Coral Reefs (2007) 26:361–373 DOI 10.1007/s00338-007-0207-0
REPORT
Coexistence of congeneric spiny lobsters on coral reefs: differential use of shelter resources and vulnerability to predators ´ lvarez Æ P. Briones-Fourza´n Æ E. Lozano-A A. Osorio-Arciniegas Æ F. Negrete-Soto Æ C. Barradas-Ortiz
Received: 29 September 2006 / Accepted: 2 February 2007 / Published online: 28 February 2007 Springer-Verlag 2007
Abstract The notion, previously generated from laboratory experiments, that the local coexistence of spiny lobsters Panulirus guttatus and Panulirus argus on Caribbean reefs may be promoted by a differential use of shelter resources and/or vulnerability to predators was explored in a coral reef in Mexico. Multiple regressions with data collected on 11 occasions on fixed back-reef and fore-reef sites suggested that the densities of the congener, other crevice-dwellers, and predators did not significantly affect the density of P. argus in either reef zone, or of P. guttatus on the back-reef, where coexistence of both lobster species was greatest. In contrast, there was a significant negative relationship between predators and the density of P. guttatus on the fore-reef, where this species was dominant. Congeneric cohabitation in dens was less than expected by chance, but this pattern may reflect a differential use of shelter resources rather than interspecific competition. P. guttatus was more prevalent in dens over the middle and upper third of the reef profile, and P. argus over the lower and middle third of the reef profile. Whether individuals cohabited with conspecifics, congeners, or resided solitarily, P. guttatus was more prevalent at the walls and/or ceiling and P. argus on the floor of dens. This differential
Communicated by Biology Editor M.I. McCormick. ´ lvarez (&) P. Briones-Fourza´n E. Lozano-A A. Osorio-Arciniegas F. Negrete-Soto C. Barradas-Ortiz Instituto de Ciencias del Mar y Limnologı´a, Unidad Acade´mica Puerto Morelos, Universidad Nacional Auto´noma de Me´xico, PO Box 1152, Cancu´n, QR 77500, Me´xico e-mail:
[email protected]
use of shelter resources may be related to the differential vulnerability to predators, which may have promoted local coexistence of these congeners in reef habitats. Keywords Coexistence Competition Coral reef habitat Predation Spiny lobsters
Introduction Spiny lobsters (Crustacea: Palinuridae) are large, nocturnal, crevice-dwelling crustaceans that represent important fishing resources in all tropical and subtropical seas of the world (Phillips 2000). In regions where two or more species of spiny lobsters co-occur, they are usually segregated by habitat (e.g., George and Main 1967; Berry 1971; ´ lvarez 1992), George 1974; Briones-Fourza´n and Lozano-A which is a common trade-off that promotes regional coexistence of similar species (reviewed by Amarasekare 2003). The spotted spiny lobster, Panulirus guttatus (Latreille, 1804), and the Caribbean spiny lobster, P. argus (Latreille, 1804), coexist regionally throughout the Caribbean Sea, the Bahamas and Bermuda (Holthuis 1991), and locally on coral reef habitats. P. guttatus is a habitat specialist that dwells permanently on the coral reef habitat after the settlement (Sharp et al. 1997). In contrast, P. argus is a habitat generalist that undergoes several habitat shifts during its benthic life (reviewed by Butler and Herrnkind 2000). The postlarvae of P. argus settle on shallow, coastal vegetated habitats where the small juveniles dwell for several months. As they grow, juveniles shift to crevice-type shelters in shallow areas. Later, they move to coral reef habitats where subadult and adult P. argus coexist with resident populations of P. guttatus.
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The two species also differ in other traits (BrionesFourza´n 1995). P. guttatus is smaller [(maximum size: 88 mm carapace length, CL (Negrete-Soto et al. 2002); size of females at the onset of sexual maturity: 32– 38 mm CL (Sharp et al. 1997; Robertson and Butler 2003)] and is a sedentary species with a limited home ´ lvarez et al. 2002) and a high level of range (Lozano-A shelter fidelity (Robertson and Butler 2003). In comparison, P. argus is larger [maximum size: 204 mm CL ´ lvarez et al. 2003); size of females at the onset (Lozano-A of sexual maturity: 75–80 mm CL (Fonseca-Larios and Briones-Fourza´n 1998)] and is a highly mobile species that may undergo extensive, organized migrations (reviewed by Herrnkind et al. 2001). Local coexistence of similar species may be promoted by differential utilization of resources, vulnerability to predators, or responses to disturbance (Holt et al. 1994; Tilman 1994; Kneitel and Chase 2004). Important resources for spiny lobsters include food and daytime shelter, on which they strongly rely for survival (e.g., Eggleston et al. 1990; Smith and Herrnkind 1992; Sharp et al. 1997). Although P. guttatus and P. argus have a similar diet (Colinas-Sa´nchez and Briones-Fourza´n 1990), the two species are unlikely to compete for food resources because P. guttatus forages on the coral reef (Sharp et al. 1997), whereas reef-dwelling individuals of P. argus forage on hard grounds and seagrass–algal beds adjacent to the coral reefs (Cox et al. 1997). Interspecific competition for shelter has not been observed under laboratory conditions (Loz´ lvarez and Briones-Fourza´n 2001), but this has not ano-A been evaluated in natural habitats. Field and laboratory observations have shown that P. argus and P. guttatus display different defensive ´ lvarez and behaviors (Herrnkind et al. 2001; Lozano-A Briones-Fourza´n 2001; Briones-Fourza´n et al. 2006). Under the risk of predation, sheltered individuals of P. argus may deter attacks of a predator at the entrance to the den (defined in the present study as any crevice harboring one or more lobsters) and exposed individuals may confront their predators, often joining in cooperative defense. In contrast, sheltered individuals of P. guttatus usually retreat deep into their den when the predator approaches, while exposed individuals do not display cooperative defense and are quickly subdued by the predator. These different defensive behaviors suggest that P. guttatus is more vulnerable to predators than P. argus. The present study used a correlative approach to explore how the abundance of congeners, other crevice-dwelling animals, and predators, influenced the abundance of P. guttatus and P. argus on a coral reef. This provided insights into the potential importance of competition and predation in influencing lobster abundance and provided hypotheses for future experimental manipulations. At the
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same time, use of shelter resources by each species of spiny lobster was described across the reef habitat.
Materials and methods Study area The study was conducted on an extended fringing reef at Puerto Morelos, Mexico (20 51¢ N, 86 53¢ W). Extended fringing reefs, which are morphologically intermediate between true fringing reefs and true barrier reefs, are the most common reef type along the continental coast of the Mexican Caribbean (Jorda´n-Dahlgren and Rodrı´guez-Martı´nez 2003). The Puerto Morelos reef is a tract composed of a series of patches of different size and structural complexity (Fig. 1). The back-reef zone (i.e., the leeward, protected portion of the reef facing the coast) is dominated by the scleractinians Acropora palmata and Montastraea annularis and varies from shallow (2–3 m), protected flat areas, to deeper (5–7 m), relatively more exposed areas with a higher relief. The fore-reef zone (i.e., the windward, exposed portion of the reef facing the open sea) also varies from areas of hard substrates with a relatively gentle slope, colonized by many small scleractinian colonies and numerous gorgonians and sponges, to high relief areas where large scleractinians dominate (Jorda´n-Dahlgren 1989; Jorda´n-Dahlgren and Rodrı´guez-Martı´nez 2003). The reef is separated from the shoreline by a reef lagoon (~500 to 1,500 m in width and 30 mm CL (Smith and Herrnkind 1992; Childress and Herrnkind 1997). Crevicedwellers are defined as animals of any other species that
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were within the size range or exceeded the size of spiny lobsters. Statistical analyses Counts of lobsters, other crevice-dwellers, and predators alone were standardized as density (number of individuals per hectare, ind ha–1). To determine the influence of reef zone on the abundance and mean size of each lobster species, and whether these attributes changed over time, density and mean size of lobsters were each assessed with a repeated-measures ANOVA (RM-ANOVA, Winer 1971), with sites as subjects. Main (fixed) factors were Reef zone (with two levels, back-reef and fore-reef, each with three replicate sites), Species (two levels, P. guttatus and P. argus), and Time (11 surveys). Time was the repeated measure. Correlation analyses of the mean densities of each lobster species at sites on the back-reef and fore-reef zones were undertaken to assess their use of the reef habitat, i.e., whether their changes in density followed a similar trend across the reef habitat. Densities of crevice-dwellers and densities of predators were also compared between Reef zones over Time (nine surveys) with RM-ANOVAs. In all cases, analyses of residuals showed skewed distributions of data, necessitating transformation to Log (count + 1) prior to RM-ANOVAs to homogenize variances (Zar 1999). Because the sampling intervals (2–3 months) may have been short relative to the persistence of lobsters and other animals on the reef habitat, the data were likely autocorrelated. Therefore, for each RM-ANOVA, the degree to which the assumption of sphericity was violated was assessed and (when appropriate) the degrees of freedom of time and its residuals were adjusted with the Huynh–Feldt correction in order to homogenize the variance–covariance matrix (Howell 2002). For each reef zone, a separate stepwise multiple regression model was used to examine which of three independent variables had a significant effect on the mean densities of each spiny lobster species (dependent variable). Independent variables were the mean densities of: (a) the other species of spiny lobster (i.e., the congener), (b) other crevice-dwellers, and (c) predators. Residuals were analyzed to detect departures from randomness. If competition or predation were potentially important regulatory processes for spiny lobsters on the coral reef, then the respective partial correlations would be expected to be significant (Hixon and Beets 1993; Mintz et al. 1994; Eggleston et al. 1997; Forrester et al. 2006). In predator– prey analyses, the nature of the relationship depends on the dynamics of the interaction: if there is a short time lag in the interaction, a positive relationship can be expected, whereas a longer time lag may show the opposite results (Begon et al. 1986; Stewart and Jones 2001).
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The distribution of P. guttatus and P. argus among individual dens pooled by reef zone was examined for a non-random pattern of species co-occurrence in a presence–absence matrix. A ‘‘checkerboard distribution’’ would describe a pattern where only one of both species occurs in a given den. Such a pattern would suggest competitive exclusion (Stone and Roberts 1990). Species co-occurrence in individual dens was tested with the software EcoSim 7.0 (Gotelli and Entsminger 2004). The null model used was SIM2, in which row (species) sums are fixed (the number of occurrences of each species in the null communities is the same as in the original data base) and column (dens) sums are equiprobable (each den has the same chance of being selected). The model was run with the data from the entire study period and with the data from each individual survey. Each run generated 5,000 random matrices and calculated a C-score index of co-occurrence (Stone and Roberts 1990), which measures the average number of checkerboard units between the two species, i.e., their tendency to not occur together. An observed C-score significantly larger than expected by chance (the average C-score of the 5,000 simulations) is suggestive of interspecific competition for dens. However, non-random patterns of species co-occurrence may result from causes other than competition. For example, ‘exclusion’ might also be due to history or different habitat or microhabitat requirements (Sfenthourakis et al. 2005), i.e., the spatial distribution of dens across the reef habitat might show some structure and this structure might be reflected by the two congeners exploiting this habitat. Therefore, v2 contingency tables (Zar 1999) were used to assess the proportion of lobsters of each species located in dens across the lower, middle, and upper portions of the reef, and on the floor or vault of the dens. Contingency tables were also used to analyze the proportion of dens that harbored conspecific and congeneric individuals, their location between reef zones and across the vertical profile of the reef, and the location of congeneric individuals within the shared dens. Results were considered as significant if p < 0.05. All results in the text are expressed as mean (± standard deviation), unless otherwise stated.
Results Density of spiny lobsters There was no difference in the mean density of lobsters (both species combined) between the fore-reef (304.4 ± 119.0 ind ha–1) and the back-reef (180.5 ± 74.7 ind ha–1) (Table 1). Across the entire reef habitat, P. guttatus (206.5 ± 116.4 ind ha–1) significantly outnumbered P. argus
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Table 1 Repeated-measures ANOVA for population density (individuals per hectare) of Panulirus guttatus and P. argus on two reef zones (back-reef and fore-reef) and across 11 surveys Effect
Reef zone
Degrees of freedom 1
Mean square 36.438
Species
1
1.687
Reef zone · species Residual
1 8
14.441 0.653
F
2.582
p
0.147
55.765
