Estuarine calanoid copepod abundance in relation to season, salinity, and land-derived nitrogen loading, Waquoit Bay, MA David Lawrence * , Ivan Valiela, Gabrielle Tomasky Boston University Marine Program, Marine Biological Laboratory, Woods Hole, MA 02543, USA Received 8 September 2000; accepted 15 June 2004 Abstract Calanoid copepod abundance and distribution were measured by monthly plankton tows from May through November in 1998 and March through August in 1999 in three subestuaries of the Waquoit Bay estuarine system. There was a dramatic seasonal change in the composition of calanoids in Waquoit Bay with a spring community consisting of Acartia hudsonica, Centropages hamatus, and Eurytemora affinis, replaced by Acartia tonsa in the summer. The abundance of A. hudsonica, A. tonsa, and C. hamatus was higher in the saltier reaches of the subestuaries, but the abundance of E. affinis and copepod nauplii was not affected by salinity. Even though different land-derived nitrogen loads created different concentrations of chlorophyll in the water of Waquoit Bay subestuaries, there was no apparent response in the abundance of most calanoid copepods to differences in nitrogen load to the subestuaries. The uncoupling of phytoplankton food from mesozooplankton consumers suggests that other factors such as water residence time, phytoplankton quality and composition, or variations in microzooplankton food play a role in the abundance dynamics of Waquoit Bay calanoid populations. Ó 2004 Elsevier Ltd. All rights reserved. Keywords: zooplankton; Copepoda; seasonal variations; salinity; chlorophyll; nitrogen loading; Cape Cod 1. Introduction Temperature, salinity, and food supply are some of the important factors that influence the demographics of calanoid copepods in estuarine environments. Temper- ate waters are characterized by seasonal changes in the composition and relative dominance of calanoids, and these changes are mediated in part by temperature (Fish, 1925; Deevey, 1948; Barlow, 1955; Conover, 1956; Jeffries, 1962, 1964; Anraku, 1964a; Durbin and Durbin, 1981). Salinity is also known to affect the distribution of calanoid copepods in estuaries. Acartia hudsonica and Acartia tonsa, two common estuarine calanoids, have been shown to be euryhaline species, although optimal salinity for respiration occurs from 11 to 36 (Lance, 1965; Tester and Turner, 1991; Cervetto et al., 1999). The respiration of Centropages hamatus, another com- mon coastal and estuarine form, was found to be significantly reduced at lower salinities (Anraku, 1964b). Such alterations in respiration may influence the feeding activity of these animals and ultimately are important in determining survival. Some estuarine calanoids such as Eurytemora affinis have been shown to be capable of osmoregulation and do not experience respiratory stress when moved from high to low salinities (Roddie et al., 1984). Such interspecific differences in salinity tolerance often explain changes in the dominant species as one * Corresponding author. Present address: School of Aquatic and Fishery Sciences, Box 355020, University of Washington, Seattle, WA 98195-5020, USA. E-mail address: [email protected](D. Lawrence). 0272-7714/$ - see front matter Ó 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2004.06.018 Estuarine, Coastal and Shelf Science 61 (2004) 547–557 www.elsevier.com/locate/ECSS
Transcript
Estuarine, Coastal and Shelf Science 61 (2004) 547–557
www.elsevier.com/locate/ECSS
Estuarine calanoid copepod abundance in relation to season,salinity, and land-derived nitrogen loading, Waquoit Bay, MA
David Lawrence*, Ivan Valiela, Gabrielle Tomasky
Boston University Marine Program, Marine Biological Laboratory, Woods Hole, MA 02543, USA
Received 8 September 2000; accepted 15 June 2004
Abstract
Calanoid copepod abundance and distribution were measured by monthly plankton tows from May through November in 1998and March through August in 1999 in three subestuaries of the Waquoit Bay estuarine system. There was a dramatic seasonalchange in the composition of calanoids in Waquoit Bay with a spring community consisting of Acartia hudsonica, Centropages
hamatus, and Eurytemora affinis, replaced by Acartia tonsa in the summer. The abundance of A. hudsonica, A. tonsa, and C. hamatuswas higher in the saltier reaches of the subestuaries, but the abundance of E. affinis and copepod nauplii was not affected by salinity.Even though different land-derived nitrogen loads created different concentrations of chlorophyll in the water of Waquoit Baysubestuaries, there was no apparent response in the abundance of most calanoid copepods to differences in nitrogen load to the
subestuaries. The uncoupling of phytoplankton food from mesozooplankton consumers suggests that other factors such as waterresidence time, phytoplankton quality and composition, or variations in microzooplankton food play a role in the abundancedynamics of Waquoit Bay calanoid populations.
Temperature, salinity, and food supply are some ofthe important factors that influence the demographics ofcalanoid copepods in estuarine environments. Temper-ate waters are characterized by seasonal changes in thecomposition and relative dominance of calanoids, andthese changes are mediated in part by temperature (Fish,1925; Deevey, 1948; Barlow, 1955; Conover, 1956;Jeffries, 1962, 1964; Anraku, 1964a; Durbin and Durbin,1981).
* Corresponding author. Present address: School of Aquatic and
Fishery Sciences, Box 355020, University of Washington, Seattle, WA
0272-7714/$ - see front matter � 2004 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ecss.2004.06.018
Salinity is also known to affect the distribution ofcalanoid copepods in estuaries. Acartia hudsonica andAcartia tonsa, two common estuarine calanoids, havebeen shown to be euryhaline species, although optimalsalinity for respiration occurs from 11 to 36 (Lance,1965; Tester and Turner, 1991; Cervetto et al., 1999).The respiration of Centropages hamatus, another com-mon coastal and estuarine form, was found to besignificantly reduced at lower salinities (Anraku, 1964b).Such alterations in respiration may influence the feedingactivity of these animals and ultimately are important indetermining survival. Some estuarine calanoids such asEurytemora affinis have been shown to be capable ofosmoregulation and do not experience respiratory stresswhen moved from high to low salinities (Roddie et al.,1984). Such interspecific differences in salinity toleranceoften explain changes in the dominant species as one
548 D. Lawrence et al. / Estuarine, Coastal and Shelf Science 61 (2004) 547–557
moves across the salinity gradient of an estuary.Furthermore, salinity tolerance may be altered withtemperature such that the interaction between thesefactors causes changes in distribution of calanoids intime and space (Bradley, 1991).
In many systems, the demographics of copepod com-munities are strongly influenced by food supply (Durbinet al., 1983; Peterson and Bellatoni, 1987; Kiorboe andNielsen, 1994). The supply of phytoplankton, an impor-tant food resource for calanoids, is controlled in turn, bythe availability of nitrogen, which often limits primaryproduction in marine systems (Ryther and Dunstan,1971). Thus, nitrogen supply can serve as an indirectcontrol on zooplankton communities.
The availability of nitrogen in coastal systems issteadily increasing as coastal watersheds become moreurbanized (Valiela et al., 1992). It is known that nutrientenriched estuaries exhibit a greater standing crop ofphytoplankton (Valiela et al., 1992, 1997a, 2000), butthere is little information on the degree of coupling be-tween nutrient supply and calanoids in estuarine envi-ronments. Given the ubiquity of nitrogen loading on aglobal scale (GESAMP, 1990), and the key trophic roleof calanoid copepods in food webs, it is important tounderstand the potential impact of changing resourcesupply on these animals.
The potential effects of nutrient enrichment on cala-noid populations may be divided into short- and long-term consequences. Short-term consequences includechanges in feeding activity and fecundity of copepodsthat take place on the order of hours or days. Long-termresponses involve changes in biomass, abundance, andcomposition of the population that take place on a timescale of weeks to months.
Mesocosm experiments have demonstrated bothshort- and long-term responses of calanoid populationsto nutrient enrichment (Gismervik et al., 2002). Fulton(1984) added nutrients to enclosures and found an in-crease in chlorophyll a concentration as well as increaseddensity of the calanoid copepod Acartia tonsa com-pared to unenriched controls. Experiments conducted inMERL mesocosms showed increased numbers, biomass,and production rates of Acartia hudsonica and A. tonsain response to nutrient enrichment (Sullivan andRitacco, 1985).
Field studies of calanoid dynamics over nutrientgradients are few (Nixon et al., 1986) and show short-term responses that may or may not lead to long-termconsequences to calanoid populations. For example,Saiz et al. (1999) found that although egg production ofcopepods increased across the natural nutrient gradientfrom ‘oligotrophic’ oceanic waters to ‘eutrophic’ shelfwaters, the abundance of copepods did not change, andsuggested that predation or advection may uncoupleproduction from abundance. In contrast, Smith et al.(1981), Capriulo et al. (2002) documented a strong
coupling between the degree of eutrophication andzooplankton biomass.
Micheli (1999) conducted ameta-analysis of data from47 marine mesocosm experiments (where nutrients andconsumers influences were manipulated) and 20 naturalsystems (with time series data on nutrients, plankton, andfishes) to evaluate bottom–up and top–down controls onconsumers. Her work suggests that these controls at-tenuate through marine food webs, and in general, theremay be a weak coupling between phytoplankton andherbivores.
Physical processes such as advective transport mayweaken the relationship between nutrients and con-sumers (Pace et al., 1992; Basu and Pick, 1996). Theresidence time of water in an estuary is an indication oftransport in and out of an aquatic system (Geyer, 1997).For endemic plankton populations to grow withinestuaries, the net growth of the population must exceedlosses of biomass due to advective transport from thesystem (Ketchum, 1954). Phytoplankton divide 1–2day�1, so that if the water remains within the estuaryfor longer times, the phytoplankton population will in-crease. Calanoids have generation times of days toweeks, and therefore, may be advected from a givensystem before being able to adjust their abundance bydemographic responses to food supplies within theestuary (Pace et al., 1992; Dagg, 1995). Hence, inestuaries with short residence times, more nutrientsmay lead to increased phytoplankton productivity, butmay not lead to a concomitant increase in zooplanktonproducers.
1.1. The Waquoit Bay system
Waquoit Bay, MA, is a temperate estuarine systemwith an average depth of 1 m, where water temperatureranges from 2 to 25 �C and salinity ranges from 0 to 32.In subestuaries of Waquoit Bay that receive significantfreshwater input (Childs River and Quashnet River)there may be strong vertical stratification between topand bottom waters, creating a two-layer circulationpattern (D’Avanzo and Kremer, 1994). Subestuaries ofWaquoit Bay receive a range of nitrogen loads due todifferent degrees of urbanization on their subwatersheds(Valiela et al., 1997b), and this range encompasses 75%of that received by marine systems worldwide (Nixonet al., 1986). By making comparisons of subestuarieswithin Waquoit Bay that receive a range of land-derivednitrogen loading rates one can study the degree of land-estuary coupling as a space-for-time substitution (Pick-ett, 1989) in subestuaries that are otherwise very similarin depth, open water area, temperature, and residencetimes (Hauxwell et al., 1998).
Waquoit Bay mesozooplankton is numerically dom-inated by calanoid copepods, accounting for greaterthan 90% of the total zooplankton, although sporadic
549D. Lawrence et al. / Estuarine, Coastal and Shelf Science 61 (2004) 547–557
bursts in polychaete larvae and gastropod veligers, attimes, outnumber copepods (D. Lawrence, unpublisheddata).
In a previous study of zooplankton in Waquoit Bay ithas been shown that egg production rate of the summer-dominant copepod Acartia tonsa was greater in sub-estuaries of Waquoit Bay receiving higher nitrogenloads, and that the enhanced production was mediatedby differential food availability (Cubbage et al., 1999).Given that within a few hours, ambient food supplyalters egg production rates; we were interested in ex-amining if short-term changes in egg production areaccompanied by changes in abundance of copepodpopulations in Waquoit Bay.
In this paper we will: (1) describe seasonal changesin abundance of calanoids across subestuaries; (2) de-termine the influence of salinity on calanoid copepoddistribution; (3) determine the relationship betweenland-derived nitrogen loading rate and calanoid cope-pod abundance; and (4) examine interactions betweennutrient supply, phytoplankton concentration, andcalanoid abundance.
2. Methods
2.1. Zooplankton
Sampling was carried out on an approximatelymonthly basis from 20 May to 5 November in 1998,and from 5 March to 20 August in 1999. Zooplanktonsamples were collected from three sites in each of thesubestuaries of Waquoit Bay (Childs River, QuashnetRiver, and Sage Lot Pond, Fig. 1) to provide a range ofnitrogen loads (601.2, 350.3, 14.2 kg N ha�1 y�1, re-spectively, Valiela et al., 1997b, 2000), and from threesites in Waquoit Bay proper.
At each site triplicate zooplankton samples werecollected during the day by towing a 60 mm, 0.12 mdiameter Nitex plankton net at 1 knot for 30–60 m(depending on the number of animals available and netclogging due to ctenophore blooms). A General Ocean-ics flowmeter attached to the net quantified the volumeof water filtered for each tow, which ranged from 330 to800 L. Tows were conducted at approximately 0.5 mdepth. Each replicate tow was taken from the middle ofthe estuary, along a line parallel to shore, while movingagainst the tide. Samples were immediately preserved in70% ethanol. Water temperature and salinity wererecorded at the time of collection. Salinity is reportedhere using the Practical Salinity Scale.
At the lab, zooplankton samples were sorted andeach species of calanoid copepod was counted. The lifehistory stage of each calanoid was recorded as nauplii,copepodid, or adult. Nauplii were recorded as ‘‘copepodnauplii’’ because of difficulty in distinguishing species.
Copepodid stages were identified to genus and wereassumed to represent the species of that genus domi-nant at the time of sampling. Adults were identified tospecies. Other non-calanoid taxa in the sample werenoted. If the count for any life history stage of a specieswas greater than 1000 in the sample, the sample was splitusing a Folsum splitter with an attached air manifoldsuch that 1000 or less were tallied. All other life historystages were counted from the entire sample.
2.2. Chlorophyll
Chlorophyll concentrations were measured from thesame sites where zooplankton was collected in 1999 foreach subestuary and Waquoit Bay proper as part ofanother study (Tomasky, in preparation). Sampling wascarried out on different dates than those of zooplanktoncollections, but the data cover the entire time course ofthe 1999 survey. Water samples for chlorophyll analysiswere collected using a 1 L Lamotte sampler. Sampleswere filtered through a 200 mm net to remove zooplank-ton and stored in 1 L Nalgene HDPE bottles (2 repli-cates) and kept on ice. Samples were filtered usingGelman GFF filters (0.7 mm nominal pore size), placedin dark centrifuge tubes, and immediately frozen at�20 �C. Analysis usually took place within 1 week ofcollection, but in some cases filters were frozen for aslong as 2 weeks. Chlorophyll samples were analyzed
41º35’N
41º34’
41º33’
70º33’ 70º32’ 70º31’WFig. 1. Map of Waquoit Bay, MA. Filled circles show sampling sites in
ChildsRiver, QuashnetRiver, Sage Lot Pond, andWaquoit Bay proper.
550 D. Lawrence et al. / Estuarine, Coastal and Shelf Science 61 (2004) 547–557
spectrophotometrically using the Lorenzen (1967) pro-cedure.
3. Results and discussion
3.1. Abundance across seasons and salinities
The abundance of calanoid copepods varied greatlyamong stations, subestuaries, and across years of thisstudy (Lawrence, 2000). To sort out the effect of seasonand salinity, so as to evaluate the differences amongsubestuaries more clearly, we first describe the seasonalchanges in abundance of adult calanoids across all sub-estuaries. The timing of seasonal events was distinct atdifferent salinities, so we will examine these events inthree different salinity ranges (0–10, 10–20, and 20–30).Second, after we have established the growth period foreach species, we will examine the variation in abundanceassociated with salinity across subestuaries during thatperiod, effectively removing time as a factor. Third, afterwe define the impact of salinity on abundance of cope-pods, we will go on to evaluate the differences amongsubestuaries presumably associated with nitrogen load-ing regimes.
In spring months Acartia hudsonica, Centropageshamatus, and Eurytemora affinis were the dominantcalanoids of Waquoit Bay (Fig. 2) and made similarcontributions to the total calanoid community in sali-nities from 20 to 30 (29G 6%, 35G 6%, 36G 9%,respectively). Eurytemora affinis dominated in salinitiesfrom 10 to 20, making up greater than 70% of the totalin the spring. This dominance was more pronounced inlow salinity waters from 0 to 10, where E. affiniscomprised 96% of the community. Eurytemora affiniscommonly occupies the upper reaches of estuaries, andis replaced with Acartia spp. as one moves seaward(Heinle, 1972; Bousfield et al., 1975; Collins andWilliams, 1981; Roddie et al., 1984; Baretta andMalschaert, 1988; Bradley, 1991). Acartia tonsa replacedthese species as the dominant summer calanoid.
The timing of species replacement differed amongsalinity ranges. In salinities ranging from 20 to 30Acartia tonsa succeeded all other species by June, com-prising more than 80% of the calanoid community(Fig. 2). The transition to A. tonsa occurred in July forsalinities 10–20. In low salinity waters (0–10), thetransition to A. tonsa was not as abrupt, where A. tonsaultimately replaced Eurytemora affinis in August. Thissuggests that a temperature–salinity interaction partlycontrols the seasonal succession between E. affinis andA. tonsa. This interaction has been reported elsewhere(Bradley, 1991; Kimmel and Bradley, 2001).
In terms of abundance, Acartia spp., Centropageshamatus, and Eurytemora affinis had a sharp increase innumbers sometime in the spring or early summer for all
subestuaries of Waquoit Bay, where nauplii outnum-bered copepodids and adults (Fig. 3). Copepod naupliiwere abundant from May through August, declining inabundance in all estuaries by the end of the summer,with the exception of Quashnet River in 1998, which hadlarge numbers of nauplii through October. Peak abun-dance for nauplii typically occurred from March to Mayoverlapping the seasonal occurrence of the adultcalanoid forms.
Acartia spp. were found in peak abundance duringthe spring and early summer, typically peaking in Mayor June (Fig. 3). The seasonal replacement of Acartiahudsonica with Acartia tonsa from spring to summer
0
20
40
60
80
100
20-30
E. affinis
C. hamatus
A. tonsa
A. hudsonica
0
20
40
60
80
100
% o
f tot
al a
dult
cala
noid
abu
ndan
ce
10-20
0
20
40
60
80
100
Month
0-10
M M J AA J
Fig. 2. Relative contribution of the different taxa of calanoid copepods
to the total adult calanoid community across season and salinity
ranges. The panels are labeled with a representative salinity range.
Data in the high salinity range were averaged for all Waquoit Bay
subestuaries and the Bay proper for 1998 and 1999. Data for the
intermediate to low salinity range represent averages for Childs River
and Quashnet River for 1998 and 1999. Bars represent standard error.
551D. Lawrence et al. / Estuarine, Coastal and Shelf Science 61 (2004) 547–557
Fig. 3. Seasonal abundance (GS.E.) of calanoid copepods in Waquoit Bay subestuaries. Acartia (hudsonicaC tonsa), Centropages hamatus, and
Eurytemora affinis represent the sum of copepodids and adults. CRdChilds River, QRdQuashnet River, SLPdSage Lot Pond, WBdWaquoit Bay
proper. For CR and QR, filled points represent mean abundance at salinities from 20–30, grey points represent mean abundance from 10 to 20, and
open points represent mean abundance from 0 to 10. Salinity !20 were not found in SLP or WB.
occurred quite quickly (Fig. 4), as documented else-where from the mid-Atlantic to New England (Fish,1925; Conover, 1956; Jeffries, 1962; Durbin and Durbin,1981). Jeffries (1962) suggests that temperature and
0
20
40
60
80
100
% o
f Aca
rtia
adu
lts
A. hudsonica
A. tonsa
M A M J J A S O N
Fig. 4. Relative percentage of Acartia hudsonica and Acartia tonsa to
the total Acartia spp. adults versus time. Data were averaged for 1998
and 1999 and pooled for all sites.
salinity regulate the replacement of A. hudsonica by A.tonsa, where A. tonsa is better able to propagate athigher temperatures and lower salinities than A.hudsonica. Additionally, Sullivan and McManus (1986)have shown that Narragansett Bay populations of A.hudsonica begin producing resting eggs at temperaturesgreater than 16 �C.
Centropages hamatus was found in greatest abun-dance during spring months, with peak abundancesometime between March and May (Fig. 3). The overallabundance of C. hamatus was low compared to Acartiaspp. and Eurytemora affinis, whose peaks exceeded 1000individuals m�3, suggesting that this species is moreephemeral in Waquoit Bay.
Eurytemora affinis was most abundant during springmonths, typically peaking in May (Fig. 3). Largenumbers of E. affinis were observed in the subestuariesof Waquoit Bay, outnumbering the other calanoid spe-cies present. The numbers of E. affinis in Waquoit Bayproper were low compared to the abundance found inthe Bay’s subestuaries. Assuming that we did not missthe peak in the Bay proper due to sample timing, this
552 D. Lawrence et al. / Estuarine, Coastal and Shelf Science 61 (2004) 547–557
may suggest that E. affinis maintains residency in thesesubestuaries. Several estuarine retention mechanismshave been documented for this species including verticalmigration in response to tidal cycling and the carrying ofeggs on females until hatching (Morgan et al., 1997;Roman et al., 2001). These mechanisms may account forthe distribution patterns observed here.
The abundance of Acartia hudsonica, Acartia tonsa,and Centropages hamatus increased significantly withsalinity during the growth period for each species (Table1, Fig. 5). This pattern of distribution is probably relatedto salinity dependent physiology of the animals (Anraku,1964b; Lance, 1965; Tester and Turner, 1991; Cervettoet al., 1999). Additionally, this pattern of distributionmay reflect a dilution effect. Here, calanoids deliveredwith salty water decrease in abundance as water travelsinto the upper reaches of the estuary where salinity islow. Eurytemora affinis abundance did not vary signif-icantly with salinity (Table 1, Fig. 5). The euryhalinecharacter that has been previously described for thisspecies (Roddie et al., 1984) is obvious from our results.
The abundance of both spring and summer assemb-lages of copepod nauplii did not vary significantly withsalinity (Fig. 5). Given the variety of copepod speciescontributing to the naupliar pool, and the varying sali-nity preferences known for these species, it is not
Table 1
Mean abundance of calanoid copepods as a function of salinity
Species Degrees of freedom H
Copepod nauplii
Spring 2 4.0 n.s.
Summer 2 1.9 n.s.
Acartia hudsonica
Copepodids 2 11.2**
Adults 2 9.2*
Acartia tonsa
Copepodids 2 18.4***
Adults 2 8.7*
Centropages hamatus
Copepodids 2 9.5**
Adults 2 11.1**
Eurytemora affinis
Copepodids 2 5.6 n.s.
Adults 2 0.8 n.s.
A Kruskal–Wallis test was used to determine differences in abundance
at the different salinity ranges. Data used for testing were limited to the
growth period for each species, i.e. the spring months of March
through May for A. hudsonica, C. hamatus, E. affinis, and spring
copepod nauplii, and summer months of June through August for A.
tonsa and summer copepod nauplii. Data were pooled for 1998 and
1999. Data for the 20–30 salinity range were pooled for all subestuaries
and the Bay proper. Data for 10–20 and 0–10 were derived by pooling
Childs River and Quashnet River sites at the respective salinities. A
log10 transformation was used to normalize the data for averaging. The
equation log(xC 1) was used with copepodid and adult data because
of zero points in the data. The H statistic is approximately distributed
as c2 (Sokal and Rohlf, 1969). H values marked with *Z significant at
the 0.05 level, **Z significant at the 0.01 level, ***Z significant at the
0.001 level, n.s.Z non-significant.
surprising that a relationship between abundance andsalinity was not observed. Identification of the nauplii tothe species level would certainly reveal more about theeffect of salinity on specific calanoid nauplii.
3.2. Calanoid abundance in relation toland-derived nitrogen loading
Due to the seasonal nature of Waquoit Bay cala-noid populations, interestuary comparisons were made
0
1
2
log
abun
danc
e (in
d. m
-3)
CopepodidsA. hudsonica
0
1
2 A. tonsa
0
1
Adults
0
0.4
0.8
0
1
2 C. hamatus
0
1
2
0
1
2
3
4
Salinity
E. affinis
0
1
0
1
2
3
4 SpringNauplii
0
1
2
3
4 Summer
0 30 0 10 20 302010
Fig. 5. Mean abundance (GS.E.) of dominant Waquoit Bay calanoids
in relation to salinity. Data used to obtain this mean were limited to the
growth period for each species and were averaged over 1998 and 1999 as
before. Data for the 20–30 salinity range were pooled for all sub-
estuaries and the Bay proper. Data for 10–20 and 0–10 were derived by
pooling Childs River and Quashnet River sites at the respective
salinities. Asterisks indicate significance according to Kruskal–Wallis
test. *Z significant at the 0.05 level, **Z significant at the 0.01 level,
***Z significant at the 0.001 level.
553D. Lawrence et al. / Estuarine, Coastal and Shelf Science 61 (2004) 547–557
during the growth/reproductive period for each species.Copepod nauplii were grouped into two seasons (springand summer) because of the difference in calanoidspecies present during these times. In addition, becausesalinity had a strong influence on the abundance of someWaquoit Bay calanoids, we restricted interestuary com-parisons to stations with comparable salinity ranges(20–30). This way we could look directly at the effect ofnitrogen loading rate on abundance without salinity asa confounding factor.
The abundance of both spring and summer assemb-lages of copepod nauplii did not vary significantly withland-derived nitrogen load (Table 2, Fig. 6). Copepodidand adult abundances of Acartia hudsonica, Acartiatonsa, and Eurytemora affinis did not vary with nitrogenloading rate (Table 2, Figs. 7 and 8). Assuming that foodis limiting to calanoids in Waquoit Bay (Durbin et al.,1983, 1992; Cubbage et al., 1999), the elevated concen-tration of food available to herbivore grazers in higherloaded subestuaries,most pronounced in summermonths(Fig. 9), could result in a greater abundance of calanoidsin those subestuaries. Egg production experiments con-ducted in the subestuaries of Waquoit Bay demonstratedthat A. tonsa has an elevated reproductive output in thehigher loaded subestuaries (Cubbage et al., 1999). Thus, itappears that although nutrient loading may result inshort-term changes in reproductive output, it does notresult in an overall difference in the abundance ofconsumers at different nitrogen loads.
Table 2
Mean abundance of calanoid copepods as a function of nitrogen
loading rate
Species Degrees of freedom H
Copepod nauplii
Spring 2 1.6 n.s.
Summer 2 0.8 n.s.
Acartia hudsonica
Copepodids 2 1.7 n.s.
Adults 2 3.5 n.s.
Acartia tonsa
Copepodids 2 5.3 n.s.
Adults 2 3.4 n.s.
Centropages hamatus
Copepodids 2 7.9*
Adults 2 10.5**
Eurytemora affinis
Copepodids 2 3.8 n.s.
Adults 2 2.0 n.s.
A Kruskal–Wallis test was used to determine differences in abundance
at different nitrogen loads. Abundance data used in testing were
limited to the growth period for each species as before. A log10transformation was applied to all data. The equation log(xC 1) was
used with copepodid and adult data because of zero points in the data.
Data from 1998 and 1999 were pooled for statistical testing and
restricted to salinities from 20 to 30. The H statistic is approximately
distributed as c2 (Sokal and Rohlf, 1969). H values marked with
*Z significant at the 0.05 level, **Z significant at the 0.01 level,
n.s.Z non-significant.
The short water residence time of Waquoit Baysubestuaries (2.3, 1.7, 1.5 d, for Childs River, QuashnetRiver, and Sage Lot Pond, respectively, based onKremer model, Valiela et al., in press) is one potentialmechanism responsible for the uncoupling of calanoidabundance from land-derived nitrogen load. For cala-noid abundance to change in relation to nitrogenloading the animals must be present in the estuary longenough to take advantage of available food supply.Generation times for these calanoid copepods are long(7–38 days dependent on temperature; Mauchline, 1998)relative to the time available for development within thesubestuaries of Waquoit Bay. Because calanoid distri-bution is determined in part by water currents, forcalanoids to be endemic in a body of water reproductivegains must balance advective losses. This does notappear to be possible for most species in Waquoit Bay.A comparative work by Pace et al. (1992) supports thisargument. They demonstrated that the biomass of zoo-plankton in the Hudson River was negatively related tothe rate of discharge and that zooplankton biomass oflakes, estuaries, and rivers differs in a manner consistentwith the differences in water residence time.
Eurytemora affinismay be a possible exception, whosesubestuary abundance was consistently larger than thatobserved in the Bay. Still this species did not vary in
Fig. 6. Abundance of copepod nauplii plotted versus nitrogen loading
rate. The spring nauplii assemblage is composed of A. hudsonica, C.
hamatus, and E. affinis, while summer nauplii are probably A. tonsa.
Abundance data shown here are log10 transformed and limited to the
growth period for each species as before. Abundance data are
restricted to salinities from 20 to 30 and pooled for 1998 and 1999.
Open circles represent a single tow at each nitrogen load.
554 D. Lawrence et al. / Estuarine, Coastal and Shelf Science 61 (2004) 547–557
abundance relative to nitrogen loading rate. In this caseother factors may be acting to uncouple differencesin food supply from a demographic response of thisspecies. Although phytoplankton concentrations may begreater in subestuaries with higher nitrogen loads thesephytoplankton may be unsuitable as food for calanoids
Fig. 7. Copepodid abundance of Acartia hudsonica, Acartia tonsa,
Centropages hamatus, and Eurytemora affinis plotted versus nitrogen
loading rate. Abundance data shown here are log10 transformed and
limited to the growth period for each species as before. The equation
log10(xC 1) was used with copepodid data due to zero points. Abun-
dance data are restricted to salinities from 20 to 30 and pooled for 1998
and 1999. Open circles represent a single tow at each nitrogen load.
Line represents results of linear regression analysis. R2 Z 0.92,
p! 0.05.
because they are too small for effective grazing, lowin nutritional value, or not easily digestible (Rytherand Sanders, 1980). A more complete description of thephytoplankton community of Waquoit Bay is necessaryto understand the impact of nutrient loading on the foodenvironment of calanoids (Tomasky, in preparation).
Fig. 8. Adult abundance of Acartia hudsonica, Acartia tonsa,
Centropages hamatus, and Eurytemora affinis plotted versus nitrogen
loading rate. Abundance data shown here are log10 transformed and
limited to the growth period for each species as before. The equation
log10(xC 1) was used with adult data due to zero points. Abundance
data are restricted to salinities from 20 to 30 and pooled for 1998 and
1999. Open circles represent a single tow at each nitrogen load. Line
represents results of linear regression analysis. R2 Z 0.94, p! 0.01.
555D. Lawrence et al. / Estuarine, Coastal and Shelf Science 61 (2004) 547–557
The uncoupling of calanoid abundance from nitrogenloading may also occur if calanoids consume a foodsource that does not vary according to nitrogen load.The diet of calanoid copepods is known to be diverse(consisting of diatoms, dinoflagellates, microzooplank-ton, and bacteria contained on detrital material), re-flecting the variety of phytoplankton and microplanktontaxa present in the environment (Kleppel, 1993). Atpresent we do not have estimates of microzooplanktonand detrital particles available as food to calanoids inWaquoit Bay and thus, we do not know if these poten-tial food sources vary across nitrogen loads. Therefore,we cannot rule out this hypothesis as a potential un-coupling mechanism.
Top–down perturbations may also contribute to theuncoupling of consumers from nutrient loads. Zoo-planktivors have been shown to weaken the coupling ofzooplankton from their food supply, and thus theavailability of nutrients (Micheli, 1999). Also, if therewere more predators at higher nutrient loads the poten-tial for top-down effects would be even more pervasive.However, Tober (2000) has shown the abundance ofMenidia menidia, the main zooplanktivorous fish inWaquoit Bay, does not vary with nitrogen loading rate.
Centropages hamatus was the only calanoid specieswhose abundance was significantly related to nitrogenload. In this case, however, the abundance was negativelyrelated to nitrogen loading rate, rather than increased inresponse to greater food supply (Table 2, Figs. 7 and 8).Estuaries with increased nitrogen loads may havenegative impacts on grazer populations, perhaps becauseof the greater frequency of low oxygen conditions thatoccur there. D’Avanzo and Kremer (1994) have recordedchronic hypoxia in bottom waters of the Childs River.Such conditions may reduce egg production (Marcuset al., 2004), decrease the viability of calanoid eggsspawned to the sediment (Marcus and Lutz, 1994), andincrease mortality of later life history stages (Stalder and
0
20
40
60
0 100 200 300 400 500 600
Chl
a (m
g m
-3)
SLP QR
Nitrogen loading rate (kg ha-1 y-1)
CR
Fig. 9. Summer whole estuary averaged chlorophyll a and measured
total nitrogen load for 1999 (G. Tomasky, CICEET unpublished data).
Summer months include June, July, and August. CRdChilds River,
QRdQuashnet River, SLPdSage Lot Pond. Line represents results of
linear regression analysis. yZ 0.08x C 3.04, R2 Z 0.98, p! 0.05.
Marcus, 1997). Centropages hamatus is known to bemore sensitive to hypoxia thanAcartia tonsa (Stalder andMarcus, 1997). Such interspecific differences in responseto hypoxia may be one possible explanation why only C.hamatus was negatively related to nitrogen load.
Alternatively, some difference in food composition ofthe subestuaries of Waquoit Bay, influenced by thedifferences in nitrogen loading rates, may be responsiblefor the negative relationship observed with Centropageshamatus. In this scenario, higher nutrient loads mayalter the food community to a type less desirable ornutritionally adequate for C. hamatus. Dietary differ-ences and food requirements are known to exist betweenspecies of calanoids (Kleppel, 1993).
3.3. Trophic interactions
The potential links between calanoid abundance andland-derived nitrogen loading that we have consideredare indirect. Nitrogen delivered from land enters theestuary and stimulates primary production. This resultsin a large standing crop of phytoplankton in the highlyenriched subestuaries (Childs River), relative to moremesotrophic subestuaries (Quashnet River, Sage LotPond; Fig. 10, top panel). The timing of the chlorophyll
Chlorophyll concentration
0
40
80
120 CRQRSLPWB
Calanoid abundance
0
400
800
1200
1600
M A M J J A S
chl a
(mg
m-3
)in
d. m
-3
Fig. 10. Seasonal distribution of mean chlorophyll a concentration and
mean calanoid abundance for three subestuaries of Waquoit Bay and
the Bay proper. Measurements of calanoid abundance and chlorophyll
concentration (G. Tomasky, CICEET unpublished data) were taken in
1999. Calanoid abundance data are restricted to high salinity sites (20–
30). Chlorophyll concentration data represent a whole estuary average.
Calanoid abundance includes all species and both copepodid and adult
life history stages. Bars represent standard error.
556 D. Lawrence et al. / Estuarine, Coastal and Shelf Science 61 (2004) 547–557
bloom, presumably a prime food source for calanoidcopepods, did not, however, coincide with the peak incalanoid abundance (Fig. 10, bottom panel). Perhapscalanoid populations exert a powerful top-down controlon phytoplankton, reducing standing crop until latesummer. Data on net primary production of chlorophyllcould be used to test this hypothesis. Net primary pro-duction is a measure of the rate at which biomass isaccumulated rather than an indicator of standing crop.If production was high during the spring while standingcrop of phytoplankton was low, losses in biomass maybe attributable to grazing.
Predators may be responsible for the low abundanceof calanoids during the summer phytoplankton bloom.A rapid reduction in Acartia tonsa abundance in latesummer has been documented for other nearby systemsand is most likely related to ctenophore blooms thatpeak in August (Hulsizer, 1976; Kremer, 1976). A bloomof the ctenophore Mnemiopsis leidyi occurs in WaquoitBay in late summer months (personal observation).After calanoid abundance becomes negligible, grazingpressure on the phytoplankton is released. This inter-action may be responsible for the late summer chloro-phyll peak consistently observed in Waquoit Bay.
Acknowledgements
This research was supported by the National Estua-rine Research Reserve Graduate Research Fellowshipfrom the National Oceanic and Atmospheric Adminis-tration (NA97OR0141). Additional funds were providedby the Boston University Ablon-Bay Graduate Fellow-ship and The Cooperative Institute for Coastal andEstuarine Environmental Technology (CICEET-UNH#99-304, NOAA NA87OR512). We thank C.Furlong, A. Evgenidou, M. Cole, and A. Cubbage fortheir assistance in the field, and N. Copley and S.Thompson who helped with copepod identification.Special thanks to the Waquoit Bay National EstuarineResearch Reserve for use of their facilities.
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