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Windowpane flounder (Scophthalmus aquosus) and winter flounder (Pseudopleuronectes americanus) responses to cold temperature extremes in a Northwest Atlantic estuary
SEARES-01355; No of Pages 8 Journal of Sea Research xxx (2015) xxx–xxx
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Windowpane flounder (Scophthalmus aquosus) and winter flounder (Pseudopleuronectes americanus) responses to cold temperature extremes in a Northwest Atlantic estuary Dara H. Wilber a,⁎, Douglas G. Clarke b, Catherine M. Alcoba c, Jenine Gallo c a b c
HX5, 664 Old Plantation Rd., Charleston, SC 29412, United States HDR Engineering Inc., One International Blvd., 10th Floor/Suite 1000, Mahwah, NJ 07495, United States U.S. Army Corps of Engineers New York District, 26 Federal Plaza, Room 2146, New York, NY 10278-0090, United States
a r t i c l e
i n f o
Article history: Received 1 January 2015 Received in revised form 24 March 2015 Accepted 7 April 2015 Available online xxxx Keywords: New York/New Jersey Harbor Flatfish Overwintering Thermal stress
a b s t r a c t The effect of climate variability on flatfish includes not only the effects of warming on sensitive life history stages, but also impacts from more frequent or unseasonal extreme cold temperatures. Cold weather events can affect the overwintering capabilities of flatfish near their low temperature range limits. We examined the responses of two flatfish species, the thin-bodied windowpane (Scophthalmus aquosus) and cold-tolerant winter flounder (Pseudopleuronectes americanus), to variable winter temperatures in a Northwest Atlantic estuary using abundance and size data collected during a monitoring study, the Aquatic Biological Survey, conducted from 2002 to 2010. Winter and spring abundances of small (50 to 120 mm total length) juvenile windowpane were positively correlated with adult densities (spawning stock) and fall temperatures (thermal conditions experienced during post-settlement development for the fall-spawned cohort) of the previous year. Windowpane abundances in the estuary were significantly reduced and the smallest size class was nearly absent after several consecutive years with cold (minimum temperatures b1 °C) winters. Interannual variation in winter flounder abundances was unrelated to the severity of winter temperatures. A Paulik diagram illustrates strong positive correlations between annual abundances of sequential winter flounder life history stages (egg, larval, Age-1 juvenile, and adult male) within the estuary, reflecting residency within the estuary through their first year of life. Temperature variables representing conditions during winter flounder larval and post-settlement development were not significant factors in multiple regression models exploring factors that affect juvenile abundances. Likewise, densities of predators known to consume winter flounder eggs and/or post-settlement juveniles were not significantly related to interannual variation in winter flounder juvenile abundances. Colder estuarine temperatures through the first year of life were associated with smaller Age-1 winter flounder body size. For example, Age-1 winter flounder developing under conditions that differed by 1.9 °C in mean daily water temperature, averaged 98.7 mm total length (TL) and 123.1 mm TL, for the relatively cold vs. moderate years, respectively. More frequent cold temperature extremes associated with climate variability may negatively impact the overwintering capabilities of some flatfish near their cold temperature range limits, whereas cold-tolerant species may experience reduced growth, which imparts the ecological challenges associated with smaller body size. © 2015 Elsevier B.V. All rights reserved.
1. Introduction Fish survival during early life history stages is a strong determinant of recruitment success (e.g., Houde, 1989; Gibson, 1994; Sogard et al., 2001; Manderson, 2008). Consequently, a better understanding of what factors influence egg, larval, and young-of-year mortality has been a research priority (Van der Veer et al., 2000). Factors mediating flatfish survival at these vulnerable stages include predation (Manderson et al., 2000; Taylor and Collie, 2003; Taylor and Danila, 2005), prey availability (Leggett and DeBlois, 1994), ⁎ Corresponding author. Tel.: +1 843 795 6599. E-mail address: [email protected] (D.H. Wilber).
temperature (Van der Veer, 1986; Henderson, 1998; Neuman and Able, 2009), habitat degradation (Gibson, 1994; Able, 1999; Able et al., 1999) and unsuitable hydrodynamic conditions (Rijnsdorp et al., 1985; Castillo et al., 1994). Warmer water temperatures resulting from climate change may intensify mechanisms that, either directly or indirectly, induce mortality. For instance, warmer temperatures may increase thermal stress for some species at the southern extent of their ranges (Desaunay et al., 2006; Rijnsdorp et al., 2009). Fish distributions may shift toward higher latitudes, reflecting either a range expansion into areas that historically were too cold (Stebbing et al., 2002) or an emigration from areas no longer cold enough (Able et al., 2014). Warmer temperatures also may increase larval mortality on a regional scale, which synchronizes interannual variation in recruitment for
http://dx.doi.org/10.1016/j.seares.2015.04.005 1385-1101/© 2015 Elsevier B.V. All rights reserved.
Please cite this article as: Wilber, D.H., et al., Windowpane flounder (Scophthalmus aquosus) and winter flounder (Pseudopleuronectes americanus) responses to cold temperature extremes in a Northwest Atlantic estuary, J. Sea Res. (2015), http://dx.doi.org/10.1016/j.seares.2015.04.005
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D.H. Wilber et al. / Journal of Sea Research xxx (2015) xxx–xxx
subpopulations and destabilizes resilience to disturbances for regional stocks (Manderson, 2008; Bell et al., 2014). Aside from warming temperatures, climate change may increase temperature variability, causing the magnitudes and frequencies of both low and high temperature extremes to increase (IPCC, 2001: Climate Change, 2001). Thus, overwintering capabilities of flatfish may be affected for species living near their cold temperature thresholds. In this study, we examined how cold temperature extremes in a Northwest Atlantic estuary were associated with variation in juvenile abundance and size for two flatfish species that differ in their cold temperature tolerances. This study was conducted in New York/New Jersey Harbor (Harbor), a heavily urbanized and industrialized estuary in the Northwest Atlantic Ocean. Winter flounder (Pseudopleuronectes americanus) supports important commercial and recreational fisheries in the region that have declined substantially for inshore populations (ASMFC, Atlantic States Marine Fisheries Commission, 2006) in part, because of overfishing in the 1980s and poor recruitment in the late 1990s and 2000s (Able et al., 2014). Winter flounder are demersal throughout their life cycle and therefore are particularly susceptible to impacts to benthic habitat, such as dredging which is needed to maintain and deepen navigation channels for port operations in the Harbor. To minimize potential dredging impacts on winter flounder eggs and larvae, the New York District United States Army Corps of Engineers conducted a multi-year, spatially-robust, sampling program, the Aquatic Biological Survey (ABS), to document the timing and location of winter flounder spawning activity in the Harbor (Wilber et al., 2013a,b). Data collected during this sampling program are a valuable resource for examining potential mechanisms by which extreme temperatures may affect flatfish growth and survival. 1.1. Study organisms Windowpane flounder (Scophthalmus aquosus, hereafter, windowpane) and winter flounder are the most abundant flatfish inhabiting the Harbor. Windowpane and winter flounder distributions overlap throughout the Northwest Atlantic, with windowpane more abundant to the south (near Chesapeake Bay) and winter flounder more abundant at higher latitudes (north of Cape Cod; Collette and Klein-MacPhee, 2002). Temperature may determine the range and local abundances of windowpane at its northern limit (Chang et al., 1999) and winter flounder at its southern limit (Able et al., 2014; Bell et al., 2014). These species differ in their physiological adaptations to thermal stress as well as seasonal patterns of reproduction; therefore individuals of each species enter their first winter at different ages and sizes and have different susceptibilities to cold temperature stress (Table 1). Windowpane spawn in the late spring and again in the fall (Wilk et al., 1990; Morse and Able, 1995; Neuman and Able, 2009), thus the
two windowpane cohorts (especially fall-spawned individuals) have limited time to grow before overwintering. Windowpane eggs are buoyant and spawned on or near the bottom (Chang et al., 1999). In contrast, winter flounder are cold tolerant, seasonally producing an antifreeze protein that protects them from cold shock (Fletcher, 1981; Fletcher et al., 1985). Winter flounder eggs are demersal and spawning occurs in the Harbor from January to March (Wilber et al., 2013a) therefore, Age-0 juveniles feed and grow throughout the summer and fall before entering their first winter in their natal estuary. Larger body size for windowpane is an effective defense to cold temperature stress (Neuman and Able, 2009) and essential to survival of overwintering windowpane near their northern range limit because they do not produce antifreeze proteins. Smaller individuals belong to the fall-spawned cohort, and because mortality is size-selective, the overwintering capability of young-of-the-year windowpane differs between the spring- and fall-spawned cohorts (Neuman and Able, 2009). The relative contribution of the two cohorts to overall windowpane population size is unknown, as is the frequency of environmental conditions that induce overwinter mortality. Overwintering impacts on windowpane and winter flounder are compared in this study because their different life history characteristics and susceptibilities to cold stress are especially relevant in an estuary that is near the northern vs. southern extents of their respective distributions, and because results may signal the likelihood of potential range shifts in an era of increasing climate variability. 2. Methods In this study, three Harbor subareas were identified: Arthur Kill/ Newark Bay (AKNB), Lower Bay (LB), and Upper Bay (UB; Fig. 1). During ABS sampling, demersal eggs and larvae were collected biweekly from mid-January to mid-June from 2002 to 2011. Ichthyoplankton samples were collected using an epibenthic sled (0.5-mm mesh plankton net with an opening of 0.25 m2 and the lowest point of the net ringer
Table 1 Life history characteristics for windowpane (Scophthalmus aquosus) and winter flounder (Pseudopleuronectes americanus) in Northwest Atlantic estuaries. Life history phase
Windowpane
Winter flounder
Egg type Spawning season Larval development Juvenile residency period Adult residency
Buoyant Spring and falla,b Summera Year-rounda Year-round with seasonal movements to nearshore habitatsa
Demersal Winter and early springc Springc Year-round for 1–2 yearsd Emigration from estuary in spring when temperatures exceed 12–15 °Ce,f
a b c d e f
Chang et al. (1999). Morse and Able (1995). Wilber et al. (2013a). Sagarese and Frisk (2011). Danila and Kennish (1981). Decelles and Cadrin (2010).
Fig. 1. Location of New York/New Jersey Harbor (black box) on the northeastern coast of the United States. Aquatic Biological Survey sampling was conducted from 2002 through 2010 in all Harbor subareas: Arthur Kill, Newark Bay, Upper Bay, and Lower Bay.
Please cite this article as: Wilber, D.H., et al., Windowpane flounder (Scophthalmus aquosus) and winter flounder (Pseudopleuronectes americanus) responses to cold temperature extremes in a Northwest Atlantic estuary, J. Sea Res. (2015), http://dx.doi.org/10.1016/j.seares.2015.04.005
D.H. Wilber et al. / Journal of Sea Research xxx (2015) xxx–xxx
2.1. Data analysis Winter flounder egg and larval abundances are well documented, as the ABS sampling was designed to characterize winter flounder spawning activity from January to June. However, since sampling only partially overlapped with windowpane spring spawning in the Harbor and did not capture fall spawning and peak larval occurrences, only spring windowpane egg abundance and distribution patterns are described here. In addition, different analytical approaches are used to examine influences on juvenile abundances for the two species. Factors that may influence recruitment to the juvenile stage, such as temperatures experienced during larval and post-settlement development are examined for both species. However, the potential relative influence of predators on early life history (ELH) stages is only examined for winter flounder because ABS sampling was not conducted during the summer and fall when predators on windowpane ELH stages could be assessed. Three size-cohorts of windowpane correspond to small juveniles (b120 mm TL), large juveniles (121 to 220 mm TL) and adults (N220 mm TL; Morse and Able, 1995). Catch-per-unit-effort (CPUE) was calculated as the number of fish per 10-min trawl and was standardized by trawl duration if tows were shorter in duration. To examine whether windowpane moved to deeper Harbor areas during cold winters, i.e., into channels, a three-factor Analysis of Variance (ANOVA) was conducted using mean windowpane CPUE as the dependent variable and season (winter, January–March; spring, April–June), station type (channel vs. non-channel), and severity of winter (cold vs. moderate) as independent variables. Seasons were defined as winter (January to March) and spring (April to June). Severity of winter was classified as ‘cold’ and ‘moderate’ for years with minimum annual temperatures below and above 1 °C, respectively. CPUE data were log(x + 1) transformed to meet the normality and homogeneity of variance assumptions of the test. Mean annual CPUEs were not autocorrelated using one-, two-, and three-year time lags (Pearson correlations) and were used as the source of replication. Potential factors influencing small juvenile windowpane annual abundances (dependent variable) were examined using multiple regression analyses. Mean adult CPUE the previous year (an estimate of spawning stock size), cumulative degree days (sum of daily mean temperatures) from October 1 through December 31 of the previous year (temperatures experienced by fall-spawned individuals), and the minimum winter water temperature (estimate of overwinter thermal stress) were included as independent factors. A two-factor ANOVA was used to test for potential differences in windowpane CPUE by size (small juveniles, large juveniles, adults) and time periods grouped by years that followed cold (2004, 2005,
and 2006) and moderate (2002, 2003, 2007–2010) winters. This test was conducted to investigate potential abundance changes consistent with overwinter mortality the previous year for fish too small to be ampled by the bottom trawl gear. Mean CPUEs for each size class by sampling event were used as the dependent variable following a log(x + 1) transformation. Winter flounder juveniles caught in the bottom trawl survey are defined as b 150 mm TL (Witherell and Burnett, 1993) and were assumed to be predominantly Age-1 individuals because the gear does not reliably collect individuals b 50 mm TL, a size corresponding to Age-0 winter flounder in the winter and spring. Age-1 winter flounder CPUE is positively correlated with the annual egg CPUE (# of eggs/1000 m3) of the previous year (Wilber et al., 2013a). The potential additional influences of temperature and predator impacts on Age-1 year class strength were explored using multiple regression analysis. Mean April and maximum annual water temperatures were included as independent variables to represent thermal conditions during larval and early post-settlement periods, respectively. CPUEs of summer flounder (Paralichthys dentatus), striped searobin (Prionotus evolans) and striped bass (Morone saxatilis), three fish that prey upon winter flounder eggs and Age-0 juveniles (Manderson et al., 2000, 2006), were also included as independent variables in multiple regression analyses conducted to examine influences on Age-1 juvenile abundances the following year. Mean CPUEs for predators in two time periods, February and March; and May and June; were used to estimate predator pressure on winter flounder eggs and newly-settled juveniles, respectively. High winter flounder egg abundances in 2003 and 2007 (Wilber et al., 2013a) corresponded to large Age-1 year classes in 2004 and 2008 (Wilber et al., 2013b), which developed over cold and moderate temperature profiles, respectively. To investigate the effects of different thermal conditions on growth, the mean sizes of Age-1 juveniles collected during each sampling event in 2004 and 2008 were compared using a one-factor ANOVA.
3. Results New York/New Jersey Harbor is composed of three subareas that are distinguished by highest salinities (25 to 28 psu) in Lower Bay (LB), intermediate salinities (21 to 24 psu) in Upper Bay (UB), and lowest salinities (17 to 21 psu) in Arthur Kill/Newark Bay (AKNB). Dissolved oxygen concentrations ranged from 5 to 11 mg/l and did not approach hypoxic conditions in any subarea. Winter water temperatures varied considerably in the Harbor during the study period, with minimum temperatures less than 1 °C in three years (2003 to 2005) and warmer minimum temperatures averaging 3.3 °C in other years (Fig. 2). Water temperatures within sampling events, however, were fairly uniform among Harbor subareas and usually differed by less than 0.5 °C between 10 8
Temperature (oC)
mounted 178 mm above the substrate). During each sampling period, between 26 and 29 stations at fixed locations in both channel and non-channel areas in each Harbor subarea were sampled. Sixteen core stations were sampled in all ten years and data from the core stations were used for inter-annual comparisons to avoid confounding potential spatial and temporal effects (Wilber et al., 2013a). Bottom trawl surveys were conducted biweekly from January to June over a nine-year time period (2002 to 2010) at 24 to 29 stations. Sixteen core stations that corresponded to the ichthyoplankton core stations were sampled each year and were used in interannual comparisons (Wilber et al., 2013b). Bottom trawls (10 min. tow duration) were conducted using a 9.1 m otter trawl with 2.5 cm square mesh wings and body and a 1.9 cm square mesh cod end with a 0.6 cm square mesh liner. Salinity, temperature, and dissolved oxygen were measured at 0.3 m above the bottom at each station using a water quality meter (YSI Model 85). To better understand the continuous temperature conditions experienced by fish throughout the study period, water temperature data were obtained from records for the NOAA gauge located within the study area (station ID 8518750) at the southern end of Manhattan Island.
3
6 4 2 0 1/1 -2
1/8
1/15
1/22
1/29
2/5
2/12
2/19
2/26
3/5
Date
Fig. 2. Winter water temperatures recorded at NOAA gauge station ID 8518750 located at the southern tip of Manhattan Island from 2002 to 2010. Years were classified by severity of winter temperatures as cold (2003, 2004, 2005; solid lines) and moderate (2002, 2006 to 2010; dashed lines).
Please cite this article as: Wilber, D.H., et al., Windowpane flounder (Scophthalmus aquosus) and winter flounder (Pseudopleuronectes americanus) responses to cold temperature extremes in a Northwest Atlantic estuary, J. Sea Res. (2015), http://dx.doi.org/10.1016/j.seares.2015.04.005
D.H. Wilber et al. / Journal of Sea Research xxx (2015) xxx–xxx
channel and non-channel stations within a subarea for all sampling periods (Wilber et al., 2013a). Windowpane eggs were among the more common eggs collected in the Harbor, accounting for 5.3% of all eggs collected over the ten years of ABS ichthyoplankton sampling. Windowpane eggs were first collected in April, increased in abundance in May and June (Fig. 3A), and were concentrated in both channel and non-channel stations in LB and at UB channel stations, with few collected in the AKNB subarea (Fig. 3A). Windowpane egg CPUE for the first three months of the spring spawning season varied among years (Fig. 3B). Windowpane juvenile/ adult CPUE did not differ by season or severity of winter temperature (Fig. 4) and was significantly higher at channel stations (F = 6.67, p b 0.05) with no interactions with the other variables. Overall, nearly 80% of juvenile and adult windowpane were collected at channel stations. Small juvenile windowpane CPUE was positively correlated with adult CPUE the previous year and cumulative degree days in the fall (r2 = 0.86; Table 2). Minimum annual overwintering temperatures were not a significant variable when added to the multiple regression model. Three modal windowpane size classes were apparent in years that followed moderate winters (Fig. 5A). Windowpane abundances were significantly lower in the years following cold winters (F = 5.0, p b 0.05) and this reduction in CPUE did not differ significantly among size classes (F = 0.4, p N 0.6; Fig. 5B). Significant positive correlations among winter flounder annual life history stages depicted through a Paulik diagram (sensu Nash, 1998; Payne et al., 2009) include; egg and adult male densities during the spawning season (r = 0.95, p b 0.001), egg and larval CPUEs (r = 0.68, p b 0.05), larval CPUE and Age-1 juvenile CPUE the next year
Windowpane Egg CPUE
A 1200 1000 800 600
AKNB CH AKNB NC LB CH LB NC UB CH UB NC
400 200
3.0
Mean Juvenile/Adult CPUE
4
Windowpane
2.5
Cold Moderate
2.0
1.5
1.0
0.5
0.0
Jan
Feb
Mar
Apr
May
June
Fig. 4. Mean monthly juvenile and adult catch-per-unit-effort (CPUE, number of fish per 10-min trawl) for windowpane in years with cold (2003, 2004, 2005; black) and moderate (2002, 2006, 2007, 2008, 2009; moderate) winter water temperatures.
(r = 0.71, p b 0.05), and adult male CPUE during the spawning season and Age-1 juvenile CPUE the next year (r = 0.83, p = 0.01; Fig. 6). Egg and adult female densities during the spawning season were unrelated, perhaps because some females were skip-spawning and foraging in the estuary (Wilber et al., 2013b). The best predictor of Age-1 winter flounder densities in the Harbor is the egg CPUE of the previous year (r = 0.89, p = 0.003; Wilber et al., 2013b). Adding annual predator (summer flounder, striped searobin, and striped bass) densities in multiple regression models did not improve the fit of this relationship. The temperature variables examined also were not significant factors in explaining interannual variation in Age-1 winter flounder juvenile abundances. Water temperatures experienced during the first year of life for Age-1 winter flounder cohorts collected in 2004 and 2008 were consistently higher for the 2008 cohort (Fig. 7). Daily temperatures experienced by the 2008-cohort were, on average, 1.9 °C higher than that experienced by the 2004-cohort, with a maximum daily temperature difference of 5.8 °C. Age-1 juveniles in the 2008 cohort were significantly larger (F = 18.7, p = 0.001) than those in the 2004 cohort, averaging 123.1 mm TL compared to 98.7 mm TL (Fig. 8).
0 Jan
Mean Egg CPUE
B
500 450 400 350 300 250 200 150 100 50 0
Feb
Mar
Apr
May
June
Windowpane
4. Discussion Negative impacts on overwintering juveniles caused by more frequent or extreme cold temperatures may affect fish population stability Table 2 Variables examined to explain interannual variation in small juvenile windowpane (r2 = 0.86) and Age-1 winter flounder (r2 = 0.79) CPUE (number of fish per 10-min trawl) as determined by multiple regression analyses. Small juvenile windowpane CPUE
2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 Fig. 3. (A) Mean (+ standard error) windowpane egg catch-per-unit-effort (CPUE; number of eggs/1000 m3) at Harbor subareas Arthur Kill/Newark Bay (AKNB), Lower Bay (LB) and Upper Bay (UB) and channel (CH) or non-channel (NC) stations and (B) interannual variation in windowpane egg CPUE.
Variable
Coefficient
Std. error
t
p-Value
Constant Adult CPUE previous year Fall temperature previous year
−2.319 1.187 0.002
0.622 0.213 0.000
−3.729 5.574 3.878
0.014 0.003 0.012
Coefficient
Std. error
t
p-Value
Age-1 winter flounder CPUE Variable Constant Egg CPUE previous year
0.843 0.001
0.268 0.000
3.145 4.253
0.020 0.005
Please cite this article as: Wilber, D.H., et al., Windowpane flounder (Scophthalmus aquosus) and winter flounder (Pseudopleuronectes americanus) responses to cold temperature extremes in a Northwest Atlantic estuary, J. Sea Res. (2015), http://dx.doi.org/10.1016/j.seares.2015.04.005
D.H. Wilber et al. / Journal of Sea Research xxx (2015) xxx–xxx
5
A
Mean CPUE
0.08
Years Following Moderate Winters
0.06 0.04 0.02 0.00 20 40 60 80 100 120 140 160 180 200 220 240 260 280 300 320 340 360 390
Windowpane Total Length (mm)
Mean CPUE
B
0.08
Years Following Cold Winters
0.06 0.04 0.02 0.00 20 40 60 80 100 120 140 160 180 200 220 240 260 280 300 320 340 360 390
Windowpane Total Length (mm) Fig. 5. Size frequency distributions from bottom trawl surveys of windowpane in the (A) years following moderate winters (2002, 2003, 2007–2010) and (B) years following cold winters (2004, 2005, 2006). CPUE is calculated as number of fish per 10-min trawl.
in areas where cold temperature stress occurs. Cold temperatures affected two flatfish species inhabiting a Northwest Atlantic estuary differently. Windowpane experience size-selective overwinter mortality under laboratory conditions, with 94% mortality for individuals b 24 mm TL compared to 50% mortality for larger fish within a
fall-spawned cohort (Neuman and Able, 2009). Spring-spawned individuals (83 to 140 mm TL) can survive overwintering at temperatures as low as −2.0 °C (Neuman and Able, 2009). In our study, small individuals (i.e., b50 mm TL) were not sampled effectively in the ABS bottom trawl survey, therefore overwinter mortality for these windowpane
Fig. 6. A Paulik diagram for winter flounder CPUEs of eggs and larvae, larvae and Age-1 juveniles the next year, adult males and Age-1 juveniles the next year, and adult males and eggs within the spawning season. Axes values are index values for illustrative purposes only, therefore numbers are not displayed.
Please cite this article as: Wilber, D.H., et al., Windowpane flounder (Scophthalmus aquosus) and winter flounder (Pseudopleuronectes americanus) responses to cold temperature extremes in a Northwest Atlantic estuary, J. Sea Res. (2015), http://dx.doi.org/10.1016/j.seares.2015.04.005
D.H. Wilber et al. / Journal of Sea Research xxx (2015) xxx–xxx
24
Eggs Larvae
Age-0
Age-1
19 14
2004 Age-1 2008 Age-1
9
Jan Feb Mar Apr May Jun
Sep Oct Nov Dec
-1
Apr May Jun Jul Aug
4
Jan Feb Mar
Mean Weekly Temperature oC
6
Fig. 7. New York/New Jersey Harbor water temperatures experienced by the 2004 (solid line) and 2008 (dashed line) Age-1 winter flounder cohorts from the egg stage through June of the Age-1 juvenile stage.
could not be inferred from samples collected during years with extreme cold temperatures (i.e., minimum temperatures b1 °C). However, lower windowpane abundances in years that followed cold winters are consistent with high overwinter mortality the previous year, especially for smaller fish, or emigration from the estuary. Because cold winters were sequential (2003 to 2005), any overwinter mortality was compounded by survivors experiencing cold conditions that may have reduced growth, further increasing the likelihood of size-selective thermal impacts. The near elimination of the smallest size class (modal size of 60–70 mm TL) following cold winters may limit recruitment to the adult stage, which could destabilize the population within the estuary. Lower estuarine windowpane abundances in years that followed cold winters also may be indicative of emigration from the Harbor. In the southern Gulf of Maine, windowpane occur in the shallowest and warmest waters available during the summer and are absent in areas where water temperatures were b1 °C (Hanson and Wilson, 2014), perhaps moving short distances offshore to overwinter (Hanson and Courtenay, 1995). Nearshore sampling was not conducted in our study to assess offshore movement. Deep areas within the Harbor (channels) were preferred by windowpane regardless of seasonal temperatures and did not provide a temperature refuge in this well-mixed estuary. Although larger windowpane are more capable of overwintering at low temperatures (e.g., mortality for windowpane N 100 mm TL occurred only when temperatures dropped rapidly below 0 °C; Neuman and Able, 2009), the lower densities of all size classes over the extended period (2003–2005) with cold winters suggests either mortality reduced estuarine population size, fish emigrated to nearshore habitat, or a combination of these events occurred. In contrast, winter flounder are cold-tolerant, i.e., they are capable of producing an antifreeze protein that reduces the probability of overwinter mortality. However, even with a lower risk of mortality due to freezing, mortality may occur if prey are limited or fish are unable to feed because of low temperatures. These potential impacts are more
relevant to smaller individuals because larger body size provides more energy reserves to combat starvation and a lower metabolic rate per unit body mass (e.g., Hurst et al., 2000). Winter flounder in Narragansett Bay, Rhode Island, did not exhibit size-dependent overwinter mortality in 2008, perhaps because they fed throughout the winter on amphipods and polychaetes and maintained lipid stores, thus reducing their risk of starvation (Bell, 2012). Winter temperatures in 2008, however, were relatively mild, remaining above 4 °C (Bell, 2012), therefore additional studies are needed to address feeding behavior in the field under colder conditions. There was no evidence of overwinter mortality for winter flounder in our Harbor study. Age-1 juvenile abundances were strongly correlated with egg abundances from the previous year. The addition of predator densities and temperature variables corresponding to periods of larval and Age-0 juvenile development did not explain any residual variation in this relationship. The importance of relative predator vs. winter flounder ELH stage densities under natural conditions has not been described; therefore the form of this potential relationship is unknown. Temperature, however, is associated with year-class strength for inshore winter flounder populations. In two estuaries, Age-1 winter flounder abundances were positively correlated with the April temperatures experienced by foraging adults two years previous, possibly because warmer temperatures promote benthic productivity and increase prey availability for adults that need to replenish exhausted energy reserves in order to spawn the following year (Wilber et al., 2013b). Overall, positive correlations in CPUE among sequential winter flounder life history stages (Fig. 5) are consistent with a population that is highly localized within the Harbor for the first year of life, as has been indicated for other estuarine populations of winter flounder through genetic studies (Crivello et al., 2004; Buckley et al., 2008) and resident contingents of populations revealed through a tagging study (Sagarese and Frisk, 2011). Colder temperatures throughout the first year of life were associated with smaller Age-1 juvenile winter flounder size, an effect also observed in Greenland halibut (Reinhardtius hippoglossoides; Sunksen et al., 2010). Age-1 winter flounder size exceeds the lower size threshold of fish effectively collected by the bottom trawl; therefore it is unlikely that a sampling bias contributed to the different size distributions of juveniles that developed over relatively cold vs. moderate conditions. Mechanisms underlying the smaller size at lower temperatures are unknown and may include a combination of lower prey availability, slower metabolic processes, and reduced foraging activity. It is unlikely that intraspecific (density-dependent) competition for food contributed to the body size disparity, as indicated with juvenile European plaice (Ciotti et al., 2013) because of the similar densities of the two cohorts for the years compared. Disadvantages to smaller body size include an increased predation risk, reduced feeding success if a correspondingly smaller gape width reduces prey availability, and a potential delay in the onset of sexual maturity. Warmer spring and summer temperatures can negatively affect winter flounder larval development (Buckley et al., 1990), however,
Number of Fish
120 100
2004
80
2008
60 40 20 0 40 60 80 100 120 140 160 180 200 220 240 260 280 300 320 340 360 380 410
Winter Flounder Total Length (mm) Fig. 8. Size frequency distributions of the 2004 (black bars) and 2008 (gray bars) Age-1 winter flounder cohorts.
Please cite this article as: Wilber, D.H., et al., Windowpane flounder (Scophthalmus aquosus) and winter flounder (Pseudopleuronectes americanus) responses to cold temperature extremes in a Northwest Atlantic estuary, J. Sea Res. (2015), http://dx.doi.org/10.1016/j.seares.2015.04.005
D.H. Wilber et al. / Journal of Sea Research xxx (2015) xxx–xxx
our study found no evidence that temperature variation in the spring during this nine-year study period affected larval developmental success and recruitment to the juvenile stage. Maximum spring water temperatures did not exceed 18 °C. Likewise, maximum summer temperatures were not correlated with recruitment to the Age-1 juvenile stage for winter flounder. Summer temperatures during the study period (maximum = 26.9 °C) were lower than temperature extremes associated with winter flounder inactivity and mortality (e.g., 30 °C; Pearcy, 1962), therefore high temperatures associated with mortality for winter flounder early life history stages may not have occurred during the course of this study. Although this study was conducted over a relatively short time series (2002–2010), the inclusion of years with highly variable winter temperatures allows a comparison of how flatfish respond to cold temperature extremes. Differences in windowpane abundances in years following cold vs. moderate winters were consistent with the size-specific mortality that was demonstrated in laboratory experiments for this species (Neuman and Able, 2009) and in other flatfish like smallmouth flounder (Hales and Able, 2001). Although winter flounder are better adapted to survive extreme cold temperatures, the smaller size of Age-1 individuals following cold winters indicates sublethal impacts occurred that could negatively affect survival, foraging success, and reproduction. Climate variability that increases the frequency or magnitude of cold winter temperatures may increase overwinter mortality in fish near their cold-temperature range limits, resulting in range retraction from these areas. Species that are coldtolerant, may survive extreme cold conditions and maintain their geographic distributions, but detrimental impacts to growth may reduce foraging success, survival, and reproduction. Acknowledgments The U.S. Army Corps of Engineers New York District (USACE NYD) and the Port Authority of New York and New Jersey funded the Aquatic Biological Survey (ABS) in support of the 50-foot Harbor Deepening Project. The expertise of many HDR Engineering Inc. staff, including David Davis and Sarah Zappala greatly contributed to the quality of the ABS program. We appreciate the assistance of Liz Duermit with figure creation. References Able, K.W., 1999. Measures of juvenile fish habitat quality: examples from a National Estuarine Research Reserve. Am. Fish. Soc. Symp. 22, 134–147. Able, K.W., Manderson, J.P., Studholme, A.L., 1999. Habitat quality for shallow water fishes in an urban estuary: the effects of man-made structures on growth. Mar. Ecol. Prog. Ser. 187, 227–235. Able, K.W., Grothues, T.M., Morson, J.M., Coleman, K.W., 2014. Temporal variation in winter flounder recruitment at the southern margin of their range: is the decline due to increasing temperatures? ICES J. Mar. Sci. http://dx.doi.org/10.1093/icesjms/ fsu094. ASMFC (Atlantic Staes Marine Fisheries Commission), 2006. Species profile: winter flounder current plan seeks to rebuild southern New England/Mid-Atlantic stock and sustain Gulf of Maine stock. Atl. States Mar. Fish. Ser. Fish. Focus 15, 4–6. Bell, R.J., 2012. Winter feeding as an overwintering survival strategy in young-of-the-year winter flounder. Trans. Am. Fish. Soc. 141, 855–871. Bell, R.J., Hare, J.A., Manderson, J.P., Richardson, D.E., 2014. Externally driven changes in the abundance of summer and winter flounder. ICES J. Mar. Sci. http://dx.doi.org/ 10.1093/icesjms/fsu069. Buckley, L.J., Smigielski, A.S., Halavik, T.A., Laurence, G.C., 1990. Effects of water temperature on size and biochemical composition of winter flounder Pseudopleuronectes americanus at hatching and feeding initiation. Fish. Bull. 88, 419–428. Buckley, L.J., Collie, J., Kaplan, L.A.E., Crivello, J., 2008. Winter flounder larval genetic population structure in Narragansett Bay, RI: recruitment to juvenile young-of-the-year. Est. Coasts 31 pp. 745–754. Castillo, G.C., Li, H.W., Golden, J.T., 1994. Environmentally induced recruitment in petrale sole, Eopsetta jordani. Fish. Bull. U.S. 92, 481–493. Chang, S., Berrien, P.L., Johnson, D.L., Morse, W.W., 1999. Essential fish habitat source document: windowpane, Scophthalmus aquosus, life history and habitat characteristics. NMFS-NE-137NOAA Tech. Mem. (32 pp.). Ciotti, B.J., Targett, T.E., Burrows, M.T., 2013. Spatial variation in growth rate of early juvenile European plaice Pleuronectes platessa. Mar. Ecol. Prog. Ser. 475, 213–232.
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Seasonal abundance and distribution of fishes in the Miramichi estuary. Can. Spec. Publ. Fish. Aquat. Sci. 123, 141–160. Hanson, J.M., Wilson, T., 2014. Abundance, distribution, and diet of a small-bodied ecotype of windowpane. Trans. Am. Fish. Soc. 143, 650–659. Henderson, P., 1998. On the variation in dab Limanda limanda recruitment: a zoogeographic study. J. Sea Res. 40, 131–142. Houde, E.D., 1989. Comparative growth, mortality, and energetics of marine fish larvae: temperature and implied latitudinal effects. Fish. Bull. 87, 471–495. Hurst, T.P., Schultz, E.T., Conover, D.O., 2000. Seasonal energy dynamics of young-of-theyear Hudson River striped bass. Trans. Am. Fish. Soc. 129, 145–157. IPCC, 2001: Climate Change, 2001. The Scientific Basis. Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change. In: Houghton, J.T., Ding, Y., Griggs, D.J., Noguer, M., Van der Linden, P.J., Dai, X., Maskel, K., Johnson, C.A. (Eds.), Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA (881 pp.). Leggett, W.C., DeBlois, E.M., 1994. Recruitment in marine fishes: is it regulated by starvation and regulation in the egg and larval stages? Neth. J. Sea Res. 32, 119–134. Manderson, J.P., 2008. The spatial scale of phase synchrony in winter flounder (Pseudopleuronectes americanus) production increased among southern New England nurseries in the 1990s. Can. J. Fish. Aquat. Sci. 65, 340–351. Manderson, J.P., Phelan, B.A., Stoner, A.W., Hilbert, J., 2000. Predator–prey relations between age-1 + summer flounder (Paralichthys dentatus, Linnaeus) and age-0 winter flounder (Pseudopleuronectes americanus, Walbaum): predator diets, prey selection, and effects of sediments and macrophytes. J. Exp. Mar. Biol. Ecol. 251, 17–39. Manderson, J.P., Pessutti, J., Shaheen, P., Juanes, F., 2006. Dynamics of early juvenile winter flounder predation risk on a North West Atlantic estuarine nursery ground. Mar. 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Bingham Oceanogr. Collect. 18, 5–78. Rijnsdorp, A.D., Van Stralen, M., Van der Veer, H.W., 1985. Selective tidal transport of North Sea plaice Pleuronectes platessa in coastal nursery areas. Trans. Am. Fish. Soc. 114, 461–470. Rijnsdorp, A.D., Peck, M.A., Engelhard, G.H., Mollmann, C., Pinnegar, J.K., 2009. Resolving the effect of climate change on fish populations. ICES J. Mar. Sci. 66, 1–14. Sagarese, S.R., Frisk, M.G., 2011. Movement patterns and residence of adult winter flounder within a Long Island estuary. Marine and Coastal Fisheries: Dynamics, Management, and Ecosystem Science. 3 pp. 295–306. Sogard, S.M., Able, K.W., Hagan, S.M., 2001. Long-term assessment of settlement and growth of juvenile winter flounder (Pseudopleuronectes americanus) in New Jersey estuaries. J. Sea Res. 45, 189–204. Stebbing, A.R.D., Turk, S.M.T., Wheeler, A., Clarke, K.R., 2002. Immigration of southern fish species to south-west England linked to warming of the North Atlantic (1960–2001). J. Mar. Biol. Assoc. UK 82, 177–180. Sunksen, K., Stenberg, C., Gronkjaer, P., 2010. Temperature effects on growth of juvenile Greenland halibut (Reinhardtius hippoglossoides Walbaum) in West Greenland waters. J. Sea Res. 64, 125–132. Taylor, D., Collie, J., 2003. Effect of temperature on the functional response and foraging behavior of the sand shrimp Crangon septemspinosa preying on juvenile winter flounder Pseudopleuronectes americanus. Mar. Ecol. Prog. Ser. 363, 217–234.
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Wilber, D.H., Davis, D., Clarke, D.G., Alcoba, C.J., Gallo, J., 2013b. Winter flounder (Pseudopleuronectes americanus) estuarine habitat use and the association between spring temperature and subsequent year class strength. Estuar. Coast. Shelf Sci. 133, 251–259. Wilk, S.J., Morse, W.W., Stehlik, L.L., 1990. Annual cycles of gonad-somatic indices as indicators of spawning activity for selected species of finfish collected from the New York Bight. Fish. Bull. 88, 775–786. Witherell, D.B., Burnett, J., 1993. Growth and maturation of winter flounder, Pleuronectes americanus, in Massachusetts. Fish. Bull. 91, 816–820.
Please cite this article as: Wilber, D.H., et al., Windowpane flounder (Scophthalmus aquosus) and winter flounder (Pseudopleuronectes americanus) responses to cold temperature extremes in a Northwest Atlantic estuary, J. Sea Res. (2015), http://dx.doi.org/10.1016/j.seares.2015.04.005
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Windowpane flounder (Scophthalmus aquosus) and winter flounder (Pseudopleuronectes americanus) responses to cold temperature extremes in a Northwest Atlantic estuary Dara H. Wilber a,⁎, Douglas G. Clarke b, Catherine M. Alcoba c, Jenine Gallo c a b c
HX5, 664 Old Plantation Rd., Charleston, SC 29412, United States HDR Engineering Inc., One International Blvd., 10th Floor/Suite 1000, Mahwah, NJ 07495, United States U.S. Army Corps of Engineers New York District, 26 Federal Plaza, Room 2146, New York, NY 10278-0090, United States
a r t i c l e
i n f o
Article history: Received 1 January 2015 Received in revised form 24 March 2015 Accepted 7 April 2015 Available online xxxx Keywords: New York/New Jersey Harbor Flatfish Overwintering Thermal stress
a b s t r a c t The effect of climate variability on flatfish includes not only the effects of warming on sensitive life history stages, but also impacts from more frequent or unseasonal extreme cold temperatures. Cold weather events can affect the overwintering capabilities of flatfish near their low temperature range limits. We examined the responses of two flatfish species, the thin-bodied windowpane (Scophthalmus aquosus) and cold-tolerant winter flounder (Pseudopleuronectes americanus), to variable winter temperatures in a Northwest Atlantic estuary using abundance and size data collected during a monitoring study, the Aquatic Biological Survey, conducted from 2002 to 2010. Winter and spring abundances of small (50 to 120 mm total length) juvenile windowpane were positively correlated with adult densities (spawning stock) and fall temperatures (thermal conditions experienced during post-settlement development for the fall-spawned cohort) of the previous year. Windowpane abundances in the estuary were significantly reduced and the smallest size class was nearly absent after several consecutive years with cold (minimum temperatures b1 °C) winters. Interannual variation in winter flounder abundances was unrelated to the severity of winter temperatures. A Paulik diagram illustrates strong positive correlations between annual abundances of sequential winter flounder life history stages (egg, larval, Age-1 juvenile, and adult male) within the estuary, reflecting residency within the estuary through their first year of life. Temperature variables representing conditions during winter flounder larval and post-settlement development were not significant factors in multiple regression models exploring factors that affect juvenile abundances. Likewise, densities of predators known to consume winter flounder eggs and/or post-settlement juveniles were not significantly related to interannual variation in winter flounder juvenile abundances. Colder estuarine temperatures through the first year of life were associated with smaller Age-1 winter flounder body size. For example, Age-1 winter flounder developing under conditions that differed by 1.9 °C in mean daily water temperature, averaged 98.7 mm total length (TL) and 123.1 mm TL, for the relatively cold vs. moderate years, respectively. More frequent cold temperature extremes associated with climate variability may negatively impact the overwintering capabilities of some flatfish near their cold temperature range limits, whereas cold-tolerant species may experience reduced growth, which imparts the ecological challenges associated with smaller body size. © 2015 Elsevier B.V. All rights reserved.
1. Introduction Fish survival during early life history stages is a strong determinant of recruitment success (e.g., Houde, 1989; Gibson, 1994; Sogard et al., 2001; Manderson, 2008). Consequently, a better understanding of what factors influence egg, larval, and young-of-year mortality has been a research priority (Van der Veer et al., 2000). Factors mediating flatfish survival at these vulnerable stages include predation (Manderson et al., 2000; Taylor and Collie, 2003; Taylor and Danila, 2005), prey availability (Leggett and DeBlois, 1994), ⁎ Corresponding author. Tel.: +1 843 795 6599. E-mail address: [email protected] (D.H. Wilber).
temperature (Van der Veer, 1986; Henderson, 1998; Neuman and Able, 2009), habitat degradation (Gibson, 1994; Able, 1999; Able et al., 1999) and unsuitable hydrodynamic conditions (Rijnsdorp et al., 1985; Castillo et al., 1994). Warmer water temperatures resulting from climate change may intensify mechanisms that, either directly or indirectly, induce mortality. For instance, warmer temperatures may increase thermal stress for some species at the southern extent of their ranges (Desaunay et al., 2006; Rijnsdorp et al., 2009). Fish distributions may shift toward higher latitudes, reflecting either a range expansion into areas that historically were too cold (Stebbing et al., 2002) or an emigration from areas no longer cold enough (Able et al., 2014). Warmer temperatures also may increase larval mortality on a regional scale, which synchronizes interannual variation in recruitment for
http://dx.doi.org/10.1016/j.seares.2015.04.005 1385-1101/© 2015 Elsevier B.V. All rights reserved.
Please cite this article as: Wilber, D.H., et al., Windowpane flounder (Scophthalmus aquosus) and winter flounder (Pseudopleuronectes americanus) responses to cold temperature extremes in a Northwest Atlantic estuary, J. Sea Res. (2015), http://dx.doi.org/10.1016/j.seares.2015.04.005
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subpopulations and destabilizes resilience to disturbances for regional stocks (Manderson, 2008; Bell et al., 2014). Aside from warming temperatures, climate change may increase temperature variability, causing the magnitudes and frequencies of both low and high temperature extremes to increase (IPCC, 2001: Climate Change, 2001). Thus, overwintering capabilities of flatfish may be affected for species living near their cold temperature thresholds. In this study, we examined how cold temperature extremes in a Northwest Atlantic estuary were associated with variation in juvenile abundance and size for two flatfish species that differ in their cold temperature tolerances. This study was conducted in New York/New Jersey Harbor (Harbor), a heavily urbanized and industrialized estuary in the Northwest Atlantic Ocean. Winter flounder (Pseudopleuronectes americanus) supports important commercial and recreational fisheries in the region that have declined substantially for inshore populations (ASMFC, Atlantic States Marine Fisheries Commission, 2006) in part, because of overfishing in the 1980s and poor recruitment in the late 1990s and 2000s (Able et al., 2014). Winter flounder are demersal throughout their life cycle and therefore are particularly susceptible to impacts to benthic habitat, such as dredging which is needed to maintain and deepen navigation channels for port operations in the Harbor. To minimize potential dredging impacts on winter flounder eggs and larvae, the New York District United States Army Corps of Engineers conducted a multi-year, spatially-robust, sampling program, the Aquatic Biological Survey (ABS), to document the timing and location of winter flounder spawning activity in the Harbor (Wilber et al., 2013a,b). Data collected during this sampling program are a valuable resource for examining potential mechanisms by which extreme temperatures may affect flatfish growth and survival. 1.1. Study organisms Windowpane flounder (Scophthalmus aquosus, hereafter, windowpane) and winter flounder are the most abundant flatfish inhabiting the Harbor. Windowpane and winter flounder distributions overlap throughout the Northwest Atlantic, with windowpane more abundant to the south (near Chesapeake Bay) and winter flounder more abundant at higher latitudes (north of Cape Cod; Collette and Klein-MacPhee, 2002). Temperature may determine the range and local abundances of windowpane at its northern limit (Chang et al., 1999) and winter flounder at its southern limit (Able et al., 2014; Bell et al., 2014). These species differ in their physiological adaptations to thermal stress as well as seasonal patterns of reproduction; therefore individuals of each species enter their first winter at different ages and sizes and have different susceptibilities to cold temperature stress (Table 1). Windowpane spawn in the late spring and again in the fall (Wilk et al., 1990; Morse and Able, 1995; Neuman and Able, 2009), thus the
two windowpane cohorts (especially fall-spawned individuals) have limited time to grow before overwintering. Windowpane eggs are buoyant and spawned on or near the bottom (Chang et al., 1999). In contrast, winter flounder are cold tolerant, seasonally producing an antifreeze protein that protects them from cold shock (Fletcher, 1981; Fletcher et al., 1985). Winter flounder eggs are demersal and spawning occurs in the Harbor from January to March (Wilber et al., 2013a) therefore, Age-0 juveniles feed and grow throughout the summer and fall before entering their first winter in their natal estuary. Larger body size for windowpane is an effective defense to cold temperature stress (Neuman and Able, 2009) and essential to survival of overwintering windowpane near their northern range limit because they do not produce antifreeze proteins. Smaller individuals belong to the fall-spawned cohort, and because mortality is size-selective, the overwintering capability of young-of-the-year windowpane differs between the spring- and fall-spawned cohorts (Neuman and Able, 2009). The relative contribution of the two cohorts to overall windowpane population size is unknown, as is the frequency of environmental conditions that induce overwinter mortality. Overwintering impacts on windowpane and winter flounder are compared in this study because their different life history characteristics and susceptibilities to cold stress are especially relevant in an estuary that is near the northern vs. southern extents of their respective distributions, and because results may signal the likelihood of potential range shifts in an era of increasing climate variability. 2. Methods In this study, three Harbor subareas were identified: Arthur Kill/ Newark Bay (AKNB), Lower Bay (LB), and Upper Bay (UB; Fig. 1). During ABS sampling, demersal eggs and larvae were collected biweekly from mid-January to mid-June from 2002 to 2011. Ichthyoplankton samples were collected using an epibenthic sled (0.5-mm mesh plankton net with an opening of 0.25 m2 and the lowest point of the net ringer
Table 1 Life history characteristics for windowpane (Scophthalmus aquosus) and winter flounder (Pseudopleuronectes americanus) in Northwest Atlantic estuaries. Life history phase
Windowpane
Winter flounder
Egg type Spawning season Larval development Juvenile residency period Adult residency
Buoyant Spring and falla,b Summera Year-rounda Year-round with seasonal movements to nearshore habitatsa
Demersal Winter and early springc Springc Year-round for 1–2 yearsd Emigration from estuary in spring when temperatures exceed 12–15 °Ce,f
a b c d e f
Chang et al. (1999). Morse and Able (1995). Wilber et al. (2013a). Sagarese and Frisk (2011). Danila and Kennish (1981). Decelles and Cadrin (2010).
Fig. 1. Location of New York/New Jersey Harbor (black box) on the northeastern coast of the United States. Aquatic Biological Survey sampling was conducted from 2002 through 2010 in all Harbor subareas: Arthur Kill, Newark Bay, Upper Bay, and Lower Bay.
Please cite this article as: Wilber, D.H., et al., Windowpane flounder (Scophthalmus aquosus) and winter flounder (Pseudopleuronectes americanus) responses to cold temperature extremes in a Northwest Atlantic estuary, J. Sea Res. (2015), http://dx.doi.org/10.1016/j.seares.2015.04.005
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2.1. Data analysis Winter flounder egg and larval abundances are well documented, as the ABS sampling was designed to characterize winter flounder spawning activity from January to June. However, since sampling only partially overlapped with windowpane spring spawning in the Harbor and did not capture fall spawning and peak larval occurrences, only spring windowpane egg abundance and distribution patterns are described here. In addition, different analytical approaches are used to examine influences on juvenile abundances for the two species. Factors that may influence recruitment to the juvenile stage, such as temperatures experienced during larval and post-settlement development are examined for both species. However, the potential relative influence of predators on early life history (ELH) stages is only examined for winter flounder because ABS sampling was not conducted during the summer and fall when predators on windowpane ELH stages could be assessed. Three size-cohorts of windowpane correspond to small juveniles (b120 mm TL), large juveniles (121 to 220 mm TL) and adults (N220 mm TL; Morse and Able, 1995). Catch-per-unit-effort (CPUE) was calculated as the number of fish per 10-min trawl and was standardized by trawl duration if tows were shorter in duration. To examine whether windowpane moved to deeper Harbor areas during cold winters, i.e., into channels, a three-factor Analysis of Variance (ANOVA) was conducted using mean windowpane CPUE as the dependent variable and season (winter, January–March; spring, April–June), station type (channel vs. non-channel), and severity of winter (cold vs. moderate) as independent variables. Seasons were defined as winter (January to March) and spring (April to June). Severity of winter was classified as ‘cold’ and ‘moderate’ for years with minimum annual temperatures below and above 1 °C, respectively. CPUE data were log(x + 1) transformed to meet the normality and homogeneity of variance assumptions of the test. Mean annual CPUEs were not autocorrelated using one-, two-, and three-year time lags (Pearson correlations) and were used as the source of replication. Potential factors influencing small juvenile windowpane annual abundances (dependent variable) were examined using multiple regression analyses. Mean adult CPUE the previous year (an estimate of spawning stock size), cumulative degree days (sum of daily mean temperatures) from October 1 through December 31 of the previous year (temperatures experienced by fall-spawned individuals), and the minimum winter water temperature (estimate of overwinter thermal stress) were included as independent factors. A two-factor ANOVA was used to test for potential differences in windowpane CPUE by size (small juveniles, large juveniles, adults) and time periods grouped by years that followed cold (2004, 2005,
and 2006) and moderate (2002, 2003, 2007–2010) winters. This test was conducted to investigate potential abundance changes consistent with overwinter mortality the previous year for fish too small to be ampled by the bottom trawl gear. Mean CPUEs for each size class by sampling event were used as the dependent variable following a log(x + 1) transformation. Winter flounder juveniles caught in the bottom trawl survey are defined as b 150 mm TL (Witherell and Burnett, 1993) and were assumed to be predominantly Age-1 individuals because the gear does not reliably collect individuals b 50 mm TL, a size corresponding to Age-0 winter flounder in the winter and spring. Age-1 winter flounder CPUE is positively correlated with the annual egg CPUE (# of eggs/1000 m3) of the previous year (Wilber et al., 2013a). The potential additional influences of temperature and predator impacts on Age-1 year class strength were explored using multiple regression analysis. Mean April and maximum annual water temperatures were included as independent variables to represent thermal conditions during larval and early post-settlement periods, respectively. CPUEs of summer flounder (Paralichthys dentatus), striped searobin (Prionotus evolans) and striped bass (Morone saxatilis), three fish that prey upon winter flounder eggs and Age-0 juveniles (Manderson et al., 2000, 2006), were also included as independent variables in multiple regression analyses conducted to examine influences on Age-1 juvenile abundances the following year. Mean CPUEs for predators in two time periods, February and March; and May and June; were used to estimate predator pressure on winter flounder eggs and newly-settled juveniles, respectively. High winter flounder egg abundances in 2003 and 2007 (Wilber et al., 2013a) corresponded to large Age-1 year classes in 2004 and 2008 (Wilber et al., 2013b), which developed over cold and moderate temperature profiles, respectively. To investigate the effects of different thermal conditions on growth, the mean sizes of Age-1 juveniles collected during each sampling event in 2004 and 2008 were compared using a one-factor ANOVA.
3. Results New York/New Jersey Harbor is composed of three subareas that are distinguished by highest salinities (25 to 28 psu) in Lower Bay (LB), intermediate salinities (21 to 24 psu) in Upper Bay (UB), and lowest salinities (17 to 21 psu) in Arthur Kill/Newark Bay (AKNB). Dissolved oxygen concentrations ranged from 5 to 11 mg/l and did not approach hypoxic conditions in any subarea. Winter water temperatures varied considerably in the Harbor during the study period, with minimum temperatures less than 1 °C in three years (2003 to 2005) and warmer minimum temperatures averaging 3.3 °C in other years (Fig. 2). Water temperatures within sampling events, however, were fairly uniform among Harbor subareas and usually differed by less than 0.5 °C between 10 8
Temperature (oC)
mounted 178 mm above the substrate). During each sampling period, between 26 and 29 stations at fixed locations in both channel and non-channel areas in each Harbor subarea were sampled. Sixteen core stations were sampled in all ten years and data from the core stations were used for inter-annual comparisons to avoid confounding potential spatial and temporal effects (Wilber et al., 2013a). Bottom trawl surveys were conducted biweekly from January to June over a nine-year time period (2002 to 2010) at 24 to 29 stations. Sixteen core stations that corresponded to the ichthyoplankton core stations were sampled each year and were used in interannual comparisons (Wilber et al., 2013b). Bottom trawls (10 min. tow duration) were conducted using a 9.1 m otter trawl with 2.5 cm square mesh wings and body and a 1.9 cm square mesh cod end with a 0.6 cm square mesh liner. Salinity, temperature, and dissolved oxygen were measured at 0.3 m above the bottom at each station using a water quality meter (YSI Model 85). To better understand the continuous temperature conditions experienced by fish throughout the study period, water temperature data were obtained from records for the NOAA gauge located within the study area (station ID 8518750) at the southern end of Manhattan Island.
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Fig. 2. Winter water temperatures recorded at NOAA gauge station ID 8518750 located at the southern tip of Manhattan Island from 2002 to 2010. Years were classified by severity of winter temperatures as cold (2003, 2004, 2005; solid lines) and moderate (2002, 2006 to 2010; dashed lines).
Please cite this article as: Wilber, D.H., et al., Windowpane flounder (Scophthalmus aquosus) and winter flounder (Pseudopleuronectes americanus) responses to cold temperature extremes in a Northwest Atlantic estuary, J. Sea Res. (2015), http://dx.doi.org/10.1016/j.seares.2015.04.005
D.H. Wilber et al. / Journal of Sea Research xxx (2015) xxx–xxx
channel and non-channel stations within a subarea for all sampling periods (Wilber et al., 2013a). Windowpane eggs were among the more common eggs collected in the Harbor, accounting for 5.3% of all eggs collected over the ten years of ABS ichthyoplankton sampling. Windowpane eggs were first collected in April, increased in abundance in May and June (Fig. 3A), and were concentrated in both channel and non-channel stations in LB and at UB channel stations, with few collected in the AKNB subarea (Fig. 3A). Windowpane egg CPUE for the first three months of the spring spawning season varied among years (Fig. 3B). Windowpane juvenile/ adult CPUE did not differ by season or severity of winter temperature (Fig. 4) and was significantly higher at channel stations (F = 6.67, p b 0.05) with no interactions with the other variables. Overall, nearly 80% of juvenile and adult windowpane were collected at channel stations. Small juvenile windowpane CPUE was positively correlated with adult CPUE the previous year and cumulative degree days in the fall (r2 = 0.86; Table 2). Minimum annual overwintering temperatures were not a significant variable when added to the multiple regression model. Three modal windowpane size classes were apparent in years that followed moderate winters (Fig. 5A). Windowpane abundances were significantly lower in the years following cold winters (F = 5.0, p b 0.05) and this reduction in CPUE did not differ significantly among size classes (F = 0.4, p N 0.6; Fig. 5B). Significant positive correlations among winter flounder annual life history stages depicted through a Paulik diagram (sensu Nash, 1998; Payne et al., 2009) include; egg and adult male densities during the spawning season (r = 0.95, p b 0.001), egg and larval CPUEs (r = 0.68, p b 0.05), larval CPUE and Age-1 juvenile CPUE the next year
Windowpane Egg CPUE
A 1200 1000 800 600
AKNB CH AKNB NC LB CH LB NC UB CH UB NC
400 200
3.0
Mean Juvenile/Adult CPUE
4
Windowpane
2.5
Cold Moderate
2.0
1.5
1.0
0.5
0.0
Jan
Feb
Mar
Apr
May
June
Fig. 4. Mean monthly juvenile and adult catch-per-unit-effort (CPUE, number of fish per 10-min trawl) for windowpane in years with cold (2003, 2004, 2005; black) and moderate (2002, 2006, 2007, 2008, 2009; moderate) winter water temperatures.
(r = 0.71, p b 0.05), and adult male CPUE during the spawning season and Age-1 juvenile CPUE the next year (r = 0.83, p = 0.01; Fig. 6). Egg and adult female densities during the spawning season were unrelated, perhaps because some females were skip-spawning and foraging in the estuary (Wilber et al., 2013b). The best predictor of Age-1 winter flounder densities in the Harbor is the egg CPUE of the previous year (r = 0.89, p = 0.003; Wilber et al., 2013b). Adding annual predator (summer flounder, striped searobin, and striped bass) densities in multiple regression models did not improve the fit of this relationship. The temperature variables examined also were not significant factors in explaining interannual variation in Age-1 winter flounder juvenile abundances. Water temperatures experienced during the first year of life for Age-1 winter flounder cohorts collected in 2004 and 2008 were consistently higher for the 2008 cohort (Fig. 7). Daily temperatures experienced by the 2008-cohort were, on average, 1.9 °C higher than that experienced by the 2004-cohort, with a maximum daily temperature difference of 5.8 °C. Age-1 juveniles in the 2008 cohort were significantly larger (F = 18.7, p = 0.001) than those in the 2004 cohort, averaging 123.1 mm TL compared to 98.7 mm TL (Fig. 8).
0 Jan
Mean Egg CPUE
B
500 450 400 350 300 250 200 150 100 50 0
Feb
Mar
Apr
May
June
Windowpane
4. Discussion Negative impacts on overwintering juveniles caused by more frequent or extreme cold temperatures may affect fish population stability Table 2 Variables examined to explain interannual variation in small juvenile windowpane (r2 = 0.86) and Age-1 winter flounder (r2 = 0.79) CPUE (number of fish per 10-min trawl) as determined by multiple regression analyses. Small juvenile windowpane CPUE
2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 Fig. 3. (A) Mean (+ standard error) windowpane egg catch-per-unit-effort (CPUE; number of eggs/1000 m3) at Harbor subareas Arthur Kill/Newark Bay (AKNB), Lower Bay (LB) and Upper Bay (UB) and channel (CH) or non-channel (NC) stations and (B) interannual variation in windowpane egg CPUE.
Variable
Coefficient
Std. error
t
p-Value
Constant Adult CPUE previous year Fall temperature previous year
−2.319 1.187 0.002
0.622 0.213 0.000
−3.729 5.574 3.878
0.014 0.003 0.012
Coefficient
Std. error
t
p-Value
Age-1 winter flounder CPUE Variable Constant Egg CPUE previous year
0.843 0.001
0.268 0.000
3.145 4.253
0.020 0.005
Please cite this article as: Wilber, D.H., et al., Windowpane flounder (Scophthalmus aquosus) and winter flounder (Pseudopleuronectes americanus) responses to cold temperature extremes in a Northwest Atlantic estuary, J. Sea Res. (2015), http://dx.doi.org/10.1016/j.seares.2015.04.005
D.H. Wilber et al. / Journal of Sea Research xxx (2015) xxx–xxx
5
A
Mean CPUE
0.08
Years Following Moderate Winters
0.06 0.04 0.02 0.00 20 40 60 80 100 120 140 160 180 200 220 240 260 280 300 320 340 360 390
Windowpane Total Length (mm)
Mean CPUE
B
0.08
Years Following Cold Winters
0.06 0.04 0.02 0.00 20 40 60 80 100 120 140 160 180 200 220 240 260 280 300 320 340 360 390
Windowpane Total Length (mm) Fig. 5. Size frequency distributions from bottom trawl surveys of windowpane in the (A) years following moderate winters (2002, 2003, 2007–2010) and (B) years following cold winters (2004, 2005, 2006). CPUE is calculated as number of fish per 10-min trawl.
in areas where cold temperature stress occurs. Cold temperatures affected two flatfish species inhabiting a Northwest Atlantic estuary differently. Windowpane experience size-selective overwinter mortality under laboratory conditions, with 94% mortality for individuals b 24 mm TL compared to 50% mortality for larger fish within a
fall-spawned cohort (Neuman and Able, 2009). Spring-spawned individuals (83 to 140 mm TL) can survive overwintering at temperatures as low as −2.0 °C (Neuman and Able, 2009). In our study, small individuals (i.e., b50 mm TL) were not sampled effectively in the ABS bottom trawl survey, therefore overwinter mortality for these windowpane
Fig. 6. A Paulik diagram for winter flounder CPUEs of eggs and larvae, larvae and Age-1 juveniles the next year, adult males and Age-1 juveniles the next year, and adult males and eggs within the spawning season. Axes values are index values for illustrative purposes only, therefore numbers are not displayed.
Please cite this article as: Wilber, D.H., et al., Windowpane flounder (Scophthalmus aquosus) and winter flounder (Pseudopleuronectes americanus) responses to cold temperature extremes in a Northwest Atlantic estuary, J. Sea Res. (2015), http://dx.doi.org/10.1016/j.seares.2015.04.005
D.H. Wilber et al. / Journal of Sea Research xxx (2015) xxx–xxx
24
Eggs Larvae
Age-0
Age-1
19 14
2004 Age-1 2008 Age-1
9
Jan Feb Mar Apr May Jun
Sep Oct Nov Dec
-1
Apr May Jun Jul Aug
4
Jan Feb Mar
Mean Weekly Temperature oC
6
Fig. 7. New York/New Jersey Harbor water temperatures experienced by the 2004 (solid line) and 2008 (dashed line) Age-1 winter flounder cohorts from the egg stage through June of the Age-1 juvenile stage.
could not be inferred from samples collected during years with extreme cold temperatures (i.e., minimum temperatures b1 °C). However, lower windowpane abundances in years that followed cold winters are consistent with high overwinter mortality the previous year, especially for smaller fish, or emigration from the estuary. Because cold winters were sequential (2003 to 2005), any overwinter mortality was compounded by survivors experiencing cold conditions that may have reduced growth, further increasing the likelihood of size-selective thermal impacts. The near elimination of the smallest size class (modal size of 60–70 mm TL) following cold winters may limit recruitment to the adult stage, which could destabilize the population within the estuary. Lower estuarine windowpane abundances in years that followed cold winters also may be indicative of emigration from the Harbor. In the southern Gulf of Maine, windowpane occur in the shallowest and warmest waters available during the summer and are absent in areas where water temperatures were b1 °C (Hanson and Wilson, 2014), perhaps moving short distances offshore to overwinter (Hanson and Courtenay, 1995). Nearshore sampling was not conducted in our study to assess offshore movement. Deep areas within the Harbor (channels) were preferred by windowpane regardless of seasonal temperatures and did not provide a temperature refuge in this well-mixed estuary. Although larger windowpane are more capable of overwintering at low temperatures (e.g., mortality for windowpane N 100 mm TL occurred only when temperatures dropped rapidly below 0 °C; Neuman and Able, 2009), the lower densities of all size classes over the extended period (2003–2005) with cold winters suggests either mortality reduced estuarine population size, fish emigrated to nearshore habitat, or a combination of these events occurred. In contrast, winter flounder are cold-tolerant, i.e., they are capable of producing an antifreeze protein that reduces the probability of overwinter mortality. However, even with a lower risk of mortality due to freezing, mortality may occur if prey are limited or fish are unable to feed because of low temperatures. These potential impacts are more
relevant to smaller individuals because larger body size provides more energy reserves to combat starvation and a lower metabolic rate per unit body mass (e.g., Hurst et al., 2000). Winter flounder in Narragansett Bay, Rhode Island, did not exhibit size-dependent overwinter mortality in 2008, perhaps because they fed throughout the winter on amphipods and polychaetes and maintained lipid stores, thus reducing their risk of starvation (Bell, 2012). Winter temperatures in 2008, however, were relatively mild, remaining above 4 °C (Bell, 2012), therefore additional studies are needed to address feeding behavior in the field under colder conditions. There was no evidence of overwinter mortality for winter flounder in our Harbor study. Age-1 juvenile abundances were strongly correlated with egg abundances from the previous year. The addition of predator densities and temperature variables corresponding to periods of larval and Age-0 juvenile development did not explain any residual variation in this relationship. The importance of relative predator vs. winter flounder ELH stage densities under natural conditions has not been described; therefore the form of this potential relationship is unknown. Temperature, however, is associated with year-class strength for inshore winter flounder populations. In two estuaries, Age-1 winter flounder abundances were positively correlated with the April temperatures experienced by foraging adults two years previous, possibly because warmer temperatures promote benthic productivity and increase prey availability for adults that need to replenish exhausted energy reserves in order to spawn the following year (Wilber et al., 2013b). Overall, positive correlations in CPUE among sequential winter flounder life history stages (Fig. 5) are consistent with a population that is highly localized within the Harbor for the first year of life, as has been indicated for other estuarine populations of winter flounder through genetic studies (Crivello et al., 2004; Buckley et al., 2008) and resident contingents of populations revealed through a tagging study (Sagarese and Frisk, 2011). Colder temperatures throughout the first year of life were associated with smaller Age-1 juvenile winter flounder size, an effect also observed in Greenland halibut (Reinhardtius hippoglossoides; Sunksen et al., 2010). Age-1 winter flounder size exceeds the lower size threshold of fish effectively collected by the bottom trawl; therefore it is unlikely that a sampling bias contributed to the different size distributions of juveniles that developed over relatively cold vs. moderate conditions. Mechanisms underlying the smaller size at lower temperatures are unknown and may include a combination of lower prey availability, slower metabolic processes, and reduced foraging activity. It is unlikely that intraspecific (density-dependent) competition for food contributed to the body size disparity, as indicated with juvenile European plaice (Ciotti et al., 2013) because of the similar densities of the two cohorts for the years compared. Disadvantages to smaller body size include an increased predation risk, reduced feeding success if a correspondingly smaller gape width reduces prey availability, and a potential delay in the onset of sexual maturity. Warmer spring and summer temperatures can negatively affect winter flounder larval development (Buckley et al., 1990), however,
Number of Fish
120 100
2004
80
2008
60 40 20 0 40 60 80 100 120 140 160 180 200 220 240 260 280 300 320 340 360 380 410
Winter Flounder Total Length (mm) Fig. 8. Size frequency distributions of the 2004 (black bars) and 2008 (gray bars) Age-1 winter flounder cohorts.
Please cite this article as: Wilber, D.H., et al., Windowpane flounder (Scophthalmus aquosus) and winter flounder (Pseudopleuronectes americanus) responses to cold temperature extremes in a Northwest Atlantic estuary, J. Sea Res. (2015), http://dx.doi.org/10.1016/j.seares.2015.04.005
D.H. Wilber et al. / Journal of Sea Research xxx (2015) xxx–xxx
our study found no evidence that temperature variation in the spring during this nine-year study period affected larval developmental success and recruitment to the juvenile stage. Maximum spring water temperatures did not exceed 18 °C. Likewise, maximum summer temperatures were not correlated with recruitment to the Age-1 juvenile stage for winter flounder. Summer temperatures during the study period (maximum = 26.9 °C) were lower than temperature extremes associated with winter flounder inactivity and mortality (e.g., 30 °C; Pearcy, 1962), therefore high temperatures associated with mortality for winter flounder early life history stages may not have occurred during the course of this study. Although this study was conducted over a relatively short time series (2002–2010), the inclusion of years with highly variable winter temperatures allows a comparison of how flatfish respond to cold temperature extremes. Differences in windowpane abundances in years following cold vs. moderate winters were consistent with the size-specific mortality that was demonstrated in laboratory experiments for this species (Neuman and Able, 2009) and in other flatfish like smallmouth flounder (Hales and Able, 2001). Although winter flounder are better adapted to survive extreme cold temperatures, the smaller size of Age-1 individuals following cold winters indicates sublethal impacts occurred that could negatively affect survival, foraging success, and reproduction. Climate variability that increases the frequency or magnitude of cold winter temperatures may increase overwinter mortality in fish near their cold-temperature range limits, resulting in range retraction from these areas. Species that are coldtolerant, may survive extreme cold conditions and maintain their geographic distributions, but detrimental impacts to growth may reduce foraging success, survival, and reproduction. Acknowledgments The U.S. Army Corps of Engineers New York District (USACE NYD) and the Port Authority of New York and New Jersey funded the Aquatic Biological Survey (ABS) in support of the 50-foot Harbor Deepening Project. The expertise of many HDR Engineering Inc. staff, including David Davis and Sarah Zappala greatly contributed to the quality of the ABS program. We appreciate the assistance of Liz Duermit with figure creation. References Able, K.W., 1999. Measures of juvenile fish habitat quality: examples from a National Estuarine Research Reserve. Am. Fish. Soc. Symp. 22, 134–147. Able, K.W., Manderson, J.P., Studholme, A.L., 1999. Habitat quality for shallow water fishes in an urban estuary: the effects of man-made structures on growth. Mar. Ecol. Prog. Ser. 187, 227–235. Able, K.W., Grothues, T.M., Morson, J.M., Coleman, K.W., 2014. Temporal variation in winter flounder recruitment at the southern margin of their range: is the decline due to increasing temperatures? ICES J. Mar. Sci. http://dx.doi.org/10.1093/icesjms/ fsu094. ASMFC (Atlantic Staes Marine Fisheries Commission), 2006. Species profile: winter flounder current plan seeks to rebuild southern New England/Mid-Atlantic stock and sustain Gulf of Maine stock. Atl. States Mar. Fish. Ser. Fish. Focus 15, 4–6. Bell, R.J., 2012. Winter feeding as an overwintering survival strategy in young-of-the-year winter flounder. Trans. Am. Fish. Soc. 141, 855–871. Bell, R.J., Hare, J.A., Manderson, J.P., Richardson, D.E., 2014. Externally driven changes in the abundance of summer and winter flounder. ICES J. Mar. Sci. http://dx.doi.org/ 10.1093/icesjms/fsu069. Buckley, L.J., Smigielski, A.S., Halavik, T.A., Laurence, G.C., 1990. Effects of water temperature on size and biochemical composition of winter flounder Pseudopleuronectes americanus at hatching and feeding initiation. Fish. Bull. 88, 419–428. Buckley, L.J., Collie, J., Kaplan, L.A.E., Crivello, J., 2008. Winter flounder larval genetic population structure in Narragansett Bay, RI: recruitment to juvenile young-of-the-year. Est. Coasts 31 pp. 745–754. Castillo, G.C., Li, H.W., Golden, J.T., 1994. Environmentally induced recruitment in petrale sole, Eopsetta jordani. Fish. Bull. U.S. 92, 481–493. Chang, S., Berrien, P.L., Johnson, D.L., Morse, W.W., 1999. Essential fish habitat source document: windowpane, Scophthalmus aquosus, life history and habitat characteristics. NMFS-NE-137NOAA Tech. Mem. (32 pp.). Ciotti, B.J., Targett, T.E., Burrows, M.T., 2013. Spatial variation in growth rate of early juvenile European plaice Pleuronectes platessa. Mar. Ecol. Prog. Ser. 475, 213–232.
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Please cite this article as: Wilber, D.H., et al., Windowpane flounder (Scophthalmus aquosus) and winter flounder (Pseudopleuronectes americanus) responses to cold temperature extremes in a Northwest Atlantic estuary, J. Sea Res. (2015), http://dx.doi.org/10.1016/j.seares.2015.04.005