Habitat Assessment of Top Predators onReefs of Paraíba and Bahia States, NE Brazil by Athila Bertoncini

Habitat Assessment of Top Predators on Reefs of Paraﾃｭba and Bahia States, NE Brazil

ﾃ》hila Bertoncini Andrade Msc. in Zoology, Universidade Federal da Paraﾃｭba

Project AWARE Foundation - Grant Program Final report

Habitat Assessment of Top Predators on Reefs of Paraíba and Bahia States, NE Brazil

Áthila Bertoncini Andrade Universidade Federal da Paraíba, Laboratory of Fish Ecology and Conservation (LAPEC) CCEN - DSE, Cidade Universitaria, João Pessoa / PB. 58059-900, Brazil. apnea@uol.com.br Home address: Praça Benedito Calixto, 186 Ed. Barão de Capanema, ap.46, - Pinheiro/SP – Brazil 05406-040. phone:+55 47 2590241.

Habitat Assessment of Top Predators on Reefs of the State of ParaĂba, NE Brazil

CONTENTS

Foreword and Acknowledgments _________________________________ iii Abstract ____________________________________________________ iv

1. Introduction _______________________________________________ 1 2. Study Site ________________________________________________ 2 3. Methods __________________________________________________ 4 4. Results and Discussion ______________________________________ 6 4.1. Species Composition, Fish Length And Diversity______________________ 6 4.2. Species Relative Abundances, Frequency Of Occurrence And Richness ____ 8 4.3. Habitat Characterization _______________________________________ 11 4.4. Species Behavior ____________________________________________ 14 4.5. Ecological interactions ________________________________________ 18

References _________________________________________________ 23

Habitat Assessment of Top Predators on Reefs of the State of Paraíba, NE Brazil

FOREWORD AND ACKNOWLEDGMENTS This final report contains information on the research work carried out by Áthila Bertoncini Andrade (author) and Leonardo Francisco Machado, focusing habitat assessment of top predators on NE Brazilian reefs, which was developed during their Master of Sciences course at Universidade Federal da Paraíba (2001-2003). Financial resources were provided by CAPES

(Brazilian

Ministry

Education)

and

PADI

Project

AWARE

Foundation. Both thesis were presented in October 2003, and were evaluated by a specialists

committee

public

presentation,

Dr.

Ricardo

Rosa

(Universidade Federal da Paraíba), Dr. Maurício Hostim-Silva (Universidade do Vale do Itajaí) and Dr. Ierecê Lucena Rosa (Universidade Federal da Paraíba), and it is with great happiness that I inform that both were approved with honor. Much has happened since I decided to submit PADI Project AWARE Foundation my project proposal, and as we work with the environment, although everything is planned, it never goes the “perfect” way we wanted. Because of that, some things changed since the proposal approval, like the fact we had to choose other sampling areas, extending it to Bahia State, where we had better diving conditions to develop the research work. Here are presented only partial results of my thesis, which focused the Serranidae family (groupers). Although with some differences in the methodology and objectives, Leonardo’s thesis focused the Lutjanidae family (snappers). Fieldwork was carried out together, as my buddy diver. Although only my results are presented, it is with great pleasure that I inform that the grant received, resulted in the conclusion of two Msc. Thesis, and it was vital in the development of the fieldwork in the study areas. Soon our research works will be published in specialized magazines, and references and acknowledgements will be done to PADI Project AWARE Foundation. Thank you very much once again, and hope to count on Project AWARE in future projects, Áthila Bertoncini Andrade

iii

Habitat Assessment of Top Predators on Reefs of the State of Paraíba, NE Brazil

ABSTRACT Serranids are considered as top predators in reef environments, playing an important role in maintaining the ecological balance of hard-bottom ecosystems. However, to fulfill this role, the species must sustain a sufficient population density and a wide size range. The presence of such ‘‘healthy’’ grouper populations is one of the known benefits of the protection measures applied to marine protected areas. The availability, in marine reserves, of areas suitable for settlement and recruitment of early juveniles can contribute to preserve a well-structured population. Thus, knowledge of habitats preferred by juvenile groupers is an important step in locating, within protected or not yet protected areas, nursery sites that might need a specific protection regime. Underwater visual census, habitat characterization, photo and video observations were carried out in 38 dives in natural and artificial reefs in the States of Paraíba and Bahia, in order to gather information on serranids’ habitat preferences. A total of 60 transects and 186 habitat and behavioral characterizations were made. Best represented species were studied by correspondence analysis (CA). Nine serranid species were recorded, Cephalopholis fulva and Epinephelus adscensionis were the most abundant and frequent species, and with the highest number of characterizations, 120 and 38, respectively. Regarding behavioral aspects, species differed significantly, showing a clear contrast between C. fulva and E. adscensionis. Ecological interactions were observed between E. adscensionis e Myrichthys ocellatus, possibly characterizing a feeding interaction.

Habitat Assessment of Top Predators on Reefs of the State of ParaĂba, NE Brazil

1. INTRODUCTION Reefs are constantly under threat from human disturbances such as

overfishing,

destruction

mangroves,

coastal

development,

trampling by tourists and damage through boat anchors, which causes severe habitat loss for many reef species. Serranids and Lutjanids are commercially and ecologically important groups of predatory reef-fish, which have been heavily exploited through their range in Brazil. The States of ParaĂba and Bahia, NE Brazil, have a rich reef-fish fauna (ROSA, 1980; ROSA et al., 1997; ROCHA et al., 1998; SAMPAIO et al., 1999; SAMPAIO, 2003), which inhabits many of the coastal natural and artificial reefs. Habitat characteristics in natural and artificial reefs vary widely especially in topographic features and sessile fauna and flora. Although assessment of habitat requirements is an important step in locating reproductive aggregation sites as well as nursery sites (areas that need specific preservation measures) no data is available for the region. Specific goals were: (1)

Estimate Serranidae species composition and diversity, frequency

occurrence,

fish

length

and

relative

abundance; (2)

To assess microhabitat preferences for most abundant Serranids correlating with the reef structural complexity and diversity;

(3)

Describe ecological interactions observed during the study.

Habitat Assessment of Top Predators on Reefs of the State of Paraíba, NE Brazil

2. STUDY SITE

Coral reefs are among the world’s most complex marine ecosystems, where fish depend upon them for food and shelter. The study area included natural and artificial reefs along Paraíba's (PB) and Bahia's (BA) coast (fig. 01). Bahia's coast was included in the surveys in a

way

complement

the

data

obtained

Paraiba,

where

oceanographic and meteorological conditions did not allow dives since the preliminary report. Surveys were conducted at Paraíba on natural reefs A) Picãozinho (07º07'S and 34º48'W) and B) Areia Vermelha (07º01'S and 34º49'W) and artificial reefs G) Alice Shipwreck (07º03'S e 034º46'W) and H) Queimado Shipwreck (07º05'S e 034º44'W). At Bahia, on natural reefs of C) Ferro Velho, D) Porto and Farol da Barra, E) Iate Clube, and F) Caminho das Âncoras, and on artificial reefs I) Cavo Artemidi Shipwreck, J) Germânia Shipwreck, K) Ho-Mei III Shipwreck and L) Cap Frio Shipwreck.

Habitat Assessment of Top Predators on Reefs of the State of ParaĂba, NE Brazil

Figure 01: Study sites, along ParaĂba's (PB) and Bahia's (BA) coast, NE Brazil.

Habitat Assessment of Top Predators on Reefs of the State of Paraíba, NE Brazil

3. METHODS The quantitative analysis of reef-fish families was accomplished through visual censuses in replicated strip transects. The protocol is based on visualizing the boundaries of a 2 m wide X 30 m long transect (fig. 02) for fish censuses, resulting in a total area of 60 m2. Each sampling starts with the diver swimming slowly (2m/min), writing down, in PVC boards (fig. 03) information concerning species, number of fishes and size (total length).

Figure 02: Equipment used for transects.

Figure 03: PVC boards.

The underwater visual census method provides data on fish communities in a simple, objective and repeatable manner (see SALE, 1997). Besides that, this methodology has been intensively used in studies of population dynamics, ecology and management of reef fishes (JONES & THOMPSON, 1978; THRESHER & GUNN, 1986; ROSA & MOURA, 1997; LA MESA & VACCHI, 1999; ROCHA & ROSA, 2001a; KIKUCHI et al., in press.). For the assessment of habitat and behavior, the diver, swimming slowly above the bottom along a random course, accurately described each grouper sighting according to a standard protocol (see LAMESA et al., 2002). Information concerning size (total length), position and movement of fishes was recorded, in order to define the ‘‘behavioral’’ context of sightings. The description of habitat, where still or swimming fishes were first observed, was based on a small spatial scale (a circle with a

Habitat Assessment of Top Predators on Reefs of the State of Paraíba, NE Brazil

diameter of 50–80 cm centered on the fish), using both biotic and abiotic variables, ranked in ordered classes (Table I). On the small spatial scale, bottom depth, some topographic features of substrate, such as orientation, slope, sheltering degree and complexity (i.e. height of relief) were recorded. The influence of abiotic and biotic variables on the microhabitat requirements of groupers has been studied by correspondence analysis (CA) (JOHNSON & WICHERN, 1998). The contingency tables were constructed by splitting each variable into different classes, which were coded 0 or 1. A χ2 test was applied in order to test if the specimens of serranids were equally distributed along each axis. The statistical analysis of data was performed by means of the Statistica 5.0 (Statsoft) software packages.

Table I. Summary of ranked variables used in describing fish behavior and habitat features. Set of Variables

Code Ranks 1

Behavioural context Size class (cm) Distance from the bottom (cm) Moviment

CT DF M

<10 0 swimming

11-20 1-5 resting

21-30 6-10 still

>30 >10

Habitat Depth (m) Ligth Intensity Concavity Slope (º) Complexity (height of the relief) (cm) Rugosity (height of micro-relief) Cavity Cavity size (cm) Cavity orientation (º) Sand Calcareous algae Non-calcareous algae Sponge Coral

P IL CC AG CP RG CV TC OC AR AC AN E C

0-5 full very concave ~0 <5 high close 5-20

6-10 medium concave ~30 5-10 low open 21-40

11-20 shade flat ~60 >10

>20

present present present present present

absent absent absent absent absent

convex >90

absent 41-100

Species were classified regarding their frequency in sampled sites in three classes: Common (>75%, occurring at least on 7 sites), Occasional (50-74%, occurring at least on 5 sites) and Rare (inferior to 50%). Surveys were undertaken from January to June 2003, as part of the Msc. thesis by the author.

Habitat Assessment of Top Predators on Reefs of the State of Paraíba, NE Brazil

4. RESULTS AND DISCUSSION Underwater visual census, habitat characterization, photo and video observations were carried out in 38 dives in natural and artificial reefs in the States of Paraíba and Bahia, in order to gather information on serranids’ habitat preferences. A total of 60 transects and 186 habitat and behavioral characterizations were made.

4.1. SPECIES COMPOSITION, FISH LENGTH AND DIVERSITY

Nine serranid species were observed during the study. Two of them had only one occurrence, and were not inside the transect’s limits: Epinephelus itajara, the goliath grouper was observed at Cavo Artemidi Shipwreck (BA), and Mycteroperca bonaci, black grouper, observed in a small tide pool at Areia Vermelha Reef (PB) (Table II).

Tabela II. Serranid species observed in the study. PB (Paraíba) and BA (Bahia) and their respective length classes CT1(<10 cm), CT2(11-20 cm), CT3(21-30 cm) and CT4(>31 cm).

Species

common name

Alphestes afer (Bloch, 1793)

Mutton Hamlet

CT2/CT3

CT2

Cephalopholis fulva (Linnaeus, 1758)

Coney

CT1/CT2/CT3

CT1/CT2/CT3/CT4

Epinephelus adscensionis (Osbeck, 1765)

Rock Hind

CT1/CT2/CT3

CT1/CT2/CT3/CT4

Epinephelus itajara (Lichtenstein, 1822)

Goliath Grouper

Mycteroperca bonaci (Poey, 1860)

Black Grouper

Rypticus saponaceus (Bloch & Schneider, 1801) Greater Soapfish

CT4 (1,2 m) CT1 CT1/CT2/CT3

CT1/CT2/CT3/CT4

Rypticus bistrispinus (Mitchill, 1818)

Freckled Soapfish

CT1/CT2

Rypticus subbifrenatus Gill, 1861

Spotted Soapfish

CT1

Paranthias furcifer (Valenciennes, 1828)

Creolefish

CT1/CT2/CT3/CT4

As shown in Table II, there was a difference in the composition of species between the two States (PB and BA), so that only four species were common in both States. Many studies were already carried out in order to evaluate the influences of habitat structure and complexity on the community structure of reef fishes in natural reefs (LUCKHURST &

Habitat Assessment of Top Predators on Reefs of the State of Paraíba, NE Brazil

LUCKHURST, 1978; GLADFELTER & GLADFELTER, 1978) and artificial reefs (RUSSEL et al., 1974; MOLLES, JR., 1978; CHANDLER et al., 1985; ALEVIZON et al., 1985). Among these, many focused only adult fishes, remaining the juveniles poorly studied. The relationship between fish size and reef complexity may suggest the importance of sheltered areas as a refuge for some fish species. Such fact may explain some differences observed in Table II. According to our data regarding habitat characterization (n=186), when Paraíba’s

and

Bahia’s

percentage

data

are

compared,

find

respectively, high rugosity (RG1) 58% against 64%, and highest complexity (CP3) 54% against 75%. This higher substrate complexity observed at Bahia’s reefs, could be providing shelter for some smallbodied reef fishes, such as the ones from the Rypticus genera, which were not observed at Paraíba, but is reported for that area (e.g. Rypticus subbifrenatus). Besides that, the variety of habitats available in coral reefs offers shelter against predation (FREIDLANDER, 2001) for many species (e.g. juvenile serranids). WICKHAM et al. (1973) and POTTS & HULBERT (1994) suggest that structural complexity moderates predation, creating more zones of refuge, thus reducing the foraging efficiency of predators. Although ROCHA et al. (1998) reported 11 species of serranids compounding the ichthyofauna of Paraíba, the absence of some species in our study is certainly due to our reduced sample effort, allied to differences in methodology, number of studied sites and sampled depths. The reported serranid species not sampled by our methods were: Diplectrum formosum (Linnaeus, 1766), Epinephelus guttatus (Linnaeus, 1758), Epinephelus itajara (Lichtenstein, 1822), Rypticus subbifrenatus Gill,1861, Serranus annularis (Günther, 1880) and Serranus flaviventris (Cuvier & Valenciennes, 1830).

Habitat Assessment of Top Predators on Reefs of the State of ParaĂba, NE Brazil

4.2. SPECIES RELATIVE ABUNDANCES, FREQUENCY OF OCCURRENCE AND RICHNESS

The coney (C. fulva) was the most abundant species (12.3 individuals 60 m-2 at Queimado Shipwreck) and the most frequent, occurring in at least in one size class in 53 of the 60 censuses. This species, as well as, the rock hind (E. adscensionis), was considered common in our samples. The greater soapfish (R. saponaceus) was an occasional species and the remaining serranid species were considered rare (Table III).

Table III. Mean (top number) species densities (number 60 m-2) and standard error (bottom number) for study sites. Artificial reefs (n=26) Queimado Alice 6 4

Species N transects Alphestes afer

0.003

Artemidi 14

Natural reefs (n=34) Areia Vermelha PicĂŁozinho 4 8

Ho-Mei 2

Farol da Barra 4

Iate Clube 5

Porto Barra 13

0.054

0.075

0.025

0.021

0.056

0.025

0.050

0.031

(0,036)

(0,019)

(0,008)

(0,019)

(0,015)

(0,008)

(0,011)

(0,025)

0.004

0.001

0.021

0.004

0.006

0.017

(0,022)

(0,003)

(0,011)

0.004

0.001

0.011

0.005

(0,004)

(0,007)

0.011

0.009

(0,004)

(0,01)

(0,002)

Cephalopholis fulva

0.206 (0,037)

Epinephelus adscensionis

0.006 (0,003)

(0,004)

Paranthias furcifer

(0,001)

0.035

0.008

(0,010)

(0,008)

0.002

Rypticus subbifrenatus

Rypticus bistrispinus

Rypticus saponaceus

0.008

0.004

(0,005)

(0,006)

(0,002)

(0,004)

(0,003)

Data from Table III can be visualized, for the most frequent species, in figure 04 (coney), figure 05 (rock hind) and figure 06 (greater soapfish), where data was converted for number of fish 1000 m-2. Relative densities had a high variation among sites. Coney had highest mean relative densities at Queimado Shipwreck, followed by Cavo Artemidi Shipwreck, while rock hind had highest mean relative densities at Areia Vermelha and Ho Mei Shipwreck. Differently, greater soapfish showed low, thus more stable, mean relative density values in the areas where it occurred. The distribution and abundance among serranids in a system may be

influenced

variety

ecological

processes,

including

recruitment, competition and habitat structure (BEETS & HIXON, 1994; HIXON, 1991; JONES, 1991; SALE, 1991).

Habitat Assessment of Top Predators on Reefs of the State of ParaĂba, NE Brazil

Figure 04: Mean coney relative densities (number of fish 1000 m-2) and standard errors (black lines) for study sites.

Figure 05: Mean rock hind relative densities (number of fish 1000 m-2) and standard errors (black lines) for study sites.

Habitat Assessment of Top Predators on Reefs of the State of Paraíba, NE Brazil

Figure 06: Mean greater soapfish relative densities (number of fish 1000 m-2) and standard errors (black lines) for study sites.

Serranids’ richness varied from two to five species at studied sites. Among artificial reefs, Cavo Artemidi shipwreck was the richest, with five species (including the sighting of E. itajara, goliath grouper), while among the natural reefs, Porto da Barra was the richest, with five species too. Different relative abundances among species are in fact expected, because each one has a different ontogenetic shift (see JOHANNES, 1978), from changes in feeding behavior to migrations from shallower waters to deeper waters (DERBAL & KARA, 1995), searching for larger caves and shelters, as well as, larger preys. To sum up, a great group of factors influences the demographic structure of these different fish populations. Many

studies

already

showed

correlations

between

fishes’

distribution in reefs, and physical and biological factors (JONES, 1991). Among groupers (family Serranidae), many species exhibit different patterns of distribution and habitat preference. Significant differences among abundance and groupers size at different habitat were observed in Madagascar (VIVIEN, 1973, WILLIAMS, 1991), Maldives Republic (SLUKA & REICHENBACH, 1996), Red Sea (SHPIGEL & FISHELSON, 1989), Bahamas 10

Habitat Assessment of Top Predators on Reefs of the State of ParaĂba, NE Brazil

(ALEVIZON et al., 1985) and Florida Keys (SLUKA & SULLIVAN, 1996, SLUKA et al., 1998, 2001). SYMS & JONES (2000) reported that there is increasing evidence that the structure of coral reef habitats can have a major influence on the abundance of reef fish populations and the structure of reef fish communities.

Correlations

between

fish

abundance

and

habitat

availability suggest that some resource provided by the habitat must play a role in limiting populations. Habitat structure can affect the magnitude of recruitment in space and time, particularly in species that exhibit strong habitat selection at the time of settlement onto the reef (JONES & MCCORMICK, 2002). Densities found for coney and rock hind in the present study are similar to the ones reported by SLUKA et al. (2001) for Florida Keys reefs, using the transect method. Nonetheless, our data for the Rypticus genera, were probably underestimated due to their cryptic habits. It is known that these species do not suffer predation and are not fished (although eventually captured for aquarium trade (SAMPAIO, 2003)) because they release a toxic mucous, avoiding predators (RANDALL, 1996), so it would be expected a higher abundance of Rypticus species, when compared with fished species. Another explanation would lay in the fact that our censuses were only carried out during daytime.

4.3. HABITAT CHARACTERIZATION

The best represented species were studied by correspondence analysis (CA), which were, Cephalopholis fulva (coney) and Epinephelus adscensionis (rock hind), with the highest number of characterizations (see Table I for variables), 120 and 38, respectively, and coincidently the most abundant and frequent species. The distribution patterns of coney and rock hind, and of variables evaluated on the habitat characterization are given in figure 07.

Habitat Assessment of Top Predators on Reefs of the State of Paraíba, NE Brazil

Axis 1 (12.99% of inertia)

Figure 07: Representation of axes 1 and 2, result of correspondence analysis for the variables of regarding the habitat. Abbreviations are listed in Table I.

The first five axes explained 42.3% of the total information (inertia). Axis 1 (12.99% of inertia) showed a clear gradient of concavity (CC1-CC3), light intensity (IL3-IL1), cavity (CV1-VC3) and angle (AG1-AG4), showing an opposition between these groups of variables. On the negative side of axis 1, the variables CC1, CV1, OC2, TC2 and IL3 were all related with the presence of a cavity, so they are related to individuals that were observed close or within a cavity, shaded areas, or structures with angles from zero to 30º (AG1 and AG2). In opposition, on the positive side of axis 1, CV3, CC3 and IL1 were the variables with highest contribution, corresponding to those fishes observed in open areas, in the absence of cavities or recesses, areas with high light intensity, and/or structures presenting angles of 90º or obtuse (AG4). Analyzing axis 2 (9.09% of inertia), the variables AC2, C2 and RG2 are observed close to ART, representing individuals associated to artificial reefs. On the opposite side are the variables AC1, C1 and RG1,

Habitat Assessment of Top Predators on Reefs of the State of ParaĂba, NE Brazil

which are also close to variable NAT, characterizing individuals observed manly on natural reefs. To sum up, axis 1 separated observations in two groups: (1) close or within a cavity and (2) open areas, not related to a cavity. Axis 2 separated observations in two other groups, considering the nature of the reefs, being the most evident group established on the positive side of this axis. This group characterized artificial reefs as areas of low rugosity and a lesser presence of calcareous algae and corals. In opposition, the negative side of axis 2 suggests that natural reefs present a higher rugosity, which is associated to the higher abundance of calcareous algae and corals. Analyses of spatial distribution of fishes showed that rock hind individuals were more abundant on the positive side of axis 1 and negative side of axis 2 (Table IV), showing some preference for open areas, well illuminated, as well as, substrate with high rugosity, thus resulting in a greater tridimensionality, which is generated by this higher presence of incrusting organisms, such as calcareous algae and mainly corals. Despite that, considerations regarding E. adscensionis preferences for natural or artificial reefs are limited due to our low sample number on artificial reefs, besides that the analysis was not significant (Table IV). Analyzing coney data, a very similar distribution along both axes was observed, not assuming a defined pattern of distribution. In this case, variables appear not to influence the distribution of these species in the environment (Table IV).

Table IV. Results of Ď&#x2021;2 test on the distribution pattern of coney (Cephalopholis fulva) and rock hind (Epinephelus adscensionis) along the axes (1 and 2) of correspondence analysis. (p= positive side of axis, and n=negative side of axis); ns=not significant. Variables

Axis

Species

Individuals

values of Ď&#x2021;2

Significance

Habitat

C. fulva E. adscensionis C. fulva

58(p)-62(n) 24(p)-14(n) 59(p)-61(n)

0.13 2.63 0.03

ns ns ns

E. adscensionis

15(p)-23(n)

1.68

Habitat Assessment of Top Predators on Reefs of the State of ParaĂba, NE Brazil

Tridimensional structures aggregate a higher number of species instead of two-dimensional structures, confirming the thesis that fishes abundance rises with the rise of habitat complexity and volume (WICKHAM et al., 1973; ROUNTREE, 1989). However, POTTS & HULBERT (1994) point out that differences in the fish community structure among habitats can not be addressed only to differences in complexity and habitat size, existing other factors that would be responsible for attraction and maintaining semi-resident fish populations. 4.4. SPECIES BEHAVIOR

The distribution patterns of coney and rock hind, and of variables to evaluate interspecific differences, as far as behavioral context is concerned (Table I) are given in figure 08.

Axis 1 (24.03% of inertia)

Figure 08: Representation of axes 1 and 2, result of correspondence analysis for the variables of regarding the behavioral context. Abbreviations are listed in Table I.

The first five axes explained 78.79% of the total information (inertia). Distance from bottom (DF) and movement (M) were the strongly dominant variables on axis 1 (24.03% of inertia), showing a

Habitat Assessment of Top Predators on Reefs of the State of Paraíba, NE Brazil

close relationship between DF1 and M2 on axis’ negative side. On its opposite side, the highest contributing variables of inertia were DF2, DF3, M3 and CT1. Variables DF1 and M2 are represented by those individuals observed close to the bottom, resting. Making an opposition to these individuals, are those observed at a certain distance from the bottom (DF2 and DF3), which were in the water column (M3). In general these individuals represent the smallest length class observed (CT1), being evident the dominance of young coney on the positive side of axis 1. Comparing

coney’s

observed

length

classes,

there

was

dominance of individuals smaller than 20 cm of total length (CT) (figure 09), and 54% of them were classified in the size class CT1 (<10 cm), considering both reef types. Axis 2 discriminated two situations: (1) individuals between 21 and 30 cm (CT3) observed in the water column, and (2) individuals larger than 30 cm (CT4), swimming actively (M1). As suggested by the results of analyses presented in Table V, distribution of species along both axes differed in a significant and opposite manner, showing a clear contrast between them. It is concluded that there is an evident separation concerning the behavior adopted by coney and the rock hind. The former prefers to stay in the water column (83.3% of samples) and in rare occasions swims among reef structures (11.7% of samples); the latter has a preference for keeping itself close to the bottom, making brief incursions among reef structures, keeping as much as possible contact with the substrate (94.7% of samples).

Table V. Results of χ2 test on the distribution pattern of coney (Cephalopholis fulva) and rock hind (Epinephelus adscensionis) along the axes (1 and 2) of correspondence analysis. (p= positive side of axis, and n=negative side of axis). Variables

Axis

Species

Individuals

values of χ2

Significance

Behavior

C. fulva E. adscensionis C. fulva E. adscensionis

93(p)-27(n) 2(p)-36(n) 35(p)-85(n) 35(p)-3(n)

36.3 30.42 20.83 26.95

P<0,01 P<0,01 P<0,01 P<0,01

Habitat Assessment of Top Predators on Reefs of the State of Paraíba, NE Brazil

As reported by LIESKE & MYERS (1997), C. fulva reaches the first maturation with a total length of 16 cm, and its sexual inversion occurs with 20 cm of total length. Thus, the pattern observed in the present study shows a dominance of young coneys in our samples. Adults (CT>40 cm, n=2) in our samples occurred in depths below 30 m, at Cavo Artemidi Shipwreck. Underwater spearfishing is a common activity along Brazilian northeastern States. Bahia State has a strong fisheries pressure on reef resources, and the presence of some hunters occurred in some of our samples. The fact that adult coneys were only observed in deeper waters could be associated to its ontogenetic shift, as well as, to the fishing pressure over these species. The influence of fishing pressure over the distribution, abundance and size of serranids (groupers) was already observed and reported by BOHNSACK (1982) and SLUKA & SULLIVAN (1998).

Figure 09: Size classes (CT) for C. fulva on Paraíba and Bahia’s reefs. CT1=<10 cm; CT2=11-20 cm; CT3=21-30 cm e CT4=>31 cm.

Considering the variables that allowed us to evaluate behavioural differences between species, one can describe coney as a species extremely active, which keeps a distance from the bottom, with exception of the young ones. On the other hand, the rock hind shows

Habitat Assessment of Top Predators on Reefs of the State of ParaĂba, NE Brazil

more sedentary habits, typical of the Epinephelinae, staying close to the bottom and recesses. Groupers are some of the top predators on coral reefs, and tend to be piscivorous K-strategists, demonstrating slow growth, late reproduction, large size and long life-spans which render them vulnerable to over-exploitation (PARRISH, 1987; BULLOCK et al., 1992; HEEMSTRA & RANDALL, 1993; BEETS & HIXON, 1994). Groupers are also placed at risk by certain behavioral characteristics: many species form large spawning aggregations, and many exhibit a high degree of territoriality and site specificity, which makes them easy targets for fishermen (MORRIS et al, 2000; SADOVY, 1996; DOMEIER & COLIN, 1997). Our results suggested that a small group of variables seems to influence the behavior adopted by coney and rock hind, as observed by LA MESA et al. (2002), for the dusky grouper (Epinephelus marginatus). Although correspondence analysis was not significant to an adequate level regarding habitat preferences between species analyzed, sessile fauna, mainly corals and calcareous algae contributed to the rise of rugosity, and consequently influenced the results concerning spatial distribution of species.

Habitat Assessment of Top Predators on Reefs of the State of ParaĂba, NE Brazil

4.5. ECOLOGICAL INTERACTIONS

4.5.1. PRESENCE OF OTHER SERRANIDS Serranid species observed showed an indifferent behavior in the presence of other serranids, as it is shown in figure 10 and 11.

Figure 10: Rock hind (Epinephelus adscensionis) (left) and freckled soapfish Rypticus bistrispinus (right) at a natural reef (Porto da Barra - BA).

Figure 11: Coney (Cephalopholis fulva)(left) and hock hind (Epinephelus adscensionis) (right) at a natural reef (Porto da BarraBA).

Habitat Assessment of Top Predators on Reefs of the State of Paraíba, NE Brazil

4.5.2. PRESENCE OF CONSPECIFICS

During our samples, coney was observed 74% alone, 23 % accompanied of another coney and in 3% there were two other coneys. None aggressive behavior was observed, nor at caves, and even at open areas. On the other hand, rock hind was observed alone in almost all samples, except for a single observation, where two rock hinds kept a distance of 30 cm from each other.

4.5.3. INTERSPECIFIC FEEDING ASSOCIATIONS

Interspecific foraging associations have been described for a wide variety of vertebrate taxa (ex. DIAMANT & SHPIGEL, 1985; SABINO & SAZIMA, 1999; GIBRAN, 2002). Foraging associations and complex interspecific and intraspecific relations are common in a coral reef community (HOBSON, 1974; ORMOND, 1980; SILVANO, 2001; GIBRAN, op. cit.; HUMANN & DELOACH, 2002). Many of the species of fish on coral reefs are predators (e.g. almost all serranids), and most of these predators are comparatively opportunistic (see GIBRAN & CASTRO, 1999; SILVANO, op.cit.). At the same time a variety of strategies maybe employed such as, “joint hunting”, “ambush”, “hunting by aggressive mimicry” and “following and scavenging” (ORMOND, op.cit.). Following behavior is a kind of diurnal association, in which the attendant, follows another species, the nuclear, while the latter is searching for food. The attendant may benefit by catching prey that try to escape from the nuclear predator (see STRAND, 1988). Feeding associations among reef fishes are common and many were already described (MONTGOMERY, 1975; DUBIM, 1982; ZANDER & NIEDER, 1997). Associations involving species from the Serranidae family were reported between Cephalopholis argus and Gymnothorax javanicus (=Lycodontis javanicus) (FRICKE, 1972), Epinephelus fasciatus

Habitat Assessment of Top Predators on Reefs of the State of Paraíba, NE Brazil

and Gymnothorax griseus (KARPLUS, 1978), E. adscensionis and C. fulva with Myrichthys breviceps (MICHAEL, 1998), and recently among Diplectrum formosum, D. radiale and Luidia senegalensis (Asteroidea) (GIBRAN, 2002). The interaction observed between Epinephelus adscensionis (Serranidae) rock hind, and Myrichthys ocellatus (Ophichthidae), goldspotted eel, occurred in shallow waters and was registered in June/2003,

Farol

barra

Reef

(BA)

during

the

morning.

Observations lasted 15 minutes, and rock hind followed M. ocellatus while it was searching for preys. Rock hind kept close to the bottom, around and very attentive to M. ocellatus’ movements (fig. 12). Sometimes it made contact with the eel, rubbing its fins on the eel’s posterior part of the body and (fig. 13).

Figure 12: Observed association between rock hind (E. adscensionis) close to the goldspotted eel’s head (M. ocellatus) while it searches for preys in the substrate and small crevices.

Habitat Assessment of Top Predators on Reefs of the State of Paraíba, NE Brazil

Figure 13: Observed association between rock hind (E. adscensionis) (A) following and rubbing the goldspotted eel (M. ocellatus) (B).

The

following

Epinephelus

and

behavior moray

among

eels

specimens

(Muraenidae)

and

the

genera

snake

eels

(Ophichthidae) was reported by KARPLUS (1978), between E. fasciatus and G. griseus, but he did not attempted to explain his observations of groupers contacting morays with their fins. KARPLUS (op. cit.) also reported that while G. griseus searched for preys, E. fasciatus followed the eel trying to get small crustaceans and fish that were chased out of their shelters by the eel, and also to steel some preys already taken by it. The hypothesis proposed by DUBIM (1982) to explain the rubbing behavior was that small fishes and invertebrates, disturbed by the moving eel, might be captured by the accompanying fish. It would thus be advantageous for the attendant, to keep “its” ell in motion. According to STRAND (1988), the following behavior is an opportunistic strategy that allows small generalized predators to capitalize

upon

the

displacement

uncovering

otherwise

Habitat Assessment of Top Predators on Reefs of the State of ParaĂba, NE Brazil

unprofitable or unavailable prey items. This was confirmed by MICHAEL (1998). We believe that there probably exists a diet overlap, although substantial, between M. ocellatus and E. adscensionis. Based on the available literature, RANDALL (1968) reported that M. ocellatus feeds mainly on crustaceans, while E. adscensionisâ&#x20AC;&#x2122; diet is composed 67% by the same item, crustaceans THOMPSON & MUNRO (1983). Although it is known that coney keeps some similar relationships with eels (see DUBIM 1982 and HUMANN & DELOACH, 1999), even being the most abundant species, it was not observed any interactions during the study. Although no feeding by eels or followers was observed, this type of interaction observed between rock hind e the goldspotted eel, is most likely a feeding association very similar to the ones described by MONTGOMERY (1975) and KARPLUS (1978).

Habitat Assessment of Top Predators on Reefs of the State of Paraíba, NE Brazil

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