Inter-cohort differences in spatial and temporal settlement patterns of young-of-the-year windowpane (Scophthalmus aquosus) in southern New Jersey
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1 Estuarine, Coastal and Shelf Science 56 (2003) Inter-cohort differences in spatial and temporal settlement patterns of young-of-the-year windowpane (Scophthalmus aquosus) in southern New Jersey M.J. Neuman*,1, K.W. Able Rutgers University, Institute of Marine and Coastal Sciences, Marine Field Station 800 c/o 132 Great Bay Boulevard, Tuckerton, NJ 08087, USA Received 16 February 2002; received in revised form 5 March 2002; accepted 5 March 2002 Abstract The timing and location of settlement of two cohorts (spring and fall) of windowpane (Scophthalmus aquosus) were identified based on collections from 64 sampling locations along a corridor from the lower estuary, through the inlet, and on to the adjacent inner continental shelf in southern New Jersey. Spatio-temporal patterns of settlement during were determined based on capture location and timing, and eye migration stage. Spring-spawned windowpanes were collected in estuarine, inlet and ocean habitats as larvae, during settlement, and after settlement. Densities of spring-spawned larvae (2 10 mm standard length (SL)) peaked in May in all habitats (estuary, inlet, and ocean). Initial settlement of spring-spawned windowpane occurred during May in the inlet and ocean when fish had grown to 7 8 mm SL (mid-point of eye migration), but fish did not appear in demersal estuarine collections until June when they were larger and more developmentally advanced (24 32 mm SL; post-eye migration). A transitional settlement period, comprised of a progressive habitat shift from pelagic to demersal habitats, is proposed for the spring cohort to explain the observed patterns. Fall-spawned fish of all developmental stages and sizes were virtually absent from estuarine collections. Fall-spawned larval (2 10 mm SL) densities peaked in October in inlet and ocean habitats and fish began settling there during the same month at sizes similar to the spring cohort (7 8 mm SL). This research confirms that there are important cohort-specific and life-stage dependent differences in young-of-the-year (YOY) windowpane habitat use in southern New Jersey and perhaps in other east coast US estuaries. These differences may affect the overall contribution that each cohort makes to a given year class and thus, may have an important role in determining the recruitment dynamics of this species. Ó 2003 Elsevier Science B.V. All rights reserved. Keywords: settlement; flatfish; early life history; multiple cohorts; Scophthalmus aquosus 1. Introduction 1 Present address: NOAA/NMFS/Southwest Regional Office, 501 West Ocean Boulevard, Suite 4200, Long Beach, CA , USA. * Corresponding author. address: melissa.neuman@noaa.gov (M.J. Neuman). A number of marine fish species undergo a habitat shift from a pelagic to a demersal existence during a process known as settlement. Settlement is characterized best in coral reef fishes and flatfishes and is often accompanied by a morphological transition from the larval to the juvenile form (Able & Fahay, 1998; Grover, Eggleston, & Shenker, 1998; Keefe & Able, 1993; Thorisson, 1994). Ontogenetic changes in morphology, behaviour and habitat during settlement result in changes in distribution patterns between larval, newly settled and larger juvenile stages. Studies of flatfish have identified localized settlement areas in shallow estuarine or near-coastal habitats, where newly settled individuals typically reside for weeks to months before dispersing to other demersal habitats (Allen, 1988; Curran & Able, 2002; Keefe & Able, 1993; Rogers, Gunderson, & Armstrong, 1989; Wennhage, 1999; Witting, 1995). While aspects of settlement have been frequently studied, seldom have the nuances of ontogeny and seasonality of settlement been addressed for multiple /03/$ - see front matter Ó 2003 Elsevier Science B.V. All rights reserved. doi: /s (02)
2 528 M.J. Neuman, K.W. Able / Estuarine, Coastal and Shelf Science 56 (2003) cohorts of the same species (but see Kneib, 1993). A unique opportunity for addressing these issues is available for windowpane (Scophthalmus aquosus) in the Middle Atlantic Bight, which has two clearly defined cohorts of young-of-the-year (YOY) within the same year. Windowpanes range from the Gulf of Saint Lawrence south to Florida, but are most abundant from Georges Bank to Chesapeake Bay (Bigelow & Schroeder, 1953; Dery & Livingstone, 1982). The timing of spawning along the north-eastern US has been determined from gonadal development of adults (Wilk, Morse, & Stehlik, 1990), collection of eggs (Berrien & Sibunka, 1999), and collection of recently hatched larvae (2 4 mm; Morse & Able, 1995). Spawning is unimodal on Georges Bank, but a split spawning season is evident from southern New Jersey southward to Cape Hatteras, North Carolina (Morse & Able, 1995). Off the coast of southern New Jersey, a spring-spawning event occurs in April May and a fall-spawning event occurs in October November; both spawning events occur when temperatures range from 16 to 19 C (Morse & Able, 1995). Large larvae (>8 mm) and recently settled fish are absent from continental shelf collections off New Jersey suggesting that large larvae from this area might settle in estuarine habitats (Morse & Able, 1995). The purpose of this study was to examine between-cohort variation in distribution and abundance of YOY windowpane and to identify the mechanisms that explain the absence of large larvae and recently settled windowpane on the continental shelf in the Middle Atlantic Bight. The specific objectives were to: (1) examine temporal and spatial aspects of the distribution of pelagic larvae from both the spring and fall cohorts; (2) quantify the timing of the transition from pelagic to demersal habitats; and (3) determine if localized settlement areas exist in near-coastal environments and, if so, whether settlement patterns differ between the spring and fall cohorts. 2. Materials and methods 2.1. Study area The study area is an estuarine to inner continental shelf corridor in southern New Jersey (Fig. 1). The Fig. 1. Sampling locations ðn ¼ 64Þ for planktonic and demersal windowpanes in the estuary (open symbols), inlet (shaded symbols) and ocean (solid symbols) in the Great Bay Little Egg Harbor estuarine system and adjacent continental shelf from The long-term estuarine ichthyoplankton sampling site, Little Sheepshead Creek Bridge, is shown by the solid square. Mean daily temperatures were recorded inside the estuary at the Rutgers University Marine Field Station (RUMFS), shown by the solid diamond, and on the inner continental shelf approximately 5 km outside of Little Egg Inlet, shown by the solid star.
3 M.J. Neuman, K.W. Able / Estuarine, Coastal and Shelf Science 56 (2003) estuarine portion of this corridor is polyhaline and shallow (average depth at mean low water is 1.7 m; Durand, 1984), with a wide annual temperature range (ÿ2 28 C; Able, Hoden, Witting, & Durand, 1992), a moderate tidal range (1.1 m near the mouth of Great Bay; Durand, 1984), and salinities that range from 12 ppt in the upper portions of Great Bay and Little Egg Harbor, to 35 ppt in lower estuarine stations (Able et al., 1992; Szedlmayer & Able, 1996). The annual input of freshwater into the drowned river estuary (Great Bay) and the barrier beach estuary (Little Egg Harbor) is low relative to the volume of the estuaries (Chant, Curran, Able, & Glenn, 2000; Durand, 1988). The primary source of ocean water moving into these estuaries is through Little Egg Inlet ( m depth, salinity ppt; Morse & Able, 1995). The geomorphological characteristics of the inlet are dynamic, with ephemeral sand bars and islands submerging and re-surfacing annually (Nordstrom, 1992). Little Egg Inlet also connects these estuaries to the adjacent inner continental shelf ( m depth, in the vicinity of sand ridges, and m depth, farther offshore; Morse & Able, 1995) Larval and juvenile fish sampling Samples of YOY windowpanes were collected from eight independent surveys with planktonic (1-m plankton net, 1-mm mesh; 1 1-m Tucker trawl, 0.5-mm mesh) and demersal sampling equipment (1- and 2-m beam trawls, 3-mm mesh; 6.1-m seine net, 3-mm mesh; 30-m seine; 6-mm mesh) from 1989 to Sampling effort and spatial temporal coverage varied during the 10-year period (Fig. 2). Details of the sampling protocols for planktonic and demersal collections have been described elsewhere (McBride, Fahay, & Able, 2002; Neuman, 1999). Briefly, 64 locations were sampled and a total of 2477 windowpanes were captured in three habitat types: (1) estuarine (Great Bay and Little Egg Harbor, n ¼ 1298); (2) inlet (Little Egg Inlet, n ¼ 838); and (3) adjacent continental shelf habitats (n ¼ 341; Figs. 1 and 2). Planktonic collections occurred at night in the estuary and during the day in the inlet and inner continental shelf. All demersal collections occurred during the day. While system-wide sampling was conducted with different sampling equipment and was not concurrent for all portions of the study, pooling survey data permitted an examination of seasonal and temporal patterns of YOY windowpane throughout this system. Windowpanes were categorized according to an eye migration staging scheme (pre-metamorphic, Fÿ, F, G, Hÿ, H, Hþ, I, post-metamorphic) devised by Keefe and Able (1993) for summer flounder (Paralichthys dentatus). Fish total length (TL) was converted to standard length (SL) using the following linear relationship: SL ¼ 1:59 þ 0:77 TL ðr 2 ¼ 0:998Þ. To ensure that windowpane extracted from these surveys were YOY, only windowpanes 120 mm SL (Morse & Able, 1995) were used in all analyses. Mean daily surface water temperatures were calculated from readings taken on a near-daily basis inside the estuary near the Rutgers University Marine Field Station (Fig. 1) via hand-held thermometer ( ) and from a location 5 km off of the New Jersey coast on the inner continental shelf (Fig. 1) via advanced very high resolution radiometer (AVHRR) satellite imagery ( ) Analyses The size at settlement for windowpane was estimated using probit analysis (SAS Institute Inc., 1990). Individuals collected in Tucker trawls or plankton nets were classified as planktonic and those collected in beam trawls or seine nets were classified as demersal. These two classifications were scored as 0 or 1, respectively. The relationship between size and occurrence in planktonic or demersal habitats was parameterized by fitting a cumulative normal distribution, using probit analysis, to the binary (0, 1) data (SAS Institute Inc., 1990). This method allowed size-at-settlement to be described as a normal distribution. Two goodness-of-fit v 2 values (Pearson v 2 and the log-likelihood ratio v 2 ) were used to assess whether the habitat transition was dependent upon size of the individual (SAS Institute Inc., 1990). Temporal and spatial analyses of windowpane densities were compared in 1991, 1992 and 1996 based on estimates (mean 1 SE) of the number of fish captured divided by either the volume of water sampled (for plankton surveys) or the area of the bottom sampled (for seine and beam trawl collections). These years were selected for further analysis as planktonic and demersal sampling occurred concurrently in multiple habitats in both spring and fall (Fig. 2). A two-way analysis of variance (ANOVA) was used to test for the independent effects of month, habitat type (estuary, inlet, and ocean), and the interaction between month and habitat type on differences between log 10 -transformed densities of planktonic and demersal windowpanes. Four separate analyses were performed for spring-spawned planktonic and demersal fish and fall-spawned planktonic and demersal fish. 3. Results 3.1. Temporal and spatial patterns of planktonic windowpane Spring-spawned windowpane larvae were abundant in estuarine, inlet, and inner continental shelf (subsequently referred to as ocean) habitats. Densities of springspawned larvae peaked in May, and then decreased
4 530 M.J. Neuman, K.W. Able / Estuarine, Coastal and Shelf Science 56 (2003) Fig. 2. Summary of windowpane sampling effort and temporal and spatial coverage of sampling with (a) planktonic and (b) demersal equipment, Pie size indicates sampling effort (tows/month) for planktonic and demersal sampling equipment and pie fill colour indicates the relative sampling effort within each habitat type, estuary (no fill), inlet (grey fill) and ocean (solid fill) by month for each year. Lack of sampling is indicated by absence of a pie chart. through July (Table 1, Fig. 3a). During May, densities in the inlet and ocean were significantly higher than those in the estuary (Table 2). During June, mean density decreased slightly in the estuary and significant declines occurred in the inlet and the ocean. In July, larvae were absent from inlet collections and abundances continued to decline in the estuary and the ocean (Fig. 3a). Larvae were absent from all ichthyoplankton collections in August. Spring-spawned larvae first appeared in plankton samples at lengths as small as 2 mm SL and increased in size from May to July (Table 1, Fig. 4). In May, June and July, larvae were larger in the estuary than they were in the inlet and ocean (Table 1, Fig. 4). The majority of fall-spawned larvae were collected in the ocean and their densities were considerably lower than those of spring-spawned larvae (Table 1, Fig. 3(a)). Fall-spawned larvae were collected from September to January, with densities peaking in October and declining through January. In October, larval concentrations were greater in the ocean compared to the estuary and in November and December larvae were only collected in the ocean (Table 1, Fig. 3a). Sizes of fallspawned larvae increased from September to November, but were similar in November and December (Table 1, Fig. 4). Peak concentrations of spring- and fall-spawned larvae occurred at similar temperatures. In May, temperatures increased from 12 to 18 C, while in October, temperatures decreased from 19 to 13 C (Fig. 3). In the spring, temperatures in the estuary were warmer
5 M.J. Neuman, K.W. Able / Estuarine, Coastal and Shelf Science 56 (2003) Table 1 Mean monthly densities, number per 1000 m 3 (1 SE) and standard lengths (1 SE) of larval windowpane collected along an estuarine to ocean corridor in southern New Jersey (estuary, n ¼ 284; inlet, n ¼ 142; and ocean, n ¼ 361) in 1991, 1992 and Tucker trawl and plankton net collections are included Mean larval density (SE) Mean Standard length (SE) Month Estuary Inlet Ocean Estuary Inlet Ocean January (0.18) February March 0.13 (0.13) April 0.41 (0.32) (7.57) May (6.53) (22.16) (10.75) 5.83 (0.16) 4.69 (0.14) 3.56 (0.06) June 3.96 (1.89) 2.93 (1.49) 0.81 (0.81) 7.65 (0.50) 5.05 (0.19) 6.91 (0.66) July 0.12 (0.12) (0.24) (2.89) August September (0.08) 3.67 (0.32) October 0.09 (0.09) 2.86 (1.38) (3.77) (0.26) 4.53 (0.20) November (1.63) 9.72 (0.78) December (0.21) (0.13) than in the ocean, and during the fall, temperatures in the ocean were greater than in the estuary (Fig. 3). Larvae were not collected in any habitat during the warmest (August) and coolest (February) months Temporal and spatial patterns of demersal windowpane Settled, spring-spawned windowpanes were collected in estuarine, inlet and ocean habitats from May to September (Table 3, Fig. 3b). In June, densities were significantly higher in the inlet than in the estuary and ocean (Tables 2 and 3, Fig. 3b). Densities continued to increase in the estuary and inlet in July, reaching a peak in the inlet, however, abundance in the ocean declined at this time (Table 3, Fig. 3b). Mean densities declined significantly in all habitats during August (Fig. 3b). In September, spring-spawned windowpanes were absent from ocean collections and densities remained low in the estuary and in the inlet (Fig. 3b). Spring-spawned Fig. 3. (a) Mean monthly densities (number per 1000 m 3 1 SE) of windowpane (120 mm SL) captured with planktonic sampling equipment in the estuary (open bars, n ¼ 284), inlet (shaded bars, n ¼ 142) and ocean (solid bars, n ¼ 361) in 1991, 1992 and Mean daily surface water temperatures ( C) from the estuary ( ) and the ocean ( ) are shown by the solid and broken lines, respectively. (b) Mean monthly densities (number per 100 m 2 1 SE) of windowpane (120 mm SL) captured with demersal sampling equipment in the estuary (open bars, n ¼ 54), inlet (shaded bars, n ¼ 296) and ocean (solid bars, n ¼ 93) in 1991, 1992 and Mean daily surface water temperatures ( C) from the estuary ( ) and the ocean ( ) are shown by the thin and thick lines, respectively.
6 532 M.J. Neuman, K.W. Able / Estuarine, Coastal and Shelf Science 56 (2003) Table 2 Results from four, separate two-way ANOVAs examining variation in windowpane log 10 -transformed densities (mean number +1 per 1000 m 3 ) among spring- and fall-spawned planktonic and demersal fish. The independent effects of month captured, capture location (habitat type = estuary, inlet or ocean), and the interaction between habitat type and month are tested. Source of variation Sample size df F-value P-value Spring larvae Habitat type Month < Habitat type month Fall larvae Habitat type Month Habitat type month Spring juveniles Habitat type < Month < Habitat type month < Fall juveniles Habitat type < Month < Habitat type month < windowpane first appeared in demersal collections at sizes as small as 7 mm SL and increased in size from June to September (Table 3, Fig. 4). Settled, fall-spawned windowpanes were collected primarily in the ocean from October through May (Table 3, Fig. 3b). Densities peaked in the inlet in November and peaked in the ocean in December. After December, demersal windowpanes were rarely collected (Table 3, Fig. 3b). Fall-spawned windowpane increased in size from October to November, and remained at similar sizes in December (Table 3, Fig. 4). From January through April, small numbers of windowpane, ranging in size from 12 to 50 mm SL, were captured in the estuary, inlet, and ocean (Table 3, Fig. 4). Peak concentrations of spring- and fall-spawned demersal windowpanes occurred at different temperatures (Fig. 3). In June and July, mean daily surface water temperatures ranged from 18 to 24 C, while in November and December temperatures ranged from 7 to15 C. During most of the summer, temperatures in the estuary were warmer than those in the ocean, and during the winter, temperatures in the ocean were 1 2 C warmer than those in the estuary (Fig. 3) Settlement Further examination of the timing and location of windowpane settlement was estimated based on the transition from pelagic to demersal habitats and morphology (eye migration stage). The transition of both cohorts of windowpane from planktonic to demersal capture was dependent upon size in the estuary, inlet and ocean (goodness-of-fit tests, v 2 ¼ 128, P < 0:0001, v 2 ¼ 29:1, P < 0:0001, v 2 ¼ 30:4, P < 0:0001, respectively; Fig. 5). Settlement occurred at larger sizes and over a broader size range in the estuary compared to the inlet and ocean (Fig. 5). Metamorphic stages of spring- and fall-spawned windowpane differed depending on the type of gear they were collected with and the habitat they were collected in. Spring-spawned fish collected in the estuary with planktonic sampling equipment exhibited an even distribution of eye migration stages, with pre- through postmetamorphic individuals represented, however, those collected in the inlet and ocean exhibited only early stages of eye migration (pre-metamorphic to G stage) (Fig. 6b). Spring-spawned windowpane captured with demersal sampling equipment in the estuary had completed eye migration, while those in the inlet ranged from Hÿ to post-metamorphic stages (Fig. 6b). Postmetamorphic spring-spawned windowpanes were absent from oceanic collections. Most fall-spawned windowpanes, encompassing all stage of eye migration, were collected in the ocean (Fig. 6c and d). Planktonic collections of fall-spawned fish included primarily premetamorphic individuals, but also those that ranged from the Fÿ to Hþ stages of eye migration (Fig. 6c and d). Demersal fall-spawned windowpane most commonly exhibited later eye migration stages (I stage and post-metamorphic; Fig. 6c and d) Post-settlement distribution Demersal sampling for juvenile windowpane occurred from 1989 to 1998 in habitats containing sediments that ranged from 0.1 to 96.1% silt/clay content (Fig. 7). The highest densities of juvenile windowpanes (>15 and 120 mm SL), belonging to both cohorts, occurred at locations with sandy sediments ( % silt/ clay content). Spring-spawned juveniles were collected almost exclusively on sandy beaches within the estuary and the inlet in July, August and September (Figs. 4 and 7). The majority of fall-spawned juveniles were captured on sandy habitats in the inlet and ocean during November, December and January (Figs. 4 and 7). 4. Discussion 4.1. Sources of multiple cohorts This study provides evidence that confirms and augments reports from earlier investigations (Berrien & Sibunka, 1999; Morse & Able, 1995; Wilk et al., 1990) that two cohorts (spring and fall) of windowpanes are spawned, settle and grow in New Jersey waters. Evidence from this study is based on the timing of occurrence of windowpane larvae and juveniles belonging to
7 M.J. Neuman, K.W. Able / Estuarine, Coastal and Shelf Science 56 (2003) Fig. 4. Monthly length frequency distributions of windowpane (120 mm SL) captured in estuary (open bars, n ¼ 1298), inlet (shaded bars, n ¼ 838) and ocean (solid bars, n ¼ 341) habitat types in southern New Jersey from with planktonic and demersal sampling equipment. Note variation in y-axis scales. the spring and fall cohorts, but interpretations of the inter-cohort differences in the patterns of occurrence of these life stages would be incomplete without considering the temporal and spatial distribution of reproduction. Greater number of adults (<21 cm and presumably mature) and eggs are collected in the spring than in the fall (Berrien & Sibunka, 1999; Morse & Able, 1995). In addition, adults and eggs collected in spring
8 534 M.J. Neuman, K.W. Able / Estuarine, Coastal and Shelf Science 56 (2003) Table 3 Mean monthly densities, number per 1000 m 3 (1 SE) and standard lengths (1 SE) of juvenile windowpane collected along an estuarine to ocean corridor in southern New Jersey (estuary, n ¼ 54; inlet, n ¼ 296; and ocean, n ¼ 93) in 1991, 1992 and Beam trawl and beach seine collections are included Mean juvenile density (SE) Mean standard length (SE) Month Estuary Inlet Ocean Estuary Inlet Ocean January (0.22) (0.89) February (0.35) March (0.13) 0.45 (0.41) (5.74) April 0.17 (0.17) (0.48) (3.93) May (2.02) 0.48 (0.48) (16.14) June 2.85 (2.02) (6.64) 5.41 (3.34) (1.77) (1.45) (1.43) July (4.80) (7.47) 0.77 (0.43) (1.88) (1.76) (20.98) August 4.43 (1.22) 3.23 (1.22) 0.19 (0.19) (5.59) (3.19) September 0.17 (0.17) 2.75 (0.81) (4.43) October (0.23) 0.93 (0.44) (3.32) (5.18) November (0.44) 3.08 (1.54) (1.81) (0.79) December (4.03) (0.41) occur over a broader area and depth range, from the estuary (<10 m depth) out to the continental shelf edge (200 m depth), than fall occurring adults and eggs which are more limited in their distribution (from inner continental shelf depths >20 m to the 100 m isobath; Berrien & Sibunka, 1999; Milstein et al., 1977; Morse & Able, 1995). The higher abundance and more widespread distribution of spring-spawned larvae and juveniles compared to fall-spawned larvae and juveniles observed in this study is consistent with the abundance and distribution of adults and eggs reported in prior studies (Fig. 3a and b) Settlement The distribution of the smallest larvae was used to infer the timing and location of spawning. Likewise, the distributions of the largest, planktonic larvae and the smallest demersal windowpanes were used to infer the timing and location of settlement for both cohorts. In the fall, Fig. 5. Length frequency distributions of windowpane (30 mm SL) captured with planktonic (open bars) and demersal (solid bars) sampling equipment in the estuary ðn ¼ 229Þ, inlet ðn ¼ 269Þ and ocean ðn ¼ 277Þ in 1991, 1992 and Transitions in sampling equipment vulnerability of windowpane within each habitat type and with respect to increase in body size (SL mm) are shown below corresponding length frequency distributions. Normal probability curves (solid line) were fit to the binary data (open circles, planktonic; solid triangles, demersal) using probit analysis and mean sizes at the transition (1 SE) were generated. Goodness-of-fit tests revealed that the transition in sampling equipment vulnerability was dependent upon size of the individual in all three habitat types (v 2 ¼ 128, P < 0:0001, v 2 ¼ 29:1, P < 0:0001, and v 2 ¼ 30:4, P < 0:0001 in the estuary, inlet and ocean, respectively). Dotted lines shown mean sizes at which individuals advance from one character state to the next.
9 M.J. Neuman, K.W. Able / Estuarine, Coastal and Shelf Science 56 (2003) Fig. 6. Length and eye migration stage frequency distributions of spring-spawned (a,b) and fall-spawned (c,d) windowpane (30 mm SL) captured in the estuary ðn ¼ 134Þ, inlet ðn ¼ 265Þ and ocean ðn ¼ 263Þ with planktonic (open bars) and demersal (solid bars) sampling equipment during 1991, 1992 and Pre, pre-metamorphic; Post, post-metamorphic. Note variation in y-axis scales. planktonic and demersal windowpane of all sizes and developmental stages were most abundant in the ocean, suggesting that spawning, larval development, and settlement occur in ocean habitats. In the spring, the largest larvae, which exhibited a wide range of eye migration stages, occurred in the estuary and the smallest, pre-metamorphic larvae occurred in the ocean. This pattern of larval occurrence suggests that spring-spawning occurs in the ocean and that larger larvae subsequently move into the estuary. The location of settlement, however, is difficult to define. Demersal individuals were captured in the inlet and ocean in May, and captured in the estuary in June. Settlement in the ocean and inlet occurred at smaller sizes (7 8 mm SL) and earlier stages of eye migration (Hÿ, H and Hþ stages) than in the estuary. Abundance of demersal fish declined in the ocean by mid-summer, but continued to increase in the inlet and estuary. The temporal and spatial patterns of settlement observed for spring-spawned windowpane may be due to one or more of the following four explanations. First, planktonic windowpane may be entering the estuary in the spring, delaying settlement, and remaining in the plankton longer than individuals in inlet and ocean habitats. Delayed settlement among fishes occurs when larvae experience suboptimal environmental conditions, primarily cold water temperatures and/or inappropriate settlement habitat (Keefe & Able, 1993; Sekai, Tanangonan, & Tanaka, 1986). It is unlikely that springspawned windowpanes are delaying settlement in the estuary due to cold water temperatures given that temperatures have already risen to C (Fig. 3) by May June. Similarly, it is unlikely that spring-spawned windowpanes are delaying settlement in the estuary due to inappropriate settlement habitat, as the habitats change little from May to June. Second, sampling biases may influence our interpretations of the data. New windowpane settlers may be present in this estuarine system in spring, but the settlement area may not have been sampled thereby explaining the paucity of new settlers, ranging in size from 9 to 28 mm SL, in the estuary. Additionally, windowpane of these sizes grow quickly (0.6 mm per day; Neuman, Witting, & Able, 2001) limiting the time they are susceptible to capture by demersal sampling equipment. However, failure to sample the settlement area in this estuary will not explain other observations such as the presence of larger, more developmentally advanced planktonic windowpane inside the estuary compared to those in the inlet and ocean. Also, sampling biases due to different sampling equipment efficiencies, both with respect to the type of equipment and the time of collection, may affect the observed patterns. Ichthyoplankton sampling inside the estuary only occurred during the night, but sampling in the inlet and ocean occurred only during the day. If young windowpane migrate vertically to feed at night, as laboratory studies suggest (Neuman & Able, 1998), then a time-of-day sampling bias may explain why planktonic windowpanes captured inside the estuary were larger and developmentally more advanced than fish captured outside the estuary. However, a day/ night sampling bias cannot explain differences in the distribution of demersally captured windowpane because all demersal sampling occurred during the day. Third, windowpane settling inside the estuary may experience higher mortality than those settling outside the estuary. Higher mortality rates could result in the estuary if invertebrate crustaceans, known to be significant predators upon other species of settling flatfishes, are more abundant inside the estuary than in the inlet or ocean (van der Veer & Bergman, 1987; Witting & Able, 1995). This supposition would explain the absence of new settlers and the presence of larger fish inside the estuary in May, but would not explain the decline of larger settled windowpane in the ocean during late summer (Figs. 3b and 4). Finally, the most likely interpretation is that settlement occurs gradually in windowpane, with an initial settlement period in the inlet and ocean, a transitional period during which windowpanes re-enter the water column in order to move to near-shore habitats, and a third period when individuals adopt a permanent, demersal lifestyle. Such movement, aided by selective tidal
10 536 M.J. Neuman, K.W. Able / Estuarine, Coastal and Shelf Science 56 (2003) Fig. 7. Densities (mean 1 SE, solid line) of (a) spring-spawned ðn ¼ 1068Þ and (b) fall-spawned ðn ¼ 58Þ YOY windowpane (>15 and 120 mm SL) over substrates of varying % silt/clay content (dotted line) at 41 stations throughout Great Bay, Little Egg Harbor, Little Egg Inlet and the adjacent continental shelf from 1989 through stream transport, has been suggested to explain the patterns of distribution of other settling flatfishes such as European plaice (Pleuronectes platessa), summer flounder, Japanese flounder (Paralichthys olivaceous), California halibut (Paralichthys californicus), and European flounder (Platichthys flesus) (Creutzberg, Eltnick, & van Noort, 1978; Kramer, 1990; Raffaelli, Richner, Summers, & Northcott, 1990; Rijnsdorp, van Stralen, & van der Veer, 1985; Tanaka, Goto, Tomiyama, & Sudo, 1989; Weinstein, Weiss, Hodson, & Gerry, 1980). If windowpanes utilize mid-water habitats during resuspension, they would not be vulnerable to planktonic sampling equipment fished at the surface or demersal sampling equipment fished on the bottom. This hypothesis explains why larger and later stages of spring-spawned windowpane are captured with planktonic sampling equipment in the estuary, why demersal windowpanes are initially collected in the inlet and ocean, and why the density of demersal windowpane continues to increase in the inlet and estuary until July while their numbers begin to decline in the ocean during July and August. This hypothesis is supported by laboratory studies that found transitional stage windowpane (8 18 mm SL) spend significantly more time in the water column and less time buried than larger juveniles (32 89 mm SL) (Neuman & Able, 1998). As with spring-spawned individuals, there is some evidence to support the hypothesis that fall-spawned fish may re-enter the water column after the initial settlement event in November and December (Fig. 3a; Neuman et al., 2001). However, sampling effort was low during the winter months and care should be taken with this interpretation. If fall-spawned windowpanes are capable of moving back into the water column, they do not appear to do so until they reach sizes >25 mm SL, during the winter months (January April). With the information reported here, we can address the hypotheses of Morse and Able (1995) concerning distribution of windowpane on the inner continental shelf of the US (>10 m depth). They reported small numbers of large larvae (>8 mm) and newly settled juveniles in Middle Atlantic Bight planktonic and demersal collections and much higher numbers of large larvae and newly settled windowpane on Georges Bank. They offered two hypotheses to explain this geographical difference in size structure: (1) large larvae were unavailable because they transformed at smaller sizes in the Middle Atlantic Bight than on Georges Bank; and (2) larger larvae entered previously unsampled near-coastal or estuarine habitats (<10 m depth) that are available in the Middle Atlantic Bight, but not in Georges Bank. The data from this study support both hypotheses.
11 M.J. Neuman, K.W. Able / Estuarine, Coastal and Shelf Science 56 (2003) Newly settled spring-spawned windowpane captured in ocean and inlet habitats were small (7 8 mm), and larger larvae were found inside Middle Atlantic Bight estuaries, however, new settlers were not captured in the estuary. The most parsimonious explanation for the patterns observed in this study, and those of Morse and Able (1995), may be that windowpane initially settle in ocean and inlet locations, and then enters shallower, estuarine habitats, if available, during a transitional period through re-suspension and subsequent settlement. Differences between estuarine and ocean water temperatures may explain settlement differences between the spring and fall windowpane cohorts. Spring-spawned windowpane moved into the estuary when water temperatures there were 3 4 C warmer than in the ocean. Fall-spawned windowpane remained in the ocean when water temperatures were 1 2 C warmer there than in the estuary. Thus, windowpane may settle in habitats where water temperatures are warmest and presumably, fish growth is faster Post-settlement distribution The distribution of larger, spring-spawned YOY windowpane (>15 mm SL) appeared to be related to depth and substrate type. The highest densities of windowpane were recorded over sandy beach habitats in the lower portion of the estuary and the inlet, especially the shallow (1.5 m), sandy habitats around Tucker s Island, situated in Little Egg Inlet (Fig. 1). Estuarine and inlet beaches may provide important nursery areas for larger, spring-spawned YOY windowpane in near-coastal habitats and these habitats may be distinct from deeper inlet and ocean habitats where windowpane initially settles. Nursery areas exhibiting similar depth and substrate characteristics as those for windowpane have been described for other flatfishes such as European plaice, European flounder, and dab, Limanda limanda (Ansell & Gibson, 1990). 5. Summary Spring-spawned windowpane exhibit very different patterns of distribution during early life than fallspawned windowpane. Spring-spawned windowpanes are more abundant and grow more rapidly (Neuman, 1999; Neuman et al., 2001) than fall-spawned fish. These dissimilarities may be related to inter-cohort differences in the distribution of spawning adults and eggs, in behaviour among the larvae and juveniles, and/or in mortality rates among eggs, larvae and juveniles. Ultimately, these differences may affect the total contribution that each cohort makes to a given year class and play an important role in determining the recruitment dynamics of this species in the Middle Atlantic Bight, and potentially in other parts of its range. This study also raises important questions about how differential patterns of production and survival of multiple cohorts may affect the recruitment patterns of other temperate species (menhaden, Brevoortia tyrannus, spotted hake, Urophycis regia, and bluefish, Pomatomus saltatrix) that spawn more than once a year (Able & Fahay, 1998). Acknowledgements We thank the staff at the Rutgers University Marine Field Station (RUMFS), especially those who helped to collect windowpanes in the Jacques Cousteau National Estuarine Research Reserve at Mullica River Great Bay from 1989 to 1998 as part of their separate research: Stan Hales, Dale Haroski, Rich McBride, Pete Rowe and Dave Witting. We thank Tom ÔMotzÕ Grothues and Bobbie Zlotnik for reviewing earlier versions of this manuscript. This work was funded by a research assistantship through the Cooperative Marine Education and Research Program (CMER; NOAA award # NA37FE0443), a graduate research fellowship through the National Estuarine Research Reserve System (NERRS; NOAA award # NA77OR0236), the Manasquan River Marlin and Tuna Club, and the Institute of Marine and Coastal Sciences (IMCS), contribution number References Able, K. W., & Fahay, M. P. (1998). The first year in the life of estuarine fishes in the Middle Atlantic Bight (342 pp.). New Brunswick: Rutgers University Press. Able, K. W., Hoden, R., Witting, D. A., & Durand, J. B. (1992). Physical parameters of the Great Bay Mullica River Estuary (with a list of research publications). New Brunswick, NJ, USA: Rutgers University, Institute of Marine and Coastal Sciences (Technical Report 92-06). Allen, L. G. (1988). Recruitment, distribution, and feeding habits of young-of-the-year California halibut (Paralichthys californicus) in the vicinity of Alamitos Bay Long Beach Harbor, California, Bulletin of the Southern California Academy of Sciences 87, Ansell, A. D., & Gibson, R. N. (1990). Patterns of feeding and movement of juvenile flatfishes on an open sandy beach. In M. Barnes, & R. N. Gibson (Eds.), Trophic relationships in the marine environment (pp ). Aberdeen, Scotland: Aberdeen University Press. Berrien, P., & Sibunka, J. (1999). Distribution patterns of fish eggs in the United States northeast continental shelf ecosystem, (310 pp.). NOAA Technical Report, 145. Bigelow, H. B., & Schroeder, W. C. (1953). Fishes of the Gulf of Maine. U.S. Fish and Wildlife Services Fishery Bulletin 74, Chant, R. J., Curran, M. C., Able, K. W., & Glenn, S. M. (2000). Delivery of winter flounder Pseudopleuronectes americanus larvae to settlement habitats in coves near tidal inlets. 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12 538 M.J. Neuman, K.W. Able / Estuarine, Coastal and Shelf Science 56 (2003) Creutzberg, F. A. T., Eltnick, G. W., & van Noort, G. J. (1978). The migration of plaice larvae Pleuronectes platessa into the western Wadden Sea. In D. S. McLusky, & A. J. Berry (Eds.), Physiology and behaviour of marine organisms (pp ). Oxford, England: Pergamon Press. Curran, M. C., & Able, K. W. (2002). Annual stability in use of coves near inlets as settlement areas for winter flounder (Pseudopleuronectes americanus). Estuaries. Dery, L., & Livingstone, R., Jr. (1982). Windowpane. In M. D. Grosslein, & T. Azarovitz (Eds.), Fish distribution. MESA N.Y. bight atlas monograph 15 (pp ). Albany, NY, USA: NY Sea Grant Institution. Durand, J. B. (1984). Nitrogen distribution in New Jersey coastal bays. In M. J. Kennish, & R. A. Lutz (Eds.), Lecture notes on coastal and estuarine studies, ecology of Barnegat Bay, New Jersey (pp ). New York, USA: Springer-Verlag. Durand, J. B. (1988). Field studies in the Mullica River Great Bay estuarine system (138 pp). New Brunswick, NJ, USA: Center for Coastal and Environmental Studies, Rutgers University. Grover, J. J., Eggleston, D. B., & Shenker, J. M. (1998). Transitions from pelagic to demersal phase in early-juvenile Nassau grouper, Epinephelus striatus: pigmentation, squamation, and ontogeny of diet. Bulletin of Marine Science 62, Keefe, M., & Able, K. W. (1993). Patterns of metamorphosis in summer flounder, Paralichthys dentatus. Journal of Fish Biology 42, doi: /jfbi Kneib, R. (1993). Growth and mortality in successive cohorts of fish within an estuarine nursery. Marine Ecology Progress Series 94, Kramer, S. H. (1990). Growth, mortality, and movements of juvenile California halibut Paralichthys californicus in shallow coastal and bay habitats of San Diego, California. Fishery Bulletin 89, McBride, R. S., Fahay, M. P., & Able, K. W. (2002). Larval and settlement periods of the northern searobin Prionotus carolinus and the striped sea robin P. evolans. Fishery Bulletin 100, Milstein, C. B., Thomas, D. L., Garlo, E. V., Swiecicki, F. A., Swiecicki, D. P., Burns, F. A., Howells, R. G., Danila, D. J., Bieder, R. C., Beckler, R. J., Saffian, N. L., Prendergast, P. A., Hamer, D. P., Tatham, T. R., & Branderberg, W. C. (December, 1977). Summary of ecological studies for in the bays and other waterways near Little Egg Inlet and in the ocean in the vicinity of the proposed site for the Atlantic generating station, N.J. progress report for January December, Bulletin no. 18, Ichthyological Associates, Inc. Morse, W. W., & Able, K. W. (1995). Distribution and life history of windowpane, Scophthalmus aquosus, off the northeastern United States. Fishery Bulletin 93, Neuman, M. J. (1999). Early life history and ecology of windowpane, Scophthalmus aquosus, in the Middle Atlantic Bight: ontogenetic transitions during the first year of life in a bi-modal spawner. PhD dissertation. New Brunswick, NJ, USA: Rutgers, the State University of New Jersey. Neuman, M. J., & Able, K. W. (1998). Experimental evidence of sediment preference by early life history stages of windowpane (Scophthalmus aquosus). Journal of Sea Research 40, Neuman, M. J., Witting, D. A., & Able, K. W. (2001). Relationships between otolith microstructure, otolith growth, somatic growth and ontogenetic transitions in two cohorts of windowpane, Scophthalmus aquosus. Journal of Fish Biology 58, doi: /jfbi Nordstrom, K. F. (1992). Estuarine beaches (225 pp). London: Elsevier Science. Raffaelli, D., Richner, H., Summers, R., & Northcott, S. (1990). Tidal migrations in the flounder (Platichthys flesus). Marine and Freshwater Behaviour and Physiology 16, 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. Transactions of the American Fisheries Society 114, Rogers, C. W., Gunderson, D. R., & Armstrong, D. A. (1989). Utilization of a Washington estuary by juvenile English sole Parophrys vetulus. Fishery Bulletin 86, SAS Institute Inc. (1990). SAS procedures guide. (3rd ed. Version 6), SAS Institute, Cary, NC, USA. Sekai, T., Tanangonan, J. B., & Tanaka, M. (1986). Temperature influence on larval growth and metamorphosis of the Japanese flounder Paralichthys olivaceous in the laboratory. Bulletin of the Japanese Society of Scientific Fisheries 52, Szedlmayer, S. T., & Able, K. W. (1996). Patterns of seasonal availability and habitat use by fishes and decapod crustaceans in a southern New Jersey estuary. Estuaries 19, Tanaka, M., Goto, T., Tomiyama, M., & Sudo, H. (1989). Immigration, settlement and mortality of flounder (Paralichthys olivaceous) larvae and juveniles in a nursery ground, Shijiki Bay, Japan. Netherlands Journal of Sea Research 24, Thorisson, K. (1994). Is metamorphosis a critical interval in the early life of marine fishes? Environmental Biology of Fishes 40, van der Veer, H. W., & Bergman, M. J. N. (1987). Predation by crustaceans on newly settled 0-group plaice Pleuronectes platessa population in the western Wadden Sea. Marine Ecology Progress Series 35, Weinstein, M. P., Weiss, S. L., Hodson, R. G., & Gerry, L. F. (1980). Retention of three taxa of postlarval fishes in an intensively flushed tidal estuary, Cape Fear River, North Carolina. Fishery Bulletin 78, Wennhage, H. (1999). Recruitment processes in the flatfish Pleuronectes platessa (L.): larval supply, habitat selection and predator prey interactions at settlement. PhD dissertation. Sweden: Go teborg University. 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. Fishery Bulletin 88, Witting, D. W. (1995). Settlement of winter flounder Pleuronectes americanus, in a southern New Jersey estuary: spatial and temporal dynamics and the effect of decapod predation. PhD dissertation. New Brunswick, NJ, USA: Rutgers, the State University of New Jersey. Witting, D. W., & Able, K. W. (1995). Predation by sevenspine bay shrimp Crangon septemspinosa on winter flounder Pleuronectes americanus during settlement: laboratory observations. Marine Ecology Progress Series 123,
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