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Journal of Plankton Research plankt.oxfordjournals.org J. Plankton Res. (2015) 37(1): 221–232. First published online November 10, 2014 doi:10.1093/plankt/fbu098 Persistence of Calanus finmarchicus in the western Gulf of Maine during recent extreme warming JEFFREYA. RUNGE1*, RUBAO JI2, CAMERON R.S. THOMPSON1, NICHOLAS R. RECORD3, CHANGSHENG CHEN4, DOUGLAS C. VANDEMARK5, JOSEPH E. SALISBURY5 AND FREDERIC MAPS6 1 SCHOOL OF MARINE SCIENCES, UNIVERSITY OF MAINE, AND GULF OF MAINE RESEARCH INSTITUTE, 350 COMMERCIAL STREET, PORTLAND, ME 04101, USA, 2 3 DEPARTMENT OF BIOLOGY, WOODS HOLE OCEANOGRAPHIC INSTITUTION, WOODS HOLE, MA 02543, USA, BIGELOW LABORATORY FOR OCEAN SCIENCES, 60 4 BIGELOW DRIVE, PO BOX 380, EAST BOOTHBAY, ME 04544, USA, UNIVERSITY OF MASSACHUSETTS DARTMOUTH, SCHOOL FOR MARINE SCIENCE AND 5 TECHNOLOGY, NEW BEDFORD, MA 02744, USA, OCEAN PROCESS ANALYSIS LABORATORY, UNIVERSITY OF NEW HAMPSHIRE, DURHAM, NH 03824, USA AND 6 DE´ PARTEMENT DE BIOLOGIE, UNIVERSITE´ LAVAL, QUE´ BEC, QC G1V 0A6, CANADA *CORRESPONDING AUTHOR: [email protected] Received July 6, 2014; accepted October 7, 2014 Corresponding editor: Roger Harris The planktonic copepod, Calanus finmarchicus, resides at the southern edge of its subarctic range in the Gulf of Maine (GoM). Here we investigate the population response of C. finmarchicus to record warming in the GoM in 2012. Demographic data from two time series stations and a plankton survey conducted in early autumn 2012 show that C. finmarchicus did not produce an autumn generation as predicted, despite warm summer and overwintering tempera- tures. On the contrary, we observed high abundances of the overwintering stage CV in the western GoM and a new cohort in early spring 2013 likely originating from egg production during a winter phytoplankton bloom. This spring cohort was the most abundant ever recorded in the 8-year time series. To account for these observations, we hypothe- size that production of females originating from the eastern GoM and Scotian Shelf, combined with growth of cope- podid stages in the Maine Coastal Current and local egg production, are the primary sources of supply maintaining high abundances in Wilkinson Basin, the primary repository of C. finmarchicus in the western GoM. Predicting fluctuations in abundance or circumstances for disappearance of C. finmarchicus in the northwest Atlantic will need models that address the roles of local production and advection. KEYWORDS: Calanus finmarchicus; Gulf of Maine; warming; climate change; resilience; population dynamics available online at www.plankt.oxfordjournals.org # The Author 2014. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected] JOURNAL OF PLANKTON RESEARCH j VOLUME 37 j NUMBER 1 j PAGES 221–232 j 2015 INTRODUCTION SST was fully 28C higher than normal (Mills et al., 2013). In addition to possible adverse effects of higher surface Calanus The predominance of the planktonic copepod, temperatures on physiological rate processes, for example finmarchicus , in the mesozooplankton assemblage through- egghatchingsuccess(Preziosi and Runge, 2014), warmer out the North Atlantic is well known. In the Gulf of Maine temperatures at depth during summer and autumn may C. finmarchicus (GoM), resides at the southern edge of its force early exit from dormancy of the overwintering, prea- subarctic range (Sundby, 2000). The species is nevertheless dult stage CV, with consequences for the timing of winter- a prominent component of the zooplankton in the GoM spring reproduction. In a one-dimensional life history et al system (e.g. Durbin ., 2003; Durbin and Casas, 2006; model, Maps et al.(Maps et al., 2012) predicted that the Kane, 2009). Wilkinson Basin, in the western GoM, already warm overwintering temperatures in Wilkinson C. finmarchicus harbors overwintering stage CV at abun- BasininthewesternGoMforceexitfromdormancyinlate . 4 22 dances ( 3.0 Â 10 inds. m )thatareequaltoorhigher summer/early autumn. In the model, the emergence of than levels observed in the species’ more northern habitat new females aligns with the autumn phytoplankton bloom, et al et al (Maps ., 2012; Melle ., 2014). In coastal regions of resulting in a new, autumn cohort that sustains the western C. finmarchicus the GoM in spring and summer, dominates GoM population through to reproduction in spring. not only biomass (Manning and Bucklin, 2005) but also Here we investigate the response of C. finmarchicus in abundance of zooplankton in the catch of plankton nets the GoM to the 2012 warming event. Using data from . m with 200 mmeshsize(Runge and Jones, 2012). two time series stations and from a research cruise con- Calanus finmarchicus has key functional significance in the ducted in early autumn 2012, we compare the seasonal et al. GoM ecosystem (Bigelow, 1924; Johnson , 2011). The abundance and demographic patterns of the 2012 lipid-rich stage CV are a primary prey for planktivorous Calanus population in the western GoM with recent his- et al fish, such as herring and sand lance (e.g. Payne ., 1990; torical data. We use the observations to (i) evaluate the Collette and Klein-MacPhee, 2002) that are fundamental extent to which abundance of C. finmarchicus was sustained trophic links in regional fisheries. Since there is no appar- in the western GoM and (ii) test the hypothesis (Maps C. finmarchicus ent functional redundancy for in the GoM et al., 2012) that the warm, overwintering waters in the C. finmarchicus ecosystem, significant shifts in abundance of GoM bring about early exit from diapause and subse- may have substantial impacts on the region’s metazoan quent production of an autumn cohort during the energy budget and consequently affect local distribution autumn phytoplankton bloom. The results of our study and abundance of planktivores and higher trophic-level lead us to consider a new hypothesis, involving local pro- et al. predators (Johnson , 2011). Wilkinson Basin plays a duction and transport of copepodid stages in the Maine particularly important role in the western GoM because it Coastal Current, that may make the C. finmarchicus popu- C. finmarchicus serves as a primary source of supply of to lation in the western GoM more resilient to climate fishing and northern right whale feeding grounds in forcing than previously predicted. waters off southern New England, including the Great South Channel and Georges Bank (Wishner et al.,1995; Miller et al., 1998; Pendleton et al., 2009). Statistical-based modeling of C. finmarchicus habitat char- METHOD acteristics, notably sea surface temperature, across the North Atlantic predicts that climate-driven ocean warming Samples were collected at survey stations (Fig. 1) during will force distribution of the species northward over the research cruise CH 0712 on the R/V Cape Hatteras next several decades (Reygondeau and Beaugrand, 2011). between 24 September and 3 October 2012 and at two This prediction has particular relevance for the western time series stations (Fig. 1), the Coastal Maine Time GoM, where water column temperatures are historically Series station (CMTS) located at the landward margin of several degrees higher than more northern C. finmarchicus the Maine Coastal Current (Lat. 43844.80N, Lon. habitats (Maps et al., 2012; Melle et al.,2014). Over the past 69830.10W; depth: 105 m), and the Wilkinson Basin decade, water column temperatures in surface and deep Time Series station (WBTS) located in the northwestern waters of the GoM have been rising at a rate (0.28C corner of Wilkinson Basin (Lat. 42851.70N, Lon. year21) that is more than ten times the observed average 69851.80.W; depth: 225 m). The CMTS was sampled at temperaturerise(0.018Cyear21) over the past century semi-monthly to monthly intervals (with some longer (Shearman and Lentz, 2011; Mills et al., 2013). In 2012, gaps) between August 2008 to December 2013, using the identified as an especially anomalous year for the GoM, University of Maine research vessel, R/V Ira C, based at sea surface temperatures in summer were as much as 58C the Darling Marine Center. The WBTS was sampled at higher than the long-term average and the mean annual monthly or longer intervals between January 2005 to July 222 J. A. RUNGE ET AL. j PERSISTENCE OF CALANUS IN THE GULF OF MAINE Fig. 1. Gulf of Maine showing general circulation of surface and deep flows, plankton survey station locations (inset: circles) and time series stations (inset: stars) in Wilkinson Basin (WBTS) and midcoast Maine (CMTS). SS, Scotian Shelf; BoF, Bay of Fundy; NeC, Northeast Channel; eMCC, eastern Maine Coastal Current; wMCC, western Maine Coastal Current; GSS, Great South Channel. 2010 and at monthly intervals between April 2012 and The methods for sampling environmental variables May 2013, using the University of New Hampshire re- and C. finmarchicus abundance at the sampling stations fol- search vessel, R/V Gulf Challenger. lowed, with variations indicated below, the protocols 223 JOURNAL OF PLANKTON RESEARCH j VOLUME 37 j NUMBER 1 j PAGES 221–232 j 2015 established by the Canadian Atlantic Zone Monitoring 1972). For the time series plot of chlorophyll a concentra- Program (Mitchell et al., 2002). Salinity and temperature tions (Fig. 2), bottle sample data were interpolated linearly were measured with a Seabird 19 plus at the CMTS, a in time and with depth from the surface to the bottom of Seabird 19 or 49 at WBTS and a Seabird 911 equipped the mixed layer, below which chlorophyll a concentration with a Wetlabs fluorometer during research cruise CH was assumed to be zero. The mixed layer depth was deter- 0712. Concentrations of chlorophyll a were routinely mea- mined as the depth showing a difference of 0.28Cwiththe sured at WBTS and during CH 0712, but not at the temperature at 10 m (Maps et al., 2012). CMTS. At WBTS, duplicate, 100 mL or 500–550 mL Calanus finmarchicus abundance was estimated from water samples were collected with Nisken bottles at the zooplankton samples collected with 0.75 m diameter, surface, 10, 20 and 40 m.

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