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VARIATIONS IN THE FEEDING HABITS OF RATHBUNAE IN LAS PALMAS LAGOON (SOUTHERN GULF OF MEXICO) ON THREE TEMPORAL SCALES

BY

M. MASCARÓ1), A. M. CASTILLO, N. SIMOES and X. CHIAPPA-CARRARA Unidad Multidisciplinaria de Docencia e Investigación, Facultad de Ciencias, Universidad Nacional Autónoma de México, Calle 8 No. 253, 97130 Mérida, Yucatán, Mexico.

ABSTRACT

Las Palmas lagoon is a part of the hydrographic system of Pom-Atasta-Puerto Rico, NE of Laguna de Términos, southern Gulf of Mexico. Swimming of the genus Callinectes abound in this area and play an important role in the complex trophic dynamics of the macrobenthos. We analysed the feeding habits of Callinectes rathbunae and its variations on three temporal scales. Sampling was carried out from August 1999 through July 2000, both on a monthly basis (9:00-13:00 h) at new moon, and for each season (every 6 h during 24 h) with a small shrimp trawl net. Samples of epi- and infauna were simultaneously taken. The stomachs of all C. rathbunae collected were dissected and the dietary components identified to the lowest taxonomic level possible. Percentage frequency of occurrence (%F ) of each taxon was calculated, together with the normalized Levins index (Ba)for each (a) season, (b) size class (20 mm intervals), and (c) day- and night-time period in each season. While the trophic niche breadth of this species does not vary significantly with season, size, or time of day, diet components differed among seasons and crab size classes. Results indicate that ontogenic differences in the feeding strategies of this species contribute most importantly to overall variations in diet.

RESUMEN

La laguna de Las Palmas forma parte del sistema hidrográfico Pom-Atasta-Puerto Rico, ubicado al NE de Laguna de Términos, en el sur del Golfo de México. Las jaibas del género Callinectes son abundantes en esta zona, y juegan un papel preponderante en la compleja dinámica trófica del macrobenthos. Se analizaron los hábitos alimenticios de Callinectes rathbunae, y sus variaciones en tres escalas temporales. Se realizaron muestreos mensuales de agosto 1999 a julio 2000 (9:00- 13:00 h en luna nueva), y estacionales (cada 6 h durante 24 h), utilizando una red de prueba camaronera. Simultáneamente, se tomaron muestras de la epi y meiofauna. Los estómagos de todos los C. rathbunae capturados fueron disecados, y se identificaron los componentes del contenido estomacal hasta grupos taxonómicos mayores. Se calcularon los valores de porcentaje de frecuencia de ocurrenciaUNCORRECTED (%F ) de cada componente, así como los valores de del índicePROOF normalizado de Levins

1) Corresponding author; email: [email protected] © Koninklijke Brill NV, Leiden, 2007 Crustaceana 00 (0): 1-22 Also available online: www.brill.nl/cr CRUS [1.35] 2006/11/21 12:14; Prn:12/12/2006; 9:45 F:crus2380.tex; p. 2 (120-170)

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(Ba) por (a) épocas del año, (b) por intervalo de talla (20 mm), y (c) para el día y la noche en cada época del año. En tanto que la amplitud del nicho trófico no varió significativamente entre épocas del año, talla u hora del día, se registraron diferencias en los componentes de la dieta a lo largo del año y entre jaibas de diferente tamaño. Los resultados indican que las diferencias ontogénicas en las estrategias alimenticias de esta especie contribuyen de manera importante en la variación general de la dieta.

INTRODUCTION

The area surrounding Laguna de Términos is a part of the hydrographic system controlling the deltaic processes of the Grijalva and Usumacinta rivers, which together have the greatest sediment and water discharge into the Mexican portion of the Gulf of Mexico. This area offers a variety of critical habitats for many aquatic species and constitutes the second most important fishing area of Mexico. It is also the primary region for the national oil industry (Yáñez-Arancibia & Lara- Domínguez, 1999). Swimming crabs of the genus Callinectes Stimpson, 1860 are abundant in coastal lagoons, estuaries, and other shallow marine environments associated with these systems, and use the wide variety of habitats at different moments throughout their life cycle (Yáñez-Arancibia & Day, 1988). They are among the dominant invertebrates in these ecosystems, and play an important role in the complex trophic dynamics of the macrobenthos (Chávez & Fernández, 1976; Sumida & Pyres-Vanin, 1997). Predation by Callinectes on the epi- and infauna determines the distribution and abundance of prey species (Krantz & Chamberlin, 1978; Seed, 1980; Blundon & Kennedy, 1982; Eggleston et al., 1992), while swimming crabs themselves are the preferred food of a variety of fish and cephalopods. While many authors have directed their interest towards the feeding habits of Callinectes sapidus Rathbun, 1896 (e.g., Tagatz, 1968; Seed, 1980; Laughlin, 1982; Hsueh et al., 1992), few have focused on Callinectes rathbunae Contreras, 1930. The latter is a very abundant species in the southern Gulf of Mexico, and, together with C. sapidus, Callinectes similis Williams, 1966, and Callinectes danae Smith, 1869, supports an important fishery (Raz-Guzmán et al., 1986; Román-Contreras, 1986). In addition, most studies dealing with the feeding habits of Callinectes do not consider differences in diet with respect to sex, size, daily cycles, or seasonal changes in prey abundance throughout the year. Most studies describing the feeding habits of other marine species have used the normalized version of the niche breadth index (Ba) proposed by Levins (1968).UNCORRECTED The distribution function that this index should usePROOF is one that ensures sample independence among prey found in any particular stomach. Distribution functions based either on the number or the relative biomass or volume of dietary CRUS [1.35] 2006/11/21 12:14; Prn:12/12/2006; 9:45 F:crus2380.tex; p. 3 (170-226)

FEEDING HABITS OF CALLINECTES RATHBUNAE IN TIME 3 components do not ensure such independence, given that all components found in any particular stomach are statistically associated (Hurlbert, 1984). Therefore, the Levins index should be calculated using the proportion of stomachs in which a certain food resource is found (Krebs, 1999). Because of the difficulty in obtaining sufficient replication (Efron & Tibshirani, 1998), statistical comparisons of Ba values are uncommon in trophic studies of aquatic organisms. By means of the bootstrap method (Mueller & Altenberg, 1985), re-sampling of the data is possible, thereby allowing approximately normal distributions of Ba values, from which confidence intervals can be calculated. Standard confidence intervals based on data sets with a large n,however,are extremely narrow, and other methods for these estimates have been recommended (Efron & Tibshirani, 1998). The aim of the present study was to describe the feeding habits of C. rathbunae from Las Palmas lagoon, and its variation on three temporal scales: (a) throughout the year, (b) throughout different size classes (i.e., life time), and (c) throughout a 24 h period. When attempting to correctly apply the Levins index, the distribution function of prey that ensures fulfilment of the property of statistical independence among sampling units was used. In order to compare estimates of the niche breadth index among crabs from different seasons, size classes, and day-night periods, methods specifically applied in bootstrapping were used to generate 95% confidence intervals.

STUDY AREA

Las Palmas lagoon is part of the hydrographic system formed by Pom-Atasta- Puerto Rico, NE of Laguna de Términos in the southern Gulf of Mexico, located at 18°30-18°35N 91°50-92°20W (fig. 1). Geomorphology, tidal influence, and water exchange with Laguna de Términos favour the presence of a semi-permanent east-west gradient of salinity (0-28h), temperature (22-34°C), and dissolved oxygen (1-10 mg · l−1). This gradient allows the existence of two distinct habitats throughout the year: a predominantly mesohaline habitat to the west, formed by Las Palmas and Puerto Rico; and an oligohaline habitat, formed by Pom and Atasta (Aguirre-León & Díaz-Ruiz, 2000). Las Palmas is a shallow lagoon, with a mean depth of 1.7 ± 0.3 m that increases slightly towards the centre (maximum depth: 1.9 ± 0.3 m). It has a circular shape and a total extension of approximately 20 ha, and it is connected eastwardUNCORRECTED with Puerto Rico through a narrow strait with two PROOF small islets (fig. 1). The internal margin of the lagoon is formed by extensive mangrove forests, which are the principal source of sediments and organic matter (Contreras, 1985). Las CRUS [1.35] 2006/11/21 12:14; Prn:12/12/2006; 9:45 F:crus2380.tex; p. 4 (226-255)

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Fig. 1. Location of Las Palmas lagoon in the southern Gulf of Mexico.

Palmas has no submerged vegetation and the lagoon bed is characterized by great accumulations of organic matter (3.28 ± 0.22% organic C; Mascaró, 2000) and clay fragments. Transport and suspension of sediments generates mean Secchi disc readings of 0.61 ± 0.22 m (Mascaró, 2000). According to Yáñez-Arancibia & Day (1988) the region has three seasons: the dry season from March to May, with a mean temperature of 28.1°C, a mean rainfall of 164.8 mm, and predominantly southeasterly winds; the rainy season, from June to September, has a mean temperature of 28.3°C, a rainfall of 976.7 mm, and north- and southeasterly winds; and the “nortes” season, from October to February, has a mean temperature of 24.4°C, a rainfall of 345.6 mm, and strong winds from the north.

UNCORRECTEDMATERIAL AND METHODS PROOF Twelve monthly surveys were conducted from August 1999 to July 2000: always between 9:00 h and 13:00 h, and always during new moon periods to restrict CRUS [1.35] 2006/11/21 12:14; Prn:12/12/2006; 9:45 F:crus2380.tex; p. 5 (255-298)

FEEDING HABITS OF CALLINECTES RATHBUNAE IN TIME 5 possible tidal influences to a minimum. Specimens of Callinectes rathbunae were collected using a small shrimp trawl net with a mouth opening of 5.3 m and 2.0 cm mesh size, operated from a 25 ft (approx. 8 m) fibreglass boat with a 65 HP outboard motor. Each month, four trawls with a mean duration of 7.6 ± 1.1 min. were carried out at an average speed of 81.1 ± 14.5 m · min −1.Inorderto determine the abundance of potential prey species, samples of the epi- and infauna were taken simultaneously. These were collected with a push net, mouth opening 0.5 m and 2.5 mm mesh size, operated manually from the boat over a distance of approximately 35 m at a mean speed of 8.75 ± 5.5 m · min −1. All specimens collected were preserved in 20% formalin to be processed in the laboratory. Water temperature (±0.2°C), salinity (±1h), dissolved oxygen (±0.1 mg · l−1), and pH (±0.02) on the lagoon bed were recorded at each station. Water samples were taken with a 1 l Van Dorn bottle. In order to determine daily variations in abundance and diet of C. rathbunae, 24 h surveys was conducted in each of the three seasons: the rainy (October 1999), the “nortes” (February 2000), and the dry season (April 2000). A total of four trawls was made, so at 9:00 h, 13:00 h, 21:00 h, and 1:00 h, using the same procedures and equipment as described for the monthly sampling. Swimming crabs were identified as C. rathbunae, and their carapace width (distance between the tips of the distal most marginal teeth: CW mm) measured with Vernier callipers (±0.1 mm). Epi- and infauna samples were sieved (600 µm), and all specimens identified to the lowest taxon possible (Dickson & Moore, 1977; McLaughlin, 1980; García-Cubas, 1981; Elner et al., 1985; Barnes, 1990) in order to create a reference collection. Stomachs were dissected and the repletion index of Walsh & Rankine (1979) was used to estimate the degree of fullness. Stomach contents were analysed with a stereoscopic microscope and dietary components identified to the lowest taxo- nomic level possible using specialized keys (Dickson & Moore, 1977; McLaugh- lin, 1980; García-Cubas, 1981; Elner et al., 1985; Barnes, 1990). Samples obtained during the monthly survey were used to calculate the percent frequency of oc- currence of each dietary component (%F ) for each (a) season and (b) size class (20 mm intervals were calculated using Sturges’ rule; Sturges, 1926). Samples ob- tained during the seasonal survey, were used to calculate %F for the day (9:00 h and 13:00 h) and night periods (21:00 h and 1:00 h) in each of the three seasons. For the analysis of trophic niche breadth, the normalized version of the index proposed by Levins (1968) was used:  − k 1 UNCORRECTED2 − PROOF pj 1 j=1 Ba = k − 1 CRUS [1.35] 2006/11/21 12:14; Prn:12/12/2006; 9:45 F:crus2380.tex; p. 6 (298-355)

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This index combines both the number of prey resources used (k), hence the trophic spectrum, and the relative frequency with which each prey resource is consumed (j). This represents the distribution function of prey proportions in the diet (Hespenheide, 1975). Because the collection of prey found in any stomach does not comprise independent samples (Hurlbert, 1984), pj was calculated as the proportion of individual crabs (N ∗) that consumed a certain food resource in relation to the total number of stomachs analysed (Krebs, 1999): N ∗ =  j pj ∗ Nj j The normalized Levins index, Ba, ranges between 0 and 1. Zero values indicate that crabs feed on only one type of prey, representing the minimum diet breadth and thus a high feeding specialization. Unity values, on the other hand, indicate that individuals consumed all k food resources in the same proportion (pj = 1/k), representing no selection among prey types, and the widest possible trophic niche (Gibson & Ezzi, 1987). Ba values were calculated on the basis of matrix resources (Colwell & Futuyma, 1971) for each season, size class, and day and night periods. Confidence intervals (CI95%)ofBa were obtained by means of the bootstrap method (Mueller & Altenberg, 1985) considering 2000 resamplings of the data (Hamilton, 1991). Intervals were estimated as the 97.5th and 2.5th percentile points of the bootstrap estimates, since these are better approximations than the standard confidence intervals (Efron & Tibshirani, 1998).

RESULTS Temperature, salinity, dissolved oxygen, and pH varied markedly throughout the year (fig. 2). The lowest temperature and salinity were registered from October to February, and only started to increase in March. While temperature gradually increases to its maximum in August, salinity increased rapidly attaining a maximum in May (fig. 2A). Dissolved oxygen and pH decreased during October, and increased rapidly towards November and February, when the maximum values were registered. The lowest dissolved oxygen and pH were observed in March and June (fig. 2B). Taking into account these results as well as those previously reported by Yáñez-Arancibia & Day (1988), three seasons were identified: the rainy season from June to October, the “nortes” season from November to February, and the dry season from March to May. DuringUNCORRECTED the monthly survey, 235 Callinectes rathbunae PROOFwere collected, while 354 were collected during the seasonal survey. Both the number and size of swimming crabs varied markedly throughout the year (fig. 3). The highest numbers CRUS [1.35] 2006/11/21 12:14; Prn:12/12/2006; 9:45 F:crus2380.tex; p. 7 (355-376)

FEEDING HABITS OF CALLINECTES RATHBUNAE IN TIME 7

Fig. 2. Monthly variation in: A, bottom water dissolved oxygen and pH; and, B, temperature and salinity in Las Palmas. Values are means ± se. of C. rathbunae were collected during the “nortes”; numbers decreased during the dry season, and reached a minimum during the rainy season. Size frequency distributions of C. rathbunae throughout the year (fig. 3) showed that the largest crabs (120-140 mm CW) appeared in Las Palmas during October. Smaller C. rathbunae began to appear in October (one individual), and their frequency increased slowly until January, when the lowest mean CW was registered (44.2 ± 1.4 mm CW). In February and March, crabs <60 mm CW were the most common, but a few larger individuals began to appear. From April onwards, the frequency of the smallest C. rathbunae decreased, while that of crabs of 60-120 mm CW increased (fig. 3). The composition and abundance of the epi- and infauna also varied throughout the yearUNCORRECTED (table I). Nine taxonomic groups were identified, PROOF out of which only bivalves, gastropods, tanaidaceans, amphipods, fish, and penaeid shrimp were part of the crabs’ diet. Taniadaceans and nematodes were the most abundant CRUS [1.35] 2006/11/21 12:14; Prn:12/12/2006; 9:45 F:crus2380.tex; p. 8 (376-424)

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Fig. 3. Monthly variation in the size frequency distribution of Callinectes rathbunae Contreras, 1930 collected in Las Palmas: n, number of crabs; CW, mean carapace width (mm ± se). groups in Las Palmas, and occurred in the highest densities during “nortes” (table I). Gastropods, mysids, and polychaetes were less abundant, whereas bivalves, amphipods, fish, and penaeid shrimps were markedly less abundant. The highest densities of bivalves, gastropods, mysids, penaeids, and fish were observed during “nortes”, while the highest density of polychaetes and amphipods occurred during the dry season. Both the repletion index and the %F of diet components varied throughout the year (fig.UNCORRECTED 4). Swimming crabs collected during the rainy season PROOF had relatively less full stomachs than those captured the rest of the year. In general terms, bivalves and plant material were the most frequent components in the diet of C. rathbunae CRUS [1.35] 2006/11/21 12:14; Prn:12/12/2006; 9:45 F:crus2380.tex; p. 9 (424-424)

FEEDING HABITS OF CALLINECTES RATHBUNAE IN TIME 9 (0.02) 3 3 − − 10 · 10 · 0.403 (8.3) 0.459 (6.3) 0.059 (3.1) 0.025 (0.5) 0.041 (2.3) 0.094 (4.5) 0.004 (0.04) 2.249 (52.3) 0.926 (22.6) ± ± ± ± ± ± ± ± ± 0.886 ± (0.02) 0.775 3 − 10 · 0.191 (0.9) 0.002 0.088 (0.5)0.266 (1.6) 0.412 0.311 0.498 (3.3) 0.155 0.105 (0.8) 0.026 0.171 (1.1) 0.112 0.421 (3.9) 0.221 8.085 (50.1) 2.582 4.450 (37.9) 1.116 ± ± ± ± ± ± ± ± ± 2.972 ± I ABLE T (0.0) 2.507 3 − 10 · sd) of the most important taxa found in the epi- and infauna at Las Palmas during the rainy season 0.059 (3.0) 0.137 0.019 (0.4) 0.254 0.128 (5.1) 0.515 0.260 (9.2) 6.003 0.022 (1.5) 0.119 0.063 (4.4) 0.170 0.369 (11.9) 0.075 2.869 (51.5) 7.921 0.239 (13.2) 0.623 ± ± ± ± ± ± ± ± ± ± 2 0.120 − ± m ·

UNCORRECTED PROOF individuals found in each season (%) is shown in parentheses. Note that swimming crab densities are expressed as number of individuals Swimming crabs 0.081 Polychaetes 0.357 AmphipodsFish 0.013 0.044 Penaeid post-larvae 0.089 GastropodsTanaidaceans 0.152 1.549 Mysids 0.398 Nematodes 0.276 Mean density (number of individuals TaxaBivalves 0.131 Rainy “Nortes” Dry (June-October 1999), the “nortes” season (November-February 2000), and the dry season (March-May 2000). Relative abundance of the total number of CRUS [1.35] 2006/11/21 12:14; Prn:12/12/2006; 9:45 F:crus2380.tex; p. 10 (424-445)

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Fig. 4. Frequency of occurrence (%F ) of dietary components of Callinectes rathbunae Contreras, 1930 collected in Las Palmas during monthly sampling. Rainy season, June-October 1999; “nortes” season, November-February 2000; and dry season, March-May 2000. The number of crabs (n)and percent fullness of stomachs (% ± se) are shown in each case: biv, bivalves; gas, gastropods; tan, tanaidaceans; anf, amphipods; pez, fish; pen, penaeids; m-v, plant material; r-a, unidentified remains; are, sediment; det, detritus.

(fig. 4). During “nortes”, bivalves, tanaidaceans, and plant material had the highest %F , but swimming crab remains, fish, and detritus were also present. During the dry season, bivalves were the group most frequently consumed, followed by tanaidaceans, gastropods, and plant material, which were consumed with approximately the same frequency. In this season, %F of swimming crabs remains and fish increased, whereas %F of remains decreased, and detritus was absent from the stomachs of C. rathbunae. The most important diet components during the rainy season were bivalves and plant material, followed by gastropods and detritus.UNCORRECTED During this season, other dietary components werePROOF absent (fig. 4). The mean values of the Levins index, Ba throughout the year lay within overlapping confidence intervals (fig. 5A). The lowest mean value was observed CRUS [1.35] 2006/11/21 12:14; Prn:12/12/2006; 9:45 F:crus2380.tex; p. 11 (445-476)

FEEDING HABITS OF CALLINECTES RATHBUNAE IN TIME 11

Fig. 5. Mean diet diversity index (Ba ± CI95%)ofCallinectes rathbunae Contreras, 1930 collected in Las Palmas: A-B, during monthly sampling; C, seasonal sampling. A, seasonal variations; B, variations by size class (CW mm); and C, daily variations (D: 9:00 and 13:00 h; N: 21:00 and 1:00 h). The overall mean value of the index (Ba; – –) and its confidence intervals (CI95%; ······) obtained during monthly (A and B) and seasonal (C) sampling are shown. during the rainy season (0.221 ± 0.234 CI95% [confidence interval], and relatively higher mean values were observed in the “nortes” (0.505 ± 0.092 CI95%) and dry seasons (0.541 ± 0.180 CI95%). The repletion index and %F of diet components also varied as C. rathbunae increased in size (fig. 6). Swimming crabs of 40-100 mm CW generally had full stomachs, while individuals of 100-140 mm CW had less full stomachs. The numbers of different diet components decreased as swimming crabs increased in size. Bivalves, gastropods, and plant material were found in all stomachs analysed and animal remains and detritus were present in almost all stomachs (except those ofUNCORRECTED swimming crabs 80-100 mm CW). The highest PROOF %F of tanaidaceans was observed among the smallest swimming crabs, and decreased gradually as crabs increased in size (fig. 6). Tanaidaceans however, were always absent in the CRUS [1.35] 2006/11/21 12:14; Prn:12/12/2006; 9:45 F:crus2380.tex; p. 12 (476-506)

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Fig. 6. Frequency of occurrence (%) of dietary components of Callinectes rathbunae Contreras, 1930 of different carapace width (mm) collected in Las Palmas during monthly sampling. The number of crabs (n) and percent fullness of stomachs (% ± se) are shown in each case. Names of components are as in fig. 4. stomachs of swimming crabs of 120-140 mm CW. Remains of swimming crabs occurred in low frequencies among small C. rathbunae (20-80 mm CW), but increased in occurrence among larger crabs (80-140 mm CW). Amphipods, fish, and penaeid shrimp appeared in low frequency in the stomachs of C. rathbunae of 20-80 mm CW (fig. 6). Mean Ba values among crabs of different size lay within overlapping confidence intervals (fig. 5B). Maximum Ba values were registered among C. rathbunae of

40-100 mm CW (mean values: 0.535 ± 0.115 to 0.548 ± 0.187 CI95%), while low Ba valuesUNCORRECTED were registered both among the smallest (20-40 mmPROOF CW; Ba: 0.344 ± 0.184 CI95%) and the largest swimming crabs (100-120 mm CW Ba: 0.454 ± 0.433 CI95% and 120-140 mm CW Ba: 0.419 ± 0.283 CI95%). CRUS [1.35] 2006/11/21 12:14; Prn:12/12/2006; 9:45 F:crus2380.tex; p. 13 (506-579)

FEEDING HABITS OF CALLINECTES RATHBUNAE IN TIME 13

TABLE II Mean carapace width (mm ± se) of Callinectes rathbunae Contreras collected in Las Palmas during the day (9:00 and 13:00 h) and at night (21:00 and 1:00 h) in the seasonal sampling. Rainy season, November 1999; “nortes” season, February 2000; and dry season, April 2000. The number of crabs collected is shown in parentheses

Hour Seasons Rainy “Nortes” Dry Day 97.3 ± 8.0 55.5 ± 1.9 52.1 ± 7.9 (7) (94) (9) Night 65.5 ± 7.1 54.4 ± 0.9 65.7 ± 6.4 (12) (274) (14)

The number of C. rathbunae collected at night was always higher than during the day, but differences in size varied seasonally (table II). During the “nortes” and dry seasons, when swimming crabs were most abundant, individuals collected throughout the 24 h period were similar in size. However, during the rainy season, when the abundance of C. rathbunae decreased, crabs collected during the day were larger than at night. Both the repletion index and the %F of diet components during day and night were similar (fig. 7). Bivalves and plant material were the most frequent components in the diet throughout the 24 h period, and only during “nortes” was plant material more frequent during the day than at night. During the rainy season, swimming crab remains were more frequent during the day than at night, whereas fish remains only occurred in stomachs from C. rathbunae collected at night (fig. 7). Mean Ba values were similar throughout a 24 h period, and always lay within overlapping confidence intervals (fig. 5C). Maximum values of Ba were recorded during the rainy and “nortes” season (0.463 ± 0.251 and 0.509 ± 0.299 CI95%,and 0.423 ± 0.142 and 0.469 ± 0.109 CI95%, for day and night, respectively), whereas minimum Ba values were recorded during the dry season (0.183 ± 0.2 and 0.214 ± 0.239 CI95%, for day and night, respectively).

DISCUSSION Callinectes rathbunae was the most abundant macrocrustacean found at Las Palmas. The local distribution of C. rathbunae within the hydrographic system of Laguna de Términos is associated to the mouth of the Palizada river and the peninsula of Atasta (Raz-Guzman et al., 1986), both areas that exert a great tidal influenceUNCORRECTED on Las Palmas. This species is well adapted PROOF to life in shallow coastal lagoons with substrates dominated by mud/sand and some gravel (Raz- Guzman et al., 1986). Both the proximity of Palizada and Atasta and the muddy CRUS [1.35] 2006/11/21 12:14; Prn:12/12/2006; 9:45 F:crus2380.tex; p. 14 (579-605)

14 M. MASCARÓ ET AL.

Fig. 7. Frequency of occurrence (%) of dietary components of Callinectes rathbunae Contreras, 1930 collected during the day (9:00 and 13:00 h) and at night (21:00 and 1:00 h) in the seasonal sampling. Rainy season, November 1999; “nortes” season, February 2000; and dry season, April 2000. The number of crabs (n) and percent fullness of stomachs (% ± se) are shown in each case. Names of components are as in fig. 4. substrate in Las Palmas help to explain the great abundance of C. rathbunae found throughout this study. In turn, spatial homogeneity of water characteristics and prey species (Mascaró, 2000), together with the great mobility of C. rathbunae, like other swimming crabs (Blackmon & Eggleston, 2001), help to explain its uniform distribution within Las Palmas. The abundance and size frequency distribution of C. rathbunae throughout the year varied markedly (fig. 3). The relationship between variations in water characteristics (fig. 2) and the population dynamics of the species suggest that seasonalUNCORRECTED changes determine variations in the abundance of thePROOF various size classes of these swimming crabs. The abundance of juvenile C. rathbunae during the “nortes” (fig. 3) suggests that a few months before, during the rainy season, CRUS [1.35] 2006/11/21 12:14; Prn:12/12/2006; 9:45 F:crus2380.tex; p. 15 (605-641)

FEEDING HABITS OF CALLINECTES RATHBUNAE IN TIME 15 there is a massive entrance of megalopae and early juveniles from the open sea. This event coincides in time with the recruitment of C. rathbunae in Laguna de Tamiahua, Veracruz (Rosas et al., 1994). Migration occurs when megalopae and early juveniles use tidal changes and sea water circulation to enter the water column during flood tides and remain at the bottom during ebb tides (Forward et al., 1997; Blackmon & Eggleston, 2001). A clockwise circulation of water within the Laguna de Términos transports megalopae and early juveniles through the mouth of Boca de Puerto Real (Gracia & Soto, 1986), helping them to settle in the adjacent system of Las Palmas. It has been reported that a decrease in salinity from the sea towards the lagoons constitutes a strong stimulus, triggering the capability of various decapod species to migrate towards estuarine habitats with low salinity (Mair, 1980). Studies on the osmoregulatory metabolism of C. rathbunae have shown that juveniles are well adapted to tolerate salinities as low as 5h, allowing colonization of oligohaline areas in coastal lagoons (Rosas et al., 1989). The abundance of juvenile C. rathbunae during the “nortes” coincides with the great abundance of epi- and infauna found in Las Palmas in this season (table I). The most important source of nutrients and organic matter in Las Palmas is the fluvial contribution generated during “nortes”, which favours the production of detritus consumers, very common among the epi- and infauna. During this season, the highest concentrations of nutrients and of total chlorophyll were recorded, as well as the greatest abundance of fish eggs, white shrimp, Litopenaeus setiferus (Linnaeus, 1767), blue swimming crabs, Callinectes sapidus, and the most representative groups of the epi- and infauna (Mascaró, 2000). Other studies have also reported that the greatest abundance of a variety of fish and species occurs during the “nortes” and rainy seasons, and that they are a consequence of the maximum water discharge from the confluence of rivers and the resulting high nutrient levels (Gracia & Soto, 1986; Yánez-Arancibia et al., 1986; Ramos & Sosa, 1999; Aguirre-León & Díaz-Ruiz, 2000). During the dry season, when salinity increased to values near 15h, C. rath- bunae decreased in abundance, and larger swimming crabs began to occur (fig. 3). During the rainy season, the lowest abundance of C. rathbunae was recorded, but crabs collected had the largest size. These results indicate that migration of adults towards the sea coincides with the first rains. Euryhaline species, such as C. rath- bunae, have developed adaptations to tolerate the salinity gradient often found in coastal lagoons. Juveniles tolerate estuarine waters with low salinity (Rosas et al., 1989), where they migrate to search for food and refuge from predators. Adults, by contrast,UNCORRECTED have limited osmoregulatory capacity when exposed PROOF to water below 20h (Rosas et al., 1989). This condition can help to explain the low abundance of large C. rathbunae in Las Palmas during the rainy season, as crabs, having attained adult CRUS [1.35] 2006/11/21 12:14; Prn:12/12/2006; 9:45 F:crus2380.tex; p. 16 (641-696)

16 M. MASCARÓ ET AL. size, start to lose osmoregulatory capacity and migrate towards the sea in search of habitats with higher salt concentrations. The diversity of food components found in C. rathbunae demonstrates that it is a generalist predator with the ability to capture highly mobile prey, such as fish and . These results support what has been observed in other , such as Scylla serrata Forskål, 1775 (cf. Hill, 1979) and Carcinus maenas (Linnaeus, 1758) (cf. Rangely & Thomas, 1987). The constant presence of semi-digested material and detritus in the stomach contents of C. rathbunae shows that rapid digestion takes place, particularly of soft-bodied preys that leave few hard structures for adequate identification. The constant presence of sand and silt can be explained by the accidental ingestion of sediments among large quantities of prey or, as has been suggested in other studies, by the ingestion of sediments that help grinding the food, accelerating the digestion of calcareous prey (Mantelatto & Christofoletti, 2001). The presence of crab remains in the stomach contents of C. rathbunae in Las Palmas reinforces the findings of previous studies regarding the importance of cannibalism on smaller individuals in the population (Paul, 1981; Choy, 1986). Overlapping confidence intervals for mean Ba values of C. rathbunae on all three temporal scales (fig. 5) indicate that the trophic niche breadth of this species does not vary significantly with season, crab size, or time of day. These results emphasize the generalist feeding strategy of C. rathbunae, and suggest that the high productivity of Las Palmas makes food abundance and diversity sufficient to maintain a relatively constant trophic niche breadth for all individuals in the population, both throughout the year and throughout a 24 h period. The results, however, do indicate seasonal variations in diet composition of C. rathbunae,as tanaidaceans, amphipods, penaeids, fish, and swimming crab remains failed to appear in the stomachs during the rainy season, while detritus failed to do so during the dry season (fig. 4). Because there is a strong temporal pattern in the size distribution of C. rathbunae occurring in Las Palmas throughout the year (fig. 3), differences in diet composition among seasons also reflected variations in diet composition between crabs of different sizes. For example, C. rathbunae of 100- 140 mm CW, predominant in samples during the rainy season, had no amphids, penaeids, or fish in their stomachs (fig. 6). When predators are opportunistic generalists, the occurrence of different diet components strongly depends on the abundance and availability of prey (Paul, 1981; Laughlin, 1982). Swimming crabs of the genus Callinectes are known to be extremely voracious predators that consume a great array of prey species, dependingUNCORRECTED on their immediate availability (Moncada & Gómez, PROOF 1980; Paul, 1981; Laughlin, 1982; Hsueh et al., 1992; Mantelatto & Christofoletti, 2001). In the present study, the %F of tanaidaceans and amphipods in the diet of C. rathbunae CRUS [1.35] 2006/11/21 12:14; Prn:12/12/2006; 9:45 F:crus2380.tex; p. 17 (696-749)

FEEDING HABITS OF CALLINECTES RATHBUNAE IN TIME 17

(fig. 4) increased during the “nortes” season as these prey became more abundant (table I). However, tanaidaceans were abundant during the rainy season, but were completely absent from stomach contents during this time of year (fig. 4). Additionally, bivalves were not particularly abundant in Las Palmas (table I) but were, together with plant material, the most frequent items found in the diet (figs. 4, 6, and 7). Previous studies underline the capacity of certain portunids to select their prey (Seed, 1980; Mascaró & Seed, 2001). Mascaró & Seed (2000) showed that Carcinus maenas consumed more mussels than oysters, even when these preys were offered in a proportion of 1 : 3, respectively. They explained their results in terms of the greater ease to manipulate mussel over oyster shells. Other authors have related food preferences in portunids to differences in profitability (Elner & Hughes, 1978) and the risk of structural damage of chelipeds and mouthparts when consuming hard-shell prey (Juanes & Hartwick, 1990). Results in the present study suggest that crab diet is not merely based on prey availability, and provide some indication of preferential feeding in C. rathbunae. Yet, laboratory experiments on the behavioural basis of prey selection are still needed, and should be designed to be able to discern between passive (the result of physical properties of prey and predator, such as velocity, chelipeds and mouth part structures, and prey abundance) and active components (active choice) of selective feeding behaviour (Barbeau & Scheibling, 1994). While ontogenic variations in mean Ba values were not significant (fig. 5B), variations in diet composition of C. rathbunae of different size class (fig. 6), indicate that small crabs include different food items than adults. Small size prey, such as tanaidaceans, amphipods, and shrimp post-larvae occurred more frequently in small C. rathbunae (20-80 mm CW), whereas larger prey, such as bivalves, swimming crabs, and fish occurred more frequently in larger individuals (80- 140 mm CW). These patterns can be partly explained as a result of the greater abundance of small C. rathbunae during “nortes”, when tanaidaceans, amphipods, and shrimp post-larvae were most abundant (fig. 3; table I). However, the results suggest that bivalves, swimming crabs, and fish were consumed by C. rathbunae of 80-140 mm CW in frequencies higher than expected, considering relative prey abundance. Bivalves, swimming crabs, and fish are probably too large and too difficult to be captured by the smallest C. rathbunae, but as crabs increase in size, they change their feeding strategy and are capable of capturing and consuming larger, more mobile prey. Experimental evidence has shown that C. sapidus of 30- 50 mmUNCORRECTED CW display a less selective feeding behaviour than PROOF larger con specifics (90-110 mm CW) when feeding on penaeid shrimp of different sizes (Mascaró et al., 2003). Other authors (Rangeley & Thomas, 1987; Mascaró & Seed, 2001) CRUS [1.35] 2006/11/21 12:14; Prn:12/12/2006; 9:45 F:crus2380.tex; p. 18 (749-799)

18 M. MASCARÓ ET AL. have explained that juvenile Carcinus maenas are less species-selective than adults, because of the morphological limitations of small crabs to capture large-sized prey. Small crabs (20-80 mm CW) were abundant during “nortes” and consumed large amounts of the most abundant prey at that time of year. By consuming the most available prey, juvenile crabs reduce feeding time, and consequently reduce predation risk (Rangeley & Thomas, 1987). This would be the result of physiolog- ical and ecological conditions unique to juvenile crabs; however, information on the energetic costs and benefits of prey selection among C. rathbunae of different size is needed. Callinectes rathbunae was consistently more abundant at night than during the day (table II). Related to this, Escobar (1987) reported the highest abundance of macro-invertebrates during night hours in El Cayo, Laguna de Términos, and associated this to the feeding and reproductive activities of species. In the present study, both stomach fullness and the %F of diet components were similar for crabs collected during the day and at night (fig. 7), suggesting that all C. rathbunae were collected while feeding and that the diet composition does not vary markedly throughout a 24 h period. The lack of statistical differences between mean Ba values indicates that the trophic spectrum of C. rathbunae feeding at different moments during the day also remains constant. The similarity between feeding habits of crabs found during the day and at night is probably because C. rathbunae occupy the same feeding areas throughout a 24 h period, and in general, consume prey that are abundant at each time of year (fig. 7). Circadian variations may be the result of an array of feeding and defence behavioural strategies, as well as competitive interactions within and between crab populations (De Coursey, 1983). In a study of the brachyuran community in Ubatuba, Brazil, Mantelatto & Franzoso (2000) suggested that feeding rhythms of Callinectes ornatus Ordway, 1863 are affected by the presence of other portunids using the same food resources. In the present study, no marked differences in dietary components between day and night periods could be found. Density of portunids in Ubatuba was one order of magnitude higher than in Las Palmas (0.016 ± 0.012 individuals · m−2 and 0.001 ± 0.002 individuals · m−2, respectively), suggesting that the feeding rhythms of C. rathbunae are not affected by intra- or inter-specific competition for food. This can further be supported by the great abundance and diversity of prey species available to crabs in Las Palmas throughout the year.

UNCORRECTEDACKNOWLEDGEMENTS PROOF The present study was part of the research project “Bases ecológicas para el manejo integral de los subsistemas lagunares de la Península de Atasta, Campeche: CRUS [1.35] 2006/11/21 12:14; Prn:12/12/2006; 9:45 F:crus2380.tex; p. 19 (799-909)

FEEDING HABITS OF CALLINECTES RATHBUNAE IN TIME 19

Laguna Las Palmas”, financed by the Fideicomiso para Estudios y Proyectos del Área Natural Protegida de la Laguna de Términos, Secretaría de Ecología del Gobierno del Estado de Campeche. We thank the participation of fishermen of the Ejido Puerto Rico, Atasta, Campeche, as well as Ing. Tomás Jesús García, Ing. Luis Enrique Hidalgo Arcos, Ing. Jaime Suárez Bautista, and M. en C. Pedro Pablo Gallardo Espinosa for technical assistance during sampling. We are grateful to M. en C. Rosa A. Florido A. for kindly verifying the taxonomic status of prey and to S. Bowers who edited the text.

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UNCORRECTED PROOF First received 24 April 2006. Final version accepted 26 September 2006.