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Feeding ecology of juvenile marine fish in a shallow coastal lagoon of southeastern Mexico/Ecologia alimentaria de peces marinos juveniles en un sistema lagunar somero del sureste de Mexico.

INTRODUCTION

Coastal lagoons are recognized as high productivity systems that provide shelter for early-life stages of many marine fish species. Juvenile fish spend time in shallow coastal waters where they feed and grow to sub-adults before migrating into deeper waters (Blay et al, 2006). Shallow soft-bottom habitats, including mangroves and mudflats, are important nurseries for juvenile fish (Laegdsgaard & Johnson, 1995; Nagelkerken & Van der Velde, 2002; Verweij et al, 2006; Tse et al, 2008; Arceo-Carranza et al., 2009). The productive and structurally complex environment provided by mangrove stands is used as feeding grounds and refuge by juvenile fishes (Ruiz et al, 1993; Laegdsgaard & Johnson, 2001) and many juveniles and sub-adults of nocturnal species use these areas as refuge habitats during the day (Cocheret de la Moriniere et al, 2004; Verweij et al, 2006). Even if mudflats are structurally less complex, they hold a great abundance and diversity of invertebrates and are used as feeding grounds for juvenile fishes (Laegdsgaard & Johnson, 2001; Tse et al, 2008).

To assess the feeding habits is fundamental for understanding the role of fish within their ecosystems, since they indicate relationships among species based on feeding resources and they indirectly indicate community energy flux (Yanez-Arancibia & Nugent, 1977; Hajisamaea et al, 2003). This allows inferences to be drawn regarding the effects of competition and predation on the community structure (Krebs, 1999). Other resources, such as space, are also important for community ecology. Ecological theory predicts that resource partitioning at the spatial, temporal, and trophic level may reduce niche overlap and thereby reduce competition pressure between co-occurring species. Ross (1986) identified that food is the main limiting factor in aquatic environments, and suggested that the use of similar prey types defines functional groups within the community, so species can be grouped in guilds according to their trophic similarity. Trophic guilds (Root, 1967) seem to be a consequence of resource partitioning and could explain how several species can co-exist in the same space by the differential use of resources in several dimensions, including time. Studies of competitive exclusion and resource partitioning in teleost fishes (Hixon, 1980; Ross, 1986) have found that habitat partitioning could be related to high dietary overlap among competing species or to interactive competition, when competing species have the same preference for prey species (Jansen et al., 2002; Ramirez-Luna et al, 2008). Under the assumption that juvenile marine fish species use shallow coastal waters as feeding and refuge grounds, the goal of this study was to analyze and compare the diet of six marine fish species that use a shallow karstic lagoon and to assess the trophic overlap among them.

MATERIALS AND METHODS

La Carbonera Lagoon is located in the northeastern part of the Yucatan Peninsula. It is a semi-enclosed water body with an average depth of 30 cm and is surrounded by mangroves, mainly Rhizophora mangle and Avicennia germinans. The lagoon bottom is dominated by mud flats. It also contains freshwater seeps, although the average salinity is 35. Samples were obtained bimonthly from beach seine landings (40 m in length and mesh size of 2.5 cm) in nine soft-bottom sites (Fig. 1), from April 2008 to December 2010. Collected specimens were euthanized in ice slurry and preserved in formaldehyde (10%). In the laboratory, standard length (SL [+ or -] 0.1 cm) of each individual was measured, and the body weight (g [+ or -] 0.1) was obtained. Among all landings, juvenile marine species that use the lagoon to feed (Gallardo et al., 2012) were selected, since they are important in the transport of matter and energy between coastal environments. Maturity stages were assessed from the available data on length at first sexual maturity (Tzeek-Tuz, 2013; Froese & Pauly, 2014). Furthermore, we choose those species whose abundance was consistently greater than 30 individuals to analyze their stomach contents. According to these criteria, the species analyzed in this study were: Caranx latus, Oligoplites saurus, Trachinotus falcatus, Synodus foetens, Lutjanus griseus and Strongylura notata. A species accumulation curve was obtained to assess the sampling effort representativeness, measured as the number of stomachs analyzed. Parameters of the Clench model (1979) were obtained using Statistica 7.0 (Jimenez-Valverde & Hortal, 2003) considering 500 permutations of data obtained with EstimateS 8.0 (Colwell, 2006). The coefficient of determination was used as an indicator of the goodness of fit, and slope values below 0.1 were considered asymptotic.

Stomach contents

The number (N), weight (W), and frequency of occurrence (FO) of each dietary component were quantified and expressed as percentages (Hyslop, 1980). The index of relative importance (IRI) was calculated for each dietary component as (Pinkas et al., 1971).

IRI = (%N + %W)% FO

Cortes (1997) suggested that IRI values should be expressed as percentages (% IRI).

Data analysis Trophic guilds

One-way analysis of similarity (ANOSIM) was used to test the null hypothesis of no differences in the diet composition between the studied species over a Bray-Curtis rank similarity matrix constructed with the fourth-root transformed data. A cluster (using groupaverage linkage) was generated to determine the trophic guilds based on the diet similarities among species. Analyses were performed using the statistical package PRIMER 6 (Clarke & Warwick, 2001).

Diet breadth

The diet breadth was calculated using the Levin's standardized index (Krebs, 1999) as:

[B.sub.i] = 1/n - 1 {(1/[SIGMA]pi[j.sup.2]) - 1)}

where [B.sub.i] is the Levin index for species i; [p.sub.ij] is the proportion of the diet of predator i that is made up of prey j, and n is number of prey species. [B.sub.i] values range between 0 and 1. Zero indicates that fish feed on only one prey type, representing the minimum diet breadth and high feeding specialization. As the index approaches 1, the species consumes all food resources in the same proportion ([p.sub.j] = 1/n), representing no selection among prey types and the widest possible trophic niche (Krebs, 1999).

Feeding strategy

The Amundsen et al. (1996) method, which is a modification of Costello's (1990) graphical method, was used to obtain the feeding strategy of each species. This method uses the frequency of occurrence (%FO) and a percent measure of abundance (%N) to provide a description of prey importance (dominant or rare), predator feeding strategy (specialized or generalized), and the degree of homogeneity of feeding in the predator population (Bacha & Amara, 2009). To determine the feeding strategy, prey species were grouped as fish, crustaceans, mollusks, insects, and "others".

Diet overlap index

Shoener's index (Shoener, 1971) of niche overlap (a) was used to assess dietary overlap considering that [alpha] = 0 indicates that diets have no common items and [alpha] = 1 indicates identical diets (Wallace, 1981).

RESULTS

We analyzed 223 individuals belonging to six species (C. latus, O. saurus, T. falcatus, S. foetens, L. griseus and S. notata). Of them, 185 (83%) presented some type of food in their stomachs while 38 (17%) were empty (Table 1). C. latus, O. saurus, T. falcatus, and S. foetens were caught only as juvenile fish, according to data on length at first sexual maturity (Froese & Pauly, 2014); S. notata was captured in juvenile and adult stage (Tzeek-Tuz, 2013), and data of length at first maturity of the lizardfish S. foetens, are not available but, according to their sizes (4.0-15 cm), they were considered as juvenile fish (Fig. 2).

Diet composition

Species accumulation curves for each species are shown in Figure 3; slope values of the Clench (1979) model are greater than 0.1, with [R.sup.2] values >0.9. C. latus fed mainly on fish (78% IRI), but crustaceans were also consumed (20% IRI). O. saurus fed on small fish (97% IRI), principally Engraulidae. T. falcatus fed on mollusks, mainly bivalves (57% IRI) and gastropods (34% IRI). Crustaceans (7% IRI) such as amphipods, tanaids, and ostracods, were also present. S. foetens fed primarily on small fish (86% IRI) such as Gerreidae (Eucinostomus spp.), Cyprinodontidae (Floridich polyommus), and Clupeidae (Opisthonema oglinum); penaeid crustaceans were also present (8% IRI). Small Synodontidae were also found in their stomachs (10% IRI), which may constitute an evidence of cannibalism. The grey snapper (Lutjanus griseus), which is a commercially important species, fed on a wide variety of crustaceans (59% IRI), such as penaeid shrimps, amphipods, mysids, and isopods but also on fishes (35% IRI) such as Ariidae, Clupeidae and Cyprinodontidae. The Needlefish S. notata also consumed fishes (91% IRI) (Cyprinodontidae, Clupeidae, Gerreidae, and Atherinopsidae, mainly Menidia sp.), as well as decapod crustaceans (8% IRI) (Table 2).

Trophic guilds

The Bray-Curtis similarity index formed three groups (Fig. 4). The first includes C. latus, O. saurus, S. foetens, and S. notata which form the piscivorous trophic guild; the second has Lutjanus griseus that displayed a mixed diet composed of fish and crustaceans; while in the third group appears T. falcatus, a specialized carnivore whose mouth and dentine adaptations allow it to crush the calcareous shells of mollusks, mainly bivalves.

In the ichthyophagous guild, the analysis of similarities (ANOSIM) showed significant differences between each species (R Global = 0.109; P = 0.001) indicating that the most important prey types in the diet of each species differ (Table 3) even if fish are their main food.

Diet breadth

The diet breadth values indicate that all species display a specialized type of feeding behavior. Values of the Levin's index fall below 0.6 (O. saurus, Bi = 0.026; T. falcatus, Bi = 0.123; L. griseus, Bi = 0.124; S. notata, Bi = 0.036; S. foetens, Bi = 0.163; C. latus, Bi = 0.042), indicating that only a few prey types dominate the diet and predators can be classified as stenophagous species.

Feeding strategy and trophic overlap

Values of the Shoener's index of trophic overlap were greater than 0.6, indicating that the piscivorous species display a significant diet overlap (Table 4).

The feeding strategy displayed by the specialist fish analyzed was confirmed by the Costello method (Fig. 5). O. saurus, S. notate, S. foetens, and C. latus were classed as piscivorous. L. griseus specializes in the consumption of penaeid crustaceans, and T. falcatus feeds mainly on mollusks.

DISCUSSION

Shallow soft-bottom habitats are recognized worldwide as important nurseries for many marine fish species. Several factors, including high structural complexity, low predation risk, and high foraging efficiency, may explain why juvenile of many marine species use these shallow habitats (Tse et al, 2008).

The six species of fish examined are considered to be marine migrants (Castro-Aguirre et al, 1999; Elliott et al., 2007) that use shallow waters as nurseries, refuge, and feeding grounds. They are carnivorous species, mainly piscivores with stenophagy and trophic specialization (Carr & Adams, 1973; Arceo-Carranza et al, 2004; Cocheret de la Moriniere et al., 2004; Cruz-Escalona et al., 2005; Guevara et al., 2007). Even if many marine fish species exhibit marked changes in their diet according to the temporal availability of prey and life stage of individuals (Blaber, 1997; Platell et al., 1997; Hajisamae, 2009), our observations allow to say that five of them show a relatively homogeneous diet over time since the overall occurrence of these species within the study area is low (Gallardo-Torres et al., 2012). The species accumulation curves did not reach the asymptote, but values of [r.sup.2] > 0.9 indicate a good fit of the Clench model. Although one or two prey types dominate the diets of the majority of the analyzed species, representativeness of prey types was not achieved indicating that a greater number of stomachs ought to be analyzed. Anyhow, this is the first report on the diet of these migratory fish species in the study area.

In general, carangid are pelagic species considered to be piscivorous. Silvano (2001) reported that C. latus feeds on crustaceans and fish, and Carr & Adams (1973) place O. saurus as a piscivorous species; indeed, juvenile O. saurus analyzed in the present study fed almost exclusively on small fishes, principally Engraulidae.

Qualitative studies (Carr & Adams, 1973) on the feeding habits of T. falcatus, in the Cristal River, Florida, indicate that juvenile fish feed primarily on fish and benthic invertebrates, including worms, mollusks, and crustaceans, mainly shrimps. In La Carbonera Lagoon, juvenile fish consumed mainly mollusks, gastropods, and bivalves. Differences in the diet composition among geographical zones demonstrate the flexibility of this tropical marine fish, whose juveniles take advantage of the available resources in the environment. It has been reported that adults feed almost exclusively on mollusks and crabs (Carr & Adams, 1973).

On the other hand, the snapper L. griseus, is an euryhaline marine species that uses coastal lagoons bordered by mangroves for feeding. In the present study the trophic groups found in the stomachs of young individuals were benthic organisms (caridean shrimp and other crustaceans), which are usually considered as evasive species (Nagelkerken et al, 2000; Cocheret de la Moriniere et al, 2004; Guevara et al, 2007). In coastal systems of the southern Gulf of Mexico, Guevara et al. (2007) found that juvenile L. griseus feed on penaeid and caridean shrimp species during the night. This probably explains the fact that few individuals were collected since samplings for the present study were during the day.

The inshore lizardfish, Synodus foetens, is one of the most common coastal demersal predators on the Gulf of Mexico's continental shelf (Cruz-Escalona et al, 2005). This is a piscivorous species that feeds mainly on juvenile of other marine fishes known to be carnivorous, so it can be considered an apex predator on sandy bottoms of the continental shelf, which uses different habitats during its feeding activity and hunts various prey types, depending on resource availability and the size of prey (Esposito et al, 2009). There are no reports on the feeding habits of this species in the Gulf of Mexico but, off the coast of Italy, Synodus saurus is also a piscivorous species that feeds on small fish like sardines and anchovies (Esposito et al, 2009).

The needlefish, S. notata, is considered a piscivore (Carr & Adams, 1973; Arceo-Carranza et al., 2004) that obtains prey throughout the water column, as demonstrated by the presence of both demersal and pelagic components in the diet (Arceo-Carranza et al., 2004). Even if in this study juvenile and adult fish were analyzed, the low number of fish collected prevented to formally compare between size classes but it has been shown that this species displays ontogenetic changes in its diet (Arceo-Carranza, 2002; Hajisamae, 2009). Arceo-Carranza et al. (2004) found that S. notata from the Alvarado Lagoon, Mexico, is an active predator with great trophic plasticity to exploit the available resources in the environment (fish, shrimp, and insects among other prey types) while in the clearer waters of the northwestern coast of the Yucatan Peninsula it behaves as a piscivorous species.

Diet breadth of predators tends to increase when food availability is low, and decreases when food availability is high (Tse et al, 2008). The behavior of large predators feeding on larger prey usually follows the traditional optimal foraging theory which states that animals should maximize their net rate of energy return when selecting prey (Shoener, 1971; Bacha & Amara, 2009). The high diversity of prey found in the stomach contents of the six species analyzed in this work indicates that numerous food resources are exploited.

Piscivory is a common phenomenon in aquatic and marine ecosystems, and is the largest cause of fish removal in most marine ecosystems, usually larger than fishery catches (Link & Garrison, 2002) but, within this fish assemblage, it is difficult to determine the relative impacts of the different piscivores on other fish populations when considered as prey. For instance, some carangids can consume large numbers of demersal juveniles that use shallow nurseries, but these predators may feed only sporadically in shallow waters, in a manner similar to their transient feeding on coral reefs (Hixon & Carr, 1997). The coexistence of pelagic and demersal prey adds further complexity to the structuring of predation pressure by carangids on individual cohorts of recruits in shallow systems (Baker & Sheaves, 2005).

This study provides important information about shallow soft bottoms, including mudflats as important feeding grounds for fish. The species studied in La Carbonera Lagoon are marine fish that use turbid and shallow waters that provide shelter and food for juvenile stages. Furthermore, these results on the diet composition of juvenile fish provide evidence on the protection value of the mudflats adjacent to mangroves.

DOI: 10.3856/vol43-issue4-fulltext-1

ACKNOWLEDGEMENTS

The authors wish to thank Maribel Badillo Aleman for the administrative and operational support during sampling; Juani Tzeek and Alfredo Gallardo for technical assistance during sampling, and help in fish identification; the POSDOC program from DGAPAUNAM for a postdoctoral scholarship to D.A.C. This project was funded by PAPIIT (IN213012, IN219515) and FOMIX-Yucatan (103229) research grants. Fish were captured under the permit for collection awarded by the National Commission of Aquaculture and Fisheries number DGOPA/04031/310510.1940

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Received: 26 September 2014; Accepted: 2 February 2015

Daniel Arceo-Carranza (1) & Xavier Chiappa-Carrara (1)

(1) Unidad Multidisciplinaria de Docencia e Investigacion, Universidad Nacional Autonoma de Mexico Laboratorio de Ecologia, Puerto de Abrigo s/n, CP 97356, Sisal, Hunucma, Yucatan, Mexico

Corresponding author: Daniel Arceo-Carranza (darceo@ciencias.unam.mx)

Corresponding editor: Claudia Bremec

Caption: Figure 1. La Carbonera Lagoon (Yucatan, Mexico) and the sampling sites.

Caption: Figure 2. Length-frequency distributions of the fish species analyzed. First maturity and maximum size are shown (Tzeek-Tuz, 2013; Froese & Pauly, 2014).

Caption: Figure 3. Prey type accumulation curve (scaled by the number of stomachs) of each of the six marine fish species in the La Carbonera Lagoon (Os: Oligoplites saurus, Tf: Trachinotus falcatus, Lg: Lutjanus griseus, Sn: Strongylura notate, Sf: Synodus foetens, Cl: Caranx latus).

Caption: Figure 4. Diet composition and trophic guilds of six marine fish species, based on the Bray-Curtis similarity index.

Caption: Figure 5. Graphic representation of the dominant prey types (frequency of occurrence % and weight %) of six marine fish species.
Table 1. Size interval of captured specimens (standard length) and
sample size (number of stomachs) of six marine fish species in La
Carbonera Lagoon.

Species        Total      Number      Percentage      Standard
              number of   of empty     of empty       length
              stomachs    stomachs   stomachs (%)      (cm)

C. latus         42          12          28.57       4.70-23.50
O. saurus        36          0             0         5.09- 8.82
T. falcatus      35          10          28.57       4.70-18.00
S. foetens       34          1           2.94        4.02-15.10
L. griseus       39          5           12.82       3.15-22.50
S. notata        37          10          27.02       3.27-41.50

Table 2. IRI values for each prey type of six carnivorous fish
species in La Carbonera Lagoon, Yucatan.

                    C. latus   O. saurus   T.
                                           falcatus

Size class          4.7-23.5   5.09-8.82   4.7-14.2
N                         42          36         35
Fish
Unidentified         77.6111     86.9352     0.7997
  fishes
Clupeidae                         0.8013
Opisthonema
  oglinum
Belonidae
Strongylura
  notata
Poecilidae
Cyprinodontidae
Floridichthys         0.5665
  polyommus
Fundulus spp.
Gerreidae                         0.2050
Eucinostomus spp.     0.0221
Ariopsis spp.
Engraulidae                       9.4364
Menidia spp.          0.0055
Mugilidae                         0.0277
Sciaenidae            0.2772      0.2050
Synodontidae          0.0118
Crustacea
Unidentified         15.5034                 1.6876
  crustaceans
Decapoda
Brachyura
Penaeidae             2.5369      1.2297     0.2349
Farfantepenaeus
Caridea                           0.0094
Portunidae            0.1604
Amphipoda
Gammaridae                                   0.7997
Corophiidae                                  1.5586
Isopoda
Cassidinidae
Tanaidacea                                   0.0399
Mysidacea             2.1676      0.8203     0.0075
Ostracoda                                    2.5901
Copepoda
Mollusca
Unidentified          0.0116      0.0811     3.3713
  gastropods
Odostomia                                    0.4139
Truncatella           0.0008                 0.7634
Caecum                                       6.4368
Bittium                                      0.0799
Cerithium                                   22.8660
Bulla                                        0.0399
Neritina                                     0.0316
Olivella                                     0.3743
Unidentified                      0.0328    16.3846
  bivalves
Musculus                                     0.2079
Anomalocardia                                3.0710
Tellina                                     34.6154
Veneridae                                    1.2497
Brachidontes                                 1.9249
Annelida
Polychaeta                                   0.0777
Insecta
Diptera
Hymenoptera                       0.1989
Foraminiferida
Quinqueloculina                              0.1758
Plant remains
Seagrass              0.3481      0.0166     0.0062
Organic matter        0.7764                 0.1901
  no identified

                    L.          S.          S. notata
                     griseus     foetens

Size class          3.13-22.5   4.02-15.1   9.24-41.5
N                          39          34          37
Fish
Unidentified          32.7878     68.1451     78.5323
  fishes
Clupeidae              0.2086      1.8587      1.9298
Opisthonema                        1.3828
  oglinum
Belonidae                                      0.6713
Strongylura                                    0.1930
  notata
Poecilidae                                     0.6713
Cyprinodontidae                                4.1490
Floridichthys          2.0174      1.9498
  polyommus
Fundulus spp.                      0.4874
Gerreidae                          1.9498      2.3234
Eucinostomus spp.                  0.4874
Ariopsis spp.          0.4246
Engraulidae                        0.4874
Menidia spp.                                   2.6852
Mugilidae
Sciaenidae
Synodontidae                       9.9735
Crustacea
Unidentified          41.0167      0.1707      1.9139
  crustaceans
Decapoda               3.4835                  0.6713
Brachyura              0.2212                  2.6852
Penaeidae              4.3734      8.7165      1.3182
Farfantepenaeus        1.3034
Caridea                0.7781
Portunidae             0.6336                  0.6453
Amphipoda              4.2152                  0.9457
Gammaridae             0.5106
Corophiidae            0.4584                  0.1483
Isopoda                0.2893
Cassidinidae           2.0424
Tanaidacea                                     0.0510
Mysidacea              0.0556
Ostracoda              0.5106
Copepoda                           0.0032
Mollusca
Unidentified
  gastropods
Odostomia              0.0409
Truncatella
Caecum
Bittium
Cerithium
Bulla
Neritina
Olivella
Unidentified
  bivalves
Musculus
Anomalocardia
Tellina
Veneridae
Brachidontes
Annelida
Polychaeta
Insecta
Diptera                            0.4389
Hymenoptera
Foraminiferida
Quinqueloculina
Plant remains
Seagrass                           0.0259
Organic matter         4.6276      4.3871
  no identified

Table 3. Similarity, R statistic and P-values of ANOSIM test
of prey types that contribute to differences of diets among
fish species. Only significant combinations are show.

Predators                  % similarity   R value     P

O. saurus & C. latus          71.33        0.051    0.019
O. saurus & S. notata         78.23        0.081    0.014
O. saurus & S. foetens        82.26        0.088    0.005
O. saurus & L. griseus        84.83        0.171    0.001
O. saurus & T. falcatus       95.95        0.344    0.001
C. latus & S. notata          81.09        0.035    0.05
C. latus & S. foetens         85.39        0.056    0.01
C. latus & L. griseus         80.40        0.062    0.031
C. latus & T. falcatus        96.76        0.359    0.001
S. notata & L. griseus        88.66        0.046    0.041
S. notata & T. falcatus       97.68        0.199    0.001
S. foetens & L. griseus       92.04        0.060    0.016
S. foetens & T. falcatus      97.83        0.149    0.001
L. griseus & T. falcatus      97.10        0.254    0.001

Table 4. Trophic overlap (Schoener index) values for the six
species of juvenile marine fish (significant values in bold).

              C. latus   O. saurus   T. falcatus

C. latus                    --           --
O. saurus      0.8078                    --
T. falcatus    0.0240     0.0212
S. foetens     0.5050     0.8325       0.0239
L. griseus     0.6413     0.4587       0.0192
S. notata      0.8733     0.9343       0.0225

              S. foetens   L. griseus   S. notata

C. latus          --           --          --
O. saurus         --           --          --
T. falcatus       --           --          --
S. foetens                     --          --
L. griseus      0.5648                     --
S. notata       0.8982       0.5212
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Title Annotation:Research Article
Author:Arceo-Carranza, Daniel; Chiappa-Carrara, Xavier
Publication:Latin American Journal of Aquatic Research
Date:Sep 1, 2015
Words:5070
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