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Decadal changes in abundance and phenology of Long Island Sound reflect interacting changes in...

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Decadal changes in zooplankton abundance and phenology of Long Island Sound reflect interacting changes in temperature and community 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, USA b 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 article info abstract

Article history: Between 1939 and 1982, several surveys indicated that zooplankton in Long Island Sound, NY (LIS) Received 29 April 2016 appeared to follow an annual cycle typical of the Mid-Atlantic coast of North America. Abundance peaked Received in revised form in both early spring and late summer and the peaks were similar in magnitude. In recent decades, this 3 August 2016 cycle appeared to have shifted. Only one large peak tended to occur, and summer abundance Accepted 5 August 2016 was consistently reduced by ~60% from 1939 to 1982 levels. In other Mid-Atlantic coastal systems such a Available online 8 August 2016 dramatic shift has been attributed to the earlier appearance of ctenophores, particularly Mnemiopsis leidyi, during warmer spring months. However, over a decade of surveys in LIS have consistently found Keywords: M. leidyi Long Island Sound near-zero values in biomass during spring months. Our multiple linear regression model in- Zooplankton dicates that summer M. leidyi biomass during this decade explains <25% of the variation in summer Phenology copepod abundance. During these recent, warmer years, summer copepod community shifts appear to Warming explain the loss of copepod abundance. Although Acartia tonsa in 2010e2011 appeared to be present all year long, it was no longer the dominant summer zooplankton species. Warmer summers have been Ctenophores associated with an increase in cyanobacteria and flagellates, which are not consumed efficiently by A. tonsa. This suggests that in warming coastal systems multiple environmental and biological factors interact and likely underlie dramatic alterations to copepod phenology, not single causes. Published by Elsevier Ltd.

1. Introduction August, September) abundance equaling or exceeding that in the spring (April, May, June) (Kremer, 1994). In coastal and marine systems, a key link between primary However, zooplankton can also respond very quickly to physical producers and higher trophic levels are the zooplankton forcings associated with climate change, such as changes in tem- (Wickstead, 1976). The zooplankton of the Mid-Atlantic is numer- perature, salinity, or stratification (Richardson, 2008). Such changes ically dominated by copepods - microcrustaceans that graze upon appear to be occurring in Northeast and Mid-Atlantic coastal sys- , microzooplankton and juveniles (nauplii) of their tems. Annual regional warming of surface waters at the rate of 1 own species as well as nauplii of other copepod species (Turner, 0.03e0.04 C yrÀ has been reported for Long Island Sound (LIS), 2004). Copepods dominate the gut contents of larval cod, Narragansett Bay, and Massachusetts Bay (Sullivan et al., 2001; haddock, and anchovy, and thus serve as an important link in Nixon et al., 2004; Rice and Stewart, 2013)(Fig 1A, Williams, aquatic foodwebs from phytoplankton and microzooplankton to 1981, Fig 1B; Lewis and Needall, 1987). larval fish (Turner, 1984). In Mid-Atlantic coastal systems, copepod In Narragansett Bay, this warming has been associated with a abundance has historically been bimodal, with peak summer (July, unimodal zooplankton abundance pattern of reduced summer copepod abundance and a single spring copepod abundance peak (Oviatt, 2004; Costello et al., 2006; Beaulieu et al., 2013). These * Corresponding author. School of Earth and Environmental Sciences, Queens changes were attributed to greater overlap between copepod prey College, City University of New York, Flushing, New York 11367, USA and The and the ctenophore Mnemiopsis leidyi (a gelatinous secondary Graduate Center, City University of New York, USA. consumer), increased grazing by zooplankton of primary E-mail address: [email protected] (G. Stewart). http://dx.doi.org/10.1016/j.marenvres.2016.08.003 0141-1136/Published by Elsevier Ltd. E. Rice, G. Stewart / Marine Environmental Research 120 (2016) 154e165 155

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 73100 (Bridgeport) to roughly 72350 (The mouth of the Connecticut River). B. Location of the Central basin of LIS (1A stations are in the 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's Island. Base map is from Lewis and Needall (1987). producers, and greater respiration losses by producers during found that the rate of copepod production was an order of warmer winter and spring months (Oviatt, 2004). magnitude higher than the rate, and ctenophore preda- Several aspects of M. leidyi life history support the hypothesis tion alone was unable to control copepod populations. More recent that M. leidyi can cause the loss of summer zooplankton: 1) it is a research by Vliestra (2014) in the Thames River estuary (adjacent to key predator of copepods during summer along Mid-Atlantic coasts LIS) found that the predation impact of M. leidyi on copepods was a 2) M. leidyi is tolerant of a wide range of environmental conditions, maximum of 2.2% of the standing stock of copepods per day. and 3) M. leidyi is able to feed on a large size range of particles and Other hydrodynamic, biotic and climatic factors may resolve the organisms (Purcell, 2009). However, estimates of M. leidyi preda- discrepancy. During years in which cnidarian predators of M. leidyi 1 tion rates on copepods can range widely, from 0.3% to 58.7% dÀ are absent from the Chesapeake Bay estuary, Purcell and Decker (Purcell, 2009). In coastal Rhode Island, Kremer (1979) found that (2005) found M. leidyi predation impact increased to 45% of the M. leidyi could typically remove 10e11% of daily copepod abun- copepod community per day. The climatic factors that appeared to dance during summers. In Chesapeake Bay, Purcell et al. (1994) increase M. leidyi predation on copepods were low salinity (which 156 E. Rice, G. Stewart / Marine Environmental Research 120 (2016) 154e165 reduces cnidarian abundance) and higher spring temperatures than those during surveys after 1985. Our intent is to test the hy- (Sullivan et al., 2001; Oviatt, 2004). Increased abundance and pothesis that a summer decline in LIS copepod abundance can be predatory impact of gelatinous zooplankton (such as M. leidyi) has conclusively linked to earlier appearance of ctenophores in spring thus been suggested as a consequence of a warmer, overfished, and as annual temperatures warm. eutrophic coastal ocean (Mills, 1995; Richardson et al., 2009). In addition, more enclosed coastal waters (with longer residence 2. Methods times) also promote ctenophore abundance (Vansteenbrugge et al., 2015). To test whether earlier appearance of ctenophores in 2.1. Historic surveys warming coastal systems causes a loss of summer copepods re- quires a long-term data set of physical factors, zooplankton, and To establish a historical context for analysis of copepod and their ctenophore predators. ctenophore abundance, previous surveys of the Central Basin One system with such a record is LIS, a large, semi-enclosed, (Table 1) were obtained from archival and published sources. partially mixed estuary at the northern end of the Virginian Where tabular data was not available (Deevey, 1956; Capriulo et al., biogeographic community (Deevey, 1956; Pelletier et al., 2012). 2002), the program DataThief (freeware graphical interpolation Since 1938, the zooplankton community of the Central Basin of LIS software) was used to reconstruct numbers from figures for 4 of 18 fi has been surveyed and quanti ed roughly every 15 years, with the annual surveys available. Although these surveys varied somewhat most continuous series of surveys beginning in 1991 (Riley, 1941; in parameters, intensity, scope, and specific location, they provide Deevey, 1956; Carlson, 1978; Peterson, 1985; Capriulo et al., 2002; the only baseline data for analysis of current trends. Dam and McManus, 2009). During 1952e1953, Deevey (1956) The copepod surveys can be divided into three classes based on noted that the LIS gelatinous zooplankton community was mainly net size: (1) a 202 mm mesh, (2) a 150e158 mm mesh, and (3) a comprised of M. leidyi and the cnidarians Aurelia Aurelia and 119 mm mesh. Since the focus of this article is changes in phenology Chrysaora quinquecirrha. Deevey (1956) noted that M. leidyi was and not absolute abundance, we have normalized each survey's abundant during late summer 1952e1953, but could only speculate data by dividing the monthly abundance by the annual mean fl that the in ux of M. leidyi caused a rapid decline in summer co- number of copepods per month. This allowed us to compare rela- fi pepods. Carlson (1978) was the rst to quantify M. leidyi biomass in tive differences in monthly abundance over time between different central LIS (Fig. 1A), recording biomass during January, March, May, surveys. The earliest zooplankton survey was a monthly 119 mm July, September, and November. mesh inshore sample obtained by Riley (1941) over 1938-39 from Besides cnidarians and M. leidyi, the only other gelatinous Milford Harbor and Welch's Point, CT (Fig. 1A). Samples were pre- zooplankton found to occur in LIS are Beroe cucumis and Pleuro- served in buffered formalin (concentration unreported). No data on brachia pileus. The latter is a small, spherical ctenophore less than ctenophores was given. For further details on these surveys, refer to half the diameter M. leidyi (2.0 cm versus 5e7.6 cm) and tends to Rice et al. (2015). occur only in winter. B. cucumis is more elongated and twice the Deevey (1956) conducted the next survey from March 1952 to size (typically 15 cm long) relative to M. leidyi. June 1953. Zooplankton tows were oblique and used a 158 mm mesh fi In Central LIS, temperatures during all seasons have signi cantly net with a Clarke-Bumpus sampler. Buffered formalin was the increased since 1948, with a consistent trend most evident since preservative, but concentration was not reported (Deevey, 1956). 1975 (Rice and Stewart, 2013). This warming has been driven by Ctenophore abundance was not quantified. Copepod abundance increasing Northern hemisphere temperature due to climate was interpolated from figures, since tabular data was provided only change, which has increased annual temperature at the rate of for zooplankton. Deevey (1956) also reported zooplankton biomass 1 0.03 C yrÀ since 1970e1980 throughout the coastal Northeast (wet-weight) and noted it had a similar phenology to zooplankton United States (Nixon et al., 2004). Spring and summer zooplankton abundance (data not shown). surveys in LIS prior to 1985 have happened under conditions cooler Carlson (1978) conducted the next survey of the Central Basin, at

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

Survey mesh size Ctenophore Year Monthly mean abundance Spring mean abundance Summer mean abundance Survey þ 3 4 3 4 3 4 quantified? (mÀ , 10 ) (mÀ , 10 ) (mÀ , 10 ) frequency    Riley (1941) 119 mm N 1938e9 4.50 6.98 9.05 Twice weekly Deevey (1956) 158 mm N 1953e4 3.40 4.77 4.58 Bi-weekly Peterson (1985) 202 mm N 1982 3.01 8.35 13.1 Weekly Capriulo et al. (2002) N 1993 1.39 4.22 0.14 Monthly and 202 mm weekly Capriulo et al. (2002) N 1994 1.08 2.77 0.69 Monthly and 202 mm weekly CT DEEP 202 mm Y 2002/ 1.80 4.45 1.50 Monthly and 2004 weekly CT DEEP 202 mm Y 2003 2.80 5.85 3.00 Monthly and weekly CT DEEP 202 mm Y 2007/ 3.64 10.2 1.25 Monthly and 2008 weekly Rice (150) mm Y 2010 1.51 2.79 1.05 Monthly and weekly Rice (150) mm Y 2011 1.31 2.58 0.97 Monthly and weekly CT DEEP 202 mm Y 2012 2.51 4.47 0.65 Monthly and weekly E. Rice, G. Stewart / Marine Environmental Research 120 (2016) 154e165 157 the tidal inlet to Flax Pond (Fig. 1A) near Stony Brook, NY, always were made after collection. From March 2010 to November 2011 during incoming tide. This survey focused on biomass (dry weight) the second phase was completed with CTDEEP from the available of zooplankton, however, so abundance data is not available. offshore Central Basin stations, (H2, H4, H6 and I2) (Fig. 1A) and in Preservation information was also not given. Carlson (1978) only addition, Station 2 from Deevey (1956) (located northeast of H4). reported the biomass of all microcrustacean zooplankton, but in Our 2010e2011 survey visited 2e3 stations (from those above) LIS, copepods typically represent ~90% of zooplankton (Deevey, during each cruise and used vertical tows with a 150 mm mesh net. 1956; Capriulo et al., 2002). Sub-sampling and preservation for analysis was performed in Peterson (1985) recorded copepod abundance during weekly situ after collection following the methods described by Kideys and cruises from March 1982 to July 1983 (Fig.1A). Peterson (1985) used Romanova (2001). If gelatinous zooplankton abundance was not so a 202 mm mesh net, hauled vertically from bottom to surface. No high as to clog the mesh, (preventing a volume estimate) contents data is given on preservation methods, but copepods were identi- of the net were rinsed through a 2 mm sieve into a 10 L container fied to species and life stage from subsamples. Ctenophores were and all ctenophores retained on the sieve were enumerated. If not sampled or identified. gelatinous abundance was higher, sub-sampling of ctenophores The next survey, by Capriulo et al. (2002), was conducted from was conducted by re-suspending all gelatinous zooplankton June 1992 to September 1995 across LIS, with one coastal station in retained by a 2 mm sieve in 10 L of seawater collected in-situ and the Central Basin. This station was co-located with the Deevey verified free of ctenophores > 2 mm in diameter. After gently stir- (1956) station near the National Oceanic and Atmospheric ring, a 500 ml clear plastic container was used to collect cteno- Administration (NOAA) Milford laboratory (Fig. 1A) and was visited phores. All ctenophores present in 500 ml were counted, and sub- monthly. Oblique tows were used with a 202 mm mesh net to collect sampling continued until three successive counts differed by <10%. copepods. The mesozooplankton samples were preserved with 10% During our ctenophore survey, copepods were also collected and buffered formalin. Capriulo et al. (2002) noted but did not quantify counted from the same locations in the Central Basin of LIS using ctenophores. Offshore Central Basin tows were not conducted, but the same 150 mm mesh net. Copepods were subsampled after being spatial gradients and seasonal abundances were similar to the later re-suspended in a 10 L container of local seawater. The contents Connecticut Department of Energy and Environmental Protection were gently stirred, and subsamples were drawn with a 50 ml (CTDEEP) survey. pipette until 500 ml was collected. A 5% Lugol's iodine preservative CTDEEP (2002e4, 2007e8, 2012) mesozooplankton samples was added for later analysis. Sub-samples were kept in coolers in were collected with oblique tows of a 202 mm mesh net from one the field, and transferred to a 10 C incubator upon return to the station in the far western Narrows (B3), two stations in the Western laboratory. Enumeration and identification of copepod samples, as Basin (D3, F2) two stations within the Central Basin, H4 and I2, and well as size analysis, was carried out via dissecting microscope one station in the Eastern Basin (K2) (Fig. 1A). Except during within a year of collection, the recommended timeframe for iden- summer (when stations were visited bi-weekly), these stations tification of zooplankton preserved in Lugol's solution (Harris et al., were visited once per month, and samples were preserved in 5% 2000). Key taxonomic features from Johnson and Allen (2005) were buffered formalin. Results and CTDEEP methods have been used to identify adult copepods. To standardize counting effort with analyzed and reported by Dam and McManus (2009). Micro- prior surveys that reported sample counts (Capriulo et al., 2002), zooplankton samples for stations H4 and I2 were pooled from 100e150 copepods were counted from each sub-sample. surface, mid-depth, and bottom Niskin-samples and preserved in Lugols (concentration not given) (Dam and McManus, 2009). To 2.3. Physical data ensure standardization, all of the copepod and gelatinous zooplankton data used in our M. leidyi and copepod models was Temperature data came from the NOAA laboratory at Milford from the 202 mm mesh CTDEEP survey. (the most extensive available) and covers the 1948e2014 period. Between 2002 and 2012, M. leidyi wet-weight biomass was We examined monthly values based on daily measurements from measured via volume displacement in-situ by CTDEEP from live 1948 to 1975 using a Bristol thermograph. From 1976 to 2012 daily gelatinous zooplankton caught with a 202 mm mesh net and measurements were continued, but with thermometer readings of separated from other zooplankton by a 1 mm sieve. After collection, sand-filtered harbor water pumped into the laboratory. No signif- CTDEEP sorted gelatinous zooplankton into Scyphozoans (Aurelia, icant change appears to have occurred during the transition be- Cyanea, Chrysaora) and Ctenophora (Mnemiopsis and Pleurobrachia) tween methods. CTDEEP measured the offshore Central Basin by genus. Beroe was not reported in the 2002e20012 CTDEEP sur- chemical and physical data used in our models from August 2002 to veys. During summer, 90e100% of ctenophore biomass was re- October 2004, March 2007 to April 2008, and January to December ported to be Mnemiopsis in the CTDEEP surveys, hence 2012. Dissolved oxygen, salinity and temperature were recorded in- “ctenophore” can be assumed to refer to Mnemiopsis in the rest of situ via a Sea-Bird model SBE-19 SeaCat Conductivity-Temperature- this paper. Regarding biomass, it should be noted that Raskoff et al. Depth (CTD) profiler. Surface and bottom dissolved oxygen samples (2003) recommended finer mesh nets for ctenophore collection were later measured via the Winkler method. (they are less likely to break apart in finer mesh), thus the CTDEEP data may underestimate ctenophore biomass. 2.4. Statistics and modeling

2.2. New surveys We investigated factors possibly influencing summer copepod abundance and ctenophore biomass with linear multiple regression We conducted our own copepod and ctenophore surveys for this modeling of summer CTDEEP data for 2002e2008. Multiple study from March 2010 to September 2011. During the 17 months of regression analysis is often used by ecologists to investigate the offshore cruises, bi-weekly surveys were conducted during the impact of various environmental factors on organismal, population, summer sampling season with CTDEEP. For ctenophore abundance, and community ecology (Graham, 2003). For our models of sum- we collected ctenophore samples in two phases. A preliminary July mer copepod abundance and M. leidyi biomass, we chose a time 2009eJuly 2010 onshore survey was performed from Central Basin range (2002e2004, 2007e2008) that allowed us to include docks at Mattituck and Stony Brook Harbor with a 150 mm mesh microzooplankton abundance and biomass, surface temperature, net, during which counts of ctenophores and classification by size chlorophyll, salinity and dissolved oxygen as potential explanatory 158 E. Rice, G. Stewart / Marine Environmental Research 120 (2016) 154e165 variables in the models. Microzooplankton are a significant food and 1983 appeared to reverse in the later surveys between 1993 source for copepods (Turner, 1984) and M. leidyi (Stoecker et al., and 2012. In 1993, 1994, Capriulo et al. (2002) found spring abun- 1987), but data was not available for other surveys, hence we did dance was an order of magnitude greater than summer (Table 1). In not attempt to create a copepod abundance or ctenophore biomass 2002/4, CTDEEP found spring copepod abundance nearly three model for those years. times summer copepod abundance. In 2007/8, this pattern For our copepod abundance model, M. leidyi biomass was continued and spring copepod abundance was almost an order of included as variable. Other predators, such as fish larvae, chaeto- magnitude larger than summer copepod abundance. These trends gnaths, and larger , rarely appear in CTDEEP continued in our 2010 and 2011 surveys and the CTDEEP, 2010 zooplankton surveys and were not included. For M. leidyi biomass, survey (Table 1). These declines in summer copepod abundance copepod abundance was included as a potential factor. M. leidyi were most pronounced for the normally summer-dominant biomass was normalized via log 1 transformation, as suggested for copepod, Acartia tonsa (abundance data not shown). þ linear regression modeling of highly variable ecological data However, it is possible these trends were actually reflective of (Mascaro et al., 2011). For 2002e2013, if ctenophore biomass for nonrandom zooplankton aggregations biasing our surveys each month was normally distributed, that data was used to (“patchiness,” Falt and Burns, 1999). To determine if this was the generate error bars for analyses of the mean values for those case, we compared zooplankton abundance at all reported stations months (SE Standard Error). visited in the Deevey (1956) 1952-4 surveys (Fig. 2A) with ¼ All statistical tests and analysis were run in R, version 2.11.1. For zooplankton abundance reported from all available CTDEEP LIS linear multiple regression models, we tested for skewness, kurtosis, stations reported by Dam and McManus (2009) (Fig. 2B). At all four non-linearity, homoscedasicity, and linkage. Stepwise Akaike In- stations visited in 1952e4, a summer peak in zooplankton abun- formation Criteria (AIC) analysis was used to identify unnecessary dance occurred that was at least 68.6% of the spring peak in variables, which were removed from the model prior to further magnitude, and the summer peak was on average 85.4% of the analysis. A Bonferroni test was used to check for outliers. Collin- spring peak. In 2007-8, all Central and Western Basin CTDEEP earity, autocorrelation, and non-linearity were ruled out by a stations had summer peaks that were between 7.98% and 41.6% of variance inflation factor test, a Breusch-Godfrey test, and spring peaks (the mean was 20.0%). The only CTDEEP stations that Component Residual and Quantile-Quantile (QQ) plots, respec- did not follow that pattern were at the extreme ends of LIS, station þ tively. For our analysis of the statistical significance of long-term B3 in the Narrows and station K2 in the Eastern Basin. changes in copepod abundance we included all available data Our analysis of normalized surveys conducted between 1938 from the 1992e2012 period, normalized to proportional abun- and 1983 indicate a recurring pattern of at least two peaks of near dance. To determine if a change in proportional abundance was or equal copepod abundance, with spring and summer similar in significant, we calculated Bayesian credible intervals from the magnitude (Fig. 3A). This pattern of bimodal copepod phenology resulting time series using a flat prior and the quantile method. was consistent across these earlier surveys of different mesh sizes Credible intervals do not require a normal distribution (Balazs and (119 mm, 158 mm, and 202 mm). Surveys between 1993 and 2012 had Chaloupka, 2004), and are useful for analyzing plankton time-series one distinct spring peak in copepod abundance, generally between (Boyce et al., 2010). late May and early June (Fig. 3B). This pattern of unimodal For Central Basin seasonal temperature timeseries analysis, we phenology between 1993 and 2012 was evident in surveys of followed the methodology that Rice et al. (2015) used for annual different mesh sizes (150 mm and 202 mm). Based on the inter- temperature timeseries analysis in the Central Basin - the Kendall annual variation in monthly series in the CTDEEP data, the late test. Since it is a nonparametric method of estimating a trend over Maye early June (spring) peak in proportional copepod abundance time, it is more robust than the ordinary least-squares approach. that defined the 1993e2012 pattern was significantly higher Using the kendall package in R, we calculated tau (correlation) and p (p 0.05) than the 1993e2012 summer abundance. ¼ values (significance). The slope of the trend was found with the In terms of abundance, during summer in 1952e3 Deevey Theil-Sen approach in the R package zyp. The Theil-Sen estimator is (1956) found that A. tonsa, Paracalanus crassiostris, and Oithona sp also a non-parametric method of analyzing linear trends (Sen, dominated the copepod community sampled with their 158 mm 1968). A Breusch-Godfrey test for serial autocorrelation was mesh net. In our 2010e2011 survey using 150 mm mesh, these three passed for annual temperature values, indicating that these copepods again dominated copepod abundance in summer sam- methods were appropriate. ples, but A. tonsa decreased from 60% in August 1952 to 36% in August 2010 and 32% in August 2011 (Fig 4). Similar declines 3. Results occurred in September: A. tonsa was 50% of the copepod commu- nity in September 1952 but only 10% of the community in 3.1. Zooplankton surveys September 2010, and 28% in September 2011. On the other hand, A. tonsa expanded its proportion in winter, increasing from 10% of The seasonal average of summer copepod abundance exceeded the copepod community in February 1952e53 to 40% in 2011. In all or nearly equaled the seasonal average of spring copepod abun- of these instances, the changes in A. tonsa percentage exceeded a dance in 1938e1939, 1953e1954, and 1982e1983 (Riley, 1941; 95% confidence interval based on interannual variation in A. tonsa Deevey, 1956; Peterson, 1985)(Table 1). Zooplankton biomass percentage. was significantly correlated (r2 0.56, p≪0.01) with copepod Carlson (1978) reported insignificant (~0) M. leidyi wet weight ¼ abundance during summer and spring 1953e1954. Summer peaks biomass for January, March 1e15, March 16e30, and May. M. leidyi 3 3 3 3 in zooplankton biomass (1.72 ml mÀ and 1.62 ml mÀ ) were also biomass during July (366 ml mÀ ) and September (182 ml mÀ ) was 3 3 larger than spring peaks (1.28 ml mÀ and 0.73 ml mÀ ) in both significantly higher, but November M. leidyi biomass was minor 3 years (Deevey, 1956). During the 1970s, Carlson (1978) recorded dry (6.92 ml mÀ ). For 2002e2012, the lowest seasonal ctenophore 3 weight biomass of Central Basin zooplankton (primarily copepods), biomass was spring (0.70 ml mÀ ), followed by winter 3 3 and found summer biomass (48.5 mg mÀ ) also nearly equal to (1.03 ml mÀ ). The lowest monthly averages for ctenophore 3 3 3 spring biomass (50.0 mg mÀ ). biomass were January (0.00 ml mÀ ) and June (0.02 ml mÀ ). For The pattern of summer copepod abundance equaling or years in which all summer months were surveyed, ctenophore exceeding that of spring in the surveys between and including 1938 biomass tended to peak in September (5 of 6 years). September also E. Rice, G. Stewart / Marine Environmental Research 120 (2016) 154e165 159

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 reported by 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).

3 3 had the highest mean ctenophore biomass of all months mÀ ) and winter (1.43 ctenophores mÀ ). The only apparent dif- 3 (363 ml mÀ / 114 SE), but was not significantly different than ference between biomass and abundance patterns during this þ À August. period was that abundance tended to peak in late July - early 3 We surveyed ctenophore abundance with CTDEEP between August (5.45 ctenophores mÀ ), a month earlier than biomass. 2010 and 2011 (Fig. 5A) and found ctenophore abundance in both M. leidyi displayed no long-term trends in biomass on an annual, years peaked earlier than ctenophore biomass tended to peak over seasonal, or monthly basis in the 2002e2012 CTDEEP survey data 2002e2012. Abundance was lowest in spring (0.17 ctenophores (Fig. 5B). 160 E. Rice, G. Stewart / Marine Environmental Research 120 (2016) 154e165

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 between 1993 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 in CTDEEP 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. E. Rice, G. Stewart / Marine Environmental Research 120 (2016) 154e165 161

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 H4 and 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).

3.2. Zooplankton modeling significantly (at a 0.05) related to higher summer copepod ¼ abundance. Central Basin station differences in salinity exceeded Linear multiple regression modeling of summer copepod temporal differences on a monthly or annual basis. Ctenophore abundance between 2002 and 2008 indicated copepod abundance biomass was not a significant (p 0.05) factor at the a 0.05 level, ¼ ¼ was negatively related to salinity and M. leidyi biomass. The model but the model was no longer significant without ctenophore was significant (p 0.008) and explained 43% of the variation in biomass and explained 25% less of the variation in copepod abun- ¼ summer copepod abundance from 2002 to 2008. Salinity and log 1 dance when M. leidyi biomass was selectively removed and the þ transformed M. leidyi biomass were the only factors not flagged as model re-run. redundant by AIC stepwise regression (Table 2). Surface values for The linear model of summer ctenophore biomass between 2002 chlorophyll, dissolved oxygen, and temperature were not signifi- and 2008 was also significant (p≪0.01) and explained 35% of the cant factors in summer copepod abundance. Lower salinity was variation in log 1 transformed summer M. leidyi biomass. Surface þ

Table 2 Key parameters and statistical test results from models of summer copepod and M. leidyi biomass. Stepwise AIC analysis (run in both directions) was used to reduce the number of 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 abundance Chlorophyll A No na na na Model r2 (adj.): 0.43 M. leidyi biomass Yes 0.05 10.9 2.05 À À Model p-value: 0.01 Salinity (surface) Yes 0.01 14.5 2.85 À À Microzooplankton biomass No na na na

Microzooplankton abundance (Log10) No na na na Dissolved O2 (surface) No na na na Temperature (surface) No na na na Summer M. leidyi biomass (log 1 transformed) Chlorophyll A No na na na 10 þ Model r2 (adj.): 0.35 Copepod abundance Yes 0.03 0.02 2.46 À À Model p-value: 0.02 Microzooplankton biomass Yes 0.03 0.02 2.39

Microzooplankton abundance (Log10) No na na na Dissolved O2 (surface) No na na na Temperature (surface) No na na na Salinity (surface) No na na na 162 E. Rice, G. Stewart / Marine Environmental Research 120 (2016) 154e165 chlorophyll, salinity, temperature, and dissolved oxygen were offshore Central Basin dissolved oxygen levels recorded from 1996 removed after stepwise AIC analysis as redundant or meaningless to 2010 were significantly higher throughout the year relative to variables, while copepod abundance and microzooplankton 1952e1954. However, bottom offshore oxygen levels during mid- biomass were retained as significant variables. Both terms were July to October 1996e2010 were not significantly higher than significant at a 0.05 (p 0.03 for copepods, p 0.04 for micro- 1952e4 levels during that same period (Fig. 6). ¼ ¼ ¼ zooplankton). Copepod abundance was negatively related to sum- mer ctenophore biomass, while microzooplankton biomass was 4. Discussion positively related. In this paper we have shown that LIS summer copepod abun- 3.3. Physical changes dance has significantly declined relative to historic levels, and that this pattern is not a function of different mesh size during surveys, Between 1948 and 2014, statistically significant warming in the zooplankton patchiness, or normal inter-annual variability. We Central Basin occurred during all seasons (positive slope, p-value have also shown that ctenophore abundance and biomass has ≪0.01), but the rate and variability of the warming trend varied consistently been near zero during spring, despite a warming trend. (Fig. 6). Fall temperatures warmed at the most consistent rate, The dramatic shift from a bimodal copepod abundance pattern to a 1 0.03 C yrÀ (tau 0.40). Summer and winter warming trends were unimodal abundance pattern occurred without significant cteno-  ¼ the next most consistent (tau 0.36), but the rates differed. phore biomass during spring. For the last decade of observations in 1 ¼ Summer warmed at 0.02 C yrÀ , while winter appeared to warm at LIS, there have been no trends of earlier appearance of ctenophores, 1 the highest rate (0.04 C yrÀ ). Spring temperatures were the most nor an increase in spring ctenophore biomass, or significant spring variable (tau 0.28), but still increased at a similar rate to summer biomass of ctenophores. 1¼ (0.02 C yrÀ ). No significant warming occurred during June be- Aside from this lack of ctenophore biomass in spring, our finding tween 1948 and 2014 (tau 0.22, p 0.14). of dramatic decreases in summer copepod abundance matches the ¼ ¼ Mean salinity during the spring months of AprileJune and the findings of Sullivan et al. (2007). This is not entirely surprising, first weeks of July increased from 25.0 to 26.5 PSU during 1952e54 given that they used a similar approach to ours (combining his- and from 26.0 to 26.8 PSU during 1991e2011. However, these torical surveys with modern surveys) and had a similar changes are mostly within 2SD of the long-term mean and could be zooplankton dataset ranging from 1951 to 2004, and were considered normal variation (Fig. 6). Mean monthly surface researching 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 for 1991e2011, 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). E. Rice, G. Stewart / Marine Environmental Research 120 (2016) 154e165 163

~100 miles from LIS). Sullivan et al. (2007) found that M. leidyi A. tonsa (Costello et al., 1999). This has been supported by Lonsdale caused a decline in summer zooplankton abundance due to their et al. (2014), who found that in Central LIS M. leidyi consume 67.2% significantly earlier appearance in Narragansett Bay during May. of the daily growth in adult A. tonsa versus 2.6% of daily growth in This did not occur during LIS between 2002 and 2012. Sullivan et al. adult Oithona similis. (2007) also did not find advancement in the phenology of A. tonsa, We did find a significant reduction in A. tonsa dominance during which we did find. summer, but despite this shift, A. tonsa has maintained its During this decade of observations, summer ctenophore approximate percent of the copepod community on an annual basis biomass did appear to be positively influenced by summer copepod (17.5e18.4% in 1952e53 versus 19.9% in 2010e11). This occurred abundance, but the reverse was not true. In our model, high sum- due to increased representation by A. tonsa during winter, which 1 mer ctenophore biomass was associated with lower copepod warmed at the highest rate of all seasons (0.04 C yrÀ ). Interest- abundance and higher microzooplankton abundance, suggesting a ingly, Deevey (1956) noted that in 1952e54 A. hudsonica (the cool trophic cascade may occur during summers when ctenophore water congener of A. tonsa) appeared to dominate LIS, representing biomass is high. However, our model of summer copepod abun- ~33% community on an annual basis, but by 2010e11 A. hudsonica dance indicated less than 25% of the variation in copepod abun- was only ~8% of the community. dance could be linked to changes in ctenophore biomass. Summer It is also possible there may have been an increase in other ctenophore biomass and copepod abundance were also unrelated copepod predators in LIS. Howell and Auster (2012) reported an to temperature increases during summer or late spring. increased abundance of warm water larval fish in LIS, but the dominant larval fish during summer 1952-4 were Bay Anchovy 4.1. Ctenophore clearance rate and temperature (Wheatland, 1956), and their recent abundance appears higher only during early July (Dunning et al., 2006). It thus seems unlikely that Since summer and spring temperatures do appear to have increased larval Bay Anchovy abundance can explain our observa- increased, we tested the hypothesis that the predation rate of tion of much lower copepod abundance during all summer months M. leidyi increased with temperature and this increase could ac- (July, August, and September) since the 1990s. count for the reduction in summer copepods. We estimated a Cnidarians endemic to LIS, such as Aurelia, Cyanea and Chrys- potentially thermally-enhanced rate of predation by calculating the aora, may also have a predatory impact during summer. However, percent by which ctenophore clearance rate could increase due to CTDEEP 2002e2012 data indicates these cnidarians are present higher summer temperatures. For comparison, we chose mean mainly during spring, early summer, and fall. This suggests one summer temperatures during 1952e54 versus 1994e2012. We reason for a lack of observed trends in spring M. leidyi biomass may based this thermally-enhanced clearance calculation on the be due to intermittent predation pressure from cnidarians, similar following formula derived by Rowshantabari et al. (2012) for to the relationship observed by Purcell and Decker (2005). clearance rate and temperature: Lower trophic level shifts during summer, such as changes in food quantity associated with higher summer temperatures, are SCR 2.999T1.400 also possible. However, Rice et al. (2015) have shown that summer ¼ chlorophyll levels do not appear significantly different since 1952- 1 1 where SCR specific clearance rate in ml mgCÀ hÀ , and 54. While the quantity of primary producers may not have changed, ¼ T temperature in Celsius. it is possible that the quality of food has shifted. Across LIS, Suter ¼ Using this formula, we found that the 0.6 C increase in mean et al. (2014) have noted a decrease in the relative proportion of summer temperatures (which occurred between 1952e4 and and an increase in mixotrophic algae from 1994 to 2010. 1994e2012) resulted in at most a 4.1% increase in ctenophore This shift appears due to an increase in organic nitrogen relative to predation rates. inorganic nitrogen. These species are less nutritious than diatoms, Since we lack quantitative information on ctenophore biomass and their consumption can cause a reduction in copepod egg pro- and abundance from before 1978, we cannot confirm whether duction (Li et al. (2013). M. leidyi abundance, or biomass, has increased relative to 1952e54. Rice and Stewart (2013) also found that although chlorophyll However, recent studies suggest the predatory impact of M. leidyi in levels during summer were consistent with historic levels reported adjacent or nearby waters to the Central Basin of LIS can be highly by S.A.M. Conover (1956), R.J. Conover (1956), higher summer variable. In the Western Basin of LIS during 2011e2012, Lonsdale temperatures in the Central Basin of LIS were associated with 3 et al. (2014) reported ctenophore biomass below 1.0 ml mÀ in increased abundance of small phytoplankton and dinoflagellates. May and early June, with peak biomass in mid-July to early August S.A.M. Conover (1956), R.J. Conover (1956) noted that A. tonsa did 3 ranging from 35.4 ± 10.4 to 71.2 ± 17.5 ml mÀ . In the nearby not appear to efficiently feed on small cells, and Turner (1984) has Thames River Estuary (which connects to LIS), Vliestra (2014) found reported research that found a diet of small flagellates can reduce 3 that M. leidyi peaked in abundance (9.9 ± 2.5 ind. mÀ ) and biomass A. tonsa abundance. Murrell and Lores (2004) also found the same 3 (26.6 ± 9.9 ml mÀ ) in July, but at these peak levels M. leidyi relationship in a Florida estuary between temperature, small appeared to consume only ~2.2% of the summer standing stock of phytoplankton, and a shift from A. tonsa to Oithona sp. A. tonsa may copepods per day. It thus seems unlikely that a 4.1% increase in a thus be decreasing during summer as small cells, mixotrophic 1 clearance rate that only reduces standing stock ~2.2% dÀ can algae, and flagellates have increased, but increasing during warmer explain the loss of more than 59% of the summer copepod com- winters when small cells and flagellates are not as abundant, and munity between 1952e4 and 1994e2012. larger diatoms remain more prevalent (S.A.M. Conover (1956), R.J. It is possible that higher rates of ctenophore predation have Conover (1956)). indirect effects that are a significant factor in summer copepod A final reason why increases in M. leidyi grazing rates or biomass declines. As noted by Rice et al. (2015) Oithona sp. relative abun- may not fully explain reduced summer copepod abundance in LIS is dance has increased relative to 1952-54 during summer months in that there appears to be a larger ratio of copepods to M. leidyi in LIS LIS. Although capture and retention efficiencies by M. leidyi are during summer relative to Chesapeake Bay and Narragansett Bay similar for A. tonsa and Oithona sp., a higher encounter rate of (Sullivan et al., 2001; Purcell and Decker, 2005). In the Central Basin A. tonsa with M. leidyi increases its predation risk, and over time of LIS, monthly M. leidyi biomass trends from 2002 to 2012 indi- 3 may contribute to a proportional increase in Oithona sp. relative to cated that M. leidyi were a significant presence (38e237 ml mÀ 164 E. Rice, G. Stewart / Marine Environmental Research 120 (2016) 154e165 biomass) only during summer (July, August, September) (Fig. 5A). waterways. Am. Fisheries Soc. Symp 51, 215e226. More recently, Treible et al. (2014) observed a peak in Central Basin Falt, C.L., Burns, C.W., 1999. Biological drivers of zooplankton patchiness. Trends 3 Ecol. Evol. 14, 300e305. M. leidyi biomass in JulyeAugust at 55 ml mÀ . These levels appear Graham, M.H., 2003. Confronting multicollinearity in multiple regression. Ecology low relative to other Mid-Atlantic systems. 84, 2809e2815. For comparison, during years when Purcell and Decker (2005) Harris, R.P., Wiebe, P.H., Lenz, J., Skjoldal, H.R., Huntley, M., 2000. ICES Zooplankton Methodology Manual. Academic Press, London, UK. speculated M. leidyi could control copepod populations in Ches- Howell, P., Auster, P.J., 2012. Phase shift in an estuarine finfish community associ- 3 apeake Bay, M. leidyi biomass was 200e600 ml mÀ Sullivan et al. ated with warming temperatures. Mar. Coast. Fish. Dyn. Manag. Ecosyst. Sci. 4, (2001) reported peak spring ctenophore densities in Narragansett 481e495. 3 Johnson, W.S., Allen, D.M., 2005. Zooplankton of the Atlantic and Gulf Coasts: A Bay an order of magnitude larger (250e350 ind. mÀ ) than peak Guide to Their Identification and Ecology. John Hopkins University Press, Bal- summer ctenophore densities in LIS during our 2010e2011 survey timore, MD. 3 (17 ind mÀ ). Despite using a smaller mesh net (64 mm), Purcell and Kideys, A., Romanova, Z., 2001. Distribution of gelatinous macrozooplankton in the southern Black Sea during 1996e1999. Mar. Biol. 139 (3), 535e547. Decker (2005) also reported summer copepod abundances in the Kremer, P., 1979. Ctenophore predation in narragansett bay. Estuaries 2, 97e105. Chesapeake during years of minimal M. leidyi abundance that were Kremer, P., 1994. Patterns of abundance for Mnemiopsis in U.S. coastal waters: a much lower (32,000 copepods m3) than summer copepod abun- comparative overview. ICES J. Mar. Sci. 51, 347e354. dances reported by Riley (90,487 ind. m 3, 1941), Deevey (45,808 Lewis, R.S., Needall, S.W., 1987. U.S. Geological Survey Miscellaneous Field Studies À Map MF-1939-A. United States Geological Survey. 3 3 ind. mÀ , 1956), and Peterson (130,812 ind. mÀ , 1985) for LIS. Li, C., Yang, G., Ning, J., Sun, J., Yang, B., Sun, S., 2013. Response of copepod grazing Research on copepod phenology shifts and warming has thus far and reproduction to different taxa of spring bloom phytoplankton in the focused on the impact of gelatinous predators, and specifically the southern Yellow sea. Deep Sea Res. II. 97, 101e108. Lonsdale, D.J., Gobler, C.J., Rawitz, D., Treible, L.M., 2014. The Influence of Gelatinous extended seasonal presence of the ctenophore M. leidiyi (e.g. Zooplankton on Nutrient Cycles, Hypoxia, and Food Webs across Long Island Beaulieu et al., 2013). Here, we have demonstrated that an increase Sound. New York Sea Grant Completion Report R/CE-31-NYCT. in abundance or grazing rate of M. leidiyi can only partially Mascaro, J., Litton, C.M., Hughes, R.F., Uowolo, A., Schnitze, S.A., 2011. Minimizing bias in biomass allometry: model selection and log-transformation of data. contribute to the dramatic decrease in LIS summer copepod pop- Biotropica 43, 649e653. ulations. It appears that ctenophores may play a larger role in other Mills, C.E., 1995. Medusae, siphonophores, and ctenophores as planktivorous systems with less abundant summer copepod populations, and predators in changing global ecosystems. ICES J. Mar. Sci. 52, 575e581. Murrell, M.C., Lores, E.M., 2004. Phytoplankton and zooplankton seasonal dynamics greater relative M. leidiyi populations. We have suggested alterna- in a subtropical estuary: importance of cyanobacteria. J. Plankton Res. 26, tive explanations for this shift in LIS, but the strongest explanation 371e382. integrates community shifts, decreased food quality, and the Nixon, S.W., Granger, S., Buckley, B., Lamont, M., Rowell, B., 2004. A one hundred and seventeen year coastal water temperature record from Woods Hole. 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