See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/306040987 Decadal changes in zooplankton abundance and phenology of Long Island Sound reflect interacting changes in... Article in Marine environmental research · August 2016 DOI: 10.1016/j.marenvres.2016.08.003 CITATIONS READS 0 123 2 authors: Edward Rice Gillian Stewart National Oceanic and Atmospheric Administr… City University of New York - Queens College 7 PUBLICATIONS 29 CITATIONS 43 PUBLICATIONS 750 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: Spatial differences in the Zooplankton Community of the Hudson River and New York City Waters View project MEDFLUX View project All content following this page was uploaded by Edward Rice on 23 August 2016. The user has requested enhancement of the downloaded file. Marine Environmental Research 120 (2016) 154e165 Contents lists available at ScienceDirect Marine Environmental Research journal homepage: www.elsevier.com/locate/marenvrev 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 copepod 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 Copepods 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- phytoplankton, 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 predation 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.