Feeding deterrence in sponges. The role of toxicity, physical defenses, energetic contents, and life-history stage.

The diverse natural products found within sponges mediate many of their ecological interactions, including predator feeding deterrence and defense against fouling. Pyrrole-imidazole compounds, often involved in such ecological interactions, are exclusively found in marine sponges, mainly from the genera Axinella and Agelas. Employing field and laboratory assays, we studied the chemical defense of 2 co-occurring Mediterranean sponges, Axinella polypoides and A. verrucosa, collected from the Gulf of Naples, Italy, against microbial fouling, as well as their feeding deterrence against the generalist shrimp Palaemon elegans. These assays revealed no activity in the extracts of A. polypoides, while the n-butanol part of the A. verrucosa extract showed activity in all assays at natural concentrations. This fraction of the extract contains the bromopyrrole hymenidin, and our assays revealed antibacterial and feeding deterrence activity for this pure compound. 1 H nuclear magnetic resonance quantification confirmed the presence of hymenidin and debromo-carteramine A, another previously isolated antibacterial compound, at ecologically relevant concentrations in the n-butanol part of the A. verrucosa extract. Our results indicate different antimicrobial and feeding deterrence defense strategies in the 2 examined sympatric sponge species, and multiple defensive roles of hymenidin in the defense of A. verrucosa, similar to those of other bromopyrroles isolated from taxonomically related Caribbean sponges. KEY WORDS: Bromopyrroles · Antifouling · Feeding deterrence · Chemical ecology · PoriferaResale or republication not permitted without written consent of the publisher

Section: Discussionmentioning

confidence: 99%

Chemical defense against predators and bacterial fouling in the Mediterranean sponges Axinella polypoides and A. verrucosa

Haber¹,

Carbone²,

Mollo³

et al. 2011

“…Contrary to what we expected, the toxicity of C. crambe was not reflected by an inhibition of settlement of the other species, as no differences in S. lophyropoda recruitment were found between control and C. crambe quadrats. Although toxicity has been located in cells of C. crambe that are extruded through the sponge surfaces ( Uriz et al 1996b), there is no definite evidence on how far from the sponge these toxic molecules can be effective in the field. Bingham & Young (1991) also report a lack of effect of toxic sponges on settlement in the field.…”

Section: Discussionmentioning

confidence: 99%

How do reproductive output, larval behaviour, and recruitment contribute to adult spatial patterns in Mediterranean encrusting sponges?

Uriz¹,

Maldonado²,

Turon³

et al. 1998

Self Cite

107

108

We studied the abundance and spatial pattern of 2 Mediterranean enci-ust~ng sponges, Crambe crambe (highly toxic) and Scopalina lophyropoda (non-toxic), at 4 spatial scales (0.5, 1, 2 and 4 m2). We also examined the reproductive output, larval behaviour and recruitment in these species, and assessed the relative importance of these parameters in explaining the abundance and spatial patterns of adults. We also determined, in field experiments, whether the presence of adults induces or inhibits recruitmenl in these 2 species. We found that C. crambe was much more abundant than S. lophyropoda at the site stu.died in both number of individuals per m? (67 * 2.7 vs 10.2 + 2.1, mean i SE) and coverage (47 + 1 9 vs l l . l * 1.4 Y o ) At the smallest scale sampled (0.5 m'), both species showed an aggregated pattern Aggregation \vas also detected for S. lophyropoda, but not for C crambe, at the scales of 1 and 2 m2 The number of embryos incubated per cm2 by C. crambe and S. lophyropoda was 76.2 + 12.5 and 1 4 * 1.7 (mean i SE), respectively. We estimated that the potential number of larvae of C. crambe released into the water column was about 20 times higher than that of S. lophyropoda. Larva! beha\.',ol?r was meni!ored in the !aSeratory and in !he fie!-'. La:...ae of S. !ophyropoda did not swim away from the release point. They maintained a vertical posture that minimised horizontal dispersal, and soon began crawling. In contrast, the larvae of C. crambe swam actively and had a comparatively delayed crawling phase. Recmitment of the 2 speries in scraped quadrats surrounded by individuals of C, cran~be and S lophyropoda, and in controls (rocky areas with no sponges), was monitored weekly for a month. Recruitment of both specles was higher in scraped quadrats surrounded by conspecifics. This effect was notably more marked for S. lophyropoda than for C. crambe recruits. The toxicity of C. crambe did not inhibit settlement of S. lophyropoda with respect to controls. The mean number of recruits per unit surface area after 1 mo (all substrates pooled) was ca 3.5 times higher for C. crambe than for S. lophyropoda. This difference was smaller than expected given that larval production of C. crambe was ca 20 times higher. This indicates that a significant proportion of C. crambe's offspring did not contribute to the maintenance of the local population. The aggregated pattern of S. lophyropoda at scales ranging from 0.5 to 2 m' and its discontinuous geographic distribution may be partially explained by strong phylopatry of its larvae due to their poor swimming ability and limited dispersal. The dominance of C crambe in littoral assemblages, its random distribution at scales larger than 0.5 m', and its ublquity along the littoral are traits that are consistent with high reproductive output, the swimming behaviour of larvae which facilitates wide dispersal, and patterns of recruitment found in this study. Therefore. S. lophyropoda populations appear to be maintained by offspring supplied by autochthonous individuals while...

“…If so, this could provide Botryllus with a significant competitive advantage because larvae of potential competitors would avoid Botryllus while it is small and presumably more vulnerable to spatial competitors. Ontogenetic differences in chemical defense have been documented in some benthic species including tunicates (Uriz et al 1996, Tarjuelo et al 2002see also Lindquist 2002). However, the hypothesis that Botryllus releases a negative settlement cue that varies ontogenetically remains untested and, because these types of defenses are likely rare, must be considered a non- parsimonious explanation for our observations.…”

Section: Comparison ------------------Settling Species --------------mentioning

confidence: 98%

Checking the landing zone: do invertebrate larvae avoid settling near superior spatial competitors?

Bullard¹,

Whitlatch²,

Osman³

2004

It has been hypothesized that larvae of benthic marine invertebrates may reduce their risk of post-settlement competition by avoiding superior competitors during settlement. Few studies, however, have directly compared the levels of larval settlement close to and away from established competitors. We conducted experiments in the New England subtidal to determine whether larvae of fouling organisms would avoid substrata (100 cm 2 PVC panels) with established adult colonies of the tunicates Botryllus schlosseri, Botrylloides violaceus, and Diplosoma listerianum compared to control substrata without tunicates. After panels had been exposed for 1 wk in the field, we assessed larval settlement on the entire surface of panels and within 1 cm of established tunicate colonies. We also monitored the fate of larvae that settled near established tunicates to determine if different tunicate species posed different risks of overgrowth to newly settled juveniles. Pair-wise comparisons revealed only 1 significant difference (out of 48 total analyses) when we examined levels of settlement on panels with tunicates relative to bare controls. We also found no significant differences in the number of settlers overgrown by different tunicate species. Thus, our results suggest that invertebrate larvae do not avoid settling near established dominant competitors (i.e. colonial tunicates). These results are in contrast to a previous study which had shown that larvae of competitively inferior species avoided settling near B. schlosseri.