Intracolonial variation in chemical defenses of the sponge Cacospongia sp. and its consequences on generalist fish predators and the specialist nudibranch predator Glossodoris pallida

Abstract

On Guam, the nudibranch Glossodoris pallida specializes in feeding on the branching sponge Cacospongia sp., which contains scalaradial and desacetylscalaradial as major secondary metabolites. The nudibranch, which accumulates both compounds for its own defense, is typically found on the base of the sponge. In this study, we quantified intracolonial variation in the production of secondary metabolites (percent yield of crude extract, filtered extract, scalaradial, and desacetylscalaradial), structural material (fiber and ash content), and protein content in Cacospongia sp. in order to assess the consequences that such variation has on feeding responses of generalist fish predators, the specialist nudibranch predator G. pallida, and on the distribution of the nudibranch on the sponge. Levels of secondary metabolites varied among the parts of the sponge analyzed (tip, base, surface, and matrix). The mean peicer,: y-ic!d of cr. ; dc cx!:zct :vs: $isher i?, the surface nf !he spc~cje. .uhi!e filtered extract and desacetylscalaradial were higher in tips than in bases Structural materials were highest in the base and in the surface of the sponge. In contrast, the inner part of the sponge contained higher levels of protein than the surface, but no differences were found between tips and bases. Compared to a control, the crude extract of Cacospongia sp. significantly deterred fish feeding at the lowest concentration found in the sponge (base concentration) In field assays. When offered a cholce between base and t~p concentrations, both the pufferfish Callthiyaster solandn in laboratory assays and the natural reef fish assemblage in the field showed no preference for extracts of bases over tips (i.e. lower levels over higher levels of chemical defenses). However, when offered a choice between pieces of sponge from the base and from the tip, the nudibranch G. pallida preferred bases over tips, which agrees with the nudibranch distribution on the sponge. Alternative factors may shape the observed distribut~on of nudibranchs on Cacospongia sp. Nudibranchs at the bases may suffer lower levels of predation because they are less accessible to predators than nudibranchs at the tips of the sponge Therefore, we also tested whether small disks of artificial squid food located on tips and bases of the sponge are equally accessible to generalist fish predators. The reef fish C. solandri in laboratory assays and the natural fish assemblage at the Cacospongia sp. community consumed equal amounts of food from tips and bases. Our data demonstrate that Cacospongia sp. extracts deter feeding by fishes at the lowest concentration found in the sponge, which suggests that the higher concentration in the tips is not a mechanism to avoid consumption by generalist fish predators. In contrast, avoidance of higher levels of chemistry appears to be the factor behind the selection of bases over tips by the specialist nudibranch predator G. pallida. Intracolonial variation in chemical defenses seems to determine the nudibranch distribution o...

Chemical bioactivity of sponges along an environmental gradient in a Mediterranean cave

“…Turon et al, 1996b;Betancourt-Lozano et al, 1998), and more rarely within specimens (Turon et al, 1996b;Becerro et al, 1998;Schupp et al, 1999). Genetic, biological, and/ or environmental factors (both biotic and abiotic) can account for this variation.…”

Biogeography of sponge chemical ecology: comparisons of tropical and temperate defenses

“…We disregarded specialist sponge predators (e.g., opisthobranchs) since, by definition, a specialist predator will feed exclusively on its prey, which a priori makes them unsuitable to test the general effectiveness of multiple chemical defenses from the diverse species collected at each location. One assay followed methods similar to those used by Becerro et al (1998) and targeted medium-sized, demersal fish predators such as Oblada melanura, Diplodus spp., Mugil spp., and Boops salpa (Spain) and Cheilinus fasciatus, Scarus schlegeli, and Naso vlamingii (Guam). Numerous specimens of these species actively participated in the feeding assays.…”

“…Many factors at multiple scales affect the production of chemical defenses (Steinberg and van Altena 1992;Harvell et al 1993;Becerro et al 1995Becerro et al , 1998, but our hypothesis examines the effect of evolution in distinct geographic regions on the effectiveness of chemical defenses. Thus, we collected tropical (IndoPacific) and temperate (Mediterranean) sponge species that are phylogenetically closely related to test whether their deterrent properties significantly differ.…”

“…Thus, we collected tropical (IndoPacific) and temperate (Mediterranean) sponge species that are phylogenetically closely related to test whether their deterrent properties significantly differ. Predator behavior and preference may also determine the outcome of feeding experiments, clearly affecting how we perceive the deterrent properties of our samples (Pennings et al 1994;Schupp and Paul 1994;Cronin et al 1997;Becerro et al 1998). To avoid a species-specific pattern generated by a single predator, we conducted two sets of feeding experiments in the field that targeted different members of the fish community.…”

Antibiotic, cytotoxic and enzyme inhibitory activity of crude extracts from Brazilian marine invertebrates

“…The storage of biologically active secondary metabolites by marine invertebrates is frequently related to their ecological success, in spite of their exposition to predation, infestation by microbial pathogens, overgrowth, fouling and competition for space and nutrients (reviewed in Amsler et al, 2001;Blunt et al, 2007;Faulkner et al, 2004;Lindquist, 2002;Paul, 1992;Pawlik, 1993;Stachowicz, 2001). Marine sponges, ascidians, soft-bodied cnidaria and bryozoans are representative groups of marine invertebrates which are chemically defended against predators (for selected examples, see Aceret et al, 2001;Becerro et al, 1998;Burns et al, 2003;Chanas et al, 1996;Epifanio et al, 1999a;Epifanio et al, 1999b;Kubanek et al, 2002;Lindel et al, 2000;Lindquist, 1996;Marin et al, 1998;McClintock and Baker, 1997;O'Neal and Pawlik, 2002;Pawlik et al, 1995;Pisut and Pawlik, 2002;Stachowicz and Lindquist, 1997;Van Alstyne et al, 1994;Vervoort et al, 1998;Waddell and Pawlik, 2000), fouling (Becerro et al, 1997;Bhosale et al, 2002;Hattori et al, 2001;Henrikson and Pawlik, 1995;Kelly et al, 2003;Wahl et al, 1994), larval settlement (reviewed in Davis et al, 1989;Fusetani, 1997;Martín and Uriz, 1993;Pawlik, 1992) and solar UV radiation (Bandaranayake et...…”