L
Journal of Experimental Marine Biology and Ecology 242 (1999) 211–231
www.elsevier.nl / locate / jembe
Predation by striped searobin (Prionotus evolans, Triglidae)
on young-of-the-year winter flounder (Pseudopleuronectes
americanus
, Walbaum): examining prey size selection and
prey choice using field observations and laboratory
experiments
*
J.P. Manderson , B.A. Phelan, A.J. Bejda, L.L. Stehlik, A.W. Stoner
Behavioral Ecology Branch NOAA /National Marine Fisheries Service, James J. Howard Marine Sciences
Laboratory, Highlands, NJ 07732, USA
Received 23 March 1999; received in revised form 28 June 1999; accepted 19 July 1999
Abstract
Laboratory experiments and field observations in shallow water habitats in the Navesink River / Sandy Hook Bay estuarine system (NSHES), New Jersey, USA, were used to examine the predator–prey relationship between the striped searobin (Prionotus evolans: Linnaeus) and young-of-the-year (YOY) winter flounder (Pseudopleuronectes americanus: Walbaum). Striped sea robins (121–367 mm total length [TL]) were present in Sandy Hook Bay but absent from the Navesink River in biweekly gillnet surveys conducted from May through October, 1998. However, juvenile winter flounder were present throughout the estuary during periodic beam trawl surveys. Although mysids and sand shrimp (Crangon septemspinosa, Say: 10–49 mm TL) were the numerically predominant prey of searobins, winter flounder (15–57 mm TL) accounted for an average of 17% (63) of prey by weight and were found in the diets of 69% of predators collected in June. In the laboratory, searobins (212–319 mm TL) presented with a range of winter flounder sizes (30–114 mm TL) selected prey ,70 mm TL (24% of predator TL) and maximum prey size appeared to be constrained by predator esophageal width. When winter flounder (40–60 mm TL) and sand shrimp (30–50 mm TL) were offered at different densities to searobins, the predators fed opportunistically, consuming the prey in proportions similar to initial relative abundances. Laboratory observations showed that searobins rely on modified pectoral finrays to detect, flush, and occasionally excavate buried winter flounder. Our field and laboratory observations indicate that striped searobins consume large numbers of winter flounder in vulnerable size classes (15–70 mm TL) in habitats where the two species co-occur. Patterns in the distribution of the two species in the NSHES suggest that predation probably varies spatially in the estuary, with flounder more at risk in nurseries in Sandy Hook Bay than in the Navesink River, which may serve as a spatial
*Corresponding author. Tel.:11-732-872-3057; fax:11-732-872-3128.
E-mail address: [email protected] (J.P. Manderson)
refuge for winter flounder from searobin predation during some years. 1999 Elsevier Science B.V. All rights reserved.
Keywords: Predator–prey; Prey choice; Size selection; Trigilid; Flatfish predator
1. Introduction
Predation risk is a critical factor determining the suitability of nursery habitats, including those used by commercially important flatfish (Gibson, 1994). Following settlement, flatfish face a suite of invertebrate, fish and bird predators that typically narrows in composition as the prey grow. While newly settled flatfish suffer high mortality from crustacean predators (Pihl and van der Veer, 1992; Seikai et al., 1993; Witting and Able, 1995), later stage juveniles are primarily preyed upon by piscivorous fishes (Ansell and Gibson, 1993; Ellis and Gibson, 1995, 1997; Gibson and Robb, 1996; Bax, 1998). Variations in the identity and capability of piscivorous fish in flatfish nurseries, along with changes in the relative size of predators and prey, are likely to result in important temporal and spatial variations in predation intensity. While relationships between predatory fish and European flatfish have been studied (Gibson and Robb, 1996; Bax, 1998), there have been no systematic studies of the potential impacts of piscivorous fish in northwest Atlantic flatfish nurseries.
The striped sea robin (Prionotus evolans) is common on soft-bottom continental shelf and estuarine habitats in the Mid-Atlantic Bight and co-occurs with a number of flatfish including the commercially important winter flounder (Pseudopleuronectes americanus) (McBride and Able, 1994; Rountree and Able, 1997; McBride et al., 1998). Although young-of-the-year (YOY) winter flounder (and other flatfishes) have been reported in the searobin’s diet (Marshall, 1946; Richards et al., 1979), the interaction between the two species has not been studied. Small flatfish are known dietary components for a number of other triglid species (searobins and gurnards) (Richards et al., 1979; Meyer and Smale, 1991; Ellis and Gibson, 1995). Triglids are opportunistic predators that use modified anterior pectoral fin rays equipped with tactile and chemosensory receptors to search soft substrata for epibenthic prey, particularly crustaceans (Bardach and Case, 1965; Silver and Finger, 1984; Ross, 1977). The ability of triglids to use finrays to search for and flush prey could make them particularly effective predators of juvenile flatfishes, which use soft sediment as refuge and burial as an escape response (Gibson and Robb, 1992; Minami et al., 1994).
In this study we report on the dietary patterns of striped searobins collected in shallow-water habitats in a mid-Atlantic estuarine system. We also present results of laboratory experiments testing the following null hypotheses:
• (1) H : Prey size selectivity of striped searobins for juvenile winter flounder prey is0
similar in the presence and absence of fine sand subtratum.
• (2) H : Searobins consume equivalent numbers of winter flounder and sand shrimp0
J.P. Manderson et al. / J. Exp. Mar. Biol. Ecol. 242 (1999) 211 –231 213
• (3) H : The proportions of winter flounder and sand shrimp consumed by searobins0
are not different from the proportions of the two prey at the start of experiments.
Finally, we report on video observations of the search and attack strategies of searobins feeding on juvenile winter flounder.
2. Materials and methods
2.1. Field collections and stomach content analysis
Striped searobins were collected in the Navesink River / Sandy Hook Bay Estuarine System (NSHES) located at the apex of the mid-Atlantic Bight in central New Jersey (Fig. 1). The Navesink River has one primary freshwater source that produces a downstream salinity gradient (10–30‰) extending from the head of the river to the north end of Sandy Hook where Sandy Hook and Raritan Bays meet the Atlantic Ocean.
Average depth also increases along the downstream axis of the study area, from ¯1 to
15 m below mean low water (bMLW). Tides are semidiurnal in the system with a range of approximately 1.4 m.
Thirteen stations with bottom depths #3 m bMLW were established for gillnet
sampling throughout the NSHES (Fig. 1). Stations in the river generally had finer grained sediments, and more vegetation (Ulva lactuca, Zostera marina, Ceramium spp.) than those located in the bay, which were adjacent to sandy beaches.
Gillnets were fished at the stations biweekly, for 2 h during daytime high tides, from late May through the beginning of November 1998. The total lengths (TLs, mm) of searobins collected in gillnets were measured and their stomachs excised for dietary analysis. Diet items were identified to species when possible, enumerated, and weighed to the nearest 0.1 g to estimate contributions of each prey to the total prey in searobin stomachs. The TLs of sand shrimp (rostrum to end of telson) and standard lengths (SLs) of winter flounder in stomachs were measured to examine predator–prey size relation-ships.
2.2. Laboratory experiments
2.2.1. Collection and maintenance of experimental animals
Striped searobins were collected with an otter trawl and winter flounder and sand shrimp were collected with a haul seine in the NSHES. Animals were transported to the Howard Marine Sciences Laboratory, Highlands, NJ, USA and maintained in aquaria with a continuous flow of ambient seawater pumped from Sandy Hook Bay
(temperature515.6–25.48C; salinity520.5–25.5‰). A 15:9 h light:dark cycle (day5
0500–2000 EST) was maintained in all laboratories. Aquaria were provided with 2–3
cm of washed sand substratum (0.5 mm, 0.82 f, sorting coefficient50.33) except
¯
where noted below. Searobins ranging from 212 to 320 mm TL (n523, x wt5229 g,
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experiments. Prey were also fed ad libitum; flounder with live Artemia and chopped clam and shrimp with frozen fish.
Predators were starved for 24 h before they were used in experiments. All of the prey were weighed (g), measured (winter flounder: TL and SL; sand shrimp TL) and fed not more than 3 h before they were exposed to predators.
2.2.2. Winter flounder size selection
Searobin selectivity for sizes of flounder prey was examined in circular tanks (1.8 m
diam.30.5 m deep) with and without sand substratum (Table 1). Starved searobins
(n512, 212–309 mm TL) were acclimated to tanks for 20 h. One hour before predators
were exposed to prey, searobins were isolated in arenas within opaque PVC cylinders
(0.7 m diam.30.6 m deep). Fourteen prey, which included two individuals in 10-mm
size classes ranging from 30 to .90 mm TL, were introduced to the area outside the
cylinders. Predators were released after 1 h and allowed to feed for 2 h (0900–1100 EST). Experiments were terminated by removing predators and draining the arenas. The sand substratum was searched with garden rakes to recover surviving flounder.
Gape sizes of freshly killed searobins (n513, 227–320 mm TL) were measured to
determine the morphological constraint on maximum prey size. Mouth width was measured with Vernier calipers as the distance between the maxillary bones in the mouth interior. To measure esophagus width, predators were decapitated at the cleithrum and calipers were inserted into the esophagus which was stretched by applying consistent pressure to the calipers. Total length and body depth (BD mm, maximum dorso-ventral
distance) were measured for flounder (n5346, 28–100 mm TL) to determine the
relationship between prey body depth and predator gape size.
Table 1
Design of laboratory experiments performed to examine relationship between striped searobin predators and winter flounder and sand shrimp prey; effective replicates were those in which prey were consumed
Experiment / Replicates No. of Temperature
treatment (Effective replicates) prey (8C)
a Flounder size selection
Sand present 15 (11) 14 18-22
Sand absent 14 (12) 14 18-22
b Prey selection
Prey ratio, period (no. flounder: no. sand shrimp)
10:10, Night 20 (15) 20 16-18
10:10, Day 20 (17) 20 16-18
5:15, Day 20 (9) 20 16-18
15:5, Day 20 (10) 20 16-18
b Behavioral observations
Searobin-winter flounder 10 (5) 10 18-22
a
Flounder ranged in size from 30 to 120 mm TL. b
2.2.3. Day–night prey selection
Diurnal variation in prey selectivity was determined by offering equal numbers of
flounder (n510) and shrimp (n510) to individual searobins (n520, 212–309 mm TL,
112–320 g) in 3 h day (1000–1300 EST) and night (2000–2300 EST) experiments (Table 1). Twenty predators were exposed to each treatment. The flounder used were within the size range of fish (40–60 mm TL) most frequently consumed in the size selection experiments. Shrimp were sized (30–50 mm TL) to match flounder as closely
as possible. Predators were introduced to tanks (2.5 m diam.30.5 m deep) with sand
substratum and fed ad libitum for the first 24 h of a 48-h acclimation period. Searobins were isolated within PVC cylinders and prey were introduced to the tanks in the same manner as in the size selection experiments. Experiments were terminated by removing predators, draining arenas, and sieving the substratum through 3-mm mesh to recover surviving prey.
2.2.4. Prey switching
The effect of relative prey density on searobin prey selection was examined by presenting three prey ratios (no. flounder:no.shrimp; 5:15, 10:10, 15:5) to individual
predators (n520; 212–309 mm TL) in 3 h experiments (Table 1). Switching
experiments were performed during the day (1000–1300 EST) because time of day did
not significantly (P50.09) influence predation rate or prey choice in the day–night
selection experiments (see Results). Equal numbers of searobins (n55) were exposed to
the 5:15 and 15:5 prey ratios in four trials producing 20 replicates per treatment. We used the daytime treatment of the day–night prey selection experiment as the 10:10 treatment in the switching experiment because switching experiments immediately followed the day / night selection experiment and experimental protocols were identical.
2.2.5. Behavioral observations
Videotaped observations of individual searobins (n510, 228–309 mm TL) feeding
on flounder (40–60 mm TL) were made in glass fronted rectangular tanks (2.5 m
long30.8 m wide 30.5 m deep) during 2-h daytime experiments (0800–1000 EST;
Table 1). Predators were isolated within the tanks in PVC cylinders and ten flounder were allowed to acclimate to the areas outside the cylinders for 1 h. Predators were then released and exposed to prey for 2 h. At the end of trials, the predator was removed and all surviving prey were collected.
Videotapes were analyzed to quantify: (1) the percent of time searobins spent ‘walking’ on or probing the substratum with modified pectoral fin rays and potentially searching for prey, (2) the number of attacks and (3) the location (bottom or water column) where attacks occurred.
2.3. Statistical analysis
2.3.1. Predator–prey body size relationships
Predator–prey body size relationships were explored using the quantile regression
technique described by Scharf et al. (1998), and implemented with STATA statistical
J.P. Manderson et al. / J. Exp. Mar. Biol. Ecol. 242 (1999) 211 –231 217
minimum and maximum prey size with changes in predator size using least absolute values regression with bootstrapped estimates of coefficient standard errors. We used the rule
n.10 /q
to determine quantiles ( q) reflecting trends in minimum and maximum prey size given sample size (n) (Scharf et al. 1998). Total length (mm) was the size parameter used in all regressions. Total lengths of flounder consumed by searobins in the field were estimated from measured standard lengths using the regression equation published in Able and Fahay (1998)
TL51.213 (SL)2 0.447
2.3.2. Winter flounder size selection
The nonlinear relationship between prey size and mortality prevented the use of a linear logistic model to test for the effects of prey size and substratum type on prey selectivity. Therefore we used logistic generalized additive models (GAMs) with spline smoothers (S-plus 4.5, 1997) to nonparametrically model the effects of prey size on the mortality of flounder in the presence and absence of sand. Logistic GAMs use the ratio of response frequencies (logits) and scatterplot smoothers to fit data-defined and unspecified functions to the relationship between response and predictor variables (Hastie, 1993). Since strong predator–prey body size relationships were not evident (see Results), replicates in which prey were consumed were pooled within treatments. Individual fish were scored as live or dead and these response frequencies were used in GAMs constructed independently for the two substrata with prey size as the predictor variable. The strength of the relationship between prey size and mortality were assessed
2
with approximate x tests (Hastie and Tibshirani, 1990; Hastie, 1993).
2.3.3. Day–night prey selection and prey switching
A two-way ANOVA was used to test for the effects of prey species (flounder / shrimp) and experimental period (day / night) on searobin prey consumption in the day–night selection experiments. Only replicates in which searobins consumed prey were used in
this analysis. Chessons ai (with food depletion; Chesson, 1983) was calculated for
replicates in which two or more prey were consumed, and used as the prey selectivity
index in the switching experiment. The null hypothesis of no prey selection (a 5 a 5i j
0.5) was tested at each ratio using a t-test and Bonferroni probability adjustment
(P,0.05 / 350.017) to guard against multiple testing errors.
3. Results
3.1. Field studies
3.1.1. Patterns of searobin abundance and diet composition
Striped searobins (n578; 121–367 mm TL) were collected in shallow water gillnets
Two size classes of fish (180–240 mm, 270–370 mm TL) were present in June, while fish collected in July and August were primarily from a single class (190–280 mm TL) (Fig. 2). Searobins were collected at four stations in Sandy Hook Bay, but were absent from the Navesink River (Fig. 1).
Sand shrimp was the dominant prey of searobins occurring in 81% of stomachs (Table 2). Mysids and YOY winter flounder were also common in diets in which amphipods (primarily Ampelisca sp. and Gammarus sp.) and lady crabs (Ovalipes ocellatus) also
occurred. Other prey, including blue crabs(Callinectes sapidus), xanthid crabs, and blue
mussels (Mytilus edulis), were present infrequently (#three stomachs).
Searobin diets were substantially different in June than in July and August (Table 2). In June, sand shrimp was the dominant prey and as many as 18 shrimp were consumed by individual predators. Winter flounder were ranked second in importance in June and occurred in 69% of stomachs. Searobins with flounder in stomachs were collected at three stations (Fig. 1a) and, in a sample of 26 predators, 85% of the searobins had
consumed an average of 360.6 flounder (maximum511). With one exception, flounder
J.
Frequency of prey occurrence and contribution to the total prey weight in the diets of striped searobins collected in shallow water gillnets in NSHES in 1998
Prey June (n536) July-August (n539) September-October (n53) Total (n578)
species Mean % Mean % Mean % Mean %
% by wt. Frequency % by wt. Frequency % by wt. Frequency % by wt. Frequency
(SE) (n) (SE) (n) (SE) (n) (SE) (n)
Pseudo- 17.7 68.6 1.5 2.56 0.0 0.00 8.8 32.5
pleuronectes (3.0) (24) (1.5) (1) (0) (1.8) (25)
americanus
Crangon 61.1 94.3 33.5 74.4 0.0 0.00 44.7 80.5
septemspinosa (4.8) (33) (5.8) (29) (0) (4.1) (62)
Mysids 8.6 57.1 52.4 71.8 0.0 0.00 30.5 57.1
(2.4) (20) (6.8) (28) (0) (4.4) (48)
Amphipods 0.6 31.4 6.2 25.64 0.0 0.00 3.4 27.3
(0.4) (11) (3.1) (10) (0) (1.6) (21)
Ovalipes 0.0 0.0 3.9 10.26 33.3 33.33 3.3 6.5
ocellatus (2.0) (4) (33.3) (1) (1.6) (5)
Other 9.1 45.7 2.6 7.7 33.3 33.3 6.7 ,3.90
were absent from searobin diets in July and August when mysids were the dominant prey (Fig. 1b).
3.1.2. Predator–prey body size
Searobins (188 –350 mm TL) consumed winter flounder ranging in size from 15 to 57
mm TL (n582; 12–48 mm SL, 5.4–24.3% of predator TL; Fig. 3a). Although slopes of
regressions estimating minimum and median prey sizes (15th and 50th quantiles) were significant, the coefficients were small, suggesting that the predator–prey size relation-ships were weak (Table 3a). Although too few searobins were collected to permit a
rigorous analysis (n535), the contribution of flounder to searobin diets did not appear to
vary with predator size.
Sand shrimp found in searobin stomachs (181–354 mm) ranged in size from 10–49
mm in total length (n5380; 4.4–17.1% of predator TL; Fig. 3b). Predator–prey body
size relationships were significantly positive at all quantiles tested (Table 3a) but the
J.P. Manderson et al. / J. Exp. Mar. Biol. Ecol. 242 (1999) 211 –231 221 Table 3
Estimates of slopes and intercepts from quantile regressions performed to determine body size relationships reflecting maximum, median, and minimum prey size for searobins (a) collected in the field and (b) used in laboratory experiments examining size selection
a
Quantile Slope estimate (6SE )b Intercept
(a) Field collections Winter flounder (n582)
ns
85th 0.02 (60.04) 31.71** (610.36)
50th 0.04* (60.02) 18.19** (66.23)
ns
50th 0.05*** (60.01) 4.80 (62.86)
ns
5th 0.03*** (60.01) 1.86 (61.72)
(b) Laboratory experiments with winter flounder prey Sand absent (n569)
ns ns
85th 20.07 (60.20) 66.22 (641.16)
ns ns
50th 20.08 (60.08) 51.85 (620.05)
ns
SE , boot strapped estimate of standard error. See methods for formula used to select quantilesb representing maximum and minimum prey size given sample sizes. *P,0.05; **P,0.01; ***P,0.001; ns, not significant.
slope estimating maximum prey size (95th quantile) was significantly higher than the
slope for minimum prey size (5th quantile; F535.53, df51,758; P,0.001). This
pattern suggests that although larger searobins consumed increasingly large shrimp, they continued to feed on small prey.
3.2. Laboratory experiments
3.2.1. Winter flounder size selection
Total consumption of flounder by searobins averaged 4.5 prey per experiment
(SE53.2, range50–10 prey) and was not influenced by the presence of sand (t-test:
t5 20.177, df526, P50.86). Searobins fed in 79% of replicates. Prey as large as 110
mm TL were eaten (40% of predator body length), but the predators failed to consume the largest prey in any replicate (Fig. 4).
Searobin size did not influence the size of prey consumed in the laboratory (Table 3b). Slopes of quantile regressions were not significant except at the 15th quantile in the absence of sand, where the coefficient was small. Estimates of maximum prey size for flounder (85th quantile) were 70.4 and 62.8 mm TL in the presence and absence of sand (25 and 24% of predator length).
Fig. 4. Body size relationships between striped searobins and winter flounder consumed in laboratory size selection experiments conducted (a) with and (b) without sand substratum. Closed circles indicate prey consumed and open circles prey which survived. Lines indicate estimated maximum prey size (mm TL) for winter flounder if mouth width (M) or esophageal width (E) imposed a morphological constraint on prey size (see Table 5).
mouth widths (33–56 mm) were larger than esophageal widths (24–30 mm) and increased more dramatically with increases in predator total length (Table 4). Based on predator length / gape and prey length / body depth relationships, predictions of maximum flounder size ranged from 120 to 173 mm TL (33–56 mm BD) if mouth width determined the maxima and from 73 to 88 mm TL (24–30 mm BD) if esophageal width determined the maxima. The largest flounders consumed were at least 39 mm TL smaller than predicted by mouth width.
Flounder mortality was strongly influenced by their size particularly in the presence of sand (Table 5, Fig. 5). Mortality probabilities estimated using logistic GAMs followed
J.P. Manderson et al. / J. Exp. Mar. Biol. Ecol. 242 (1999) 211 –231 223 Table 4
Results of linear regressions performed to determine the relationships between searobin total length (n513, 227–320 mm TL) and mouth and esophageal widths (mm), and between winter flounder total length (TL mm) and body depth (n5346, 30–110 mm TL)
2
Dependent variable Effect Coefficient t P r
(SE)
Searobin mouth width Intercept 210.587 21.130 0.282 0.795
(mm) (9.367)
Searobin length 0.218 6.651 ,0.001
(TL mm) (0.033)
Searobin esophageal width Intercept 9.714 1.726 0.112 0.411
(mm) (5.629)
Searobin length 0.059 2.948 0.013
(TL mm) (0.020)
Flounder length Intercept 6.792 9.407 ,0.001 0.930
(TL mm) (0.722)
Flounder body depth 2.856 67.556 ,0.001
(mm) (0.042)
flounder in the 40–50 mm size class in the absence of sand and 65% (SE53.5) for the
50–60 mm size class when sand substratum was present. Although mortality declined for larger sized flounders in both treatments, substratum type appeared to influence the likelihood that searobins consumed fish in the size classes. The mortality curve for flounder on sand substratum was shifted to the right of the curve for fish without sand,
suggesting that larger fish (50–70 mm) were more at risk on sand, while small fish (,50
mm) were more vulnerable when sand was absent.
3.2.2. Day–night prey selection
More searobins fed (day: n517; night: n515) and slightly more flounder were
consumed than sand shrimp during the daytime treatment (Fig. 6a). However, the effects
of prey type and diurnal period were not significant at the traditional P,0.05 level in
the ANOVA (Table 6).
Table 5
Fig. 5. (a) Proportion of total prey consumed and (b) GAM predictions of mortality for winter flounder size classes in laboratory experiments of searobin size selectivity with and without sand substrata. Error bars indicate 2 standard errors in probability plot.
3.2.3. Prey switching
Searobins consumed shrimp and flounder in proportions which were not different
from initial relative prey densities (Fig. 6b; Table 6b). t-Tests on Chessonsa showed no
prey selectivity at all three ratios when a Bonferroni correction was applied (critical
P50.017). Predators consumed 10% or more prey offered in >9 replicates for each
prey ratio, and as many as 13 winter flounder and nine sand shrimp were consumed in 15:5 and 5:15 treatments.
3.2.4. Predator behavior
Searobins fed in half of the 2 h trials (5 of 10) and individual predators consumed as
¯
many as ten flounders (x55.4). Flounder were ingested head or tail first and consumed
whole. An average of 65% (627) of attacks (total n542) resulted in captures, and most
J.P. Manderson et al. / J. Exp. Mar. Biol. Ecol. 242 (1999) 211 –231 225
Fig. 6. Results of (a) day–night prey selection and (b) daytime prey switching experiments examining striped searobin selection for winter flounder and sand shrimp in the laboratory.
number of flounder consumed was significantly correlated (Pearson’s r50.85, P5
0.002) with the time predators spent ‘walking’ on or probing the substratum with modified pectoral fin rays and thus potentially searching the substratum for prey. Prey were flushed from the sediment as a result of this behavior in 55% of attacks. Three searobins exhibited ‘digging’ behavior in which they anchored themselves with posterior pectoral fin rays and moved the sediment with anterior free fin rays. Buried flounder were flushed from sand substratum as a result of this behavior and attacked.
4. Discussion
Table 6
(a) Results of 2-way ANOVA test for the effects of prey type and time of day on selection of sand shrimp and winter flounder by searobins in the day-night prey selection experiment; (b) results of t-tests for searobin prey selection (Chessons a) for winter flounder and sand shrimp at the three ratios in the daytime switching
a experiment
(a) Source of variation Degrees of freedom Mean square F P
Prey species 1 13.825 3.619 0.062
Day / night 1 3.036 3.063 0.085
Interaction 1 5.700 1.492 0.277
Error 60 3.820
(b) Prey ratio (flounder: shrimp) Chessonsa(mean6SE) t P
Flounder Shrimp
15:5 9 0.47160.093 0.52960.093 0.225 0.827
10:10 15 0.62360.090 0.37760.090 1.367 0.192
5:15 8 0.28160.129 0.71960.129 2.352 0.047
a
Only replicates in which two or more prey were consumed were included in the analysis. Chessons a values50.5 indicate no selection. Bonferroni correcteda 50.05 / 350.017.
laboratory (Gibson, 1994; Keefe and Able, 1994; Moles and Norcross, 1995; Neuman and Able, 1998). These preferences are thought to be related, in part, to the refuge that soft substrata provide to flatfish that use burial and crypsis to evade predators (Kruuk, 1963; Lanzing, 1977; Gibson and Robb, 1992; Ellis et al., 1997). However, the efficacy of prey escape behavior is a function of the search and attack strategies of specific predators. Our laboratory experiments, along with studies of the structure and function of triglid anterior pectoral fin rays, suggest that soft sediments are relatively ineffective refuges from searobins for small burrowing animals like juvenile flounder.
Striped searobins use pectoral finrays to search for, flush, and occasionally excavate buried flounder prey. In our video observations, more flounder were consumed in trials in which predators spent more time ‘walking’ on the substratum, and several searobins were observed ‘digging’ in the sand with fin rays prior to attacks. These behaviors resulted in the flushing of flounder buried in the sand or at least cryptically colored. Our observations are consistent with several studies identifying triglid pectoral finrays as sensory appendages used during feeding. Searobins have previously been observed manipulating the substratum with finrays during feeding (Goode, 1884; Morrill, 1895) and are known to exhibit strong neurological responses and ‘digging’ behavior when finrays are exposed to mechanical stimulation, food, and amino acids common in the tissues of marine invertebrates and fish (Bardach and Case, 1965; Silver and Finger, 1984).
Our winter flounder size selection experiments support the hypothesis that burial is relatively ineffective against searobin predation. All sizes of flounder used in these
experiments (302901 mm TL) were capable of burying in fine sand (0.5 mm; personal
J.P. Manderson et al. / J. Exp. Mar. Biol. Ecol. 242 (1999) 211 –231 227
in the presence and absence of sand. In their study, however, mortality was lower for flatfish exposed to a pelagic predator (pollack) on sand. The authors concluded that the success of burial as an escape strategy for juvenile plaice was contingent on the search and attack strategies unique to the specific predators (see also Minello et al., 1987).
Although total prey consumption did not vary with substratum type, the presence of sand influenced the vulnerability of larger sized flounders to searobin predation. Mortality in larger flounder (50–70 mm TL) was slightly higher in sand than without sand, while small flounder (30–50 mm TL) were more vulnerable when sand was absent. Although we were unable to videotape encounters, substratum type may have modified predator and prey behaviors in several ways. In the absence of sand, searobins have difficulty using finrays and appear to rely on vision and swimming to find prey (personal observation). Small flounder may have suffered higher mortality in the absence of sand because flight was the only available escape response and prey swimming speeds, which increase with increasing body size in flatfishes (Williams and Brown, 1992; Gibson and Johnston, 1995), determined mortality. When sand was available, flounder may have resorted to burial or crypsis, delaying flight to avoid detection by predators. These behaviors may have reduced the reactive distances of larger prey to a degree that allowed searobins to detect and capture them on sand. Ellis et al. (1997) showed that the presence of sand reduced the reactive distance of juvenile sole (Solea
solea) by 50%, and more buried fish failed to respond to an artificial predator, than in
treatments without sand substratum.
We found no evidence of selective feeding by striped searobins in our day / night prey selection and daytime switching experiments. In all experiments, predators consumed similarly sized flounder and shrimp in proportions equivalent to their initial relative abundances. Searobins appeared to used pectoral finrays to detect and flush sand shrimp that, like flounder, frequently buried in sand substrata (personal observation). The absence of prey selection in our experiments is consistent with previous field studies classifying striped searobins and other triglids as opportunistic predators capable of consuming a variety of small demersal invertebrate and fish prey (Ross, 1977; Richards et al., 1979; Moreno-Amich, 1992; Labropoulou and Machias, 1998).
Although striped searobins are opportunistic predators, they consume prey whole and thus predator gape and prey body depth limit maximum prey size. Predictions of prey size limitation based on predator esophageal width, rather than mouth width, were much
closer to estimates of maximum prey size (|70 mm TL) in laboratory experiments. This
finding is consistent with other studies of gape limitation in piscivores (Lawrence, 1958; Hoyle and Keast, 1987). Previous studies of predation on small flatfishes have also shown that prey body depth is a limiting factor in prey size selection (Ellis and Gibson, 1995; 1997).
Substantial increases in maximum prey size with increases in searobin size were only evident for sand shrimp in the field. All sizes of searobins (field: 180–350 mm TL;
laboratory: 212–309 mm TL) consumed small flounder (field |15–25 mm TL;
laboratory: 30–40 mm TL) and shrimp (field: |10 mm TL) and slopes of regressions
increases in minimum and maximum prey size have been observed in other fishes including flatfish predators (Hoyle and Keast, 1987; Juanes, 1994; Juanes and Conover, 1995; Ellis and Gibson, 1995, 1997; Scharf et al., 1997). The absence of such a pattern for winter flounder was probably related to the narrow size range of searobins used in laboratory experiments and the rarity of large flounder in NSHES habitats in June (Stoner et al., in review).
Winter flounder are likely to be vulnerable to searobin predation for a period of at least 1.5 months following larval settlement. Based on our observations, searobins
(188–350 mm TL) consumed flounder ranging from 15 to .70 mm TL. Thus, the
smallest prey were only a few millimeters (TL) larger than flounder at settlement (i.e. 10–15 mm TL, 9–13 mm SL; Able and Fahay, 1998). Growth rates of YOY flounder
measured in experimental cages in the Navesink River range from 20.7 to 1.2 mm
21
day (Phelan et al., in preparation) and are similar to estimates compiled from the
21
literature (0.23 to 1.3 mm day ; Able and Fahay, 1998). Flounder that settle at a large
21
size (15 mm TL) and achieve a high growth rate (1.2 mm day ) may reach a size
refuge (|70 mm TL) from searobins (.200 mm TL) after approximately 46 days.
The diets of striped searobins in Sandy Hook Bay were generally similar to patterns previously reported for the species in Long Island Sound and southern New England (Marshall, 1946; Richards et al., 1979). We observed an apparent seasonal shift in the diet of searobins from sand shrimp, the dominant prey in June, to mysids later in the summer. Most of the fish collected in July and August were small compared with fish in June (Fig. 2), and thus we are unable to determine if the diet shift was related to predator size, the seasonal availability of prey, or perhaps both.
In June, winter flounder were consumed by the majority of striped searobins collected and as many as 11 flounder were eaten by individual predators. Flatfishes including winter flounder and windowpane flounder (Scophthalmus aquosus) have been reported in striped searobin diets in other studies, but occurrences were rare (Marshall, 1946; Richards et al., 1979). Searobins used in these studies were primarily collected in deep
water habitats (>5 m) where small flatfishes may be relatively uncommon, while our
surveys were conducted in shallow habitats (#3 m) where large numbers of juvenile
winter flounder are seasonally abundant (Able and Fahay, 1998; Stoner et al., in review). The absence of flounder in searobin diets during July and August in the NSHES may have been related to a decline in the availability of appropriately sized prey. Following settlement in May, flounder densities decrease in shallow habitats in the NSHES, perhaps as a result of mortality and the diffusion of fish from settlement areas (Stoner et al., in review). Furthermore, the proportion of the flounder population reaching as size
refuge from searobins (|70 mm TL) could be expected to increase as the summer
progresses.
We speculate that predation by searobins is likely to result in significant flounder mortality during episodic events localized in shallow habitats in Sandy Hook Bay. In our
study, most searobins were collected in a few 2 h gillnet sets (n53, >17 individuals)
J.P. Manderson et al. / J. Exp. Mar. Biol. Ecol. 242 (1999) 211 –231 229
estuary in beam trawl surveys, and in May, recently settled fish (,20 mm) occurred
within two regions, in the central portions of the Navesink River and Sandy Hook Bay. Thus episodes of intense searobin predation are more likely in Sandy Hook Bay where the two species co-occur, while the Navesink River may serve as a spatial refuge for winter flounder from searobin predation during some years.
Several studies have reported flatfishes in the diets of searobins and gurnards. Tongue fish (Cynoglossus zanzibarensis) are the dominant prey of South African lesser gurnard (Chelidonichthys queketti ) (Meyer and Smale, 1991), and grey gurnards (Eutrigla
gurnardus) consumed the flatfishes Pleuronectes platessa and Limanda limanda in
shallow habitats adjacent to Scottish beaches (Ellis and Gibson, 1995). Our laboratory and field studies show that striped searobins, like other triglids, possess sensory appendages that make them particularly adept at finding flatfish prey, and that the predators consume large numbers of winter flounder where the species co-ocurr. Striped searobins are abundant in mid-Atlantic estuaries and are consistently ranked among the top five species in terms of abundance and frequency of occurrence in demersal trawl surveys of the Hudson-Raritan estuary (Wilk and Silverman, 1976; McBride and Able, 1994; McBride et al., 1998; Wilk et al., 1996). Patterns in the distribution of the predators in the NSHES which is a nursery for winter flounder (Phelan, 1992; Scarlett, 1991; Stoner et al., in review), suggest the searobin predation may be localized in habitats within specific regions of the estuary. Thus, the importance of searobin predation may be in its contribution to the spatial and temporal variation in the mortality of juvenile winter flounder in the estuarine nursery.
Acknowledgements
The authors would like to thank John Rosendale, Jeff Pessutti, Mike Nunez, Bob Bevilacqua, Jeanie Sanchez, and numerous volunteers from Brookdale Community College and Rutgers University for help in the laboratory and field. We also thank Fred Scharf and Jeff Buckel for advice related to statistics, experimental design, and revisions to the manuscript.
References
Able, K.W., Fahay, M.P., 1998. The First Year in the Life of Estuarine Fishes in the Middle Atlantic Bight, Rutgers University Press, New Jersey.
Ansell, A.D., Gibson, R.N., 1993. The effect of sand and light on predation of juvenile place (Pleuronectes
platessa) by fishes and crustaceans. J. Fish Biol. 43, 837–845.
Bardach, J.E., Case, J., 1965. Sensory capabilities of the modified fins of squirrel hake (Urophycis chuss) and searobins (Prionotus carolinus and P. evolans). Copeia 2, 194–206.
Bax, N.J., 1998. The significance and prediction of predation in marine fisheries. ICES J. Mar. Sci. 55, 997–1030.
Ellis, T., Gibson, R.N., 1995. Size-selective predation of 0-group flatfish on a Scottish nursery ground. Mar. Ecol. Progr. Ser. 127, 27–37.
Ellis, T., Gibson, R.N., 1997. Predation of 0-group flatfishes by 0-group cod: handling times and size selection. Mar. Ecol. Progr. Ser. 149, 83–90.
Ellis, T., Howell, B.R., Hughes, R.N., 1997. The cryptic responses of hatchery-reared sole to a natural sand substratum. J. Fish Biol. 51, 389–401.
Gibson, R.N., 1994. Impact of habitat quality and quantity on the recruitment of juvenile flatfish. Neth. J. Sea Res. 32 (2), 191–206.
Gibson, R.N., Robb, L., 1992. The relationship between body size, sediment grain size and the burying ability of juvenile plaice, Pleuronectes platessa L. J. Fish Biol. 40, 771–778.
Gibson, R.N., Robb, L., 1996. Piscine predation on juvenile fishes on a Scottish sandy beach. J. Fish Biol. 49, 120–138.
Gibson, S., Johnston, I.A., 1995. Scaling relationships, individual variation and the influence of temperature on maximum swimming speed in early settled juveniles of the turbot. Scophthalmus maximus. Mar. Biol. 121, 401–408.
Goode, G.B., 1884. The food fishes of the United States. In: Goode, G.B. (Ed.), The fisheries and fishery industries of the United States, Vol. 3, pp. 163–682.
Hastie, T.J., 1993. Generalized additive models. In: Chambers, J.M., Hastie, T.J. (Eds.), Statistical Models in S, Chapman Hall, London, pp. 249–307.
Hastie, T.J., Tibshirani, R.J., 1990. Generalized Additive Models, Chapman and Hall, London.
Hoyle, J.A., Keast, A., 1987. The effect of prey morphology and size on handling time in a piscivore, the largemouth bass (Micropterus salmoides). Can. J. Zool. 65, 1972–1977.
Juanes, F., 1994. What determines prey size selectivity in piscivorous fishes. In: Strouder, D.J., Fresh, K.L., Feller, R.J. (Eds.), Theory and Application in Fish Feeding Ecology, USC Press, South Carolina, pp. 79–100.
Juanes, F., Conover, D.O., 1995. Size structured piscivory: advection and the linkage between predator and prey recruitment in young-of-the-year bluefish. Mar. Ecol. Progr. Ser. 128, 287–304.
Keefe, M.L., Able, K.W., 1994. Contributions of abiotic and biotic factors to settlement in summer flounder,
Paralichthys dentatus. Copeia 1994 (2), 458–465.
Kruuk, H., 1963. Diurnal periodicity in the activity of the common sole, Solea vulgaris Quensel. Neth. J. Sea Res. 2, 1–28.
Labropoulou, M., Machias, A., 1998. Effect of habitat selection on the dietary patterns of two Trigilid species. Mar. Ecol. Progr. Ser. 173, 275–288.
Lanzing, W.J.R., 1977. Reassessment of chromatophore pattern regulation in two species of flatfish (Scophthalmus maximus; Pleuronectes platessa). Neth. J. Sea Res. 11, 213–222.
Lawrence, J.M., 1958. Estimated sizes of various forage fishes largemouth bass can swallow. Proc. Ann. Conf. SE Assn. Game and Fish Comm. 11 (1957), 220–225.
Marshall, N., 1946. Observations of the comparative ecology and life history of two searobins, Prionotus
carolinus and Prionotus evolans strigatus. Copeia 1946 (3), 118–144.
McBride, R.S., Able, K.W., 1994. Reproductive seasonality, distribution, and abundance of Prionotus carolinus and P. evolans (Pisces: Triglidae) in the New York Bight. Est. Coast. Shelf Sci. 38, 173–188.
McBride, R.S., O’Gorman, J.O., Able, K.W., 1998. Interspecific comparisons of searobin (Prionotus spp.) movements, size structure and abundance in the temperate western North Atlantic. Fish. Bull. 96, 303–314. Meyer, M., Smale, M.J., 1991. Predation patterns of demersal teleosts from the south and west coasts of South
Africa. 2. Benthic and epibenthic predators. S. Afr. J. Mar. Sci. 11, 409–442.
Minami, T., Sawano, K., Nakagawa, T., Watanabe, K., 1994. Substrata preference by juvenile flounder
Verasper moseri. Bull. Hokkaido Natl. Fish. Res. Inst. 58, 53–60.
Minello, T.J., Zimmerman, R.J., Martinez, E., 1987. Fish predation on juvenile brown shrimp, Penaeus aztecus Ives: effects of turbidity and substratum on predation rates. Fish. Bull. 85 (1), 59–70.
Moles, A., Norcross, B.L., 1995. Sediment preference in juvenile Pacific flatfishes. Neth. J. Sea Res. 34 (1–3), 177–185.
Moreno-Amich, R., 1992. Feeding habits of red gurnard, Aspitrigla (L. 1758) (Scorpeaniformes Triglidae), along the Catalan coast (Northwestern Mediterranean). Hydrobiol. 228 (3), 175–184.
J.P. Manderson et al. / J. Exp. Mar. Biol. Ecol. 242 (1999) 211 –231 231 Neuman, M.J., Able, K.W., 1998. Experimental evidence of sediment preference by early life history stages of
windowpane (Scophthalmus aquosus). J. Sea Res. 40, 33–41.
Phelan, B.A., 1992. Winter flounder movements in the inner New York Bight. Trans. Amer. Fish. Soc. 121, 777–784.
Phelan, B.A., Goldberg, R., Bejda, A.J., Pereira, J., Hagan, S., Clark, P., Studholme, A.L. Calabrese, A., Able, K.W. Estuarine and habitat-related differences in growth rates of young-of-the-year winter flounder (Pseudopleuronectes americanus) and tautog (Tautoga onitis) in three northeastern US estuaries, in preparation.
Pihl, L., van der Veer, H.W., 1992. Importance of habitat exposure and habitat structure for the population density of 0-group plaice, Pleuronectes platessa L., in a coastal nursery area. Neth. J. Sea. Res. 29, 173–192.
Richards, S.W., Mann, J.M., Walker, J.A., 1979. Comparison of spawning season, age, growth rates and food of two sympatric species of searobins, Prionotus carolinus and Prionotus evolans, from Long Island Sound. Estuaries 2 (4), 255–268.
Ross, S.T., 1977. Patterns of resource partitioning in searobins (Pisces: Triglidae). Copeia 1977 (3), 561–571. Rountree, R.A., Able, K.W., 1997. Nocturnal fish use of New Jersey marsh creek and adjacent bay shoal
habitats. Est. Coast. Shelf Sci. 44, 703–711.
Scarlett, P.G., 1991. Temporal and Spatial Distribution of Winter Flounder (Pseudopleuronectes americanus) Spawning in the Navesink and Shrewsbury Rivers, Dept. Fish Game and Wildlife, New Jersey. Scharf, F.S., Buckel, J.A., Juanes, F., Conover, D.O., 1997. Estimating piscine prey size from partial remains:
testing for shifts in foraging mode by juvenile bluefish. Environ. Biol. Fish. 49, 377–388.
Scharf, F.S., Juanes, F., Sutherland, M., 1998. Inferring ecological relationships from the edges of scatter diagrams: comparison of regression techniques. Ecology 79 (2), 448–460.
Seikai, T., Kinoshita, I., Tanaka, M., 1993. Predation by crangonid shrimp on juvenile Japanese flounder under laboratory conditions. Nipp. Suis. Gak. 59, 321–326.
Silver, W.L., Finger, T.E., 1984. Electrophysiological examination of a non-olfactory, non-gustatory chemosense in the searobin, Prionotus carolinus. J. Comp. Physiol. A 154, 167–174.
Stoner, A.W., Manderson, J.P., Pessutti, J. Spatially-explicit analysis of estuarine habitat for juvenile winter flounder (Pseudopleuronectes americanus): combining Generalized Addictive Models and Geographic Information Systems (submitted to Marine Ecology Progress Series), in review.
Data Analysis Products Division, 1997. S-Plus 4. In: S-PLUS 4 Guide to Statistics, Mathsoft, Seattle. StataCorp, 1995. Stata Statistical Software: Release 4.0, Stata Corporation, College Station, TX.
Williams, P.J., Brown, J.A., 1992. Development changes in the escape response of larval winter flounder
Pleuronectes americanus from hatch through metamorphosis. Mar. Ecol. Progr. Ser. 88, 185–193.
Wilk, S.J., MacHaffie, E.M., McMillan, D.G., Pacheco, A.J., Pickanowski, R.A. 1996. Fish, megainvertebrates, and associated hydrographic observations collected in the Hudson-Raritan Estuary, January 1992-December 1993. N.E. Fish. Sci. Cent. Ref. Doc. 96-14, 95 p.
Wilk, S.J., Silverman, M.J., 1976. Summer Benthic Fish Fauna of Sandy Hook Bay, New Jersey, NOAA Tech Rept. SSRF-698.
