taxawere distributed in the water column. Finally, the het-erotrophic/mixotrophic aloricate ciliates (except Myri-onecta rubra) displayed the most significant differ-ences in vertical distribution on all time scales, with
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Predator Nanoplankton (5 to 20 µm)Chl a Diatoms Dinoflag Aflag Hflag Total
Dry season 0.73*** – – 0.67** – –Day 0.46* – – – – –Night – – – 0.48* 0.60* –San Pablo Bay – – – 0.48* 0.71** –South Bay – –0.61** – 0.61** – –
Table 6. Weighted mean depth (WMD) of heterotrophic microplankton pre-dators vs. WMD of prey. Pearson’s correlation coefficients for comparisons be-tween WMD of loricate ciliates, aloricate ciliates and dinoflagellates and WMDof major categories of potential nanoplankton prey taxa. Dinoflag: dinoflagel-lates; Aflag: autotrophic nanoflagellates; Hflag: heterotrophic nanoflagellates.
Rollwagen-Bollens et al.: Microplankton vertical distribution in San Francisco Estuary
the other major taxa groups (loricate ciliates, M.rubra, diatoms and dinoflagellates) varying only withrespect to season.
The ANOVA results provided a valuable base onwhich to make a more focused examination of tempo-ral patterns in the vertical distributions of ciliates, aswell as a framework for the discussion of the potentialinfluence of hydrography (i.e. salinity stratification)and planktonic predators on the observed trends.
Temporal patterns in ciliate vertical distribution
Seasonal and interannual cycles
Non-Myrionecta aloricate ciliates were generallydistributed at a deeper depth in 1998 than in 1999, butsignificant interannual differences in vertical distribu-tion were few and showed no consistent pattern as afunction of location, season or time of day. Conversely,there were frequent seasonal differences in aloricateciliate WMD in both South Bay and San Pablo Bayduring 1998 and 1999, as well as during daytime andnighttime. Similarly, loricate ciliates displayed nointerannual differences in vertical distribution, andonly limited seasonal differences in WMD. In general,loricate ciliates were found deeper during the wetseason than during the dry season, but only in daytimesamples during 1999 in South Bay.
The lack of consistent interannual or seasonal trends invertical distribution among any ciliate taxa in the SFE issomewhat unexpected, given the substantial climaticand hydrographic differences between years (1998 vs.1999) and seasons (wet vs. dry). The 1997 to 1998 ENSOevent produced record rainfall in the Bay area duringwinter/spring 1998, leading to substantial salinitystratification in the SFE. The lack of an interannual trendis particularly surprising for San Pablo Bay, wherefreshwater flow is such a dominant physical force.Seasonal trends in ciliate vertical distribution have beendocumented in the coastal ocean and in lakes, althoughpublished reports of seasonal cycles in ciliate verticaldistribution in other estuarine systems are extremelylimited.
For instance, in the only study known to us that explic-itly examined vertical distributions in an estuary over afull year, Dolan & Coats (1990) found ciliates in Chesa-peake Bay to be concentrated primarily near the bottomduring the spring, but concentrated in surface watersduring the summer and autumn. In the DamariscottaRiver estuary in Maine, testing for differences in verticaldistribution on a seasonal basis was not a stated goal;however, Sanders (1987) reported qualitative differencesin the vertical distribution of loricate and aloricate cili-ates during 1981. Maximum loricate ciliate abundance
was deep (~20 m) in the water column in March, at inter-mediate depths (~7 m) in July, and near the surface (0 to7 m) in September and December. Aloricate ciliates alsofollowed the same general trend (Sanders 1987, presentTable 2).
Seasonal patterns in ciliate vertical distribution werealso inferred from studies conducted in marine coastalregions. In Kastela Bay (central Adriatic Sea), aloricateciliates showed a bimodal distribution in March (localmaxima in abundance at 5 and 25 m), and were highlyconcentrated (5 m) in May, and aloricate ciliate verticaldistributions were more homogeneous during summerand fall (Bojanic et al. 2001, their Fig. 3). However, dur-ing the same study loricate ciliates were found exclu-sively above 10 m in the spring (February to May) butwere concentrated at 15 m during October (Bojanic etal. 2001, their Fig. 5).
Evidence for seasonal variability among ciliate distri-butions has also been documented for temperate fresh-water lakes. Pace (1982) observed the distributions ofboth loricate and heterotrophic aloricate ciliates to beuniform with depth during the winter in a small lake inGeorgia, but to be mostly in the surface layer duringthe spring. Similarly, in a French humic lake, aloricateciliates were distributed evenly through the water col-umn during April, but were substantially more abun-dant between 0 and 5 m in June and between 10 and15 m in October (Carrias et al. 1994).
These reports of marked seasonal variability inciliate vertical distribution contrast with our results offar fewer seasonal differences in the SFE.
Diel cycles
In the SFE, diel differences in vertical distributionoccurred even less frequently than seasonal differ-ences; however, in nearly every case, the WMD of cili-ates was deeper during the night than during the day,and the qualitative patterns of daytime and nighttimevertical distributions were generally more consistent.
For example, in San Pablo Bay, non-Myrionecta alor-icate ciliates showed diel differences in WMD in 4 of 6sampling periods, and in every case the organismswere highly concentrated near the surface during theday but distributed throughout the water column dur-ing the night (Figs. 2 & 3). Heterotrophic/mixotrophicaloricate ciliates (except M. rubra) only showed a dieldifference in vertical distribution in South Bay duringAugust 1999; however, the pattern was the same as inSan Pablo Bay, with a daytime peak at 2 m and a morehomogeneous distribution during the night (Fig. 5).
The unusual mixotrophic aloricate ciliates Myri-onecta rubra were only observed to have significantlydifferent vertical distributions between day and night
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Aquat Microb Ecol 44: 143–163, 2006
on 2 occasions throughout the study period, duringApril 1998 and August 1999 in South Bay. Loricate cili-ates showed differences in diel vertical distributiononly during the dry season, and primarily in San PabloBay, although in one case WMD was deeper during thenight and in the other WMD was deeper during the day.
Whereas the lack of a consistent seasonal change invertical distribution in the SFE contrasted with othertemperate systems, on a diel basis ciliate vertical distri-bution in the SFE appears to fall within the wide rangeof patterns observed elsewhere. Strong swimmingcapabilities have been observed in the laboratory for arange of ciliate taxa (Jonsson 1989, Jonsson & Tiselius1990); however, in the field ciliates have been ob-served to migrate vertically in some systems and not inothers. Several, but not all, heterotrophic ciliates werefound to migrate toward the surface during the day ina Norwegian fjord (Dale 1987). And Favella sp., aloricate ciliate, was found near the surface in the morn-ing and near the bottom at night during 2 separate28 h periods in a small tidal estuary in Massachusetts(Stoecker et al. 1984). Diel vertical migration amongheterotrophic aloricate ciliates was also documented inthe NW Mediterranean Sea, although in an oppositepattern, with ciliates migrating toward the surface atnight (Perez et al. 2000). However, no diel verticalmigrations were observed among ciliates over two48 h sampling periods in the northern Adriatic Sea(Revelante & Gilmartin 1990).
Similarly, there is a lack of consensus as to when andunder what conditions Myrionecta rubra may verticallymigrate. In the laboratory, the swimming speed of M.rubra was as high as 8.5 mm s–1 (Lindholm 1985, Jons-son & Tiselius 1990), and diel vertical migration of M.rubra has been demonstrated in a wide range of marineenvironments, including a Norwegian fjord (Dale1987), an estuary in NW Spain (Villarino et al. 1995),and the Baltic Sea (Passow 1991, Olli et al. 1998).
However, a number of investigations into the behav-ior of Myrionecta rubra have shown that verticalmigration of this phototrophic ciliate may be quite vari-able. For instance, the vertical distribution of M. rubrawas not related to the time of day in the NW Mediter-ranean Sea (Dolan & Marrasé 1995) or a brackish inleton the coast of Finland (Crawford & Lindholm 1997).Crawford & Purdie (1992) have suggested that turbu-lence may be the major cue for vertical migration of M.rubra to maintain position in estuaries, while otherspropose that migration of these ciliates is a response tolight levels (Lindholm & Mork 1990, Passow 1991).
Thus, the lack of a strong seasonal pattern in verticaldistribution along with no evidence of diel migrationbehavior among Myrionecta rubra in the SFE suggeststhat other factors besides seasonal changes and time ofday may influence its distribution.
Factors influencing vertical distributions in the SFE
Stratification
We did not observe any consistent correlationbetween the degree of stratification in the water col-umn and the WMD of micro- or nanoplankton. Explicitexaminations in estuaries of protozoan vertical distrib-utions in relation to hydrography are very few. How-ever, in a highly stratified Norwegian fjord, Andersen& Nielsen (2002) similarly found the vertical distribu-tion of ciliates to be only marginally affected by thepresence of a large salinity gradient, although not allciliate taxa showed the same salinity tolerances.
In the coastal ocean, on the other hand, stratificationand other physical conditions have been shown toexert measurable influence on ciliate vertical distribu-tion. In the northern Aegean Sea, ciliates were foundto cluster near the surface only under stratified condi-tions, whereas their vertical distribution was homoge-neous with depth when the water column was well-mixed (Pitta & Giannakourou 2000). In addition,Montagnes et al. (1999) observed both finescale (cm)and microscale (m) patchiness in ciliate vertical distri-butions in the Irish Sea, and attributed much of thesepatterns to hydrographic features such as fronts andpycnoclines. Finally, ciliate vertical distribution of cili-ates was also strongly related to the pycnocline depthoff the west coast of New Zealand, with high and con-sistently negative correlations between ciliates andwater density (sigma-t) at all stations sampled (James& Hall 1995). However, the ciliates in the NewZealand study were also highly positively correlatedwith chlorophyll and picophytoplankton abundancethroughout the water column, suggesting that bothphysical and biological variables may have affectedtheir distribution.
Predation
In the present study, the significant correlationsobserved between the vertical distribution of copepodpredators and potential microplankton prey, as wellas between microplankton consumers and potentialnanoplankton prey, suggest that in the SFE predator–prey interactions may have more influence on the dis-tribution of plankton than stratification in the watercolumn.
Acartia spp. were the most abundant copepods inboth San Pablo Bay and South Bay during our studyperiod, and also showed the highest incidence of sig-nificant correlation with the vertical distribution ofmicroplankton taxa, in particular heterotrophic alori-cate ciliates (Table 5). It is interesting, however, that
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the correlations were both positive and negative forthe same microplankton taxa during different timeperiods. Closer examination of the data revealed thatthe negative correlations between Acartia spp. andseveral microplankton taxa were driven largely bydramatic differences in daytime vertical distributionsin South Bay during August 1999 (Fig. 5c). When these2 replicate daytime casts were removed from theanalyses, virtually all the negative correlations disap-peared. Moreover, removal of these casts and re-analysis of the entire data set resulted in additional sig-nificant positive correlations between Acartia spp. andtotal microplankton (specifically non-Myrionecta alori-cate ciliates, diatoms and dinoflagellates).
Correlations were also quite strong between the ver-tical distribution of microplankton consumer taxa (lori-cate ciliates, aloricate ciliates and dinoflagellates) andtheir potential food resources (chlorophyll a andnanoflagellates) in the SFE (Table 6). Of particularnote is the fact that the vertical distribution of non-Myrionecta aloricate ciliates was correlated withchlorophyll only during periods when they were notstatistically related to the distribution of Acartia spp.
To our knowledge, the only other published studiesto specifically test the relationship between the verticaldistribution of copepods and ciliates in estuaries havebeen conducted in Norwegian fjords. Titelman &Tiselius (1998) found the abundance of copepods(mostly Pseudocalanus sp. but also Acartia spp.) to cor-relate weakly with chlorophyll a on only 1 of 4 sam-pling dates during spring 1996 in the Gullmarsfjorden,but never to correlate with ciliate abundance. How-ever in the Hylsfjorden, several copepod taxa (includ-ing A. longiremis and Oithona spp.) showed significantpositive correlations with potential food (mostly lori-cate ciliate abundance) (Andersen & Nielsen 2002).
The relationship between the vertical distribution ofciliates and their potential food resources has beenstudied more frequently, and a significant relationshipbetween their distributions appears to be common inmany aquatic systems. In estuaries, the vertical distrib-ution of heterotrophic ciliates was positively correlatedwith that of heterotrophic flagellates in the Chesa-peake Bay (Dolan & Coats 1990), while in NarragansettBay the vertical distribution of certain loricate ciliates(Tintinnopsis minuta, Stenosemella spp.) was highlycorrelated with chlorophyll concentration (Verity1987). In oceanic waters, the vertical distribution ofciliates was also closely related to the distribution ofchlorophyll in the Catalan Sea, NW Mediterranean(Dolan & Marrasé 1995), in the Adriatic Sea (Revelante& Gilmartin 1990), and in several locations in the west-ern Pacific (Suzuki & Taniguchi 1998). Ciliate distribu-tions have also been found to be closely associatedwith both chlorophyll and microbial food resources in a
number of freshwater lakes (Pace 1982, Carrias et al.1994, Zingel & Ott 2000).
The fact that Acartia spp. distribution was not corre-lated more frequently with that of microplankton preysuggests that additional factors other than prey for-aging may have affected copepod distribution, suchas avoidance of predators (e.g. Bollens & Frost 1989,1991) or position maintenance in the estuary (e.g.Laprise & Dodson 1994, Kimmerer et al. 1998). Titel-man & Tiselius (1998) suggested that the vertical distri-bution of copepods would only be correlated with thatof their food resources when moderately food limited;under either severe food limitation or food saturatingconditions, copepods would lack the motivation tosearch and aggregate around food patches.
Measurements of the specific ingestion rates andprey selectivity of Acartia spp. in both San Pablo Bayand South Bay during 2000 showed that non-Myri-onecta ciliates were always a significant proportion ofthe copepods’ diet, and that Acartia spp. often selec-tively consumed these ciliates over diatoms. However,Acartia spp. ingestion rates on all prey were consis-tently low and probably never high enough to enablesubstantial growth except during peak bloom condi-tions, which suggests that copepods may be food lim-ited during non-bloom periods in the SFE (Rollwagen-Bollens & Penry 2003).
In the present study, the vertical distribution of Acar-tia spp. only showed significant correlation with that ofnon-Myrionecta aloricate ciliates during bloom peri-ods, especially in 1998 when the chlorophyll bloomwas exceptionally high. Perhaps the positive correla-tions between the vertical distributions of Acartia spp.and microplankton were due to high but non-saturat-ing food conditions providing motivation for the cope-pods to aggregate at the same depth as their prey. Incontrast, overall ciliate (and diatom) abundance mayhave been too low during the dry seasons for Acartiaspp. to be induced to respond to the vertical distri-bution of their prey. Finally, 3 additional points areimportant:
First, as this was part of a larger program to investi-gate the role of heterotrophic protists in copepod diet,we only enumerated nanoplankton >5 µm in our sam-ples (the lowest size efficiently grazed by Acartia spp.).Small heterotrophic nanoplankton (2 to 5 µm) might behighly abundant in coastal waters (e.g. Kuuppo 1994),and if we had included very small flagellates in ouranalyses we may have observed different, and possiblymore significant, correlations between the WMD ofmicroplankton predators and nanoplankton prey.
Second, we sampled the water column on a some-what coarse scale, i.e. at 2 m increments. Although thisdepth spacing is comparable to that in the previousfield studies discussed above, there is growing aware-
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ness that planktonic organisms can aggregate intoeven smaller, i.e. centimeter scale, ‘thin layers.’ Evi-dence for this comes from both field observations (e.g.Cowles & Fessenden 1995, Montagnes et al. 1999,Dekshenieks et al. 2001, Alldredge et al. 2002, Rines etal. 2002) and experimental studies (Speekmann et al.2000, Lougee et al. 2002, Bochdansky & Bollens 2004,Clay et al. 2004, Ignoffo et al. 2005). It is possible thatmore highly vertically resolved sampling of micro- andnanoplankton in the SFE could reveal greater hetero-geneity in vertical distributions than the results pre-sented here based on 2 m depth increments.
Third, it was not within the scope of this study todirectly measure other hydrographic parameters thatmay influence plankton distributions beyond stratifica-tion, such as tidal currents and freshwater flow,although we did record tidal stage at the beginning ofeach sampling cast (Table 1). A qualitative review ofthe tidal stage data in relation to the temporal variabil-ity in plankton weighted mean depths did not showany consistent patterns. It would be interesting to moreexplicitly measure how vertical distributions varyspecifically on a tidal cycle. However, the fact thatthere were such dramatic diel differences in stratifica-tion, and at times tidal stage, but few if any differencesin plankton vertical distributions, strengthens theargument that hydrography has little effect on plank-ton distributions in the SFE.
SUMMARY AND CONCLUSIONS
An important issue in marine ecology is whether it ispossible to make reasonable predictions about the ver-tical distribution of plankton. Our data suggest that thevertical distribution of micro- and nanoplankton, inparticular that of ciliates, is not directly related to thephysical structure (i.e. the degree of stratification) ofthe SFE but instead is more influenced by biologicalinteractions between potential predators and prey.
When overall microplankton abundance was low(i.e. San Pablo Bay, 1999, dry seasons) the vertical dis-tribution of loricate ciliates, non-Myrionecta aloricateciliates and dinoflagellates were all more strongly cor-related with the distribution of their potential food(chlorophyll and autotrophic nanoflagellates) than thatof their potential copepod predators (Acartia spp.,Oithona davisae, Limnoithona tetraspina). This sug-gests that ‘bottom–up’ factors may be more importantthan ‘top–down’ factors in controlling microplanktonvertical distribution in the SFE, at least during the dryseason. However, when microplankton abundancewas relatively high (i.e. South Bay, 1998, wet seasons),ciliate vertical distribution (especially that of aloricateforms) was more closely correlated to the distribution
of their copepod predators (Acartia spp.), suggestinggreater influence of ‘top–down’ factors.
In conclusion, distributions of micro- and nanoplank-ton in the SFE were often relatively homogeneous withdepth and were surprisingly unrelated to water col-umn hydrography. Vertical distributions of micro- andnanoplankton also showed limited variability on diel,seasonal and interannual time scales, as well asbetween 2 hydrodynamically very different locationswithin the SFE. However, on those occasions whentemporal and/or spatial differences in planktonic verti-cal distributions did occur, correlation analyses led usto conclude that these patterns were more likely drivenby biological pressures (predator–prey interactions)than by physical stratification of the water column.
Acknowledgements. The authors thank the marine opera-tions staff at the Romberg Tiburon Center for EnvironmentalStudies at San Francisco State University for field supprtaboard the RV ‘Questuary’. We also thank 4 anonymousreviewers for their thoughful comments. This research wassupported in large part by a National Science FoundationAlan T. Waterman award (OCE-9320572) to D.L.P.
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