The Response of the Mesozooplankton Community in the Western Gulf of Maine to Changing Oceanographic Conditions: the 2010 Regime Shift

INTRODUCTIONThe mesozooplankton community represents an important link in energy transfer from lower to higher trophic levels in the marine environment, both as grazers of primary producers and as a food source for a variety of consumers from pelagic forage fish to baleen whales. Therefore, observing and assessing changes in mesozooplankton diversity and biomass provides a means for understanding broader changes in marine ecosystems and informing management decisions. The Gulf of Maine is a semi-enclosed shelf sea within the broader North Atlantic biome (Pershing and Stamieskin, 2020). Its mesozooplankton community is largely comprised of copepods, with Calanus finmarchicus the historically dominant species (Bigelow, 1924; Johnson et al., 2011; Melle et al., 2014). Because of its rich lipid stores, C. finmarchicus is a valuable energy source for the North Atlantic right whale and many planktivorous pelagic fish such as sand lance and Atlantic herring (Meyer Gutbrod et al. 2021; Suca et al., 2022; Becker et al., 2020). Other copepods commonly found in the Gulf of Maine, including species the generaCentropages , Pseudocalanus , Metridia , andOithona, are also a food source for planktivores, but have a smaller body size and lipid stores compared to C. finmarchicus (e.g., Lee et al., 2006; Carlowicz et al., 2024).Climate scenario models applying statistical relationships indicate thatC. finmarchicus abundance will disappear or decline substantially in this region in the next five decades as surface and bottom waters in the Gulf of Maine continue to warm (Reygondeau and Beaugrand, 2011; Chust et al., 2014; Grieve et al., 2017). While these projections simplify the complex dynamic processes controlling circulation and production in the Gulf of Maine (e.g. Runge et al., 2015), there is nevertheless the possibility of the loss of C. finmarchicus and consequently the subarctic character of the Gulf of Maine’s ecosystem function (Pershing et al., 2021).Populations of the common resident mesozooplankton exhibit strong seasonal cycles. For example, C. finmarchicus andPseudocalanus spp. reach peak abundance in late spring and early summer, whereas Centropages typicus attains peak abundance in late summer and autumn (Durbin and Kane 2007; Ji et al. 2009; Melle et al. 2014). In addition to seasonal variations, interannual and decadal variations in abundance, diversity, and evenness have been reported (e.g., Pershing et al., 2005, Record et al., 2010, Johnson et al., 2011, Kane 2007, Pershing and Kemberling 2023). Most notably, the annual abundance of late-stage C. finmarchicus (CV-adult) was relatively high in the 1980s, decreased for much of the 1990s, and then increased again between 2000-2010 (Ji et al. 2022: autumn data; Pershing and Kemberling 2023). A reverse pattern of interdecadal increase and decrease is evident in Gulf of Maine populations of Centropages typicus , Pseudocalanus spp. and Oithona spp., as well asC. finmarchicus stages CI-CIV (Pershing and Kemberling, 2023).In or around 2010, a likely climate-driven shift in the oceanographic regime in the Gulf of Maine occurred, characterized by a marked increase in sea surface temperature (GMRI 2022) and a change in the external sources of deep water (Record et al., 2019, Meyer-Gutbrod et al., 2021, Townsend et al., 2023 ). Importantly, an increased influence of Warm Slope Water driven by a northward shift in the Gulf Stream is considered to have supplanted the flow of Labrador Slope Water into the Gulf of Maine via the Northeast Channel (Thibodeau et al., 2018, Seidov et al., 2021; Neto et al. , 2021: see Fig. 1). In addition, Townsend et al. (2023) report variability in the strength of Scotian Shelf Water inflow during winter through spring, which sets up a seasonal barrier to intrusions of Warm Slope Water and modified Gulf Stream water into the Gulf of Maine the following summer and autumn. This increase in influence from Warm Slope Water in the Gulf of Maine is consistent with observations of weakening of the Atlantic Meridional Overturning Circulation (Saba et al., 2016, Caesar et al., 2021, Seidov et al., 2021; Meyer Gutbrod et al., 2021).Correlated with the 2010 shift in in oceanographic conditions is a marked decline in summer through winter late- stage C. finmarchicus (Record et al., 2019; Meyer-Gutbrod et al., 2021; Pershing and Kemberling 2023; Shank et al. 2024; Runge et al. in review). Concurrently, there is evidence of an increase since 2010 of smaller copepods, including Centropages, Pseudocalanus andMetridia species (Pershing and Kemberling 2023,) and an increase in early-stage C. finmarchicus copepodid stages in spring and early summer (Ji et al., 2022; Honda et al., 2024; Runge et al., in review). These changes in the mesozooplankton community drew interest because of their potential link to declines in the populations of endangered and commercially important species (Record et al., 2019, Richards and Hunter, 2021, Meyer-Gutbrod et al., 2021). Notably, the foraging behavior of the critically endangered North Atlantic right whale (NARW) population has shifted in the past decade, moving from their traditional summer feeding grounds in the eastern Gulf of Maine and Bay of Fundy to the Gulf of St. Lawrence (Meyer-Gutbrod et al., 2021). Recent declining trends in lobster recruitment were also shown to correlate with C. finmarchicus abundance and phenology (Carloni et al., 2024; Shank et al. 2024). These oceanographic and ecosystem changes occurring in the Gulf of Maine around 2010 have been called a regime shift in a number of studies (Meyer Gutbrod et al. 2021; Pershing and Kemberling, 2023; Shank et al. 2024). To explain the shift in the mesozooplankton community in 2010, Pershing and Kemberling (2023) proposed that decadal variations in community structure are driven by external physical forcings that enhance water column stratification in the Gulf of Maine, due to freshening (in decades prior to 2010) or surface warming (since 2010), in either case favoring ‘summer-time communities’ of the smaller mesozooplankton taxa (e.g.,Centropages , Pseudocalanus , Metridia , andOithona ). In addition, shifts in phenology, increased predation pressure and the resulting lower autumn-winter abundance of C. finmarchicus (as predators on early copepod life stages and competitive grazers), are recognized to play a role in shaping the mesozooplankton community (Ji et al, 2022; Wiebe et al., 2022; Pershing and Kemberling, 2023; Honda et al., 2024).The effects of the 2010 shift in oceanographic conditions and the mechanisms underlying change in the Gulf of Maine mesozooplankton community merit further investigation, not only to better understand how the western Gulf of Maine ecosystem will respond to future oceanographic change, but also to provide insight into mechanisms driving mesozooplankton dynamics across the margin of the North Atlantic biome. Here we use data from two time series stations in the western Gulf of Maine to document change in the periods immediately before and after the 2010 oceanographic shift. Recent studies indicate the importance of seasonal drivers in regulating the abundance of C. finmarchicus , such that the decadal scale patterns of abundance of C. finmarchicus stages CI-CIV (driven by processes occurring between late winter through mid summer) are in many ways opposite to the pattern of abundance of stages CV-CVI (Pershing and Kemberling, 2023; Honda et al.,2024; Runge et al., in review). We apply the lens of seasonality in drivers to examine how C. finmarchicus and other species and the overall diversity of the mesozoplankton community responded at subannual to annual scales, and whether the integration of responses across species sustained or changed total mesozooplankton biomass. We examine the evidence for the hypothesis that the oceanographic shift led to an expansion of the summertime mesozooplankton community adapted to more stratified, oligotrophic conditions with higher abundance and diversity of predators (Pershing and Kemberling, 2023). We find that the observations from these two time series stations provide insight into the complex interactions among changes in external advective supply, atmospheric forcing and local production in the western Gulf of Maine, where the direct socioeconomic impacts of a pelagic ecosystems shift are particularly important.

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