An exclusion experiment to study the influence of habitat structure provided by Mussismilia corals (Cnidaria; Anthozoa) on the predation of associated crustaceans

Abstract

Predation is an interaction between species that influences community organisation by the direct consumption of prey, influencing prey numbers, behaviours and traits. The intensity of predation is greatly influenced by the environment, and the physical structure of habitats may influence predation intensity by providing refuge for prey or reducing the foraging efficiency of predators. In this context, the aim of the present study is to verify the influence of predation on the richness and density patterns of crustaceans inhabiting different species of Mussismilia corals, which provide various habitat structures for the associated fauna. We conducted an exclusion experiment to include total, partial and no cage treatments. The richness and density of crustaceans differed among coral species and cage treatments, except between partial cage and no cage treatment. Mussismilia harttii showed higher richness and density in uncaged and partial cage treatments compared with M. braziliensis, which in turn showed higher values than M. hispida. These findings indicate the importance of predation in the structure of crustacean assemblage associated with Mussismilia species and that differences in the richness and abundance of associated fauna result from the different habitat structures provided by each species of Mussismilia.

Background

Predation is an intra-and interspecific interaction that is thought to markedly influence community organisation by the direct consumption of prey, influencing prey numbers, behaviours and traits. However, some studies found that predation did not significantly influence the structure of communities [1, 2]. Predators and prey are almost always part of complex communities with multiple species interactions and a diversity of indirect interactions [3]. Therefore, understanding the impact of predation is an immense challenge. Manipulative studies may provide important tools to identify such processes, as suggested by Virnstein [4], Posey and Ambrose Jr. [5] and Galván et al. [6].

Predator effects may increase community diversity at intermediate intensity levels, but at low or high intensity, they may decrease diversity [7]. These effects may influence the community by enhancing species coexistence, preventing resource monopolies by reducing superior competitors and releasing niche space for other species [8]. However, they can also hamper the coexistence of species, e.g., by forcing prey into a limited number of refuges, leading to more intense competition for resources within the spaces [3, 9], or when predators preferentially feed on rare species, leading to local extinction [10]. As Begon et al. [11] suggested, the effect of predation on a community depends on different factors, such as predation intensity, ecosystem productivity, and, partly, the characteristics of the prey species. Gilinsky [12], in a study evaluating both the predation effect and role of habitat structure, emphasized the importance of predator identity, the season of the year and the complexity level of the habitat.

The effects of predation in various marine environments, for example, soft bottom [1, 2, 6], artificial reefs [13], coral reefs [14], offshore rock outcrops [5], and marine rock intertidal communities [8, 15] are well documented. Although the effects of predation are often studied by manipulating predator density, in some cases, this strategy may not be the most efficient. Hall et al. [1] observed that predators enclosed in cages failed to feed on the available prey and lost weight, whereas Karlson [16] manipulated the density of echinoids and verified that there was not significant differences on the local macrofauna.

The intensity of predation (the probability that an individual prey will be killed by a predator) is strongly influenced by both physical and biotic characteristics of the environment [17]. The physical structure of the habitat, for instance, may reduce the impact of predation by providing a refuge for prey and/or reduce the foraging efficiency of predators [12, 15, 18]. Habitat structure has been defined as a two axis concept: habitat complexity, represented by the amount of a physical structure; and habitat heterogeneity, which represents the addition of different kinds of physical elements to the system [19,20,21].

Scleractinian corals are one of the organisms that provide habitat and shelter for invertebrates in coral reefs. Their large carbonate skeletons harbour a great variety of invertebrate species, and their morphological patterns of growth may influence the distribution of these invertebrates. Despite the fact that crustaceans represent the majority of species living directly associated with corals, most coral reef research has focused on fish species, while invertebrates have been neglected [22].

Nogueira et al. [23], evaluating the effects of the habitat structures provided by three different species of the endemic Brazilian coral Mussismilia, identified M. harttii as the species harbouring a richer and more abundant collection of associated crustaceans, compared to the congeners M. braziliensis and M. hispida. The larger number of species associated with M. harttii corals is related to its phaceloid growth pattern, in which the polyps grow at distance from each other, providing space in between (Fig. 1). Based on the suggestion by Menge and Sutherland [18] that habitat structure effects the foraging efficiency of predators, we aimed to evaluate if predation is important in influencing the richness and abundance of crustaceans associated with the habitat structures provided by three different Mussismilia coral species. We tested if there was a difference in the richness and abundance (density) of crustaceans associated with Mussismilia species in colonies subjected to total cage, partial cage and uncaged treatments.

Fig. 1

Images showing the morphological pattern of Mussismilia species: a Mussismilia harttii, b M. braziliensis and c M. hispida (modified from Nogueira et al. [23])

Methods

To identify the effectiveness of habitat structures in Mussismilia corals as refuges for invertebrates against predators, a field experiment was carried out at Caramuanas reef (Todos-os-Santos Bay, Salvador, Bahia State, Brazil) in March 2013. Cages were systematically placed along the top of the reef, at least 3 metres apart, around Mussismilia corals (M. harttii, M. braziliensis and M. hispida) to exclude predators. These coral species were selected due to their close phylogenetic relationships; in this way, the influence of other factors, such as chemical defences is unlikely. The same species were never encaged consecutively (e.g., after sampling M. harttii, the following species caged was M. braziliensis, then M. hispida). Each cage was constructed in a cylindrical format, with plastic mesh (0.5 cm aperture) attached to 2 iron circles (40 cm diameter and 30 cm height). To fix these cages to the bottom, 3 iron pickets were inserted into the substratum for each cage, which was tied to the pickets with plastic cable ties (Fig. 2). To avoid forming a gap between the cage and the substratum bottom, the cage mesh was attached to the iron picket base. To identify possible damage and certify the efficiency of cages in excluding predators, the experiment was checked every 15 days until the final sampling, to remove seaweed and other debris.

Fig. 2

Scheme of experimental cages: a Partial cage (procedural control) with 5 apertures (20 cm diameter), 4 on the side and 1 on the top; b total cage, without apertures; c corals without cages

To identify the influence of cages, rather than the exclusion of predators, we constructed partial cages (procedural controls) with 5 apertures (20 cm diameter) (4 on the side and 1 on the top (Fig. 2), to allow access for predators) surrounding each coral species, intercalating them with caged corals and corals without cages in a systematic sampling.

The experiment was set up for 3 months and when the cages were removed (in June 2013) the corals were immediately covered with plastic bags and collected by free diving with a hammer and chisel. For each coral species, we systematically placed 8 complete cages, 8 partial cages and 8 corals without cages, interspersed at a distance of at least three metres.

At the end of experiment, only five cages from each treatment were found and sampled, due to some cages being removed by people. In this case, we also collected 5 colonies of each coral species that had not undergone the treatment, to identify the effects of coral habitat structure under predation influence.

After sampling, corals were washed and the water was filtered in a 150 µm mesh and fixed in 70% alcohol. Then, with the aid of a stereomicroscope, crustaceans were sorted and separated into groups of numbered morphospecies (when there were more than one morphospecies of a single taxonomical level, they were numbered consecutively). The number of individuals was divided by the coral diameter, providing a density value and preventing the effect of different coral areas.

We transformed richness and density of the crustaceans associated with Mussismilia species into log x + 1 (base 10) to achieve normality. We conducted a two-way ANOVA in the open-source software R Program, to compare the difference in richness of associated crustaceans between Mussismilia species under cage treatments, and we performed the same procedure to identify differences in density of associated crustaceans. A post hoc analysis with Tukey’s test was also completed for paired comparisons. Significance was set at p < 0.05. Species that contributed most to significant dissimilarities between the coral species were determined using the SIMPER (similarity percentages) procedure from the Primer 6 package.

Results

We collected 6158 individual crustaceans, comprising a total of 102 different taxa, of which the most abundant group was Copepoda (4280), Peracarida (1149), Ostracoda (569) and Decapoda (159). Among Copepoda, the Halectinosoma sp., Idomene sp. and Canuelidae 1 species were the most abundant. In uncaged corals, all three copepods were more abundant in M. harttii and the same pattern was observed in partially caged corals. However, in caged corals, they were more often associated with M. braziliensis. The most common Ostracoda taxa were Sigilliocopina 1, Podocopina 1 and Sigilliocopina 2, and they presented the same density trend among Mussismilia corals as was shown by copepods (Fig. 4).

Two-way ANOVA showed that the richness and density of crustaceans varied significantly with their associated Mussismilia species and cage treatment and that there was a highly significant interaction effect (Table 1).

Table 1 Results of two-way ANOVA of the effect of Mussismilia species (M. harttii, M. braziliensis, M. hispida) and cage treatment (total cage, partial cage, no cage) on the richness and density of associated crustaceans

For richness of associated crustaceans, a post hoc Tukey test found significant differences between M. harttii and M. hispida, and for M. braziliensis and M. hispida, while no significant differences were found between M. harttii and M. braziliensis. For density, all comparisons showed significant differences between Mussismilia corals. When we analysed the differences in richness between the cage treatments we found that total cage showed significant differences compared with partial cage and no cage treatments, and the same pattern was found for density. No significant differences were identified for partial cage and no cage treatments for richness or density (Table 2).

Table 2 Results of post hoc Tukey test for comparisons of richness and density of crustaceans between Mussismilia species (M. harttii, M. braziliensis, M. hispida) and cage treatments (total cage, partial cage, no cage)

When we compared the richness and density of uncaged corals, M. harttii showed higher values than M. braziliensis and M. hispida, while M. braziliensis had higher values than M. hispida. The same pattern was seen in the partial cage treatment. For total cage, there was an increase in the richness and density of crustaceans associated with M. braziliensis and M. hispida, compared with partial cage and no cage (Fig. 3).

Fig. 3

Mean richness and density (Ind.cm⁻²) of crustaceans associated with Mussismilia species in treatments. PC, partial cage, TC, total cage; NC, no cage; MHA, Mussismilia harttii; MB, M. braziliensis; MH, M. hispida

For the most abundant decapod species (Mithraculus forceps, Petrolisthes galathinus and Pachycheles monilifer), higher densities were found in colonies of M. harttii in all treatments. For peracarids, the most abundant species presented different patterns: Carpias sp. and Ceiriphotis megacheles showed a similar pattern to the decapods, and Ianiropsis sp. did not present any clear pattern (Fig. 4).

Fig. 4

Mean density of the most abundant species of crustacean orders associated with Mussismilia species in treatments. PC, partial cage, TC, total cage; NC, no cage; C, caramuanas; B, boipeba; MHA, Mussismilia harttii; MB, M. braziliensis; and MH, M. hispida

When we compared the composition of crustaceans associated with the corals, the SIMPER identified significant dissimilarities between all comparisons of cage treatments for M. hispida, with greater dissimilarities between partial cage vs. no cage, and the taxa that contributed most were Cyclopinidae 3 and Podocopina 2. Mussismilia braziliensis was second with high dissimilarity values for comparisons of all treatments, and a higher value was verified between total cage vs. no cage treatment, with Halectinosoma sp. 1 and Idomene sp. contributing more to these dissimilarities. Minor dissimilarities were identified for M. harttii; for these coral, higher dissimilarities were verified between partial cage vs. no cage treatments, with Carpias sp. and Idomene sp. contributing most to the dissimilarities (Table 3).

Table 3 Average dissimilarities between cage treatments and correlations of the most important species contributing to the dissimilarities

Discussion

Predation can be affected by habitat structure, e.g., by reducing the foraging efficiency of predators by providing refuge space [12]). Based on differences in the use of habitats as a refuge against predators, habitat structure may provide axes for niche diversification among prey, even if there is no competition for resources [9].

In coral reefs, crustaceans have been identified as the largest component of the most abundant reef fishes’ diet [13]. Hiatt and Strasburg [14] verified that crustaceans associated with corals are consumed by many species of reef fishes, especially when they move between coral colonies [24]. However, when crustaceans are protected by a suitable refuge space within their coral host, fish are usually unable to predate them [22].

In the present study, the significant differences in richness and density patterns of crustaceans associated with Mussismilia corals between the treatments (total cage vs. partial cage, and total cage vs. no cage treatments) is evidence of the importance of predation in structuring the associated community. The absence of significant differences between partial cage and no cage treatments indicates there was no artefact influence of the structures used to construct exclusion cages. The exclusion of predators is known to impact communities by increasing their density and richness [4]. Our results also show that once predators were excluded in caged M. braziliensis and M. hispida, the richness and abundance of crustaceans grew to values close to those found in M. harttii, which is a species structurally more complex and provides additional refuge against predators.

Of the three Mussismilia species, M. harttii has been previously identified to harbour the richest and most abundant fauna [23]. This result was confirmed in the present study by comparison of Mussismilia species in uncaged and partial cage treatments: there was a significant difference in the richness and abundance of associated carcinofauna among species of Mussismilia corals.

Higher richness and densities associated with M. harttii in uncaged and partial cage treatments, compared with M. braziliensis and M. hispida, indicates that the partial cages allowed the predators to freely access the colonies. Nogueira et al. [23] identified the space among corallites, an exclusive feature of M. harttii, as the most important factor influencing the richness and abundance of associated fauna. The space among corallites acts as a refuge against predators, which is confirmed by the results obtained from caged corals, in which no statistical difference was observed for richness and density once the predators had been excluded.

Our results for the most abundant copepods and ostracods showed higher mean values of density in caged colonies of M. braziliensis. This indicates that copepods and ostracods associated with uncaged colonies and partial cages of M. braziliensis were affected by predators feeding preferentially on the most abundant species, reducing their population size. The habitat structure of M. braziliensis may provide other benefits beyond protection against predators, e.g., easier access to resources, allowing the growth of populations of small animals like copepods and ostracods. In normal conditions (uncaged), those benefits are suppressed by the harshness of predation.

For decapods, we found higher densities associated with caged M. harttii, compared with caged M. braziliensis and M. hispida. As found by Nogueira et al. [23], Mithraculus forceps was the most abundant decapod species, with higher values associated with M. harttii. The association of this crab with corals was described as mutualistic by Stachowicz and Hay [25]. According to these authors, the crab obtains food and protection by living among the coral branches and benefits the coral host by preventing the overgrowth of algae.

The most abundant medium-sized species (2–10 mm), the peracarids Cheiriphotes megacheles and Carpias sp. [26], displayed the same pattern as the most abundant decapods, however, this could be due to cage artefacts. The mesh size used to construct cage artefacts are much smaller than most crabs species, thus, once cages were placed around coral species, crabs associated with the corals remained confined and others could not access the cage interiors. Consequently, the number of species and individuals associated with corals remained the same as at the beginning of the experiment. This is corroborated by the higher values recorded for small crustaceans, e.g., copepods (0.1–1.2 mm) [27] of caged M. braziliensis colonies.

Results of SIMPER showed high dissimilarities in the crustacean assemblage between exclusion cage treatments for all three Mussismilia species; even with differences in richness and density among cage treatments, the composition of crustaceans was very variable, which may have produced the high dissimilarities found.

Conclusions

The present study indicates the high importance of predation in structuring the assemblage of crustaceans associated with the endemic coral species of the genus Mussismilia. We have confirmed the results of Nogueira et al. [23], who concluded that differences in the richness and abundance of associated fauna among the Mussismilia species are a result of the different habitat structures provided by each species, with M. harttii being the species that harbours the richest and most abundant associated fauna.