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Decadal changes in zooplankton abundance and phenology of LongIsland Sound reflect interacting changes in temperature andcommunity composition

Edward Rice a, b, Gillian Stewart a, b, *

a School of Earth and Environmental Sciences, Queens College, City University of New York, Flushing, New York 11367, USAb School of Earth and Environmental Sciences, Queens College, and The Graduate Center, City University of New York, 365 Fifth Ave, New York, NY, 10016,USA

a r t i c l e i n f o

Article history:Received 29 April 2016Received in revised form3 August 2016Accepted 5 August 2016Available online 8 August 2016

Keywords:Long Island SoundZooplanktonPhenologyWarmingCopepodsCtenophores

a b s t r a c t

Between 1939 and 1982, several surveys indicated that zooplankton in Long Island Sound, NY (LIS)appeared to follow an annual cycle typical of the Mid-Atlantic coast of North America. Abundance peakedin both early spring and late summer and the peaks were similar in magnitude. In recent decades, thiscycle appeared to have shifted. Only one large peak tended to occur, and summer copepod abundancewas consistently reduced by ~60% from 1939 to 1982 levels. In other Mid-Atlantic coastal systems such adramatic shift has been attributed to the earlier appearance of ctenophores, particularly Mnemiopsisleidyi, during warmer spring months. However, over a decade of surveys in LIS have consistently foundnear-zero values in M. leidyi biomass during spring months. Our multiple linear regression model in-dicates that summer M. leidyi biomass during this decade explains <25% of the variation in summercopepod abundance. During these recent, warmer years, summer copepod community shifts appear toexplain the loss of copepod abundance. Although Acartia tonsa in 2010e2011 appeared to be present allyear long, it was no longer the dominant summer zooplankton species. Warmer summers have beenassociated with an increase in cyanobacteria and flagellates, which are not consumed efficiently byA. tonsa. This suggests that in warming coastal systems multiple environmental and biological factorsinteract and likely underlie dramatic alterations to copepod phenology, not single causes.

Published by Elsevier Ltd.

1. Introduction

In coastal and marine systems, a key link between primaryproducers and higher trophic levels are the zooplankton(Wickstead, 1976). The zooplankton of the Mid-Atlantic is numer-ically dominated by copepods - microcrustaceans that graze uponphytoplankton, microzooplankton and juveniles (nauplii) of theirown species as well as nauplii of other copepod species (Turner,2004). Copepods dominate the gut contents of larval cod,haddock, and anchovy, and thus serve as an important link inaquatic foodwebs from phytoplankton and microzooplankton tolarval fish (Turner, 1984). In Mid-Atlantic coastal systems, copepodabundance has historically been bimodal, with peak summer (July,

August, September) abundance equaling or exceeding that in thespring (April, May, June) (Kremer, 1994).

However, zooplankton can also respond very quickly to physicalforcings associated with climate change, such as changes in tem-perature, salinity, or stratification (Richardson, 2008). Such changesappear to be occurring in Northeast and Mid-Atlantic coastal sys-tems. Annual regional warming of surface waters at the rate of0.03e0.04 !C yr"1 has been reported for Long Island Sound (LIS),Narragansett Bay, and Massachusetts Bay (Sullivan et al., 2001;Nixon et al., 2004; Rice and Stewart, 2013) (Fig 1A, Williams,1981, Fig 1B; Lewis and Needall, 1987).

In Narragansett Bay, this warming has been associated with aunimodal zooplankton abundance pattern of reduced summercopepod abundance and a single spring copepod abundance peak(Oviatt, 2004; Costello et al., 2006; Beaulieu et al., 2013). Thesechanges were attributed to greater overlap between copepod preyand the ctenophore Mnemiopsis leidyi (a gelatinous secondaryconsumer), increased grazing by zooplankton of primary

* Corresponding author. School of Earth and Environmental Sciences, QueensCollege, City University of New York, Flushing, New York 11367, USA and TheGraduate Center, City University of New York, USA.

E-mail address: [email protected] (G. Stewart).

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http://dx.doi.org/10.1016/j.marenvres.2016.08.0030141-1136/Published by Elsevier Ltd.

Marine Environmental Research 120 (2016) 154e165

producers, and greater respiration losses by producers duringwarmer winter and spring months (Oviatt, 2004).

Several aspects of M. leidyi life history support the hypothesisthat M. leidyi can cause the loss of summer zooplankton: 1) it is akey predator of copepods during summer alongMid-Atlantic coasts2) M. leidyi is tolerant of a wide range of environmental conditions,and 3) M. leidyi is able to feed on a large size range of particles andorganisms (Purcell, 2009). However, estimates of M. leidyi preda-tion rates on copepods can range widely, from 0.3% to 58.7% d"1

(Purcell, 2009). In coastal Rhode Island, Kremer (1979) found thatM. leidyi could typically remove 10e11% of daily copepod abun-dance during summers. In Chesapeake Bay, Purcell et al. (1994)

found that the rate of copepod production was an order ofmagnitude higher than the predation rate, and ctenophore preda-tion alone was unable to control copepod populations. More recentresearch by Vliestra (2014) in the Thames River estuary (adjacent toLIS) found that the predation impact ofM. leidyi on copepods was amaximum of 2.2% of the standing stock of copepods per day.

Other hydrodynamic, biotic and climatic factors may resolve thediscrepancy. During years in which cnidarian predators of M. leidyiare absent from the Chesapeake Bay estuary, Purcell and Decker(2005) found M. leidyi predation impact increased to 45% of thecopepod community per day. The climatic factors that appeared toincrease M. leidyi predation on copepods were low salinity (which

Fig. 1. A. LIS locations and survey stations referenced in this article. Deevey (1956) stations referenced elsewhere are numbered (where indicated). Base map is from Williams(1981). The Central Basin extends from 73!100 (Bridgeport) to roughly 72!350 (The mouth of the Connecticut River). B. Location of the Central basin of LIS (1A stations are inthe shaded box) in relation to coastal systems referenced in this article. Narragansett Bay is between Rhode Island and Massachusetts. The Thames River Estuary is north of Fisher'sIsland. Base map is from Lewis and Needall (1987).

E. Rice, G. Stewart / Marine Environmental Research 120 (2016) 154e165 155

reduces cnidarian abundance) and higher spring temperatures(Sullivan et al., 2001; Oviatt, 2004). Increased abundance andpredatory impact of gelatinous zooplankton (such as M. leidyi) hasthus been suggested as a consequence of a warmer, overfished, andeutrophic coastal ocean (Mills, 1995; Richardson et al., 2009). Inaddition, more enclosed coastal waters (with longer residencetimes) also promote ctenophore abundance (Vansteenbrugge et al.,2015). To test whether earlier appearance of ctenophores inwarming coastal systems causes a loss of summer copepods re-quires a long-term data set of physical factors, zooplankton, andtheir ctenophore predators.

One system with such a record is LIS, a large, semi-enclosed,partially mixed estuary at the northern end of the Virginianbiogeographic community (Deevey, 1956; Pelletier et al., 2012).Since 1938, the zooplankton community of the Central Basin of LIShas been surveyed and quantified roughly every 15 years, with themost continuous series of surveys beginning in 1991 (Riley, 1941;Deevey, 1956; Carlson, 1978; Peterson, 1985; Capriulo et al., 2002;Dam and McManus, 2009). During 1952e1953, Deevey (1956)noted that the LIS gelatinous zooplankton community was mainlycomprised of M. leidyi and the cnidarians Aurelia Aurelia andChrysaora quinquecirrha. Deevey (1956) noted that M. leidyi wasabundant during late summer 1952e1953, but could only speculatethat the influx of M. leidyi caused a rapid decline in summer co-pepods. Carlson (1978) was the first to quantifyM. leidyi biomass incentral LIS (Fig. 1A), recording biomass during January, March, May,July, September, and November.

Besides cnidarians and M. leidyi, the only other gelatinouszooplankton found to occur in LIS are Beroe cucumis and Pleuro-brachia pileus. The latter is a small, spherical ctenophore less thanhalf the diameter M. leidyi (2.0 cm versus 5e7.6 cm) and tends tooccur only in winter. B. cucumis is more elongated and twice thesize (typically 15 cm long) relative to M. leidyi.

In Central LIS, temperatures during all seasons have significantlyincreased since 1948, with a consistent trend most evident since1975 (Rice and Stewart, 2013). This warming has been driven byincreasing Northern hemisphere temperature due to climatechange, which has increased annual temperature at the rate of0.03 !C yr"1 since 1970e1980 throughout the coastal NortheastUnited States (Nixon et al., 2004). Spring and summer zooplanktonsurveys in LIS prior to 1985 have happened under conditions cooler

than those during surveys after 1985. Our intent is to test the hy-pothesis that a summer decline in LIS copepod abundance can beconclusively linked to earlier appearance of ctenophores in springas annual temperatures warm.

2. Methods

2.1. Historic surveys

To establish a historical context for analysis of copepod andctenophore abundance, previous surveys of the Central Basin(Table 1) were obtained from archival and published sources.Where tabular data was not available (Deevey, 1956; Capriulo et al.,2002), the program DataThief (freeware graphical interpolationsoftware) was used to reconstruct numbers from figures for 4 of 18annual surveys available. Although these surveys varied somewhatin parameters, intensity, scope, and specific location, they providethe only baseline data for analysis of current trends.

The copepod surveys can be divided into three classes based onnet size: (1) a 202 mm mesh, (2) a 150e158 mm mesh, and (3) a119 mmmesh. Since the focus of this article is changes in phenologyand not absolute abundance, we have normalized each survey'sdata by dividing the monthly abundance by the annual meannumber of copepods per month. This allowed us to compare rela-tive differences in monthly abundance over time between differentsurveys. The earliest zooplankton survey was a monthly 119 mmmesh inshore sample obtained by Riley (1941) over 1938-39 fromMilford Harbor and Welch's Point, CT (Fig. 1A). Samples were pre-served in buffered formalin (concentration unreported). No data onctenophores was given. For further details on these surveys, refer toRice et al. (2015).

Deevey (1956) conducted the next survey from March 1952 toJune 1953. Zooplankton towswere oblique and used a 158 mmmeshnet with a Clarke-Bumpus sampler. Buffered formalin was thepreservative, but concentration was not reported (Deevey, 1956).Ctenophore abundance was not quantified. Copepod abundancewas interpolated from figures, since tabular data was provided onlyfor zooplankton. Deevey (1956) also reported zooplankton biomass(wet-weight) and noted it had a similar phenology to zooplanktonabundance (data not shown).

Carlson (1978) conducted the next survey of the Central Basin, at

Table 1LIS Central Basin zooplankton surveys enumerated by year and mesh size, whether ctenophores were quantified, mean monthly copepod abundance, mean spring copepodabundance, mean summer copepod abundance and sampling frequency (monthly and weekly surveys were typically bi-weekly during summer). Largest seasonal abundancesfor each survey/year are in italics and bold.

Survey þ mesh size Ctenophorequantified?

Year Monthly mean abundance(m"3, $ 104)

Spring mean abundance(m"3, $104)

Summer mean abundance(m"3, $104)

Surveyfrequency

Riley (1941) 119 mm N 1938e9 4.50 6.98 9.05 Twice weeklyDeevey (1956) 158 mm N 1953e4 3.40 4.77 4.58 Bi-weeklyPeterson (1985) 202 mm N 1982 3.01 8.35 13.1 WeeklyCapriulo et al. (2002)

202 mmN 1993 1.39 4.22 0.14 Monthly and

weeklyCapriulo et al. (2002)

202 mmN 1994 1.08 2.77 0.69 Monthly and

weeklyCT DEEP 202 mm Y 2002/

20041.80 4.45 1.50 Monthly and

weeklyCT DEEP 202 mm Y 2003 2.80 5.85 3.00 Monthly and

weeklyCT DEEP 202 mm Y 2007/

20083.64 10.2 1.25 Monthly and

weeklyRice (150) mm Y 2010 1.51 2.79 1.05 Monthly and

weeklyRice (150) mm Y 2011 1.31 2.58 0.97 Monthly and

weeklyCT DEEP 202 mm Y 2012 2.51 4.47 0.65 Monthly and

weekly

E. Rice, G. Stewart / Marine Environmental Research 120 (2016) 154e165156

the tidal inlet to Flax Pond (Fig. 1A) near Stony Brook, NY, alwaysduring incoming tide. This survey focused on biomass (dry weight)of zooplankton, however, so abundance data is not available.Preservation information was also not given. Carlson (1978) onlyreported the biomass of all microcrustacean zooplankton, but inLIS, copepods typically represent ~90% of zooplankton (Deevey,1956; Capriulo et al., 2002).

Peterson (1985) recorded copepod abundance during weeklycruises fromMarch 1982 to July 1983 (Fig.1A). Peterson (1985) useda 202 mm mesh net, hauled vertically from bottom to surface. Nodata is given on preservation methods, but copepods were identi-fied to species and life stage from subsamples. Ctenophores werenot sampled or identified.

The next survey, by Capriulo et al. (2002), was conducted fromJune 1992 to September 1995 across LIS, with one coastal station inthe Central Basin. This station was co-located with the Deevey(1956) station near the National Oceanic and AtmosphericAdministration (NOAA) Milford laboratory (Fig. 1A) and was visitedmonthly. Oblique towswere usedwith a 202 mmmesh net to collectcopepods. The mesozooplankton samples were preserved with 10%buffered formalin. Capriulo et al. (2002) noted but did not quantifyctenophores. Offshore Central Basin tows were not conducted, butspatial gradients and seasonal abundances were similar to the laterConnecticut Department of Energy and Environmental Protection(CTDEEP) survey.

CTDEEP (2002e4, 2007e8, 2012) mesozooplankton sampleswere collected with oblique tows of a 202 mm mesh net from onestation in the far western Narrows (B3), two stations in theWesternBasin (D3, F2) two stations within the Central Basin, H4 and I2, andone station in the Eastern Basin (K2) (Fig. 1A). Except duringsummer (when stations were visited bi-weekly), these stationswere visited once per month, and samples were preserved in 5%buffered formalin. Results and CTDEEP methods have beenanalyzed and reported by Dam and McManus (2009). Micro-zooplankton samples for stations H4 and I2 were pooled fromsurface, mid-depth, and bottom Niskin-samples and preserved inLugols (concentration not given) (Dam and McManus, 2009). Toensure standardization, all of the copepod and gelatinouszooplankton data used in our M. leidyi and copepod models wasfrom the 202 mm mesh CTDEEP survey.

Between 2002 and 2012, M. leidyi wet-weight biomass wasmeasured via volume displacement in-situ by CTDEEP from livegelatinous zooplankton caught with a 202 mm mesh net andseparated from other zooplankton by a 1mm sieve. After collection,CTDEEP sorted gelatinous zooplankton into Scyphozoans (Aurelia,Cyanea, Chrysaora) and Ctenophora (Mnemiopsis and Pleurobrachia)by genus. Beroe was not reported in the 2002e20012 CTDEEP sur-veys. During summer, 90e100% of ctenophore biomass was re-ported to be Mnemiopsis in the CTDEEP surveys, hence“ctenophore” can be assumed to refer to Mnemiopsis in the rest ofthis paper. Regarding biomass, it should be noted that Raskoff et al.(2003) recommended finer mesh nets for ctenophore collection(they are less likely to break apart in finer mesh), thus the CTDEEPdata may underestimate ctenophore biomass.

2.2. New surveys

We conducted our own copepod and ctenophore surveys for thisstudy fromMarch 2010 to September 2011. During the 17months ofoffshore cruises, bi-weekly surveys were conducted during thesummer sampling seasonwith CTDEEP. For ctenophore abundance,we collected ctenophore samples in two phases. A preliminary July2009eJuly 2010 onshore survey was performed from Central Basindocks at Mattituck and Stony Brook Harbor with a 150 mm meshnet, during which counts of ctenophores and classification by size

were made after collection. From March 2010 to November 2011the second phase was completed with CTDEEP from the availableoffshore Central Basin stations, (H2, H4, H6 and I2) (Fig. 1A) and inaddition, Station 2 from Deevey (1956) (located northeast of H4).Our 2010e2011 survey visited 2e3 stations (from those above)during each cruise and used vertical tows with a 150 mm mesh net.

Sub-sampling and preservation for analysis was performed insitu after collection following the methods described by Kideys andRomanova (2001). If gelatinous zooplankton abundance was not sohigh as to clog the mesh, (preventing a volume estimate) contentsof the net were rinsed through a 2 mm sieve into a 10 L containerand all ctenophores retained on the sieve were enumerated. Ifgelatinous abundance was higher, sub-sampling of ctenophoreswas conducted by re-suspending all gelatinous zooplanktonretained by a 2 mm sieve in 10 L of seawater collected in-situ andverified free of ctenophores > 2 mm in diameter. After gently stir-ring, a 500 ml clear plastic container was used to collect cteno-phores. All ctenophores present in 500 ml were counted, and sub-sampling continued until three successive counts differed by <10%.

During our ctenophore survey, copepodswere also collected andcounted from the same locations in the Central Basin of LIS usingthe same 150 mmmesh net. Copepods were subsampled after beingre-suspended in a 10 L container of local seawater. The contentswere gently stirred, and subsamples were drawn with a 50 mlpipette until 500 ml was collected. A 5% Lugol's iodine preservativewas added for later analysis. Sub-samples were kept in coolers inthe field, and transferred to a 10 !C incubator upon return to thelaboratory. Enumeration and identification of copepod samples, aswell as size analysis, was carried out via dissecting microscopewithin a year of collection, the recommended timeframe for iden-tification of zooplankton preserved in Lugol's solution (Harris et al.,2000). Key taxonomic features from Johnson and Allen (2005) wereused to identify adult copepods. To standardize counting effort withprior surveys that reported sample counts (Capriulo et al., 2002),100e150 copepods were counted from each sub-sample.

2.3. Physical data

Temperature data came from the NOAA laboratory at Milford(the most extensive available) and covers the 1948e2014 period.We examined monthly values based on daily measurements from1948 to 1975 using a Bristol thermograph. From 1976 to 2012 dailymeasurements were continued, but with thermometer readings ofsand-filtered harbor water pumped into the laboratory. No signif-icant change appears to have occurred during the transition be-tween methods. CTDEEP measured the offshore Central Basinchemical and physical data used in our models fromAugust 2002 toOctober 2004, March 2007 to April 2008, and January to December2012. Dissolved oxygen, salinity and temperaturewere recorded in-situ via a Sea-Birdmodel SBE-19 SeaCat Conductivity-Temperature-Depth (CTD) profiler. Surface and bottom dissolved oxygen sampleswere later measured via the Winkler method.

2.4. Statistics and modeling

We investigated factors possibly influencing summer copepodabundance and ctenophore biomass with linearmultiple regressionmodeling of summer CTDEEP data for 2002e2008. Multipleregression analysis is often used by ecologists to investigate theimpact of various environmental factors on organismal, population,and community ecology (Graham, 2003). For our models of sum-mer copepod abundance and M. leidyi biomass, we chose a timerange (2002e2004, 2007e2008) that allowed us to includemicrozooplankton abundance and biomass, surface temperature,chlorophyll, salinity and dissolved oxygen as potential explanatory


variables in the models. Microzooplankton are a significant foodsource for copepods (Turner, 1984) and M. leidyi (Stoecker et al.,1987), but data was not available for other surveys, hence we didnot attempt to create a copepod abundance or ctenophore biomassmodel for those years.

For our copepod abundance model, M. leidyi biomass wasincluded as variable. Other predators, such as fish larvae, chaeto-gnaths, and larger crustaceans, rarely appear in CTDEEPzooplankton surveys and were not included. For M. leidyi biomass,copepod abundance was included as a potential factor. M. leidyibiomass was normalized via logþ1 transformation, as suggested forlinear regression modeling of highly variable ecological data(Mascaro et al., 2011). For 2002e2013, if ctenophore biomass foreach month was normally distributed, that data was used togenerate error bars for analyses of the mean values for thosemonths (SE¼Standard Error).

All statistical tests and analysis were run in R, version 2.11.1. Forlinear multiple regressionmodels, we tested for skewness, kurtosis,non-linearity, homoscedasicity, and linkage. Stepwise Akaike In-formation Criteria (AIC) analysis was used to identify unnecessaryvariables, which were removed from the model prior to furtheranalysis. A Bonferroni test was used to check for outliers. Collin-earity, autocorrelation, and non-linearity were ruled out by avariance inflation factor test, a Breusch-Godfrey test, andComponent þ Residual and Quantile-Quantile (QQ) plots, respec-tively. For our analysis of the statistical significance of long-termchanges in copepod abundance we included all available datafrom the 1992e2012 period, normalized to proportional abun-dance. To determine if a change in proportional abundance wassignificant, we calculated Bayesian credible intervals from theresulting time series using a flat prior and the quantile method.Credible intervals do not require a normal distribution (Balazs andChaloupka, 2004), and are useful for analyzing plankton time-series(Boyce et al., 2010).

For Central Basin seasonal temperature timeseries analysis, wefollowed the methodology that Rice et al. (2015) used for annualtemperature timeseries analysis in the Central Basin - the Kendalltest. Since it is a nonparametric method of estimating a trend overtime, it is more robust than the ordinary least-squares approach.Using the kendall package in R, we calculated tau (correlation) and pvalues (significance). The slope of the trend was found with theTheil-Sen approach in the R package zyp. The Theil-Sen estimator isalso a non-parametric method of analyzing linear trends (Sen,1968). A Breusch-Godfrey test for serial autocorrelation waspassed for annual temperature values, indicating that thesemethods were appropriate.

3. Results

3.1. Zooplankton surveys

The seasonal average of summer copepod abundance exceededor nearly equaled the seasonal average of spring copepod abun-dance in 1938e1939, 1953e1954, and 1982e1983 (Riley, 1941;Deevey, 1956; Peterson, 1985) (Table 1). Zooplankton biomasswas significantly correlated (r2 ¼ 0.56, p≪0.01) with copepodabundance during summer and spring 1953e1954. Summer peaksin zooplankton biomass (1.72 ml m"3 and 1.62 ml m"3) were alsolarger than spring peaks (1.28 ml m"3 and 0.73 ml m"3) in bothyears (Deevey,1956). During the 1970s, Carlson (1978) recorded dryweight biomass of Central Basin zooplankton (primarily copepods),and found summer biomass (48.5 mg m"3) also nearly equal tospring biomass (50.0 mg m"3).

The pattern of summer copepod abundance equaling orexceeding that of spring in the surveys between and including 1938

and 1983 appeared to reverse in the later surveys between 1993and 2012. In 1993, 1994, Capriulo et al. (2002) found spring abun-dance was an order of magnitude greater than summer (Table 1). In2002/4, CTDEEP found spring copepod abundance nearly threetimes summer copepod abundance. In 2007/8, this patterncontinued and spring copepod abundance was almost an order ofmagnitude larger than summer copepod abundance. These trendscontinued in our 2010 and 2011 surveys and the CTDEEP, 2010survey (Table 1). These declines in summer copepod abundancewere most pronounced for the normally summer-dominantcopepod, Acartia tonsa (abundance data not shown).

However, it is possible these trends were actually reflective ofnonrandom zooplankton aggregations biasing our surveys(“patchiness,” Falt and Burns, 1999). To determine if this was thecase, we compared zooplankton abundance at all reported stationsvisited in the Deevey (1956) 1952-4 surveys (Fig. 2A) withzooplankton abundance reported from all available CTDEEP LISstations reported by Dam and McManus (2009) (Fig. 2B). At all fourstations visited in 1952e4, a summer peak in zooplankton abun-dance occurred that was at least 68.6% of the spring peak inmagnitude, and the summer peak was on average 85.4% of thespring peak. In 2007-8, all Central and Western Basin CTDEEPstations had summer peaks that were between 7.98% and 41.6% ofspring peaks (the mean was 20.0%). The only CTDEEP stations thatdid not follow that pattern were at the extreme ends of LIS, stationB3 in the Narrows and station K2 in the Eastern Basin.

Our analysis of normalized surveys conducted between 1938and 1983 indicate a recurring pattern of at least two peaks of nearor equal copepod abundance, with spring and summer similar inmagnitude (Fig. 3A). This pattern of bimodal copepod phenologywas consistent across these earlier surveys of different mesh sizes(119 mm,158 mm, and 202 mm). Surveys between 1993 and 2012 hadone distinct spring peak in copepod abundance, generally betweenlate May and early June (Fig. 3B). This pattern of unimodalphenology between 1993 and 2012 was evident in surveys ofdifferent mesh sizes (150 mm and 202 mm). Based on the inter-annual variation in monthly series in the CTDEEP data, the lateMaye early June (spring) peak in proportional copepod abundancethat defined the 1993e2012 pattern was significantly higher(p ¼ 0.05) than the 1993e2012 summer abundance.

In terms of abundance, during summer in 1952e3 Deevey(1956) found that A. tonsa, Paracalanus crassiostris, and Oithona spdominated the copepod community sampled with their 158 mmmesh net. In our 2010e2011 survey using 150 mmmesh, these threecopepods again dominated copepod abundance in summer sam-ples, but A. tonsa decreased from 60% in August 1952 to 36% inAugust 2010 and 32% in August 2011 (Fig 4). Similar declinesoccurred in September: A. tonsa was 50% of the copepod commu-nity in September 1952 but only 10% of the community inSeptember 2010, and 28% in September 2011. On the other hand,A. tonsa expanded its proportion in winter, increasing from 10% ofthe copepod community in February 1952e53 to 40% in 2011. In allof these instances, the changes in A. tonsa percentage exceeded a95% confidence interval based on interannual variation in A. tonsapercentage.

Carlson (1978) reported insignificant (~0) M. leidyi wet weightbiomass for January, March 1e15, March 16e30, and May. M. leidyibiomass during July (366mlm"3) and September (182mlm"3) wassignificantly higher, but November M. leidyi biomass was minor(6.92 ml m"3). For 2002e2012, the lowest seasonal ctenophorebiomass was spring (0.70 ml m"3), followed by winter(1.03 ml m"3). The lowest monthly averages for ctenophorebiomass were January (0.00 ml m"3) and June (0.02 ml m"3). Foryears in which all summer months were surveyed, ctenophorebiomass tended to peak in September (5 of 6 years). September also


had the highest mean ctenophore biomass of all months(363 ml m"3 þ/"114 SE), but was not significantly different thanAugust.

We surveyed ctenophore abundance with CTDEEP between2010 and 2011 (Fig. 5A) and found ctenophore abundance in bothyears peaked earlier than ctenophore biomass tended to peak over2002e2012. Abundance was lowest in spring (0.17 ctenophores

m"3) and winter (1.43 ctenophores m"3). The only apparent dif-ference between biomass and abundance patterns during thisperiod was that abundance tended to peak in late July - earlyAugust (5.45 ctenophores m"3), a month earlier than biomass.M. leidyi displayed no long-term trends in biomass on an annual,seasonal, or monthly basis in the 2002e2012 CTDEEP survey data(Fig. 5B).

Fig. 2. A. Monthly zooplankton abundance reported by Deevey (1956) from Stations 1, 2, 5, and 8 in the Central Basin of LIS. B. Monthly zooplankton abundance for LIS as reportedby CTDEEP (Dam and McManus, 2009) in 2007e2008: the Narrows (Station B3), the Western Basin (D3 and F2), the Central Basin (H4, I2), and the Eastern Basin (K2).


Fig. 3. A. Monthly copepod abundance for surveys of the Central Basin of LIS between 1938 and 1982. B. Monthly copepod abundance for surveys of the Central Basin of LIS between1993 and 2012. All monthly values are normalized to mean monthly proportion for each year. Error bars (white boxes) represent 95% credible intervals for interannual variation inCTDEEP data.

Fig. 4. Percentage of the copepod community in 1952e4 represented by adult A. tonsa vs the percentage of the copepod community in 2010 and 2011 represented by adult A. tonsa.Error bars are Bayesian Credible Intervals based on monthly variation in A. tonsa community percentage during 1982e3, 1992-4, 2002e2004, and 2007e8.


3.2. Zooplankton modeling

Linear multiple regression modeling of summer copepodabundance between 2002 and 2008 indicated copepod abundancewas negatively related to salinity and M. leidyi biomass. The modelwas significant (p ¼ 0.008) and explained 43% of the variation insummer copepod abundance from 2002 to 2008. Salinity and logþ1transformed M. leidyi biomass were the only factors not flagged asredundant by AIC stepwise regression (Table 2). Surface values forchlorophyll, dissolved oxygen, and temperature were not signifi-cant factors in summer copepod abundance. Lower salinity was

significantly (at a ¼ 0.05) related to higher summer copepodabundance. Central Basin station differences in salinity exceededtemporal differences on a monthly or annual basis. Ctenophorebiomass was not a significant (p ¼ 0.05) factor at the a ¼ 0.05 level,but the model was no longer significant without ctenophorebiomass and explained 25% less of the variation in copepod abun-dance when M. leidyi biomass was selectively removed and themodel re-run.

The linear model of summer ctenophore biomass between 2002and 2008 was also significant (p≪0.01) and explained 35% of thevariation in logþ1 transformed summer M. leidyi biomass. Surface

Fig. 5. A. Left axis: Monthly and bi-weekly (during summer) observations of ctenophore biomass by the CTDEEP during 2002e2012 at offshore Central Basin CTDEEP stations H4and I2. Right axis: Monthly and bi-weekly (during summer) observations of ctenophore abundance by Rice during 2010e2011 at offshore Central Basin CTDEEP stations H2, H4, H6,and I2. B. Spring (April, May, June), Summer (July, August, September), and Annual mean M. leidyi biomass from 2002e2012 (“Cteno” refers to M. leidyi).

Table 2Key parameters and statistical test results frommodels of summer copepod andM. leidyi biomass. Stepwise AIC analysis (run in both directions) was used to reduce the numberof initial parameters and avoid over-fitting the model. In the table “na” refers to “not applicable.”

Linear Model Variables examined Retained after AIC? P-value Coefficient T-statistic

Summer copepod abundanceModel r2 (adj.): 0.43Model p-value: 0.01

Chlorophyll A No na na naM. leidyi biomass Yes 0.05 "10.9 "2.05Salinity (surface) Yes 0.01 "14.5 "2.85Microzooplankton biomass No na na naMicrozooplankton abundance (Log10) No na na naDissolved O2 (surface) No na na naTemperature (surface) No na na na

Summer M. leidyi biomass (log10 þ1 transformed)Model r2 (adj.): 0.35Model p-value: 0.02

Chlorophyll A No na na naCopepod abundance Yes 0.03 "0.02 "2.46Microzooplankton biomass Yes 0.03 0.02 2.39Microzooplankton abundance (Log10) No na na naDissolved O2 (surface) No na na naTemperature (surface) No na na naSalinity (surface) No na na na


chlorophyll, salinity, temperature, and dissolved oxygen wereremoved after stepwise AIC analysis as redundant or meaninglessvariables, while copepod abundance and microzooplanktonbiomass were retained as significant variables. Both terms weresignificant at a ¼ 0.05 (p ¼ 0.03 for copepods, p ¼ 0.04 for micro-zooplankton). Copepod abundance was negatively related to sum-mer ctenophore biomass, while microzooplankton biomass waspositively related.

3.3. Physical changes

Between 1948 and 2014, statistically significant warming in theCentral Basin occurred during all seasons (positive slope, p-value≪0.01), but the rate and variability of the warming trend varied(Fig. 6). Fall temperatures warmed at the most consistent rate,0.03 !C yr"1 (tau¼ 0.40). Summer andwinter warming trends werethe next most consistent (tau ¼ 0.36), but the rates differed.Summer warmed at 0.02 !C yr"1, while winter appeared to warm atthe highest rate (0.04 !C yr"1). Spring temperatures were the mostvariable (tau ¼ 0.28), but still increased at a similar rate to summer(0.02 !C yr"1). No significant warming occurred during June be-tween 1948 and 2014 (tau ¼ 0.22, p ¼ 0.14).

Mean salinity during the spring months of AprileJune and thefirst weeks of July increased from 25.0 to 26.5 PSU during 1952e54and from 26.0 to 26.8 PSU during 1991e2011. However, thesechanges are mostly within 2SD of the long-termmean and could beconsidered normal variation (Fig. 6). Mean monthly surface

offshore Central Basin dissolved oxygen levels recorded from 1996to 2010 were significantly higher throughout the year relative to1952e1954. However, bottom offshore oxygen levels during mid-July to October 1996e2010 were not significantly higher than1952e4 levels during that same period (Fig. 6).

4. Discussion

In this paper we have shown that LIS summer copepod abun-dance has significantly declined relative to historic levels, and thatthis pattern is not a function of different mesh size during surveys,zooplankton patchiness, or normal inter-annual variability. Wehave also shown that ctenophore abundance and biomass hasconsistently been near zero during spring, despite awarming trend.The dramatic shift from a bimodal copepod abundance pattern to aunimodal abundance pattern occurred without significant cteno-phore biomass during spring. For the last decade of observations inLIS, there have been no trends of earlier appearance of ctenophores,nor an increase in spring ctenophore biomass, or significant springbiomass of ctenophores.

Aside from this lack of ctenophore biomass in spring, our findingof dramatic decreases in summer copepod abundance matches thefindings of Sullivan et al. (2007). This is not entirely surprising,given that they used a similar approach to ours (combining his-torical surveys with modern surveys) and had a similarzooplankton dataset ranging from 1951 to 2004, and wereresearching a coastal ecosystem near ours (Narragansett Bay is

Fig. 6. A. Central Basin 1948e2014 summer (July, August, and September) inshore temperature deviations from 1948 to 2014 summer mean. B. Central Basin 1948e2014 spring(April, May, and June) inshore temperature deviations from 1948 to 2014 spring mean. C. Salinity recorded by Riley et al. (1956) for 1952e1954 and CT DEEP mean salinity for1991e2011, error bars are 2SD based on the CT DEEP interannual variation in monthly values for 1991e2011. D. Surface and bottom dissolved oxygen levels recorded by Riley et al.(1956) for 1952e1953 and mean CT DEEP surface dissolved oxygen (available for1996-2010) and bottom dissolved oxygen (available for 1991e2010).


~100 miles from LIS). Sullivan et al. (2007) found that M. leidyicaused a decline in summer zooplankton abundance due to theirsignificantly earlier appearance in Narragansett Bay during May.This did not occur during LIS between 2002 and 2012. Sullivan et al.(2007) also did not find advancement in the phenology of A. tonsa,which we did find.

During this decade of observations, summer ctenophorebiomass did appear to be positively influenced by summer copepodabundance, but the reverse was not true. In our model, high sum-mer ctenophore biomass was associated with lower copepodabundance and higher microzooplankton abundance, suggesting atrophic cascade may occur during summers when ctenophorebiomass is high. However, our model of summer copepod abun-dance indicated less than 25% of the variation in copepod abun-dance could be linked to changes in ctenophore biomass. Summerctenophore biomass and copepod abundance were also unrelatedto temperature increases during summer or late spring.

4.1. Ctenophore clearance rate and temperature

Since summer and spring temperatures do appear to haveincreased, we tested the hypothesis that the predation rate ofM. leidyi increased with temperature and this increase could ac-count for the reduction in summer copepods. We estimated apotentially thermally-enhanced rate of predation by calculating thepercent by which ctenophore clearance rate could increase due tohigher summer temperatures. For comparison, we chose meansummer temperatures during 1952e54 versus 1994e2012. Webased this thermally-enhanced clearance calculation on thefollowing formula derived by Rowshantabari et al. (2012) forclearance rate and temperature:

SCR ¼ 2.999T1.400

where SCR ¼ specific clearance rate in ml mgC"1 h"1, andT ¼ temperature in Celsius.

Using this formula, we found that the 0.6 !C increase in meansummer temperatures (which occurred between 1952e4 and1994e2012) resulted in at most a 4.1% increase in ctenophorepredation rates.

Since we lack quantitative information on ctenophore biomassand abundance from before 1978, we cannot confirm whetherM. leidyi abundance, or biomass, has increased relative to 1952e54.However, recent studies suggest the predatory impact ofM. leidyi inadjacent or nearby waters to the Central Basin of LIS can be highlyvariable. In the Western Basin of LIS during 2011e2012, Lonsdaleet al. (2014) reported ctenophore biomass below 1.0 ml m"3 inMay and early June, with peak biomass in mid-July to early Augustranging from 35.4 ± 10.4 to 71.2 ± 17.5 ml m"3. In the nearbyThames River Estuary (which connects to LIS), Vliestra (2014) foundthatM. leidyi peaked in abundance (9.9 ± 2.5 ind. m"3) and biomass(26.6 ± 9.9 ml m"3) in July, but at these peak levels M. leidyiappeared to consume only ~2.2% of the summer standing stock ofcopepods per day. It thus seems unlikely that a 4.1% increase in aclearance rate that only reduces standing stock ~2.2% d"1 canexplain the loss of more than 59% of the summer copepod com-munity between 1952e4 and 1994e2012.

It is possible that higher rates of ctenophore predation haveindirect effects that are a significant factor in summer copepoddeclines. As noted by Rice et al. (2015) Oithona sp. relative abun-dance has increased relative to 1952-54 during summer months inLIS. Although capture and retention efficiencies by M. leidyi aresimilar for A. tonsa and Oithona sp., a higher encounter rate ofA. tonsa with M. leidyi increases its predation risk, and over timemay contribute to a proportional increase in Oithona sp. relative to

A. tonsa (Costello et al., 1999). This has been supported by Lonsdaleet al. (2014), who found that in Central LIS M. leidyi consume 67.2%of the daily growth in adult A. tonsa versus 2.6% of daily growth inadult Oithona similis.

We did find a significant reduction in A. tonsa dominance duringsummer, but despite this shift, A. tonsa has maintained itsapproximate percent of the copepod community on an annual basis(17.5e18.4% in 1952e53 versus 19.9% in 2010e11). This occurreddue to increased representation by A. tonsa during winter, whichwarmed at the highest rate of all seasons (0.04 !C yr"1). Interest-ingly, Deevey (1956) noted that in 1952e54 A. hudsonica (the coolwater congener of A. tonsa) appeared to dominate LIS, representing~33% community on an annual basis, but by 2010e11 A. hudsonicawas only ~8% of the community.

It is also possible there may have been an increase in othercopepod predators in LIS. Howell and Auster (2012) reported anincreased abundance of warm water larval fish in LIS, but thedominant larval fish during summer 1952-4 were Bay Anchovy(Wheatland,1956), and their recent abundance appears higher onlyduring early July (Dunning et al., 2006). It thus seems unlikely thatincreased larval Bay Anchovy abundance can explain our observa-tion of much lower copepod abundance during all summer months(July, August, and September) since the 1990s.

Cnidarians endemic to LIS, such as Aurelia, Cyanea and Chrys-aora, may also have a predatory impact during summer. However,CTDEEP 2002e2012 data indicates these cnidarians are presentmainly during spring, early summer, and fall. This suggests onereason for a lack of observed trends in springM. leidyi biomass maybe due to intermittent predation pressure from cnidarians, similarto the relationship observed by Purcell and Decker (2005).

Lower trophic level shifts during summer, such as changes infood quantity associated with higher summer temperatures, arealso possible. However, Rice et al. (2015) have shown that summerchlorophyll levels do not appear significantly different since 1952-54.While the quantity of primary producers may not have changed,it is possible that the quality of food has shifted. Across LIS, Suteret al. (2014) have noted a decrease in the relative proportion ofdiatoms and an increase in mixotrophic algae from 1994 to 2010.This shift appears due to an increase in organic nitrogen relative toinorganic nitrogen. These species are less nutritious than diatoms,and their consumption can cause a reduction in copepod egg pro-duction (Li et al. (2013).

Rice and Stewart (2013) also found that although chlorophylllevels during summer were consistent with historic levels reportedby S.A.M. Conover (1956), R.J. Conover (1956), higher summertemperatures in the Central Basin of LIS were associated withincreased abundance of small phytoplankton and dinoflagellates.S.A.M. Conover (1956), R.J. Conover (1956) noted that A. tonsa didnot appear to efficiently feed on small cells, and Turner (1984) hasreported research that found a diet of small flagellates can reduceA. tonsa abundance. Murrell and Lores (2004) also found the samerelationship in a Florida estuary between temperature, smallphytoplankton, and a shift from A. tonsa to Oithona sp. A. tonsamaythus be decreasing during summer as small cells, mixotrophicalgae, and flagellates have increased, but increasing during warmerwinters when small cells and flagellates are not as abundant, andlarger diatoms remain more prevalent (S.A.M. Conover (1956), R.J.Conover (1956)).

A final reasonwhy increases inM. leidyi grazing rates or biomassmay not fully explain reduced summer copepod abundance in LIS isthat there appears to be a larger ratio of copepods toM. leidyi in LISduring summer relative to Chesapeake Bay and Narragansett Bay(Sullivan et al., 2001; Purcell and Decker, 2005). In the Central Basinof LIS, monthly M. leidyi biomass trends from 2002 to 2012 indi-cated that M. leidyi were a significant presence (38e237 ml m"3


biomass) only during summer (July, August, September) (Fig. 5A).More recently, Treible et al. (2014) observed a peak in Central BasinM. leidyi biomass in JulyeAugust at 55 ml m"3. These levels appearlow relative to other Mid-Atlantic systems.

For comparison, during years when Purcell and Decker (2005)speculated M. leidyi could control copepod populations in Ches-apeake Bay, M. leidyi biomass was 200e600 ml m"3 Sullivan et al.(2001) reported peak spring ctenophore densities in NarragansettBay an order of magnitude larger (250e350 ind. m"3) than peaksummer ctenophore densities in LIS during our 2010e2011 survey(17 ind m"3). Despite using a smaller mesh net (64 mm), Purcell andDecker (2005) also reported summer copepod abundances in theChesapeake during years of minimalM. leidyi abundance that weremuch lower (32,000 copepods m3) than summer copepod abun-dances reported by Riley (90,487 ind. m"3, 1941), Deevey (45,808ind. m"3, 1956), and Peterson (130,812 ind. m"3, 1985) for LIS.

Research on copepod phenology shifts andwarming has thus farfocused on the impact of gelatinous predators, and specifically theextended seasonal presence of the ctenophore M. leidiyi (e.g.Beaulieu et al., 2013). Here, we have demonstrated that an increasein abundance or grazing rate of M. leidiyi can only partiallycontribute to the dramatic decrease in LIS summer copepod pop-ulations. It appears that ctenophores may play a larger role in othersystems with less abundant summer copepod populations, andgreater relative M. leidiyi populations. We have suggested alterna-tive explanations for this shift in LIS, but the strongest explanationintegrates community shifts, decreased food quality, and thepredatory impact of ctenophores.

Acknowledgements

We would like to acknowledge the NMFS/NOAA Milford labo-ratory for providing the temperature data. We thank the CTDEEPfor their assistance in collecting zooplankton samples. We aregrateful to the captains and crews of the RV John Dempsey, RVPatricia Lynn, and RV Victor Loosanoff. Lastly, we would like tothank the thesis committee members of the first author, ProfessorJohn Waldman, Professor Greg O'Mullan, Professor John Marra andespecially Dr. Julie Rose for their support.

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