TY - JOUR
AU1 - Chigbu,, Paulinus
AU2 - Malinis,, Lauren
AU3 - Malagon,, Hector
AU4 - Doctor,, Steve
AB - Abstract Sand shrimp, Crangon septemspinosaSay, 1818, is one of the most abundant decapod crustaceans in estuaries and coastal waters of the northwestern Atlantic Ocean, though little is known about its population dynamics in polyhaline lagoons of the mid-Atlantic region. Seasonal and spatial patterns of abundance and distribution of C. septemspinosa were evaluated in relation to temperature, salinity, and dissolved oxygen in Maryland coastal bays (MCBs) using monthly data (April to October 1994 to 2012). We tested the hypothesis that temperature influences the occurrence and distribution of sand shrimp in the lagoons. A consistent pattern of high relative abundance of shrimp in spring and its scarcity in summer and early fall was observed. Shrimp abundance was highest in the northern bays and at sites closest to the Ocean City Inlet during April, but lowest at sites in the upper parts of Chincoteague Bay and MCBs tributaries. As mean temperature increased from April (12.2–17.1 oC) to June (21.8–26.7 oC), the relative abundance of the shrimp decreased substantially at most sites except at two sites where mean water temperature was comparatively low (21.8–23.3 oC). By July, when mean temperature was at its maximum (23.1–28.9 oC) in the bays, shrimp were rarely caught in trawls even in early fall in spite of the decline in temperature. It is likely that shrimp moved into nearshore waters with cooler temperature or suffered high mortality due to high temperature during this period. Generalized linear models suggest that temperature, and temperature and dissolved oxygen combined, were the most important abiotic factors examined that influenced the spatial distribution of C. septemspinosa in May and June, respectively. Considering their trophic importance, the spatio-temporal variations in the occurrence and abundance of the shrimp have implications for food web dynamics in the MCBs. Introduction The caridean genus CrangonFabricius, 1798 consists of 20 species and subspecies (De Grave & Fransen, 2011; Campos et al., 2012) that perform important ecosystem functions as prey and/or predators of fishes in many aquatic systems in the Northern Hemisphere (Siegfried, 1980; Henderson & Holmes, 1987; Yamashita et al., 1996), although little is known about the population dynamics of many of the species (Campos et al., 2012). Sand shrimp (Crangon septemspinosaSay, 1818), distributed from the Gulf of St. Lawrence to eastern Florida, is one of the most abundant decapod crustaceans in estuaries and coastal waters of the northwestern Atlantic Ocean (Haefner, 1979; Heck et al., 1989; Viscido et al., 1997; Able et al., 2002; Lazzari, 2002). They are major components of the diets of many fishes (Friedland et al., 1988; Creaser & Perkins, 1994; Manderson et al., 2000), and are also consumed by seabirds (Blackwell et al., 1995). As omnivores, they consume detritus and marine invertebrates such as mysids, amphipods, molluscs, and polychaetes (Price, 1962; Wilcox & Jeffries, 1974; Squires, 1996; Albright, 2006). They have also been reported to feed on eggs and juveniles of flatfishes (Witting & Able, 1995; Taylor, 2003, 2004, 2005; Taylor & Collie, 2003a, b). Much of what is known about the life history of C. septemspinosa is based on populations inhabiting some river-dominated estuaries along the northwestern Atlantic coast and associated nearshore continental shelf (e.g., Williams, 1965; Haefner, 1972, 1976, 1979; Wilcox & Jeffries, 1973; Modlin, 1980; Corey, 1981, 1987; Grabe, 2003; Locke et al., 2005; Albright, 2006). The seasonal and spatial distribution of sand shrimp larvae in York River Estuary and adjacent lower Chesapeake Bay (Sandifer, 1973) and coastal waters adjacent to Chesapeake Bay, Maryland (Wehrtmann, 1994) were investigated and the abundance was found to be highest in spring. Price (1962) described feeding, growth, and reproduction of the shrimp in Delaware Bay. He captured adults throughout the year in shallow waters along the shores of the bay. No marked onshore-offshore migration of the shrimp was observed, but the oldest-year class disappeared from the area during the summer. It was not determined whether the disappearance was due to mortality or migration into deeper water. Sand shrimp abundance in the channels of the York River-Chesapeake Bay Estuary varied seasonally; it was highest in winter, and absent in the summer months of August and September (Haefner, 1976). Locke et al. (2005) studied sand shrimp in Kouchibouguac River Estuary, New Brunswick, Canada and noted that a part of the adult population remained in shallow waters of the estuary during the summer at temperatures as high as 28 oC. These previous studies suggest that some aspects of the life history and distribution pattern of sand shrimp vary among the populations in its geographical range, which may be related to differences in the seasonal temperatures in the areas (Corey, 1981). Additional studies are therefore, needed to determine the influence of temperature on the population dynamics of sand shrimp, especially in shallow (mean depth < 2 m), polyhaline lagoons in the mid-Atlantic region such as the Maryland coastal bays (MCBs) where information is lacking on its life history. These lagoons are thermally unstratified, lacking cool, deep water layers that could serve as thermal refugia. We therefore expected that the relative abundance of sand shrimp would be highest during the seasons (as well as in the areas) with temperature and salinity levels where their probability of dying from physiological stress would be minimal. Results from laboratory studies by Haefner (1969) suggest that adult sand shrimp would likely experience 100% survival in a normoxic natural environment in which temperature ranges from 6 oC to 18 oC and salinity from 19 to 36 psu for males, and from 5 oC to 19 oC and 18 to 36 psu for non-ovigerous females, respectively. The objectives of this study were to determine the seasonal variation in the relative abundance of sand shrimp in the MCBs, and assess their spatial distribution in relation to water temperature, salinity, and dissolved oxygen. In particular, we tested the hypothesis that temperature influences the seasonal occurrence and spatial distribution of sand shrimp in the lagoons. MATERIALS AND METHODS Sampling was conducted monthly (April to October) by the Maryland Department of Natural Resources at 20 sites from 1994 to 2012 in the Maryland coastal bays (MCBs) (Fig. 1). We used a 4.9 m (16 ft) semi-balloon trawl with an outer net of 3.18 cm stretch mesh, cod end of 2.86 cm stretch mesh, and inner liner of 1.27 cm stretch mesh (Bolinger et al., 2007). Sampling sites ranged in depth from 0.75 to 2 m. Trawling was for 6 min at a speed of ~5.2 km hr–1. Considering the large mesh size (~13 mm) of the inner liner of the trawl, sand shrimp < 15 mm, if available, would likely have been inadequately captured during the study. Physico-chemical characteristics, particularly temperature, salinity, and dissolved oxygen (DO) were measured at each site using a Yellow Spring Instrument (YSI) Water Quality meter (Yellow Springs, OH, USA). The numbers of sand shrimp captured in each trawl were estimated (1994–2005) or individually counted (2006–2012). Mean number of sand shrimp caught each month was calculated by averaging catch across the 20 sites. Because sand shrimp were rarely caught from July to October, the mean number of shrimp captured at each site during each month (April, May, June) was calculated by averaging catch per tow across years from 1994 to 2012. Temperature, salinity, and dissolved oxygen were also averaged across years at each site and month. Relationships between sand shrimp catch-per-unit-effort (CPUE) and temperature, salinity, and DO were assessed using Spearman’s rank correlation. To evaluate the influence of temperature, salinity, and dissolved oxygen on the CPUE of sand shrimp at various sites, generalized linear models (GLMs) with negative binomial distribution were conducted with data averaged across years for each month. The model with the lowest Akaike information criterion (AIC) value in each month was selected as the best for predicting sand shrimp CPUE at the various sites. The statistical analyses were run with SPSS Statistics 24. Figure 1. Open in new tabDownload slide Sampling stations in the Maryland coastal bays. Figure 1. Open in new tabDownload slide Sampling stations in the Maryland coastal bays. RESULTS Variation in temperature, salinity, and dissolved oxygen The average water temperature in the MCBs during each month is presented in Fig. 2A. The highest mean temperature (27.5 oC) was recorded in July; lowest mean temperature (15.7 oC) was in April. Average temperatures exceeded 23 oC from June to August. Mean salinity ranged from 24.9 psu in April to 29.0 psu in July (Fig. 2B). Monthly mean DO level was above 5 mg l–l during all the months (Fig. 2C). Figure 2. Open in new tabDownload slide Monthly mean temperature (A), salinity (B), and dissolved oxygen (C) at various sites in the Maryland coastal bays averaged for 1994 to 2012. Error bars are for standard error (SE). Figure 2. Open in new tabDownload slide Monthly mean temperature (A), salinity (B), and dissolved oxygen (C) at various sites in the Maryland coastal bays averaged for 1994 to 2012. Error bars are for standard error (SE). The lowest mean temperatures were recorded at sites 7, 8, and 9 near the Ocean City Inlet, which in April were 13.7 oC, 12.2 oC, and 12.9 oC, respectively (Fig. 3A). The lowest mean temperatures in May were 17.7 oC (site 7), 17.0 oC (site 8), and 17.8 oC (site 9), whereas the lowest mean temperatures in June were 23.3 oC (site 7), 21.8 oC (site 8), and 23.3 oC (site 9). The highest mean temperatures were recorded at site 5 in St. Martin River in April (17.1 oC), May (21.9 oC), and June (26.7 oC) and site 6 in Turville Creek in April (16.3 oC), May (21.3 oC), and June (26.0 oC). Average salinity values were lowest at site 5, 18.58–22.00 psu (St. Martin River) and site 12, 19.39–21.40 psu (Newport Bay) close to the mouth of Trappe Creek (Fig. 3B). The highest salinity values were observed at sites 7 to 10 (27.00–29.44 psu) close to Ocean City Inlet, and site 19 (26.16–28.42 psu) and site 20 (27.62–29.47 psu) close to Chincoteague Inlet. Mean DO levels were higher than 5 mg l–l at all the sites from April to June (Fig. 3C), and did not reach 3 mg l–l even in the summer months. Individual DO measurements at the sites in all months and years were rarely below 3 mg l–l. Figure 3. Open in new tabDownload slide Temperature (A), salinity (B), and dissolved oxygen (C) at various sites in the Maryland coastal bays averaged for 1994 to 2012. Error bars are for standard error (SE). Figure 3. Open in new tabDownload slide Temperature (A), salinity (B), and dissolved oxygen (C) at various sites in the Maryland coastal bays averaged for 1994 to 2012. Error bars are for standard error (SE). Relative abundance of sand shrimp The relative abundance of shrimp varied between years, but was comparatively high from April to June; the relative abundance decreased to near zero by July through September and October (Fig. 4A, B). Figure 4. Open in new tabDownload slide Monthly mean catch-per-unit effort (CPUE) of sand shrimp (Crangon septemspinosa) based on estimates of the numbers of shrimp caught in the Maryland coastal bays from 1994 to 2005 (A) and on individual counts of shrimp caught from 2006 to 2012 (B). This figure is available in color at Journal of Crustacean Biology online. Figure 4. Open in new tabDownload slide Monthly mean catch-per-unit effort (CPUE) of sand shrimp (Crangon septemspinosa) based on estimates of the numbers of shrimp caught in the Maryland coastal bays from 1994 to 2005 (A) and on individual counts of shrimp caught from 2006 to 2012 (B). This figure is available in color at Journal of Crustacean Biology online. Shrimp abundance in April was relatively high in the northern bays (Assawoman and Isle of Wight Bays) at sites closest to the Ocean City Inlet, in the southern part of the Chincoteague Bay close to the Chincoteague Inlet, and in the upper part of Sinepuxent Bay (Fig. 5A, 6A). Abundance was relatively low in St. Martin River (site 5), Newport Bay (sites 11 and 12), and in the northern part of Chincoteague Bay (sites 13–15). By May (Fig. 5B, 6B) and June (Fig. 5C, 6C), the majority of the shrimp were captured at sites 7–9 closest to the Ocean City Inlet. Figure 5. Open in new tabDownload slide Abundance of sand shrimp (Crangon septemspinosa) at various sites in the Maryland coastal bays averaged from 1994 to 2012 in April (A), May (B), and June (C). CPUE, catch-per- unit-effort. Error bars are for standard error (SE). Figure 5. Open in new tabDownload slide Abundance of sand shrimp (Crangon septemspinosa) at various sites in the Maryland coastal bays averaged from 1994 to 2012 in April (A), May (B), and June (C). CPUE, catch-per- unit-effort. Error bars are for standard error (SE). Figure 6. Open in new tabDownload slide Catch-per-unit-effort (CPUE) of sand shrimp (Crangon septemspinosa) at various sites in the Maryland coastal Bays averaged for 1994 to 2012 in April (A), May (B) and June (C). Figure 6. Open in new tabDownload slide Catch-per-unit-effort (CPUE) of sand shrimp (Crangon septemspinosa) at various sites in the Maryland coastal Bays averaged for 1994 to 2012 in April (A), May (B) and June (C). Relationships between the spatial distribution of sand shrimp and temperature, salinity, and dissolved oxygen There were significant negative correlations between CPUE of shrimp and water temperature (Fig. 7A–C) at the sites in May (Spearman’s rank; rs = –0.58, P = 0.008) and June (rs = –0.67, P = 0.001), but not in April (rs = –0.41, P = 0.073). No significant correlations were observed between shrimp CPUE and DO (rs = 0.02–0.18, P > 0.440), and salinity (rs = 0.20–0.27, P > 0.242), except in May (rs = 0.56, P = 0.01), when significant positive relationship was observed with salinity. Results of the GLM analyses (Tables 1, 2) showed that temperature was the best predictor of CPUE of shrimp at the 20 sites sampled in May (AIC = 212.88), whereas temperature and dissolved oxygen were the best predictor variables in June (AIC = 155.45). Table 1. Generalized linear model with negative binomial distribution results used to examine the relationship between CPUE of sand shrimp (Crangon septemspinosa) and environmental factors at Maryland coastal bays sites in May and June averaged across years (1994–2012). The parameters that are the best predictors of sand shrimp distribution based on the lowest Akaike information criterion (AIC) values calculated are highlighted in bold. Sal, salinity (psu); Temp, temperature (oC); DO, dissolved oxygen (mg l–l). Model AIC May June Sand shrimp CPUE ~ Sal + Temp + DO 215.14 157.27 Sand shrimp CPUE ~ Sal + Temp 214.75 163.37 Sand shrimp CPUE ~ Sal 220.05 191.44 Sand shrimp CPUE ~ Temp + DO 213.57 155.45 Sand shrimp CPUE ~ Temp 212.88 161.38 Sand shrimp CPUE ~ DO 224.73 202.27 Sand shrimp CPUE ~ Sal + DO 221.98 193.44 Model AIC May June Sand shrimp CPUE ~ Sal + Temp + DO 215.14 157.27 Sand shrimp CPUE ~ Sal + Temp 214.75 163.37 Sand shrimp CPUE ~ Sal 220.05 191.44 Sand shrimp CPUE ~ Temp + DO 213.57 155.45 Sand shrimp CPUE ~ Temp 212.88 161.38 Sand shrimp CPUE ~ DO 224.73 202.27 Sand shrimp CPUE ~ Sal + DO 221.98 193.44 Open in new tab Table 1. Generalized linear model with negative binomial distribution results used to examine the relationship between CPUE of sand shrimp (Crangon septemspinosa) and environmental factors at Maryland coastal bays sites in May and June averaged across years (1994–2012). The parameters that are the best predictors of sand shrimp distribution based on the lowest Akaike information criterion (AIC) values calculated are highlighted in bold. Sal, salinity (psu); Temp, temperature (oC); DO, dissolved oxygen (mg l–l). Model AIC May June Sand shrimp CPUE ~ Sal + Temp + DO 215.14 157.27 Sand shrimp CPUE ~ Sal + Temp 214.75 163.37 Sand shrimp CPUE ~ Sal 220.05 191.44 Sand shrimp CPUE ~ Temp + DO 213.57 155.45 Sand shrimp CPUE ~ Temp 212.88 161.38 Sand shrimp CPUE ~ DO 224.73 202.27 Sand shrimp CPUE ~ Sal + DO 221.98 193.44 Model AIC May June Sand shrimp CPUE ~ Sal + Temp + DO 215.14 157.27 Sand shrimp CPUE ~ Sal + Temp 214.75 163.37 Sand shrimp CPUE ~ Sal 220.05 191.44 Sand shrimp CPUE ~ Temp + DO 213.57 155.45 Sand shrimp CPUE ~ Temp 212.88 161.38 Sand shrimp CPUE ~ DO 224.73 202.27 Sand shrimp CPUE ~ Sal + DO 221.98 193.44 Open in new tab Table 2. Results from the generalized linear models (with negative binomial distribution) with the lowest Akaike information criterion (AIC) for each month, used to examine the relationship between CPUE of sand shrimp (Crangon septemspinosa) and environmental factors at Maryland coastal bays sites in May and June, averaged across years (1994–2012). Standard errors (SEs) and 95% confidence intervals (CIs) are given for estimates. DO, dissolved oxygen (mg l–l). May Estimate SE Wald Chi-square P 95% CI Intercept 19.98 3.51 32.33 0.000 13.09–26.87 Temperature −0.80 0.18 20.18 0.000 −1.15–(−0.45) June Intercept 66.09 11.20 34.83 0.000 44.14–88.04 DO −2.72 0.99 7.54 0.006 −4.67–(−0.78) Temperature −1.86 0.28 44.36 0.000 −2.40–(−1.31) May Estimate SE Wald Chi-square P 95% CI Intercept 19.98 3.51 32.33 0.000 13.09–26.87 Temperature −0.80 0.18 20.18 0.000 −1.15–(−0.45) June Intercept 66.09 11.20 34.83 0.000 44.14–88.04 DO −2.72 0.99 7.54 0.006 −4.67–(−0.78) Temperature −1.86 0.28 44.36 0.000 −2.40–(−1.31) Open in new tab Table 2. Results from the generalized linear models (with negative binomial distribution) with the lowest Akaike information criterion (AIC) for each month, used to examine the relationship between CPUE of sand shrimp (Crangon septemspinosa) and environmental factors at Maryland coastal bays sites in May and June, averaged across years (1994–2012). Standard errors (SEs) and 95% confidence intervals (CIs) are given for estimates. DO, dissolved oxygen (mg l–l). May Estimate SE Wald Chi-square P 95% CI Intercept 19.98 3.51 32.33 0.000 13.09–26.87 Temperature −0.80 0.18 20.18 0.000 −1.15–(−0.45) June Intercept 66.09 11.20 34.83 0.000 44.14–88.04 DO −2.72 0.99 7.54 0.006 −4.67–(−0.78) Temperature −1.86 0.28 44.36 0.000 −2.40–(−1.31) May Estimate SE Wald Chi-square P 95% CI Intercept 19.98 3.51 32.33 0.000 13.09–26.87 Temperature −0.80 0.18 20.18 0.000 −1.15–(−0.45) June Intercept 66.09 11.20 34.83 0.000 44.14–88.04 DO −2.72 0.99 7.54 0.006 −4.67–(−0.78) Temperature −1.86 0.28 44.36 0.000 −2.40–(−1.31) Open in new tab Figure 7. Open in new tabDownload slide Relationships between catch-per-unit-effort (CPUE) of sand shrimp (Crangon septemspinosa) and temperature at various sites in Maryland coastal bays averaged for 1994 to 2012 in April (A), May (B) and June (C). Figure 7. Open in new tabDownload slide Relationships between catch-per-unit-effort (CPUE) of sand shrimp (Crangon septemspinosa) and temperature at various sites in Maryland coastal bays averaged for 1994 to 2012 in April (A), May (B) and June (C). Discussion Temperature was found to be an important factor affecting the seasonal occurrence and spatial distribution of sand shrimp in MCBs. Temperature, salinity, and dissolved oxygen have been reported to influence the occurrence, distribution, and survival of sand shrimp in other aquatic ecosystems and under laboratory conditions (e.g., Haefner, 1969, 1970, 1971, 1976, 1979; Albright, 2006). Our study is the first to show quantitatively the relationship between the spatial distribution of sand shrimp and water temperature and salinity in the field. Unlike in the MCBs, adult sand shrimp were abundant in Penobscot River estuary, Maine from April to early December when temperature and salinity ranged 6–21 oC and 11–29 psu, respectively, except when DO was less than 2.6 mg l–l (Haefner, 1969, 1979). Albright (2006) captured shrimp in three estuaries located along the mid-coast of Maine at temperatures of 9.4–25.9 oC, salinities of 3–34 psu, and DO of 6.5 mg l–l –13.1 mg l–l, although the highest numbers of the shrimp were caught between 10–18 oC and salinities ≥22 psu. In Port au Port Bay, Gulf of St. Lawrence, Canada shrimp probably migrate from shallow areas into offshore deeper waters during winter (Squires, 1996). Adult sand shrimp can survive in a wide range of salinities, from 19 to 36 psu (Haefner, 1976, 1979). Shrimp abundance in the MCBs was relatively high in spring from April to June, but individuals were scarce or not captured during the warm summer months of July to September and through early fall (October). This was probably due to high temperatures, which exceeded 23 oC during the summer months. Since the bays are shallow and lack deeper cooler water layers that can serve as refuge for shrimp from warmer surface waters, the shrimp might have been forced to move out of the bays into the cooler waters of the coastal ocean or they suffered high mortality. Because samples were not collected from November to March, it is unknown if shrimp occurred in the bays during these months. Their scarcity in the summer and prevalence in spring, nevertheless suggest that they likely entered the bays between fall and winter to reproduce, which was the period that Haefner (1976) began to capture them in York River-Chesapeake Bay Estuary. Other investigators reported onshore-offshore migration of sand shrimp and in the brown shrimp, Crangon crangon (Linnaeus, 1758), though to varying degrees. Populations of C. crangon in the northern Atlantic coastal waters undergo seasonal migrations triggered by a number of environmental factors, particularly salinity and temperature (Boddeke, 1976; Boddeke et al., 1976; Gellin et al., 2001; Lapinska & Szaniawka, 2006; Bilgin et al., 2008; Campos et al., 2012), and use selective tidal-stream transport behavior influenced by pressure and depth for their inshore and offshore migrations (Hufnagl et al., 2014; Tielmann et al., 2015). Brown shrimp adults move offshore into deeper, relatively warmer waters in autumn to overwinter as water temperature falls below 5 oC (Norte-Campos & Temming, 1998; Spaargaren, 2000) and return in spring. They can survive at temperatures between 6 oC and 30 oC (Jeffery & Revill, 2002), although the optimal thermal range for the juveniles and adults is between 5 oC and ~25 oC (Campos & van der Veer, 2008). Brown shrimp reproduction occurs offshore in highly saline, deeper waters. The larvae then move into shallow estuarine nursery areas (Tiews, 1970; Boddeke et al., 1976; Kuipers & Dapper, 1984). The abundance of the juveniles in the nursery areas is relatively high in spring/summer, and as they grow, their distribution shifts toward deeper waters. The abundance of the adults is at its peak in fall (Boddeke et al., 1976). Modlin (1980) reported that adult sand shrimp migrated from the coastal ocean into the Mystic River Estuary in spring to hatch their eggs, after which they returned to the ocean when the water temperature in the estuary rose above 20 oC. This appears also to be the case in the MCBs. Locke et al. (2005) reported that a part of the adult population of sand shrimp in Kouchibouguac River Estuary, Canada remained in the shallow estuary waters during the summer at temperatures as high as 28 oC. In contrast, Haefner (1969) found that in Maine waters, the upper thermal limit for maximum survival of shrimp was 18 oC, and reported offshore-onshore migration of shrimp in response to changes in water temperature in Lamoine, Maine (Haefner, 1972). Haefner (1972), citing Williams (1965), also stated that shrimp moved into deeper water in North Carolina during the summer, perhaps due to high water temperatures. Furthermore, shrimp abundance in the channels of the York River-Chesapeake Bay Estuary was highest in winter when bottom water temperature was between 5 oC and 11 oC, but decreased in spring when temperature was more than 15 oC (Haefner, 1976). The abundance of the shrimp in the channels in summer was very low or the shrimp were absent, which was attributed to rising temperatures (> 23 oC) and low dissolved oxygen (2–5 mg l–l) that perhaps triggered the migration of the shrimp (Haefner, 1969, 1970, 1971) into shallow areas of the Chesapeake Bay or deep, cool coastal waters. Haefner (1969) predicted that shrimp would suffer high mortality if subjected for several days to estuarine habitats with DO levels less than or equal to 3 mg l–l. Average daytime DO levels were nevertheless above 5 mg l–l in the summer in the MCBs, and individual DO measurements at the sites were rarely < 3 mg l–l. It is therefore unlikely that low dissolved oxygen was primarily responsible for the low abundance of shrimp at most sites sampled during the summer. Laboratory experiments conducted at various salinity and temperature combinations by Haefner (1969) demonstrated that both factors influenced the survival of adult shrimp. He computed the percentage of shrimp that would likely die at various temperature and salinity conditions. Based on his predictions, shrimp would suffer little or no mortality due to physiological stress at the levels of mean salinity (18.6–28.3 psu) and mean temperatures (12.2–17.1 oC) that were observed in April (spring) in MCBs, a month when no significant relationship was observed between shrimp CPUE and temperature at the sites during this study. In contrast, at the mean salinity (20.4–29.0 psu) and mean temperatures (17.0–21.9 oC) observed in May in MCBs, about 8 to 30% of the shrimp would die compared to 20 to 50% that would die in June when mean salinity (21.3–29.5 psu) and mean temperatures (21.8–26.7 oC) were higher (Haefner, 1969, 1979). Mean temperatures in July when shrimp was scarce were 23.1 to 28.9 oC, and mean salinity ranged from 23.2 psu to 30.2 psu. At these temperature and salinity combinations, ~30 to > 90% of the shrimp would likely die, if they did not emigrate from the system into deeper cooler waters (Haefner, 1969, 1979). The temporal patterns of shrimp abundance in the MCBs are, therefore, consistent with results of laboratory experiments by Haefner (1969), and field observations on adult shrimp disappearance in the channels of York River-Chesapeake Bay estuary during the summer (Haefner, 1976). Salinity and temperature values in MCBs are such that sites where the survival of shrimp would be highest in April and May, based on the predictions of Haefner (1969), are located in Isle of Wight (site 7) and Sinepuxent (site 8) bays close to the Ocean City Inlet, and the shrimp were observed to be most abundant at both sites. Results of the GLMs suggest that of the factors examined, temperature is the most important abiotic factor that influenced the occurrence and abundance of sand shrimp in the lagoons. Fish species increase in abundance from April through July in this ecosystem (Murphy & Secor, 2006; Peters & Chigbu, 2017) and predation by fishes along with mortality due to high temperature and emigration might also have contributed to the decline in abundance of shrimp. As global temperatures increase, it is therefore likely that sand shrimp populations in shallow coastal lagoons such as the MCBs that experience wide variations in temperature and salinity will be more negatively impacted than populations in deeper coastal waters with cooler bottom layers that can provide them refuge from the warmer surface waters. Spatio-temporal variations in the occurrence and abundance of sand shrimp could also have important implications for the food-web dynamics in the MCBs. ACKNOWLEDGEMENTS We thank the reviewers for their valuable comments that enhanced the quality of the manuscript, and E.D. Mayor for assistance with the preparation of figures. This study was funded by the National Science Foundation Center for Research Excellence in Science and Technology (NSF-CREST) Center for the Integrated Study of Ecosystem Processes and Dynamics award #1036586 and in part by the NOAA Educational Partnership Program Award NA16SEC4810007 to the Living Marine Resources Cooperative Science Center. LM was an intern supported by NSF REU grant DBI-1156919. References Able , K.W. , Fahay , M.P. , Heck , K.L. Jr. , Roman , C.T. , Lazzari , M.A. & Kaiser , S.C . 2002 . Seasonal distribution and abundance of fishes and decapod crustaceans in a Cape Cod estuary . Northeastern Naturalist , 9 : 285 – 302 . Google Scholar Crossref Search ADS WorldCat Albright , J.L . 2006 . Distribution, relative abundance, and diet of the sand shrimp (Crangon septemspinosa Say) in the Sheepscot, Kennebec, and Damariscotta River estuaries, Maine . M.S. thesis, University of Maine , Orono, ME, USA . 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TI - Influence of temperature on the occurrence and distribution of the sand shrimp Crangon septemspinosa (Decapoda: Caridea: Crangonidae) in polyhaline lagoons in Maryland, USA
JF - The Journal of Crustacean Biology
DO - 10.1093/jcbiol/ruz045
DA - 2019-09-18
UR - https://www.deepdyve.com/lp/oxford-university-press/influence-of-temperature-on-the-occurrence-and-distribution-of-the-27B0KB100S
SP - 586
VL - 39
IS - 5
DP - DeepDyve
ER -