The Fish Community of a Shallow Tropical Lagoon in Belize, Central America

Transcription

1 Estuaries Vol. 16, No. 2, p June 1993 The Fish Community of a Shallow Tropical Lagoon in Belize, Central America GEORGE R. SEDBERRY Marine Resources Research Institute P.O. Box Charleston, South Carolina JACQUE CARTER Wildlife Conservation International and University of New England Hills Beach Road Biddeford, Maine ABSTRACT: Trawl collections indicate that the fish community of the Belize barrier reef lagoon is dominated numerically and in biomass by grunts (Haemulidae), especially Haemulon sciurus and Haemulon flavolineatum. Although the gear selected for small sizes, length frequency analysis indicated seasonality in recruitment of the dominant species of grunts. Apogonids and tetraodontiform fishes were also dominant components of the community. Most fishes collected were juveniles of species that occur as adults on the main reef, or were small species that are resident in the lagoon. Of three habitats sampled, the mangrove creek had the greatest relative abundance and biomass of fishes, followed by the seagrass bed and the sand-rubble zone. There were no significant seasonal differences in fish relative abundance or biomass. Community structure analysis indicated a uniqueness in the mangrove fish community. Diversity (H') was high, and was due to high species richness and evenness of distribution of individuals among species. The Belize barrier reef lagoon serves as an important nursery habitat for juvenile fishes. Introduction Shallow tropical lagoons located between a barrier reef and a land mass comprise several habitats, including reef flats, seagrass beds, and mangrove creeks. The barrier reef complex of Belize, Central America, encompasses a large (approximately 6,000 km 2) lagoon that includes extensive sand-rubble, seagrass, and mangrove creek habitats, some of which are important fishing grounds (Craig 1966, 1969; Rfitzler and Macintyre 1982; Perkins and Carr 1985). These tranquil habitats landward of the reef crest can be high in productivity, relative to adjacent reef front sites, and serve as important nursery habitats that provide food and shelter for juvenile stages of many economically valuable reef fishes (Parrish 1989). Although similar in depth, temperature, and other physical variables, lagoon habitats differ in proximity to the barrier reef, in the amount of shelter from predation provided for juveniles, and in fi~.eding opportunities for fishes that inhabit them. Because of these factors, fish communities associated with forereef, backreef, seagrass, and mangrove creek sites should differ from one another with respect to species composition, relative abundance, and biomass of fishes. Relatively little is known of the ichthyofauna of the Caribbean coastal waters of Central America Estuarine Research Federation 198 (Weinstein and Heck 1979; Greenfield and Johnson 1981). As noted by Robins (1972), this coast, including the coast of Belize, contains a mix of insular reef species, as well as a continental fauna associated with bays and estuaries, where the lagoon, protected by the barrier reef, offers additional sheltered habitats such as seagrass beds and mangrove swamps. These areas contribute to the overall richness of the fauna found on the Central American coast (Robins 1972). Robins (1972) noted the need for assessment of the fish fauna of the coast of Honduras and Yucatan, the area under consideration in the present study. Subsequent collecting and studies have increased the knowledge of specific groups (Greenfield and Johnson 1981; Hay 1981; Lewis and Wainwright 1985; Greenfield and Johnson 1990a, b), increased known number of species from the area, and resulted in the collection of new species (Colin 1974; Collette 1983; Johnson and Brothers 1989). Consequently, our knowledge of fishery resources and structure of fish communities from some habitats has expanded (Perkins 1983). Ilowever, little quantitative sampling has been conducted, and community structure of most habitats remains poorly described. The purpose of the present study was to survey /93/ /0

2 Belize Lagoon Fish Community 199 Fig. 1. Belize. Location of sampling sites in the mangrove creek (A), seagrass bed (B), and sand-rubble zone (C) near Ambergris Cay, habitats suspected of being important nursery habitats in order to determine the relative abundance and biomass of juvenile and other fishes associated with lagoon habitats and to describe the composition of the ichthyofauna of a portion of the Belize northern lagoon. The spatial heterogeneity offered by the various shallow habitats within the lagoon allowed us to examine the hypothesis that relative abundance of juvenile fishes increases with distance from the main reef and its piscivorous predators, and with increased food and shelter offered by lagoon habitats that are spatially removed from concentrations of adults. Methods STUDY SITE Sampling was conducted in the vicinity of San Pedro Town, Ambergris Cay, located in the northern lagoon of Belize (Fig. 1). The shallow-water habitats associated with the Belize barrier reef, including the area near Ambergris Cay, have been described in detail (Craig 1966; Rfitzler and Macintyre 1982; Perkins and Carr 1985; Carter et al. 1988; Greenfield and Johnson 1990a). Habitats sampled include a channel separating two mangrove cays, hereafter referred to as the mangrove creek habitat. The mangrove creek was fringed with red mangrove, Rhizophora mangle, and the creek bottom was covered with fine sand and a dense stand of turtle grass, Thalassia testudinum. A second site, henceforth referred to as the seagrass site, consisted of a similar dense stand of turtle grass in the open lagoon. Although not measured, sand grain size was obviously coarser in the open lagoon seagrass bed than in the creek, and the water was less turbid in the open lagoon (10-12 m horizontal visibility) than in the creek (3-5 m visibility). The third habitat sampled was a sand and coral rubble zone just inshore of the coral pavement zone that graded offshore into a patch reef and rubble zone before emerging at the barrier reef crest, and graded inshore to the sandy lagoon floor that was covered with dense beds of T. testudinum. This zone corresponded to the sand and rubble zone of Rfitzler and Macintyre (1982). The sandrubble zone was located 60 m inshore of the reef crest, and the sampling site was located 50 m from the nearest patch reefs and 50 m from the nearest seagrass stand. The mangrove creek site was located 500 m inshore of the reef crest, which included a 30 m x 5 m deep cut through the barrier

3 200 G.R. Sodtmm/and J. Cart0~ TABLE 1. Sampling data. Number of Season Date Habitat Samples Winter 1985 February 26-March 29, 1985 Mangrove creek 6 Seagrass bed 4 Sand-rubble zone 3 Spring 1985 April l 1-May 29, 1985 Mangrove creek 3 Seagrass bed 3 Sand-rubble zone 3 Summer 1985 July 17-September 27, 1985 Mangrove creek 4 Seagrass bed 4 Sand-rubble zone 3 Fall 1985 October 28-November 30, 1985 Mangrove creek 2 Seagrass bed 2 Sand-rubble zone 2 Winter 1986 January 22-February 20, 1986 Mangrove creek 2 Seagrass bed 2 Sand-rubble zone 2 Spring 1986 April 8, 1986 Mangrove creek 1 Seagrass bed 1 Sand-rubble zone 1 reef. The seagrass site was located 200 m inshore of the reef crest and 25 m offshore of a sandy beach on Ambergris Cay. All sites were subjected to the same tidal amplitude (about 15 cm) and were 2 m deep. Ambergris Cay in the vicinity of the sampling sites is separated from the mainland by a km wide (up to 20 m deep) lagoon and from the barrier reef by a 200 m wide (5 m deep) lagoon. SAMPLING Sampling was conducted with a 5-meter-footrope semiballoon otter trawl, with the following mesh dimensions (stretched mesh, cm): 1.9 in the wings, 1.9 in the body, and 0.6 in the cod end. All trawl sampling was conducted during daylight, and tows were of 10 min duration. There were no observable differences in performance of the trawl in the three habitats. Following each tow, water temperature was measured with a stem thermometer, and salinity was measured with a refractometer. In order to minimize habitat damage, replicate tows were not done during each sampling trip. However, attempts were made to sample each site at least twice monthly, from February 1985 through April 1986, and samples completed within the same three-month period within a habitat were treated as replicates for biomass and relative abundance analysis. Gear and weather problems prevented us from completing all planned sampling (Table 1). Although trawls have limitations (Taylor 1953), they have proven to be suitable for sampling fishes for community analysis in shallow lagoon waters (Weinstein and Heck 1979; Stoner 1986). Catches were sorted to species and individuals were counted and measured. Total weight of each species in a trawl collection was measured to the nearest g, and standard length (SL) measured to the nearest mm for all individuals. DATA ANALYSES Relative abundance, biomass, and mean length were comparedamong months and habitats sampled by using one-way ANOVA on log-transformed abundance and weight per tow, and on mean SL. Transformed abundance and weight values were considered more reliable and were used to test for significant differences, because the problems of non-normality of fish distributions and trawl catches are reduced by transformation (Taylor 1953; Elliot 1977). The Fma X test indicated significantly heterogeneous variances (Sokai and Rohlf 1981); log-transformation reduced heterogeneity to acceptable levels for ANOVA. Because pooling resulted in unbalanced ANOVA, the general linear model (GLM) of the Statistical Analysis System (SAS) was applied to the data to test for significance (SAS Institute 1985). ANOVA was also run on ranked abundance and weight data for unbalanced comparisons, resulting in a nonparametric comparison of means (Kruskal-Wallace test). Generally results of these analyses and significance testing agreed, and ANOVA and the Scheffe test for significance were considered to be the most reliable for the one-way ANOVAs performed, and are reported herein. All seasonal comparisons (relative abundance, biomass) were based on data pooled on a trimonthly basis, which corresponded to the following seasons: winter or dry season (January-March); spring or dry-wet transition (April-June); summer or wet

4 B~e Lagoon Fish C~rnm~y 201 season (July-September); and fall or wet-dry transition (October-December). Length data were analyzed to detect monthly changes in growth and to determine the periodicity of recruitment of juveniles to the habitat and samplin. g gear. Normal cluster analysis was used to compare similarity of trawl collections in terms of species composition and relative abundance (log-transformed abundances). Inverse cluster analysis was used to define species assemblages, based on distribution and abundance (log-transformed). The Bray-Curtis coefficient (Clifford and Stephenson 1975) was used to measure similarity among collections and species distributions, and flexible sorting (Lance and Williams 1967) was used to group clustered entities. Very rare species (those occurring in only one tow) were excluded, since rare species have no discernable distribution or abundance pattern and their inclusion adds little to understanding of community structure (Boesch 1977). Nodal analysis (Boesch 1977) was used to determine affinities of species groups from inverse analysis to the clusters of stations defined by normal clustering. Constancy and fidelity diagrams were used to describe patterns of species group occurrence and affinity for certain habitats. Bray-Curtis (Bray and Curtis 1957) similarity values were also calculated for comparison of similarity among samples pooled by habitat. The Bray- Curtis measure was chosen as the most appropriate index for determining percent similarity and for cluster analysis because it accurately reflects similarity in species composition and abundance (Bloom 1981). Additional measures of community structure, species diversity (H') and its components, evenness (J'), and species richness were calculated for trawl collections by habitat and season. Diversity indices (H', J', and species richness) were calculated according to the methods of Pielou (1969) and Margalef (1968). Results Bottom water temperatures ranged from 25.5~ to 29.0~ and were typical of lagoon waters behind the barrier reef (Ferraris 1981). Salinities generally did not vary much, ranging from 33.0% to 35.0%. An exception was trawl samples collected on October 28, 1985, when salinities at the three sites ranged from 27.0% to 28.0%. BIOMASS AND ABUNDANCE Trawl catches were dominated by juvenile fishes and by various life history stages of small species. Many specimens represented life history stages of species more closely associated with the reef prop- er, and which may depend on lagoon habitats as nursery areas, whereas other species commonly spend their entire lives within the shelter of the lagoon. A total of 3,296 individuals representing at least 87 species and weighing kg was collected. Mean catch per tow was 68.7 individuals and kg. The mangrove creek had the highest relative abundance (135.8 individuals per tow and kg per tow), and 74.2% of all individuals were collected from the mangrove creek. Theseagrass bed had the second highest fish abundance (29.8 per tow), and also ranked second in biomass (1.040 kg per tow). The sand-rubble zone had the lowest standing stock of fishes, averaging 26.7 per tow. Biomass was very low in that zone, and averaged kg per tow. The mangrove creek had significantly higher mean catch per tow (relative abundance) than the other two habitats (one-way ANOVA, Scheffe; a = 0.05); however, biomass in the mangrove creek was significantly greater than in the sand-rubble reef flat, but not in the seagrass bed. Comparisons of relative abundance and biomass among seasons indicated no significant differences in relative abundance of fishes throughout the year within each habitat and for all sites combined. Generally, however, relative abundance in all three habitats, especially the mangrove habitat, was greatest during the spring and summer of 1985 (Fig. 2). Biomass was highest in the period from July to September in all three habitats (Fig. 2). Relative abundance and biomass in the mangrove creek habitat showed a wider seasonal variation in values than did other habitats (Fig. 2). Abundance of fishes in the mangrove creek habitat increased from the winter of 1985, reaching a maximum in spring (April-June). Biomass was maximum in middle and late summer (July-September). Biomass reached a maximum during this period in all three habitats (Fig. 2). DOMINANT SPECIES Grunts (Haemulidae) dominated the catches (Appendix 1), and consisted primarily of Haemulon sciurus (bluestriped grunt), Haemulon flavolineatum (French grunt) and Haemulon plurnieri (white grunt). Haemulon sciurus ranked first in overall abundance (Table 2) and weight (Table 3), and dominated in number in the mangrove and seagrass habitats (Table 4). Catches increased with distance from the barrier reef and were greatest in the mangrove creek (50.6 individuals per tow and kg per tow) and in the seagrass bed (7.1 individuals per tow and 408 g per tow) and were lowest in the sand-rubble zone (1.3 and 52 g per tow). Abundance and biomass was significantly higher in the mangrove creek than the other two habitats, but

5 202 G.R. Sedberry and J. Carter TABLE 2. Abundance,.weight (g), and frequency of occurrence in trawl collections of the ten most abundant species captured. Species Number (%) Weight (%) Frequency (%) Haemulon sciurus 1,041 (31.6) 25,854 (46.3) 37 (77.1) Haemulon flavolineatum 251 (7.6) 2,082 (3.7) 27 (56.2) Apogon aurolineatus 231 (7.0) 251 (0.4) 11 (22.9) Monacanthus ciliatus 211 (6.4) 1,037 (1.9) 37 (77.1) Jenkinsia stolifera 183 (5.6) 73 (0.1) 19 (39.6) Haemulon plumieri 154 (4.7) 3,763 (6.8) 20 (41.7) Canthigaster rostrata 84 (2.6) 388 (0.7) 23 (47.9) Chaetodon capistratus 73 (2.2) 278 (0.5) 13 (27.1) Astrapogon alutus 72 (2.2) 87 (0.2) 9 (18.8) Monacanthus tuckeri 69 (2.1) 113 (0.2) 11 (22.9) Total 2,369 (71.9) 32,926 (60.8) Fig. 2. Mean (+ one standard deviation) catch per tow as number of individuals (A) and weight (B) of fishes from lagoon habitats, by trimonthly seasonal interval. there was no significant difference between the sand-rubble zone and the seagrass bed. There were no significant differences among seasons in biomass or abundance. In the habitat of their greatest relative abundance, the mangrove creek, H. sciurus appeared to increase in abundance from January to June, then decrease from July through December, increasing in abundance again the following January (Fig. 3). Seasonal abundance patterns in the seagrass bed lagged behind the pattern for the mangrove creek habitat, but had a similar trend. The minimum monthly mean size for H. sciurus occurred during February 1985 (mean = 69.4 mm, n = 61). Maximum mean size was noted in September 1985 (mean = mm, n = 176), when mean lengths were significantly greater than in February. Length frequency was usually bimodal, with a strong mode of smaller fish during the winter and early spring months. Mean SL, all months combined, was 88.4 mm (range mm) in the mangrove creek, mm (range mm) in the seagrass bed, and 96.5 mm (range mm) in the rubble zone. Mean SL was significantly longer in the seagrass bed than in other habitats. Another haemulid, H. flavolineatum, ranked sec- ond in relative abundance and third in weight (Tables 2 and 3). Like H. sciurus, H. flavolineatum was most abundant in the mangrove creek and least abundant in the rubble zone (Tables 2 and 4). Mean catch per tow was significantly greater in the mangrove creek than in other habitats for abundance (12.8 individuals per tow) and weight (99.2 g per tow). Catches in seagrass and rubble habitats averaged 0.9 individuals (10.1 g) and 0.5 individuals (9.6 g), respectively. There was no significant difference in mean catch per tow between these two habitats or among seasons. Abundance in the mangrove habitat (where most H. flavolineatum occurred) was greatest from January to June 1985 (Fig. 3). Trawl collections indicated recruitment of the smallest H. flavolineatum (-<3 cm SL) in March and April 1985, and 93% of fishes collected at that time were in the mangrove creek habitat. Mean overall SL was 64.1 mm, and varied with habitat sampled, increasing with proximity to the main reef. Mean SL ofh. flavolineatum collected in the rubble zone (88.1 mm) was significantly longer than that for the mangrove creek (62.3 mm). The seagrass bed had intermediate mean length (75.6 mm). Several apogonids were collected (Appendix 1), and one species, Apogon aurolineatus (bridle cardinalfish), ranked third in overall relative abundance (Table 2). Astrapogon alutus, the bronze cardinalfish, was another apogonid that dominated numerically. Because of their relatively small size, apogonids contributed little to overall biomass. Apogon aurolineatus ranked third in relative abundance but only 29th by weight. Overall mean catch per tow for A. aurolineatus was 4.8 individuals and 5.2 g. All A. aurolineatus were trawled in the mangrove creek habitat where they made up about ten percent of the catch by number (Table 4). Catches within the mangrove creek were 12.8 individuals per tow and 13.9 g per tow. Catches fluctuated

6 Belize Lagoon Fish Community 203 TABLE 3. Weight (g), abundance, and frequency of occurrence in trawl collections of the ten species that dominated by weight in trawl collections. W~o~ht Number Frequency Species (%) (%) Haemulon sciurus Haemulon plumieri 24,854 (46.3) 3,763 (6.8) 1,041 (31.6) 154 (4.7) 37 (77.1) 20 (41.7) Haemulonflavolineatum 2,082 (3.7) 251 (7.6) 27 (56.2) Sparisoma chrysopterum 1,988 (3.6) 60 (1.8) 18 (37.5) Lactophms quadricornis 1,955 (3.6) 35 (1.1) 16 (33.3) Lutjanu,~ apodus 1,759 (3.2) 28 (0.8) 14 (29.2) Urolophus jamaicensis 1,598 (2.9) 21 (0.6) 14 (29.2) Lachnolaimus maximus 1,322 (2.4) 13 (0.4) 7 (14.6) Diodon holocanthus Monacanthus ciliatus 1,234 (2.2) 1,037 (1.9) 14 (0.4) 211 (6.4) 10 (20.8) 37 (77.1) Total 42,592 (76.3) 1,828 (55.5) seasonally (Fig. 3), but significant differences were not detected by ANOVA. Mean length ofa. aurolineatus was 27.5 mm SL, and all fish collected were less than 4 cm SL. Monthly mean lengths reached a minimum in October 1985 (mean = 16.3), which was significantly lower than other months. Tetraodontiform fishes were represented by four families and 14 species, several of which were dominant by number and weight (Appendix 1). Lactophrys quadricornis, Diodon holocanthus, and Canthigaster rostrata were occasionally caught, whereas Monocanthus ciliatus (fringed filefish) and M. tuckeri (slender filefish) were among the most abundant species (Tables 2 and 3). Monacanthus ciliatus ranked fourth in relative abundance (Table 2) and tenth by weight (Table 3), and was caught at the rate of 4.4 individuals per tow and 21.6 g per tow. Most individuals were collected in the mangrove creek (Appendix 1), but it was the most abundant species in the rubble zone (Table 4). Catches in the mangrove creek were 6.6 individuals and 15.0 g per tow. Mean catch per tow in the seagrass and rubble habitats were 2.0 individuals (17.3 g) and 4.3 individuals (35.0 g) per tow, respectively. Mean catches were not significantly different among habitats. There were no significant differences in mean catch per tow by season, although catches in the mangrove creek decreased markedly in October 1985 and in- TABLE 4. Species that ranked in the five most abundant species in any stratum. Percent of the total catch (by number) and rank for each stratum is given. Mangrove Creek Seagrass Bed Sand-Rubble Total Species % (Rank) % (Rank) 5~ (Rank) 9~ (Rank) Clupeidae Jenkinsia lamprotaenia Jenkinsia stolifera 0.3 (33) 1.2 (13) 21.0 (2) 4.8 (5) 14.7 (2) 0.8 (24) 5.6 (5) Apogonidae Apogon aurolineatus 9.4 (2) 7.1 (3) ttaemulidae Haemulonflavolineatum 9.4 (3) 2.9 (7) 1.9 (17) 7.5 (2) tlaemulon plumieri 5.6 (4) 1.0 (16) 3.2 (7) 4.8 (6) Haemulon sciurus 37.2 (1) 23.7 (1) 4.8 (4) 30.7 (1) Sparidae Sparisoma chrysopterum 1.2 (14) 6.1 (4) 0.8 (26) 1.8 (11) Acanthurldae Acanthurus bahianus 9.6 (3) 1.1 (13) Balistidae Monacanthus ciliatus 4.9 (5) 6.7 (3) 16.0 (1) 6.5 (4) Ostraciidae Lactophrys quadricornis < 0.1 (64) 5.9 (5) 1.6 (20) 1.1 (14) Total number of fishes collected 2, ,296

7 204 G.R. Sedberry and J. Carter Fig. 3. Mean (+ one standard deviation) catch per tow (number of individuals) of dominant species from lagoon habitats, by trimonthly seasonal interval. creased in the rubble zone during that time (Fig. 3). Mean SL of M. cileatus was 44.1 mm. Monthly length frequency distribution indicated that M. cileatus was first vulnerable to the gear at about 17 mm SL. Fish mm SL were collected during February and March 1985 and monthly mean length was at a minimum (mean = 33.4 mm, n = 15) in February Mean length decreased with distance from the barrier reef, and mean length of fish from the rubble zone (58.1 mm) was significantly greater than that from the mangrove creek (35.6 mm). Jenkinsia stolifera (shortband herring) was the fifth ranking species by number (Table 2), but only ranked 51st by weight. Jenkinsia stolifera was numerically dominant in the seagrass (6.2 individuals and 2.8 g per tow) and rubble (3.9 individuals and 1.1 g) habitats, where they ranked second in relative abundance (Table 4). They were also common (1.6 individuals per tow and 0.8 g per tow) in the mangrove creek, and there was no significant difference in mean catch per tow among habitats. There was similarly no significant difference in mean catch by season. Jenkinsia stolifera were represented by nearly equal numbers of fish in 1, 2, and 3 cm SL length categories (45, 48, and 41 fish, respectively). Mean length was highest in the seagrass bed (30.5 mm SL) and least in the rubble zone (25.7 mm SL), but differences in mean length were not significant among habitats or seasons. Additional dominant species varied in abundance by habitat. Haemulon plumieri, the sixth most abundant species, was similar to H. sciurus and H. flavolineatum, in that most were trawled from the mangrove habitat. Mean catch per tow in the mangrove creek (7.6 individuals) was significantly greater than the other two habitats, where < 1 individual per tow was collected. Canthigaster rostrata and Chaetodon capistratus were also significantly more abundant in the mangrove creek than in other habitats. Astrapogon alutus had significantly higher mean number per tow in the mangrove creek than in the seagrass. Differences in means between the mangrove creek and the rubble zone were not significant. Monacanthus tuckeri showed no significant difference in mean number per tow among habitats. Serranid fishes were diverse in the habitats sampled (seven species), but were not a dominant family by abundance or biomass. An economically valuable serranid, Epinephelus striatus (Nassau grouper) was frequently collected (Appendix 1). Mean number per tow of E. striatus (ranked 22nd by number and 23rd by weight) was significantly higher in the mangrove creek. ASSEMBLAGES The mangrove creek ichthyofauna had more unique components than did other habitats, and 14 species occurred only in the mangrove creek (Appendix 1). The mangrove creek habitat was dominated by H. sciurus, A. aurolineatus, H. flavolineatum, H. plumieri, and M. cileatus, which made up 66.6% of the total number of fishes collected from the mangroves (Table 4). Haemulon sciurus, H. plumieri, and H. flavolineatum dominated by weight, followed by Lachnolaimus maximus and Lutjanus apodus. These species made up 77.4% of the total biomass in the mangrove creek habitat. The seagrass habitat was dominated numerically by H. sciurus, J. stolifera, M. cileatus, Sparisoma chrysopterum, and Lactophrys quadricornis, which made up 63.3% of the total number of individuals. Haemulon sciurus, L. quadricornis, S. chrysopterum, Urolophus jamaicensis, and Diodon holocanthus ranked highest by weight and made up 67.2% of the weight of fishes collected in the seagrass site. Two species,

8 Belize Lagoon Fish Community 205 Gymnothorax vicinus and Chilomycterus schoepfi, were only collected at the seagrass site (Appendix 1). The rubble zone had the lowest fish abundance, and was dominated numerically by M. cileatus, J. stolifera, Acanthurus bahianus, H. sciurus, and Jenkinsia lamprotaenia. Those species were 50.0% of the total fishes trawled in the rubble. Haemulon sciurus, U. jamaicensis, Diodon holocanthus, Sphoeroides nephelus, and M. cileatus dominated by weight. Acanthurus bahianus and Holocentrus ascensionis were collected only in the rubble zone. Although relative abundance of each species varied by month, only two species, Hypoatherina harringtonensis and Sparisoma aurofrenatum, were collected exclusively in one month, May Normal cluster analysis resulted in groups of trawl collections that indicated the similarity of collections from the same habitat (Fig. 4). Most samples from the mangrove creek were grouped together (Fig. 4, Group 1). The exception was three samples from March 1985 that were grouped with samples from the two other habitats (Group 7). Group 2 consisted of collections from the seagrass bed, as were most of the collections in Group 3. Group 4 consisted mainly of stations from the seagrass bed, whereas Group 5 was collections made entirely in the rubble zone. Groups 6-8 consisted of collections from all three habitats. Group 6 comprised many samples from seagrass and rubble habitats that were taken in winter and spring, and Group 7 consisted of samples from all three habitats that were also mainly collected from winter and early spring. Group 8 consisted of two collections that were similar in composition, although they were from different habitats. Inverse cluster analysis resulted in 11 groups of species that were similar in spatial and temporal distribution (Figs. 5 and 6, Table 5). Some species groups (e.g., Group K) were frequent (i.e., high in constancy) at several site groups, whereas other species groups (e.g., Group J) appeared to be more restricted to specific habitat types. Species Group A was low in constancy in most site groups (Fig. 6), but was high in fidelity to the rubble zone habitat (Site Group 5). Group B species were high in constancy and fidelity to site Group 3 (mainly seagrass collections). Urolophusjamaicensis, Sphoeroides spengleri, and D. holocanthus in this group were among the most frequently collected species in seagrass habitats. Group C species were low in constancy among site groups, but showed moderate fidelity to site Group 2, which consisted entirely of collections from the seagrass habitat. Sphoeroides nephelus and L. quadricornis in this species group were among the most frequently collected species in the seagrass bed. Species Group D consisted of relatively uncommon species; almost all individuals of these species were collected in the mangrove habitat and they showed very low fidelity to collection groups from other habitats. Species in Group E were somewhat more abundant than those in Group D, but were similar in distribution and fidelity to the mangrove site. Species Group F consisted mainly of uncommon species that were found in small numbers in all habitats. The most abundant species in the group, J. lamprotaenia, was most abundant in the reef flat rubble zone. Species Group G also contained several species that, while uncommon, were found in all three habitats and were, consequently, low in fidelity to any site group. Sparisoma chrysopterum, the most common species in this group, was collected in all three habitats, but was most abundant in the mangrove and seagrass habitats. The remaining species were found in small numbers in all habitats. Species Group H was dominated by Hypoplectrus unicolor and Bodianus rufus, both of which were found exclusively in the mangrove creek habitat. Chaetodipterus faber, Coryphopterus glaucofraenum, Hippocampus erectus, and Archosargus rhomboidalis, uncommon species in Group H, were also found exclusively in the mangrove creek. One specimen ofacanthurus coeruleus was taken in the rubble zone. Group H species were highly faithful to the mangrove creek. Species Group I consisted of species that were found exclusively, or more frequently, in the rubble zone. Acanthurus bahianus, the most abundant species in this group, was found only in the rubble zone. All but one specimen of Scorpaenodes caribbaeus, a relatively common species, was trawled in the rubble zone. Species in Group I demonstrated low constancy but high fidelity to site Group 6, which consisted mostly of winter and spring collections from the rubble zone, with winter and spring collections from seagrass habitats also. Most of the species in Group J were collected mainly from the mangrove creek, and were thus higher in constancy and fidelity to site Group 1, which included most collections from the mangrove creek. Epinephelus striatus, Apogon binotatus, and A. aurolineatus were common to abundant species that were found exclusively in the mangrove creek. The remaining species in GroupJ were common species that dominated in the mangrove creek, but were also taken in one or more of the other habitats. Group K comprised those species that were the most abundant overall in trawl collections, and were somewhat ubiquitous in all habitats. They were

9 206 G.R. Sedberry and J. Carter Fig. 4. Dendrogram depicting normal cluster analysis of trawl collections by habitat (M = mangrove, S = seagrass, R = rubble zone) and month (year = 1985, unless indicated otherwise). very high in constancy in site Group 1, but occurred in high and moderate frequency in other site groups as well. Consequently, there was low fidelity of this species group for site groups. Species that were joined to form Group K were the two most abundant species collected (H. sciurus, H. flavolineatum), as well as other species that ranked among the ten most numerous species (3//. cileatus, J. stolifera, H. plumieri, C. rostrata, C. capistratus, and M. tuckeri). Many of the species in Group K were dominant in more than one habitat. Percent similarity values of collections (pooled by site) indicated that trawl collections from rubble and seagrass habitats were moderately similar in species composition and relative abundance (Tables 6). The mangrove habitat was dissimilar, and apparently harbored some unique components. Diversity (H') values were relatively high, but showed no consistent relation to season or habitat (Fig. 7). Diversity values tended to be higher in the summer and fall. Evenness values indicated a lack of dominance of the community in any of the three habitats by a single species. Species richness Fig. 5. Dendrogram depicting inverse cluster analysis of trawl collections. Letter designations correspond to the species groups in Table 5.

10 Belize Lagoon Fish Community 207 Fig. 6. Normal and inverse cluster hierarchies and nodal constancy and fidelity diagrams for trawl collections. values were generally greater in the mangrove habitat than in the other two sites. Discussion The ichthyofauna of the Belize northern lagoon has some components in common with other lagoon systems studied in the Caribbean region, although there were marked differences. Stoner (1986) found that soleids and gerreids dominated a lagoon in Puerto Rico, whereas haemulids were a minor component. Yfifiez-Arancibia et al. (1980) and Thayer et al. (1987) found that engraulids and gerreids dominated trawl collections in Terminos Lagoon on the western Yucatan and in seagrass beds adjacent to Florida Bay mangroves. Lasserre and Toffart (1977) found that gerreids, engraulids, and sciaenids dominated in mangrove swamps of variable salinity in Guadeloupe, West Indies. Haetoulon sciurus and H. flavolineatum, which dominated in the present study, were absent in the lagoons that Stoner (1986), Yfifiez-Arancibia et al. (1980), Thayer et al. (1987), and Lasserre and Toffart (1977) sampled. The difference in dominant species between those four sites and others (Louis et al. 1985; Sogard et al. 1989; Thayer and Chester 1989) and the present study, where haemulids dominated, may be related to physical conditions and proximity of the main reef. The lagoons trawled by Stoner (1986), Y~tfiez-Arancibia et al. (1980), and Thayer et al. (1987) were more restricted in access to open water, and were lower and more variable in salinity, (i.e., more estuarine conditions), whereas salinities in the present study were relatively constant and high. The fish community in the present study was dominated by juveniles of species common on Caribbean reefs as adults, and extensive nearby barrier reef formations such as that in Belize are not found near the lagoons studied by Stoner (1986), Y~tfiez-Arancibia et al. (1980), and others (see Pollard 1984). In addition, the northern lagoon community showed less seasonal variability than previous lagoon studies, probably as a result of a lower influence of terrestrial runoff. Weinstein and Heck (1979) found that juveniles of many reef species dominated in seagrass beds along the Caribbean coast of Panama, and many of their dominant species were also dominant species in seagrass in Belize. The results of the present study, like those of Weinstein and Heck (1979),

11 208 G.R. Sedberry and J. Carter TABLE 5. Species groups determined from inverse cluster analysis of trawl collections. Group A Sparisorna radians Lutjanus synagris Scorpaena grandicornis ltolocentrus ascensionis Lactophrys polygonius Group B Sphoeroides testudineus Halichoeres bivittatus Urolophus jamaicensis Sphoeroides spengleri Atherinidae Scorpaena sp. Diodon holocanthus Fistularia tabacaria Group C Pseudupeneus maculatus Lactophrys quadricornis Sphoeroides nephelus Astrapogon puncticulatus Chilomycterus schoepfi ttypoatherina harringtonensis G.~qnnothorax vicinus Group D Lachnolaimus maximus Hvpoplectrus sp. Eucinostomus sp. Status croicensis Group E Scaridae A Scaridae B Scaridae C Pomacanthus paru Calamus pennatula Cryptotomus roseus Sparisoma aurofrenatum Group F Trinectes inscriptus Mycteroperca bonaci Chaetodon ocellatus Bothus lunatus Jenkinsia lamprotaenia Group G Sparisoma chrysopterum Phaeoptyx pigmentaria Lutjanus analis Hypoplectrus puella Phaeoptyx conklini Ocyurus chrysurus Pomacentrus leucostictus Group H Chaetodipterus faber Acanthurus coeruleus ttypoplectrus unicolor Bodianus rufus Cor~'phopterus glaucoj(raenum ttippocampus erectus Archosargals rhomboidalis Group l Aluterus scripta Scaridae Acanthurus bahianus Scorpaenodes ca ribbaeus Group j Fpinephelus striatus Apogon binotatus Apogon aurolineatus Lutja nus griseus Lutja nus apodus Coryphopterus sp. Astrapogon alutus Group K Chaetodon capistratus Canthigaster rostrata Monacanthus tuckeri Acanthurus chirurgus llaemulon flavolineatum Haemulon plumieri Haemulon sciurus Monacanthus ciliatus Jenkmsia stolifera indicate that seagrass beds of the lagoon behind the barrier reef of Belize are an important nursery habitat for fishes that occupy the reef as adults. Overall, fish abundance and biomass in the present study increased with increasing distance from the barrier reef, that is, from the rubble zone to the seagrass habitat to the mangrove creek. Shulman (1985a), in a smaller scale experimental study of recruitment and juvenile reef fish abundance, found that Caribbean reef fish juveniles associated with reef and rubble zones were higher in abundance with increased distance from the main reef. Shulman (1985a) attributed this to reduced abundance of predators with distance from the reef. Fig. 7. Community structure values for trawl collections, pooled by season and habitat. Reduced abundance of predators in shallow lagoon waters and additional protection provided by increased turbidity, seagrass shoots, and mangrove roots, results in large numbers of juveniles using these habitats. Spatial separation of juveniles from adults that reside on the reef also reduces intraspecific competition and results in the more numerous (relative to adults)juvenile stages being concentrated in areas remote from the reef, such as seagrass beds and, especially, mangrove creeks. Three factors have been cited as contributing to the increased biomass and distinctiveness of the ichthyofauna of mangrove habitats relative to adjacent waters (Robertson and Duke 1987): differences in physical factors; differences in structural heterogeneity and thus predation intensity; and dif- TABLE 6. Bray-Curtis similarity values for habitats sampled, based on percent similarity of fish species composition and relative abundance. Mangrove Seagrass Seagrass Rubble

12 Belize Lagoon Rsh Community 209 ferences in productivity and food availability. Physical factors such as salinity and temperature were similar among the Ambergris Cay sites, although increased turbidity in the mangrove creek may have resulted in increased juvenile fish biomass by reducing susceptibility to predation (Blaber and Blaber 1980). Blaber et al. (1985) found a greater biomass and diversity of piscivores (sphyraenids, carangids, scombrids, carcharinids) in mangrove creeks in northwestern Australia and reduced abundance of juveniles of offshore species than were found in the present study. Mangrove creek habitats that do not have reduced turbidity are not effective nursery areas for juvenile fishes, since abundance of visual-feeding piscivores is high (Blaberet al. 1985). The mangrove creek near Ambergris Cay offered increased protection from piscivores by increased turbidity and availability of habitat complexity (seagrass and mangroves) in which to shelter from predators (Blaber and Blaber 1980; Robertson and Duke 1987), in addition to being distant from concentrations of reef-dwelling predators. Also, increased productivity of detritivorous benthic and planktonic prey organisms, important foods for juvenile fishes in these habitats (Odum and Heald 1972, 1975), probably results in increased fish biomass and diversity in mangrove creeks relative to other habitats. Abundance and biomass in the mangrove habitat showed a wider seasonal variation relative to other habitats, as noted in other studies (Robertson and Duke 1987), indicating importance of seasonal recruitment of many juveniles to this habitat. For example, length frequency for H. sciurus showed recruitment of large numbers of small juvenile fish, less than 5 cm SL, in the winter and early spring. This corresponds to the known spawning period (winter-spring) for H. sciurus (Munro et ai. 1973; Erdman 1976; Garcia-Cagide 1986), and these juveniles represent fish that are recruited to the mangrove creek following winter and early spring spawning. Although not significant, mean length of H. sciurus increased with proximity to the main reef, indicating a dominance of abundant small juveniles with distance from the reef. This is consistent with the documented life history ofh. sciurus, which move to reef areas to take up residence with increasing size. In addition to small juveniles, larger H. sciurus were present in the study areas, particularly in September-October. These larger fishes (15-18 cm SL) are sexually mature (Garcia- Cagide 1986) and may be adults foraging away from residence sites on the barrier reef or the nearby patch reefs that dot the lagoon. Visual census data confirm that larger H. sciurus occur on patch reefs, whereas smaller juveniles occupy seagrass beds in the lagoon (Barrick 1990). Haemulon flavolineatum settle into seagrass beds and other lagoon habitats by the time they have attained about 8.5 mm SL (McFarland et al. 1985), with peaks in settlement in May-June and October-November and little recruitment in winter in the Virgin Islands (McFarland et al. 1985). Based on seasonal availability to the trawl, it appears that peak settlement times for H.flavolineatum in Belize precedes that in the Virgin Islands, and a modal peak of fish from 1 cm to 4 cm SL was present in the collections made in March. The increased mean length with increasing proximity of sample sites to the main reef may reflect the ontogenetic movement of H. flavolineatum to the barrier reef from mangrove and seagrass nursery habitats (Helfman et al. 1982). The life history ofa. aurolineatus, the third most abundant species in this study, is unknown. It is considered a deeper water (> 12.2 m) cardinalfish (Bohike and Chaplin 1968). Results of the present study indicate that smaller individuals are abundant in shallow water, but were found only in the mangrove creek. The known life histories of cardinalfishes indicate that they are oral brooders, and that juveniles may occur in different habitats (e.g., lower salinities, in estuaries) than adults (Charney 1976; Chrystal et al. 1985; Kuwamura 1985). Most M. cileatus were collected from the mangrove creek. Previous studies have shown that M. cileatus prefers seagrass beds (Tabb and Manning 1961; Bohlke and Chaplin 1968; Clements 1982), and while most abundant in the seagrass-covered mangrove creek, M. cileatus were also common in the rubble zone, where it was the most abundant species. Monacanthus cileatus collected from the rubble habitat were significantly larger than those from the mangrove creek. It is likely that large adult M. cileatus occur in reef and rubble habitats, whereas the juveniles prefer seagrass and mangrove habitats, where they feed on invertebrates associated with seagrasses, as well as Thalassia itself (Clements 1982; Clements and Livingston 1983). Monacanthus cileatus in the present study did not demonstrate the marked seasonal changes in abundance that Clements and Livingston (1983) found, but were found in small numbers in all months sampled, perhaps because of the seasonal environmental stability found in Belize relative to northern Florida. Clements (1982) suggested winter spawning of M. cileatus in northern Florida, which was also suggested by minimum monthly mean lengths in February in the present study. Diversity (H') values for trawl collections were relatively high, and were comparable to summer diversity values for trawl collections in sandy coastal and reef habitat in the southeastern United States (Sedberry and Van Dolah 1984; Wenner and Sed-

13 210 G.R. Sedberry and J. Carter berry 1989). Number of species in seagrass beds in Belize was similar to that found in Caribbean seagrass beds in Panama (Weinstein and Heck 1979) and Costa Rica (Phillips and Perez-Cruet 1984), but was lower than that collected by Springer and McErlean (1962) in a monthly seine and pushnet survey of a seagrass bed in the Florida Keys (106 species). Diversity values tended to be higher in the summer and fall, and reflected growth and recruitment to the gear of many species spawned during peak spawning periods the previous spring (Munro et al. 1973). Evenness values in the present study were much higher than those noted for temperate reefs and smooth bottom habitats (Sedberry and Van Dolah 1984; Wenner and Sedberry 1989), but were similar to comparable habitats sampled by Phillips and Perez-Cruet (1984) in Costa Rica. Species richness values were higher in the mangrove habitat than in the other two sites, reflecting the increased habitat complexity provided by the mangroves and the seagrass occupying the bottom in the mangrove creek, and the recruitment of juveniles of many species to the mangrove creek. Thayer et al. (1987) also noted a greater number of species in mangroves relative to nearby seagrass beds in south Florida. Number of species, H', and J' values in the mangroves in the present study were higher than those reported by Bell et al. (1984) in a temperate mangrove creek. This is probably due to the relative stability of temperature and salinity in the present study, as well as increased habitat complexity afforded by the combination of seagrass and mangrove in the creek. Cluster and similarity analyses indicated a distinct pattern of species composition and abundance in the mangrove habitat. Seagrass collections were usually distinct, but often showed similarity to sandrubble collections. Greenfield and Johnson (1990a) noted distinct assemblages of blennioid fishes associated with shallow seagrass and mangrove habitats in Belize, based on ordination of ichthyocide collections. Robertson and Duke (1987) noted distinct mangrove and seagrass fish faunas in cluster analysis of seine catches in shallow estuarine habitats in northeastern Australia. Within the mangrove assemblage, collections also clustered seasonally by summer (February, December, April) and winter (July, August, October) (Robertson and Duke 1987). In the present study, subgroups within site Group 1 (which included most mangrove collections) tended to group seasonally (Fig. 4, Group 1). In spite of the importance of the mangroves as habitat for juveniles of many species, other species were more abundant in the sand-rubble zone. Acanthurus bahianus was found exclusively in the rubble zone. Lewis and Wainwright (1985) found that A. bahianus was absent from Thalassia beds, but was very abundant in the rubble and pavement zone of the barrier reef at Carrie Bow Cay, Belize. Acanthurus bahianus feeds on red algae that predominate in back reef rubble zones (Hay 1981; Lewis and Wainwright 1985; Kilar and McLachlan 1986), and occupies territorial holes in substrate that may not be available in seagrass and mangrove habitats (Shulman 1985b). Shulman (1984) described an assemblage of species typical of Caribbean and sand-rubble habitats, which included the abundant species Pomacentrus leucostictus, Gnatholepis thompsoni, Cor~phopterus glaucofraenum, Acanthurus bahianus, A. chirurgus, Haemulon flavolineatum, and Halichoeres bivittatus. Less common species in this assemblage from St. Croix were Canthigaster rostrata, Ocyurus chrysurus, and Chaetodon capistratus. Cluster analysis in the present study indicated that C. capistratus, C. rostrata, A. chirurgus, and H. flavolineatum clustered together but were frequently taken in all three habitats and showed little fidelity to site clusters representing any one habitat. Ocyurus chrysurus and P. leucostictus were in the same species group, but were uncommon in the collections, and that group was low in fidelity to all site groups. Acanthurus bahianus occurred in a species group that was moderate in fidelity to a site group that included many rubble zone collections. The few Coryphopterus glaucofraenum that were collected were all collected m the mangroves and were included in a species group that demonstrated m~)derate fidelity to mangrove sites. With the exception of Acanthurus bahianus, the sand-rubble species noted by Shulman (1984) do not appear to be restricted to rubble habitats in Belize. Shallow lagoon habitats, especially those adjacent to mangrove cays, appear to be major nursery sites for economically important species that are a large component of reef and lagoon fisheries in Belize and the Caribbean. Juveniles of Nassau grouper, Epinephelus striatus, the most important Caribbean commercial grouper (Craig 1966, 1969; Smith 1978) were taken only in the mangrove creek. Their small size (SL range = mm; mean = 54.9 mm) indicated that juveniles were utilizing the mangroves. Black grouper, Mycteroperca bonaci, while not abundant in the present study, is an important fishery species and occurred as juveniles ( mm SL; mean SL = mm) exclusively in the mangroves. Postlarval M. bonaci apparently settle into high salinity, turbid nursery habitats such as salt-marsh creeks (Keener et al. 1988) and mangroves (present study), which serve as nursery habitat for this species. Snappers, Lutjanus apodus and L. analis, are fished within the

14 Belize Lagoon Fish Community 211 lagoon in Belize (Craig 1966), and both of these species were found predominantly in the mangrove and seagrass habitats, where juvenile life-history stages predominated (mean SL = and mm, respectively). Other economically valuable species, the juveniles of which were most abundant in the mangrove creek, included the snappers Ocyurus chrysurus (mean SL = 65.3 mm; range ) and L. griseus (mean SL = mm; range ); white grunt (H. plumieri, mean SL = 88.1 mm; range ); and hogfish (Lachnolaimus maximus, mean SL = mm; range ). The mangrove creeks are an important habitat for juvenile stages of many economically valuable fishes in Belize as well as many other species of reef fishes that are found as adults on the barrier reef but which commonly occur as juveniles in the mangroves (e.g., scarids in the present study). Mangrove nursery grounds are currently subject to increasing degradation as a result of deforestation for export-oriented agriculture throughout the Caribbean slope of Central America (Nations and Leonard 1986). Increased sediment loading of coastal waters by deforestation and clearing of mangroves for Charcoal, lumber, and pasture are having serious effects on important commercial and subsistence fishery resources (Nations and Leonard 1986), as well as on the structure of reef and other fish communities, and should be carefully controlled and effects monitored in future biological surveys. ACKNOWLEDGMENTS We thank the government of Belize and V. Gillett, Fisheries Administrator, for cooperation in this research. For their help in field work, we thank J. Carter, E. Marron, J. Phipps, M. Rivero, I. Stains, and S. Younkin. K. Swanson assisted with graphics, and P. Keener and S. Sogard provided helpful reviews of the manuscript. 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