Diet of juvenile gag Mycteroperca microlepis

BULLETIN OF MARINE SCIENCE. 87(1):31–43. 2011 doi:10.5343/bms.2010.1028

Diet of juvenile gag Mycteroperca microlepis from a non-estuarine seagrass bed habitat in the southern Gulf of Mexico Thierry Brulé, Andy Mena-Loría, Esperanza Pérez-Díaz, and Ximena Renán ABSTRACT Diet composition, including seasonal and ontogenetic variations, was evaluated in juvenile gag, Mycteroperca microlepis (Goode and Bean, 1880), from a nearshore open marine seagrass bed on the north coast of the Yucatán Peninsula. Stomach contents from 322 juveniles (6.6–36.0 cm total length, TL) were analyzed using percentage frequency of occurrence (%F), percentage number (%N), percentage weight (%W), and a dietary index (Q = %N · %W). Young gag preyed heavily on caridean shrimps (Q = 791, %F = 38), fishes (Q = 327, %F = 13), penaeid shrimps (Q = 287, %F = 16), and unidentified decapods (Q = 114, %F = 26). Dominant prey in stomach contents shifted from caridean shrimps (Q = 1072, %F = 41) during the warm season to fishes (Q = 1392, %F = 21) and penaeid shrimps (Q = 1098, %F = 33) during the cold season. Size-dependent shifts in diet were also observed, particularly when organisms reached a size of ~17 cm TL. Dominant prey were caridean shrimps (Q = 1186, %F = 45) for gag ≤ 17 cm TL and fishes (Q = 2379, %F = 35) and penaeid shrimps (Q = 1005, %F = 27) for gag > 17 cm TL. Diet composition and ontogenetic changes in juvenile gag diet were similar, independent of nursery habitat (seagrass or oyster shell bed inside or outside of an estuarine system). Gag is therefore best considered an estuarine opportunist, with nursery ground habitat (i.e., seagrass meadows) being the final factor controlling juvenile settlement and growth.

Estuarine dependence in tropical fish implies that an estuary, or similar habitat, is required during some portion of a species’ life cycle, and that without access to this habitat, a viable population would cease to exist (Blaber et al. 1989). An estuarine system is a coastal indentation with a restricted connection to the ocean which remains open at least intermittently (Day et al. 1989). This functional definition encompasses a range of diverse coastal systems including lagoons, estuarine lagoons, estuaries, estuarine deltas, and deltas. A decrease in wave energy (marine action) coupled with an increase in river sediments (river processes) can shift a particular system from the lagoon extreme toward the delta extreme. In the southeast Gulf of Mexico, on the northern coast of the Yucatán Peninsula, only barred inner shelf or organic coastal lagoons exist. The well-developed karst topography of the Yucatán Platform results in a land surface almost without relief and consequently lacking river runoff (Lankford 1977). Coastal lagoons in the region therefore only receive freshwater input directly from rainfall or through coastal freshwater springs (Herrera-Silveira et al. 1998). Gag, Mycteroperca microlepis (Goode and Bean, 1880), is one of the most abundant and valuable groupers off the southern Atlantic coast of the US and in the eastern and southern Gulf of Mexico (Bullock and Smith 1991, Heemstra and Randall 1993, Brulé et al. 2009). Like other protogynous groupers, gag has a suite of life history characteristics which make it particularly susceptible to overexploitation (Coleman Bulletin of Marine Science

© 2011 Rosenstiel School of Marine and Atmospheric Science of the University of Miami

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BULLETIN OF MARINE SCIENCE. VOL 87, NO 1. 2011

et al. 1999). In contrast to deeper-dwelling adults, juvenile grouper tend to occupy nearshore habitats where they can find ample cover and food, and form part of a complex food web (Bullock and Smith 1991, Sluka et al. 1994, 1999). Gag is considered estuary-dependent because its young-of-the-year settle in nursery habitats located in estuaries (Keener et al. 1988, Koenig and Coleman 1998, Lindeman et al. 2000). For example, seagrass meadows or oyster shell beds are important nursery ground habitats for juvenile gag in estuaries along the coasts of North and South Carolina (Mullaney 1994, Ross and Moser 1995, Mullaney and Gale 1996), as well as along the east central (Gilmore 1977) and Gulf coasts of Florida (McErlean 1963, Koenig and Coleman 1998, Fitzhugh et al. 2005). More favorable temperatures, lower predation risk, and ready food availability may be the principle advantages of estuaries for juvenile fish (Miller et al. 1985). However, on the north coast of the Yucatán Peninsula in the southeastern Gulf of Mexico, young gag settle to nursery grounds in seagrass meadows located in nearshore open marine environments outside of coastal lagoons (Renán et al. 2003, 2004, 2006). Gag is a bottom-dwelling apex predator that exercises a strong influence on the trophic web of coral reef ecosystems (Parrish 1987, Sierra et al. 2001, Sluka et al. 2001). Dietary data for young gag are currently limited to estuarine nursery grounds on the southern Atlantic coast of the US, including the east coast of Florida (Bullock and Smith 1991, Mullaney 1994, Ross and Moser 1995, Mullaney and Gale 1996). The food habits of juvenile gag from other regions of the Gulf of Mexico and nursery habitats located outside estuarine systems remains largely unknown. Food quantity and type can differ between estuaries and adjacent waters (Blaber 1997). The present study objective was to (1) characterize diet composition for juvenile gag from an open marine nursery ground and (2) determine how seasonal changes in water temperature and ontogenetic changes affect gag diet in the nearshore zone. We compare these results to gag diet data from estuarine habitats to better understand the estuarine dependence of gag during the juvenile phase. Materials and Methods Study data were collected at Punta Caracol, near the Yalahau Lagoon inlet, off the northeast coast of the Yucatán Peninsula (Fig. 1). This site is characterized by a long extension of low, narrow beach consisting of coarse calcareous sand with shell fragments and a conspicuous seagrass bed containing Thalassia testudinum Banks & Soland. ex Koenig, Halodule wrightii Ashers, and Syringodium filiforme Kütz in association with various algae species (Renán et al. 2006). Direct rainfall and subterranean freshwater upwelling in the coastal zone are the only potential causes of seasonal seawater salinity variations in this region. Renán et al. (2006) observed that salinity remained relatively constant at this site during 2001 (mean ± SD = 36.8 ± 1.4). Juvenile gag (N = 406) were caught monthly during a 2-d period in July 2000 and from January to October 2001 during daylight hours (0700–1400) using a small trawl net (5 m length, 2 m wing spread, and 1.7 cm mesh). Juvenile gag have generally been observed in inshore coastal waters < 10 m deep (Keener et al. 1988, Ross and Moser 1995, Koenig and Coleman 1998, Lindeman et al. 2000). To sample this habitat, trawl runs were performed parallel to shore between 0.5 and 2.5 m depth at a speed of about 1.5–2.5 m s−1. Specimens were stored on ice immediately after capture and examined at the end of each sampling day. Data on total and standard lengths (TL, SL) and whole and gutted weights (WW, GW) were recorded for each fish, and the stomach was removed and preserved in 10% formalin. All specimens (size range: 6.6– 41.5 cm TL) were considered to be juvenile because the smallest sexually mature

brulé et al.: diet of juvenile gag

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Figure 1. Location of study site (Punta Caracol) off the northeast coast of the Yucatán Peninsula, in the southern Gulf of Mexico. female gag reported to date for the Gulf of Mexico measured 49 cm TL (Coleman et al. 1996, Koenig et al. 1996). Excess formaldehyde was removed by soaking the stomachs in several changes of water, and stomach contents were stored in 70% ethanol. Stomach contents (i.e., prey) were sorted and identified to the lowest possible taxon, counted (except for plant material and unidentified remains), drained, and weighed to the nearest 0.01 g. All items identified as the same taxon within the same stomach were recorded as a single individual prey, unless two (or more) items clearly came from two (or more) individuals. Stomach contents were analyzed using percentage frequency of occurrence (%F), percentage number (%N), percentage weight (%W), and a dietary index (Q = %N ∙ %W; Hureau 1970, Hyslop 1980). Based on the range of Q and %F values observed in the present study, prey were classified as: main prey (Q ≥ 500, %F ≥ 20), secondary prey (100 ≤ Q < 500, %F ≥ 10), or minor prey (Q < 100, %F < 10). Seasonal change in gag diet was analyzed separately for the “cold” (or “dry”) season (November–April) and “warm” (or “wet”) season (May–October). This two-season division is based on sea surface temperature fluctuations in the southern Gulf of Mexico (Rivas 1970, Piñeiro et al. 2001) and rainfall variability off the north coast of the Yucatán Peninsula (Espejel 1987). Ontogenic changes in diet were analyzed by grouping the specimens into nine size classes with a 3.5 cm interval, following Sturge’s method (Scherrer 1984). Diet overlap between specimens caught in different seasons and between those of different size classes was estimated by calculating Schoener’s index (C xy, Schoener 1970), using prey %F, %N, and %W. Unidentified remains were discarded from this analysis. Index values > 0.6 were considered to be a significant overlap (Zaret and Rand 1971).

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Table 1. Prey species recorded in the stomachs of juvenile gag from seagrass meadows along the northern coast of the Yucatán Peninsula. Plant material Crustaceans Tanaidacea Amphipoda Decapoda Dendrobranchiata

Caridea

Penaeidae

Sergestidae Hippolytidae

Palaemonidae

Unidentified Gastropoda Osteichthyes Clupeiformes Aulopiformes

Engraulidae Synodontidae

Batrachoidiformes Gasterosteiformes

Batrachoididae Syngnathidae

Perciformes

Labrisomidae Gobiidae

Tetraodontiformes Unidentified remains

Monacanthidae

Litopenaeus setiferus (Linnaeus, 1767) Farfantepenaeus dourarum (Burkenroad, 1939) Panaeus sp. Unidentified Acetes sp. Hippolyte zostericola (S. I. Smith, 1873) Hippolyte sp. Thor floridanus Kingsley, 1878 Thor manningi Chace, 1972 Thor sp. Tozeuma carolinense Kingsley, 1878 Unidentified Paleomonetes sp. Periclimenes sp. Unidentified

Anchoa sp. Synodus foetens (Linnaeus, 1766) Unidentified Anarchopterus criniger (Bean and Dresel, 1884) Unidentified Paraclinus fasciatus (Steindachner, 1876) Unidentified Gobionellus sp. Unidentified Monacanthus sp. Unidentified

Results Of the 406 juvenile gag caught in the Punta Caracol seagrass bed, 84 (21%) had no stomach contents, thus the analysis of stomach contents was based on 322 specimens (6.6–36.0 cm TL). In total, 20 prey items were identified, which were classified into nine taxonomic categories: plant material, tanaids, amphipods, penaeid shrimps, caridean shrimps, unidentified decapods, gastropods, fishes, and unidentified remains (Table 1). Juvenile gag diet was dominated by decapods and fishes (Table 2). Based on Q and %F values, caridean shrimps were the main prey; followed by fishes, penaeid


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Table 2. Percent frequency of occurrence (%F), percent number (%N), percent weight (%W), and dietary index (Q) of prey categories in global diet of juvenile gag (N = 322) from seagrass meadow of the northern coast of the Yucatán Peninsula. Prey categories Plant material Tanaids Amphipods Penaeidean shrimps Caridean shrimps Unidentified decapods Gastropods Fishes Unidentified remains

%F 4.0 1.9 0.3 16.1 38.5 26.1 0.6 13.0 23.0

%N – 2.2 0.2 9.6 58.6 22.0 0.3 7.1 –

%W 1.7 < 0.1 < 0.1 29.9 13.5 5.2 < 0.1 46.0 3.6

Q – – – 287 791 114 – 327 –

shrimps, and unidentified decapods as secondary prey; and tanaids, amphipods and gastropods as minor prey (Table 2, Fig. 2). Seasonal shifts were observed in gag intake of caridean shrimps, penaeid shrimps, and fishes (Fig. 2). During the warm season, caridean shrimps (Q = 1072, %F = 41) were the main prey; fishes (Q = 260, %F = 12), penaeid shrimps (Q = 252, %F = 15) and unidentified decapods (Q = 152, %F = 27) were secondary prey; and tanaids, amphipods, and gastropods were minor prey (Q < 0.2, %F < 2). During the cold season, by contrast, fishes (Q= 1392, %F = 21) and penaeid shrimps (Q = 1098, %F = 33) were the main prey, while caridean shrimps (Q = 96, %F = 8), unidentified decapods (Q = 10, %F = 8), and tanaids (Q < 0.8, %F = 4) were minor prey. Schoener’s index indicated that no significant interseasonal dietary overlap occurred when frequency of occurrence and percentage number of the prey were considered (%F, C xy = 0.57; %N, C xy = 0.45; %W, C xy = 0.79). However, individual gag collected during the warm season (mean ± SD = 13.0 ± 4.0 cm TL, N = 298) were also significantly smaller (MannWhitney U-test: df = 1, P < 0.001) than those captured during the cold season (21.3 ± 5.2 cm TL, N = 24). Furthermore, the cold season sample size was smaller than warm season sample size. We also observed an ontogenetic shift in juvenile gag diet. Tanaids and amphipods were only present in the stomachs of small individuals (≤ 17 cm TL). Considering Q and %F over larger predator size classes, penaeid shrimps and fishes increased in importance while caridean shrimps and unidentified decapods decreased in importance (Fig. 3A). These ontogenetic changes in diet were particularly important when young gag attained ~17 cm TL in size. Schoener’s index generally showed little significant dietary overlap between individuals in the 6.5–17.0 cm TL size classes and those in the 17.1–36.0 cm TL size classes (Table 3). When only two main size-groups were considered (small ≤ 17 cm TL and large > 17 cm TL), caridean shrimps (Q = 1186, %F = 45) were the main prey for smaller gag, while fishes (Q = 2379, %F = 35) and penaeid shrimps (Q = 1005, %F = 27) were the main prey for larger gag (Fig. 3B). Based on the frequency and number of prey in stomachs, there was no significant overlap in diet between the smaller and larger size groups (%F, C xy = 0.45; %N, C xy = 0.41; %W, C xy =0.71).

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Figure 2. Global and seasonal composition of diet for juvenile gag from seagrass meadows along the northern coast of the Yucatán Peninsula. A: amphipods; C: caridean shrimps; F: fishes; G: gastropods; P: penaeid shrimps; T: tanaids; UD: unidentified decapods. (Angles of sector are proportional to Q and radius is proportional to %F).

Discussion Juvenile gag are voracious, carnivorous predators in seagrass bed habitats (Ross and Moser 1995). Prey richness (20 items) in the juvenile gag stomachs analyzed in the present study was lower than observed for juveniles from seagrass beds (30 items) or oyster shell habitats (44 items) in North Carolina (Ross and Moser 1995) and South Carolina (Mullaney 1994). Copepods, mysids, and isopods were not observed in the Yucatán coast specimens, and amphipods were less abundant than reported in the Carolinas. In contrast, small tanaids were recorded in the present study, but have


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Figure 3. Diet composition of juvenile gag from seagrass meadows along the northern coast of the Yucatán Peninsula, according to size of the predator. (A) 3.5 cm TL size class intervals. (B) small (TL ≤ 17 cm) and large (TL > 17 cm) juvenile gag. A: amphipods; C: caridean shrimps; F: fishes; G: gastropods; P: penaeid shrimps; T: tanaids; UD: unidentified decapods. (Angles of sector are proportional to Q and radius is proportional to %F).

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Table 3. Dietary overlap in stomach contents among size classes of juvenile gag from seagrass meadows along the northern coast of the Yucatán Peninsula (* significant dietary overlap based on Schoener’s index). %F = percent frequency of occurrence; %N = percent number; %W = percent weight; N = sample size. Size classes TL (cm) 6.6–10.0 %F N = 58 %N %W

> 27.5 0.06 0.05 0.18

10.1–13.5 %F N = 130 %N %W

0.47 0.11 0.36

0.31 0.11 0.52

0.62* 0.35 0.54

0.48 0.57 0.62*

0.80* 0.50 0.82*

13.6–17.0 %F N = 83 %N %W

0.32 0.19 0.50

0.38 0.19 0.65*

0.68* 0.35 0.71*

0.62* 0.75* 0.82*

– – –

17.1–20.5 %F N = 26 %N %W

0.66* 0.52 0.74*

0.63* 0.52 0.57

0.77* 0.71* 0.89*

– – –

20.6–24.0 %F N = 10 %N %W

0.54 0.67* 0.76*

0.68* 0.67* 0.63*

– – –

24.1–27.5 %F N=6 %N %W

0.64* 0.93* 0.41

– – –

> 27.5 N=9

%F %N %W

24.1–27.5 20.6–24.0 17.1–20.5 13.6–17.0 10.1–13.5 6.6–10.0 0.18 0.49 0.36 0.73* 0.85* – 0.05 0.34 0.50 0.79* 0.91* – 0.19 0.21 0.30 0.49 0.67* – – – –

– – –

not been reported in juvenile gag from North Carolina and South Carolina or the Gulf coast of Florida. Geographic differences in feeding habits in fish may reflect opportunistic predator responses to locally variable food resource quality and quantity (Starck 1970). The density and diversity of suitable foods, such as polychaetes, small crustaceans, and mollusks, as well as the availability of prey of broader size ranges, are thought to be higher in estuaries than in adjacent habitats (Blaber 1997). If spatial variation in copepod, mysid, and isopod predation by juvenile gags is not considered, the diet differences between juveniles from the southern Atlantic coast of the US and the Yucatán Peninsula may be largely the result of variations in specimen size. The gag analyzed in the present study were larger than those analyzed from North and South Carolina (size range: 1.0–18.6 cm SL). In addition, copepods, mysids, isopods, and amphipods are exclusively consumed by small individuals (< 7–9 cm SL), with a notable dominance of copepods and mysids in the diet of very small gag (2–6 cm SL; Mullaney 1994, Ross and Moser 1995). However, independent of the sampled nursery habitat (seagrass or oyster shell bed inside or outside an estuarine system), caridean, penaeid shrimps, and fishes were always the dominant prey food


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among juvenile gag from the southern Atlantic coast of the US (Mullaney 1994, Ross and Moser 1995), as well as the northeastern (Stallings et al. 2010), eastern (Bullock and Smith 1991), and southeastern Gulf of Mexico (the present study). Feeding experiments conducted with juvenile gag (16.9–21.3 cm SL) produced no evidence of preference for a particular prey (shrimp or pinfish, Stallings 2010). Therefore, these prey are probably abundant regardless of the coastal location of the nursery grounds (although abundance is particularly high in seagrass beds), and young gag feed opportunistically on these prey, regardless of whether they are in estuarine conditions. The main prey category in the diet of juvenile gag in our study area shifted from caridean shrimps during the warm season to fishes and penaeid shrimps during the cold season (Fig. 2). Ross and Moser (1995) observed seasonal changes in the diversity of juvenile gag diets in North Carolina estuaries in that a wider variety of food items was ingested during late summer than during spring or early summer. The seasonal shifts in diet of juvenile gag from the north coast of the Yucatán may have been biased by interseasonal variations in specimen size and sample size. Gag were more abundant and smaller in size during the warm season than during the cold season. Seasonal variation in juvenile gag size and abundance was associated with the seasonal ingress, growth, and egress of young-of-the-year in nursery habitats in the southern Gulf of Mexico. Peak ingress of small, newly-settled gag (1.5–2.8 cm SL) into the sampled site occurred from March to May. Juveniles (8.0–18.2 cm SL) attained maximum abundance by July and began to leave the nursery area between September and December at ~19.5 cm SL (Renán et al. 2006). Ontogenetic changes in juvenile gag diet in our study area were similar to those reported elsewhere, independent of nursery habitat (seagrass or oyster shell beds inside or outside an estuarine system). Elsewhere, juvenile gag exhibit size-dependent shifts in diet, changing from a diet composed of small macrocrustaceans to one of larger crustaceans and fishes as gag increased in size (Mullaney 1994, Ross and Moser 1995, Stallings et al. 2010). This trophic ontogeny may be partially related to changes in food availability. For instance, in North Carolina seagrass beds, the decline in the proportion of amphipods in gag diets as the seasons change and gag size increases have been correlated to a seasonal decline in amphipod abundance (Ross and Moser 1995). In Charleston Harbor, trophic ontogeny in gag generally follows seasonal trends in the abundance of invertebrate organisms in oyster reef habitats (Mullaney 1994). Size-dependent shifts in gag diet are probably also facilitated by ontogenetic changes in the gag feeding apparatus (Ross and Moser 1995). Mullaney and Gale (1996) observed that the onset of piscivory in young gag at ~12.5 cm SL correlates to complete acquisition of caniniform, ankylosed teeth. Equivalent to about 16.3 cm TL based on the TL to SL relationship calculated by Ross and Moser (1995; TL = 1.03 + 1.22 [SL], r2 = 0.99), this size is similar to that at which the juvenile gag we examined (17 cm TL) changed their diet from small tanaids, amphipods, and caridean crustaceans to larger penaeid shrimps and fishes. According to Stallings et al. (2010), this dietary transition in young gag, ranging from 12.7 to 15.0 cm SL (16.5– 19.3 cm TL), coincides with a general increase in caloric densities of prey consumed as well as with a decrease in juvenile somatic growth just prior to emigration from nursery grounds. These authors state that the decline in growth rate is probably due to a shift in energy utilization from growth to storage. Lipid storage at this early stage in life history may serve as insurance for survival in unpredictable environments during migration and/or winter.

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Clear species-specific habitat associations have been observed among young grouper along the north coast of the Yucatán Peninsula. Gag settle in seagrass beds, while red and black grouper young-of-the-year prefer sandy-rocky bottoms with some ridges and crevices (Renán et al. 2003). Grouper habitat dependency is probably linked more closely to the need for shelter than to food availability (Parrish 1987). In a shelter-closure experiment, Lindberg et al. (2006) observed that post-seagrass phase gag exhibited density-dependent habitat selection and initially selected habitat on the basis of shelter rather than food. Levin and Hay (2003) used experimental mesocosms to analyze juvenile gag selection of estuarine habitats and concluded that they selected seagrass or oyster reefs over unstructured habitat, and clearly preferred high-density to low-density seagrass patches. The relative importance of estuary nursery grounds is still not clear because marine areas adjoining estuaries are generally not sampled for comparison (Blaber et al. 1989). However, inshore marine environments have been reported to provide an alternative to estuaries as a nursery area for some commercially important fishes of southwestern Australia (Lenanton 1982, Lenanton and Potter 1987). Under these circumstances, juveniles of species that live in estuaries and in neighboring inshore marine waters may be more appropriately termed “estuarine opportunists” rather than “estuarine dependent” (Lenanton and Potter 1987, Blaber et al. 1989). Therefore, our results, together with previous reports from other Gulf and western Atlantic regions, suggest that gag is best considered an estuarine opportunist. The presence of seagrass meadows and similar benthic habitats, regardless of estuarine influence, may constitute the final, most important factor defining suitable gag nursery habitat. Acknowledgments This research was funded by the Science and Technology Council of Mexico (CONACYT), grant 37606-B. Collection was authorized by fishing license No. 030400-213-03 from SEMARNAP. We owe our thanks to T Colás-Marrufo (CINVESTAV) and K Cervera-Cervera (INP/CRIPY) for their technical assistance during this study, and to the manager (F Ávila) and fishermen from the fishing cooperative SCPP “El Cuyo” for their collaboration in all aspects of field collection. This manuscript was greatly improved by comments from three anonymous reviewers.

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address: Departamento de recursos del Mar, ciNVestaV-ipN Unidad Mérida, antigua carretera a progreso Km. 6, apartado 73 “cordemex,” código postal 97310, Mérida, yucatán, Mexico. corresponding author: (tb) e-mail: .