The Relative Importance of the Sedge Island Marine Conservation Zone for Adult Blue Crabs in Barnegat Bay, New Jersey

Marine protected areas (MPAs), no-take zones, or marine reserves, where harvesting is banned or limited to some degree, have become an increasingly used strategy for conserving economically important species (Edgar et al., 2014). MPAs have been established worldwide, and their effects on species assemblages and diversity (Barrett, Buxton, and Edgar, 2009; Bell, 1983; Holland and Schnier, 2006; Lipej, Bonaca, and Sisko, 2003), fisheries productivity (Alcala et al., 2005; Gell and Roberts, 2003; Goni, Quetglas, and Renones, 2006; Hart, 2006; Roberts et al., 2001), and population characteristics of a variety of fish (Le Port, Lavery, and Montgomery, 2012; Macpherson, Garcia-Rubies, and Gordoa, 2000) and invertebrates (Barrett, Buxton, and Edgar, 2009; Branch, and Odendaal, 2003; Jack and Wing, 2010; Leite et al., 2009) have been well studied. Although the positive effects of MPAs are not universal (Edgar et al., 2014), the benefits of MPAs to individual species as a result of reduced fishing effort include increased abundance (Curley et al., 2013; Golbuu and Friedlander, 2011; Jack and Wing, 2010; Moland et al., 2013) and body size (Beukers-Stewart et al., 2005; Bevacqua et al., 2010; Branch and Odendaal, 2003; Pillans et al., 2005), particularly of reproducing adults, suggesting MPAs can enhance the reproductive capacity of species they protect (Kaiser et al., 2007). Assessing the influence of MPAs on particular species often involves comparisons of population characteristics or life history traits of organisms inside an MPA with those outside the MPA. One criticism of that technique is that areas outside the MPA may vary in habitat type or quality (Curley et al., 2013), particularly if the MPA is designed to protect habitats that are essential for some aspect of an organism's life history, such as spawning (Golbuu and Friedlander, 2011). Therefore, it is important for empirical studies that seek to assess the importance of MPAs by comparing them with areas outside the realm of protection to control for factors, other than the lack of fishing, that may influence the variables being measured.

The Sedge Island Marine Conservation Zone (SIMCZ) in Barnegat Bay is New Jersey's first marine conservation zone. Established in 2001, the SIMCZ was designed to better manage wildlife, recreation, and traditional uses of the area; reduce the environmental impacts of personal watercraft; and preserve and protect sensitive habitats, especially for economically and ecologically important species. Only recreational fishing is allowed inside the SIMCZ; thus, it is analogous to an MPA where fishing is limited but not banned. Despite its designation as a conservation zone, there has been no assessment of its effect. The objective of this study is to provide the first evaluation of the relative importance of the SIMCZ on an economically and ecologically important species.

Blue crabs, Callinectes sapidus, are an excellent model organism for assessing the importance of the SIMCZ as a conservation zone in Barnegat Bay. Blue crabs are one of the most important commercially and recreationally fished species in New Jersey (Kahn and Helser, 2005; Kennish et al., 1984; Stehlik, Scarlett, and Dobarro, 1998). They are ecologically relevant as a dominant part of the estuarine benthic community in this (Jivoff and Able, 2001; Wilson, Able, and Heck, 1990) and other estuaries (Lipcius et al., 2007; Meise and Stehlik, 2003), and they serve as both important predators and prey (Hines, 2007). Blue crabs are known to use the habitats found within the SIMCZ, including shallow areas with submerged aquatic vegetation (SAV; Perkins, Wolcott, and Wolcott, 1996; Wilson, Able, and Heck, 1990), macroalgae, or both (Epifanio et al., 2003) and deeper areas with little or no structure (Hines et al., 1995). The SIMCZ is adjacent to Barnegat Inlet, an opening to the ocean that may be part of the spawning grounds for female blue crabs, as seen in other estuaries (Tankersley et al., 1998; Van Engel, 1958). Indeed, in Chesapeake Bay, the spawning grounds near the mouth of the estuary were traditionally an MPA, protecting females at the spawning grounds from harvesting. More recently, the corridor females use to migrate to the spawning grounds was included in this MPA to protect females en route to the spawning grounds, as well (Lipcius et al., 2003). The expanded MPA and corridor provide protection to considerably more females, particularly during the spawning season, than the historical MPA and thus may be critical to maintaining the spawning stock (Lipcius et al., 2003). Establishing an MPA large enough to protect females moving to the spawning grounds may be a key feature if the MPA is designed to protect the spawning stock (Eggleston, Bell, and Searcy, 2009). This study provides the opportunity to determine whether the SIMCZ helps to protect the spawning stock of females in Barnegat Bay.

The overall goal of the project is to assess the value of the SIMCZ to sustain a key recreationally and commercially important species by comparing temporal and spatial variation in population characteristics of adult blue crabs inside vs. outside the SIMCZ. Specifically, the abundance and size of adult blue crabs, as well as the incidence of ovigerous females, inside the SIMCZ were compared with physically similar outside locations that (1) provide straight-line access to Barnegat Inlet but with varied habitats and (2) vary in distance from an inlet and share the same habitat.

Barnegat Bay is a narrow (2–6-km-wide) lagoonal estuary extending approximately 67 km along the central New Jersey coastline between Tuckerton and Pt. Pleasant, New Jersey (39°31′N, 74°02′W to 40°06′N, 74°02′W). Barnegat Bay is separated from the Atlantic Ocean by a barrier island complex, including Long Beach Island and Island Beach State Park, with two inlets to the Atlantic Ocean: Barnegat Inlet, about 35 km south of Pt. Pleasant, and Little Egg Inlet, at the southern boundary (Figure 1). The SIMCZ, on the bayside of Island Beach State Park (Figure 1), is an area of approximately 650 ha (1600 acres) containing marsh islands, dominated by Spartina alterniflora, and open water. Benthic habitats are dominated by shallow areas with submerged aquatic vegetation SAV, but macroalgae and unvegetated areas of varying depth are also present.

This study assessed the relative role of the SIMCZ on adult blue crabs by examining temporal and spatial variation in abundance and differences in the size frequency distribution of crabs in the SIMCZ compared with locations outside the conservation zone. Sampling along the east-west axis of the bay occurred within a narrow corridor of straight-line access to Barnegat Inlet at three locations: SIMCZ, midbay, and western shore (Figure 1). This minimized variation in physical characteristics among the sampling locations and allowed comparison of blue crab population characteristics inside the SIMCZ with those outside but close to the SIMCZ. However, sampling sites at these locations varied in habitat type: SIMCZ sites were dominated by SAV, midbay sites included SAV-dominated and open bay habitats, and western shore sites included open bay habitats and the mouths of marsh creeks. The drawback to this design is that spatial variation in bottom type can influence population characteristics of blue crabs in this system (Jivoff and Able, 2001; Szedlmayer and Able, 1996). Simultaneously, as part of a different study, blue crab population characteristics within three habitats, including SAV, were examined along the north-south axis of Barnegat Bay. This additional study provided the opportunity to compare locations that are physically similar to the SIMCZ and are also dominated by SAV. While the north-south sampling primarily allows within-habitat comparisons of blue crab population characteristics, this sampling occurred in clusters that also contained open bay habitats and the mouths of marsh creeks, which allowed the importance of the SIMCZ relative to these different habitat types to be assessed.

Aspects of adult blue crab population structure (abundance, size composition) in each year (2012–2013) were sampled using baited (menhaden) commercial-style traps (60 cm high × 60 cm wide × 60 cm deep with 3.8-cm hexagonal mesh), fished daily for 4 consecutive days, each month from May to August. During each day of east-west sampling, three traps were randomly assigned to one of four sites in each sampling location (Figure 1). During north-south sampling (except in the SIMCZ), two traps were randomly assigned to one of four sites in each sampling location or cluster (Figure 1). SIMCZ data from east-west sampling were also used to compare with locations in the north-south sampling. Each sampling day, physical characteristics near the first and last trap in each site, including depth, salinity, temperature, and dissolved oxygen, were taken with a hand-held YSI datalogger (model 6800).

Crabs were separated by trap in moist burlap bags, returned to the Rutgers University Marine Field Station, and assessed for carapace width between the tips of the lateral spines (to the nearest millimeter), age, sex, sexual maturity (see below), molt stage (see below), limb loss and regeneration, and ovigerous stage (adult females only). Sexual maturity and molt stage were determined using previously established methods (Jivoff, 1997). Briefly, molt stage was determined by examining the propodus on the fifth appendage for evidence of epidermal retraction and color variation (Van Engel, 1958) and, for recently molted (postmolt) crabs, the relative hardness of the newly formed carapace (Freeman et al., 1987). Males were designated adults according to the following criteria: the secondary pleopods lay within the primary pleopods (intromittent organs); the penes were inserted into the secondary pleopods; and the abdomen easily pulled away from the sternum (Van Engel, 1990).

This study concentrated on adult crabs; therefore, traps were used as collecting gear because they are efficient at capturing blue crabs in the adult size range (Guillory, 1998) and are more efficient than other types of gear at capturing adults (e.g., trawl) (Bellchambers and de Lestang, 2005). Furthermore, because the study area was in a conservation zone, not using an otter trawl minimized the effect of sampling on the benthic community. Traps have been criticized as a gear for estimating crab abundance because variation among traps (e.g., soak time and presence of bait, conspecifics, or both) (Sturdivant and Clark, 2011) and in crab behavior (e.g., aggressiveness, feeding) may influence free crabs from entering (Murray and Seed, 2009; Sturdivant and Clark, 2011) and captured crabs from escaping the trap (Sturdivant and Clark, 2011). In another portunid (Portunus pelagicus), there is also some evidence that traps preferentially capture males compared with females (Bellchambers and de Lestang, 2005); however, the sexes are equally attracted to traps and put forth equal effort to enter traps (Smith and Sumpton, 1989). In this study, traps were used systematically to minimize variation in trap soak time (24 h for all traps), bait content (renewed daily), trap integrity (e.g., traps checked daily and damages repaired immediately), and the extent of fouling (traps were power-washed periodically). Sturdivant and Clark (2011) found no evidence in blue crabs that aggressive interactions with captured crabs deterred free crabs from entering traps. Murray and Seed (2009) found that traps were especially ineffective when colder temperatures reduced green crab feeding time. During the current study, all of the physical variables were well within tolerance limits of blue crabs, suggesting crabs were behaving normally (e.g., feeding) throughout the study period.

For each sampling scheme, the number of crabs captured each day in the replicate traps were combined to produce “composite” daily samples (preliminary analysis indicated that the trap did not explain a significant amount of variation in abundance). In the east-west sampling, the composite daily sample represented the estimate of abundance. To compare the SIMCZ with clusters in the north-south sampling, the abundance of crabs was converted to catch per unit effort (CPUE) because the number of traps used differed (three traps for east-west sampling; two traps for north-south sampling). CPUE was calculated as the number of crabs captured divided by the number of traps used. For each sampling scheme, temporal and spatial variation in abundance (sexes analyzed separately) were analyzed using three-way analysis of variance (ANOVA) with year (2012 and 2013), month (5–8), and location as factors (including each two-way and the three-way interaction). Abundance data were square root–transformed to produce homogeneous variances confirmed by the Levene's test. The Tukey multiple comparisons test (Tukey HSD) was used to identify significant differences among multilevel independent variables. Size distributions (sexes analyzed separately) were compared among sampling locations using Kolmogorov-Smirnov (KS) tests. All ANOVA and KS analyses were interpreted using p values adjusted for the number of comparisons (0.05/no. of comparisons). For each sampling scheme, temporal and spatial variation in physical characteristics was analyzed using three-way ANOVA with year (2012 and 2013), month (5-8), and location as factors (including each two-way and three-way interaction). Statistically significant variation occurred in some physical variables but lacked consistent patterns and was based on very small absolute differences in physical characteristics (Table 1). Furthermore, physical parameters never reached limiting levels; therefore, any statistical differences in the physical characteristics are considered biologically unimportant. Statistical analyses were performed using SYSTAT (SYSTAT, 1992), and unless otherwise indicated, x¯ ± 1 SE are shown.

The locations along the east-west axis of the estuary were very similar in all physical characteristics (Table 1). On average, the differences among the locations were no more than 2°C in temperature, 1 ppt in salinity, 1 mg/L in dissolved oxygen, and 0.5 m in depth.

During the course of this study, a total of 1269 adult crabs were captured at the locations along the east-west axis of the Bay: 743 males and 526 females. The total abundance of crabs varied by month (F_3,69 = 33.8, p < 0.001) and location (F_2,69 = 11.8, p < 0.001), with a greater number of crabs at the SIMCZ and west locations than at the midbay location (Tukey, both comparisons, p < 0.001).

Males and females exhibited different abundance patterns; therefore, separate analyses were performed for each sex. The abundance of males varied by month (F_3,69 = 34.7, p < 0.001), increasing monthly until a peak in July, followed by a decrease in August. Male abundance also varied by location (F_2,69 = 33.1, p < 0.001), with a greater number of males at the SIMCZ and west locations than the midbay location (Tukey, both comparisons, p < 0.001; Figure 2).

The abundance of females varied by month (F_3,69 = 6.5, p = 0.001); more females were present in August compared with May and June (Tukey, both comparisons, p < 0.008). Female abundance did not vary by location (F_2,69 = 2.6, p = 0.08; Figure 2), but females in the different locations did exhibit slight differences in abundance across the months (F_6,69 = 6.4, p < 0.001). However, this variation was the result of one difference between the locations confined to one month rather than a consistent monthly pattern between locations. Except for May, the proportion of ovigerous females in the SIMCZ remained high through the months and was consistently larger than at the other sampling locations (Table 2).

The size frequency distribution of males (KS test, all comparisons, p > 0.05; Figure 3A) and females (KS test, all comparisons, p > 0.05; Figure 3B) were similar among sampling locations.

The locations along the north-south axis of the estuary were very similar in all physical characteristics (Table 1). On average, the differences among the locations were no more than 2°C in temperature, 2 ppt in salinity, 1 mg/L in dissolved oxygen, and 0.5 m in depth.

During the course of this study, a total of 2339 adult crabs were captured at the locations along the north-south axis of the Bay: 1859 males and 480 females. The total abundance of crabs varied by location (F_3,50 = 9.7, p < 0.001), with a greater number of crabs at the SIMCZ than at cluster 3 (Tukey, p < 0.001), cluster 2 (Tukey, p = 0.001), or cluster 1 (Tukey, p = 0.01).

The abundance of males varied by location (F_3,50 = 11.9, p < 0.001; Figure 4). Male abundance was greater in the SIMCZ than in cluster 2 (Tukey, p = 0.03) or cluster 1 (Tukey, p < 0.001). Cluster 1 had the fewest males of all the sampling locations.

The abundance of females varied by location (F_3,50 = 5.7, p = 0.002; Figure 4). Female abundance was greater in the SIMCZ than in cluster 3 (Tukey, p = 0.02) or cluster 2 (Tukey, p = 0.02). Female abundance was also greater in cluster 1 than in cluster 3 (Tukey, p = 0.03) or cluster 2 (Tukey, p = 0.03). Except for May, the proportion of ovigerous females in the SIMCZ and in cluster 1 remained high through the months and was consistently larger than at the other sampling locations (Table 2). The total number of adult females was consistently greatest in the SIMCZ (Table 2).

The size frequency distribution of males (KS test, all comparisons, p < 0.008) was significantly different in the SIMCZ compared with all other locations (Figure 5A). In the SIMCZ, more males were in all size categories greater than 115 mm carapace width compared with all other sampling locations. In contrast, the size frequency distribution of females was similar among the sampling locations (KS test, all comparisons, p > 0.05; Figure 5B).

Sampling along the north-south axis of the bay occurred in clusters that contained habitats other than SAV: open bay (deeper with little or no structure present) and near the mouths of marsh creeks. As a result, it is also possible to examine blue crab abundance in the SIMCZ relative to habitats in addition to SAV. A three-way ANOVA including year, month, and habitat as independent variables showed that males (F_3,226 = 16.1, p < 0.001) and females (F_3,226 = 11.4, p < 0.001) vary significantly across these habitats but show slightly different spatial patterns relative to the SIMCZ (Figure 6). In the SIMCZ, males are more abundant compared with SAV (Tukey, p = 0.01) and open bay (Tukey, p < 0.001) areas, whereas females are more abundant compared with SAV (Tukey, p < 0.001). Indeed, if the abundance patterns among these habitats were ranked, males would exhibit the pattern SIMCZ = Creek Mouth > SAV > Bay, whereas the female pattern would be SIMCZ = Creek Mouth = Bay > SAV, suggesting the SIMCZ and creek mouths are equally important for both sexes, and bay habitats are more important for females than for males.

Assessing the importance of protected areas often involves comparing the structure of the ecological community (Babcock et al., 1999; Edgar and Barrett, 1999), populations of select organisms inside protected areas with those outside (Lester et al., 2009; Mosqueira et al., 2000), or both. The east-west comparisons showed only a few differences that typically lacked consistent patterns. The abundance and size of females was similar among locations, but, except in May, the SIMCZ had a consistently higher percentage of ovigerous females compared with the other locations. In this and other estuaries (Ogburn and Habegger, 2015; Tankersley et al., 1998; Van Engel, 1958), ovigerous females spawn near the entrance to the bay; therefore, ovigerous females may accumulate in the SIMCZ because of its proximity to Barnegat Inlet and the spawning grounds. Interestingly, the high incidence of ovigerous females in May at the west locations may be due to variation in physical characteristics among the sampling sites within that location. One of the west sites is near Oyster Creek, which accepts heated effluent from the Oyster Creek Nuclear Generating Station. The heated effluent may stimulate egg development and thus may contribute to the relatively high number and percentage of ovigerous females in May when ambient temperatures are still low. The SIMCZ contained a greater number of crabs, particularly males, compared with midbay locations, but abundance was equivalent to west locations. However, these differences may be confounded by habitat variation among sampling sites in the locations: the SIMCZ is dominated by SAV, midbay sites include SAV-dominated as well as open bay habitats (with little or no structure), and west sites include open bay habitats and the mouths of marsh creeks. The results, and those in other estuaries (Hines, 2007; Hines, Lipcius, and Haddon, 1987), show that population characteristics of blue crabs vary among habitats, making the differences observed among the east-west locations somewhat difficult to interpret. However, when the model controls for habitat, more consistent and interesting patterns emerge that suggest an important role of the SIMCZ for adult blue crabs.

The comparisons along the north-south axis eliminate the confounding effect of habitat because the locations are all SAV-dominated. The abundance of males is higher in the SIMCZ compared with other SAV-dominated locations, although not significantly, compared with the neighboring location, suggesting the SIMCZ does not significantly enhance the abundance of males in adjacent areas via a “spill-over” effect, as seen in other species protected by MPAs (Pillans et al., 2005; Russ, Alcala, and Maypa, 2003; Stobart et al., 2009). Additionally, the SIMCZ has a distinct size frequency distribution of males compared with all other locations, with more males greater than 115 mm carapace width. The (commercial) legal size limit for blue crabs in New Jersey is 117 mm (4.5 inches) carapace width, suggesting, as has been observed for other commercially important species in other marine protected areas (Lester et al., 2009), that the unique size frequency distribution inside the SIMCZ may be the result of relaxed fishing pressure inside the conservation zone. This would be particularly true for males during the time of this study (May–August, 2012–13) because the trap fishery during the summer predominantly captures male crabs. Consistent with this interpretation, the size frequency distribution of females inside the SIMCZ is similar to that of other SAV-dominated locations. However, unlike the abundance of males, the abundance of females, particularly ovigerous females, inside the SIMCZ is greater compared with those locations further from an inlet but also neighboring locations that provide similar proximity to Barnegat Inlet, suggesting that the SIMCZ is important for spawning females for reasons in addition to proximity to the inlet. For example, comparisons among different habitats in the north-south axis sampling suggest that female abundance is greater in open bay areas compared with SAV-dominated habitats, which is consistent with the habitats adult females use in other estuaries during their migration to the spawning area (Aguilar et al., 2005; Lipcius et al., 2003). Female abundance in the SIMZC was equivalent to open bay areas but greater than other SAV-dominated habitats. The SIMCZ contains some open bay habitats; therefore, females may accumulate in the SIMCZ because it provides easy access to both SAV-dominated and open bay habitats. In Chesapeake Bay, a protected area established specifically for adult females moving toward and within the spawning grounds, offers significant protection to the spawning stock there (Lipcius et al., 2003). The results of this study suggest that the SIMCZ may be offering similar protection to the blue crab spawning stock in Barnegat Bay.

Although the results suggest that the SIMCZ positively affects population characteristics of adult blue crabs (e.g., enhanced abundance of females, particularly ovigerous females, and of legal-sized males), the relative effect these characteristics have on the Barnegat Bay blue crab population is unclear. The effect of the SIMCZ is suspected to be relatively small, given that it represents only about 2% of the total area of Barnegat Bay and thus contains a small proportion of the entire population of blue crabs in Barnegat Bay. By contrast, the protected area in Chesapeake Bay represents approximately 14% of the total area of the Bay. Protected areas that are spatially small or isolated, or both, are more effective if multiple areas can be “combined” into a network of reserves (Gaines et al., 2010; Lubchenco et al., 2003). The New Jersey Department of Environmental Protection has identified several “ecologically sensitive” areas in Barnegat Bay that may warrant future protection because they contain critical habitats that may be subjected to various human impacts. Combining these ecologically sensitive areas with the SIMCZ to form a network of conservation zones within Barnegat Bay could increase the relative effect of the SIMCZ on the blue crab population in the Bay.

The relative importance of the Sedge Island Marine Conservation Zone for adult blue crabs was tested by comparing population characteristics (1) along the east-west axis of the bay where habitats varied and (2) along the north-south axis of the bay within the same habitat. Compared with other SAV-dominated areas with similar physical characteristics, the SIMCZ contained (1) more adult, particularly legal-sized, males and (2) more adult, especially egg-bearing, females, even compared with adjacent SAV-dominated areas with similar proximity to Barnegat Inlet. Taken together, these results suggest that the SIMCZ is unique as a SAV-dominated area important for adult male and female blue crabs, particularly females that are members of the current spawning stock. One potential effect of the lack of commercial fishing inside the SIMCZ (especially during the summer) may be a preponderance of relatively large males because more males are taken by the commercial fishery during this time of year.

The authors thank the Rutgers University Marine Field Station for providing a considerable amount of logistical support, as well as student housing, lab space, and boat access, and are very grateful to the New Jersey Department of Environmental Protection for funding this work. The authors also thank two anonymous reviewers whose comments and suggestions improved this manuscript.