Phototactic responses of larvae from the marine sponges Neopetrosia proxima and Xestospongia bocatorensis (Haplosclerida: Petrosiidae)

Previous studies suggest that phototaxis in sponge larvae is generated by the bending of a tuft of long posterior cilia (LPC). The photoresponsiveness of these cilia is often assayed by examining their reaction to sudden changes in light intensity. Here, we document and describe the larvae of the tropical marine sponges Neopetrosia proxima and Xestospongia bocatorensis and examine the phototactic behavior of their larvae. Both species brood ovoid, tufted parenchymella larvae, clearly countering an earlier hypothesis that all petrosid sponges are oviparous. Larvae of N. proxima were positively phototactic and settled after 2 d, while larvae of X. bocatorensis were negatively phototactic and settled in as little as 4 h. In both species, LPC quickly responded to changes in the light intensity. When the light intensity is reduced, the larvae of N. proxima fold the cilia inwards immediately without beating, then flare them outwards, beating for a few seconds, and then gradually return to the neutral position while continuing to beat. In contrast, the larvae of X. bocatorensis flare the cilia outwards when the light intensity is reduced and fold them inwards when the light intensity is increased. Comparisons with reported ciliary responses to light for other species demonstrate that these responses do not show the hypothesized one-to-one correspondence with phototactic behaviors and are, therefore, of limited use in explaining the mechanisms that coordinate larval swimming. Additional key words: Porifera, parenchymella larvae, larval ecology Although relatively little is known about the behavior of sponge larvae compared with the larvae of other marine invertebrates, it is clear that light plays an important role in their ecology. Light can be a key trigger for larval release either via the onset of darkness before release (Amano 1986), via increased light intensity the day before release (Amano 1988), or via intense light exposure (Maldonado & Young 1996). Light can also influence the choice of settlement sites, with most species showing either a preference for shaded sites or no preference at all. In field studies, increased recruitment of Tedania ignis (DUCHASSAING & MICHELOTTI 1864) and Crambe crambe (SCHMIDT 1862) was observed on shaded areas of settlement tiles, but no difference in the recruitment of Sigmadocia caerulea (HECHTEL 1965) was observed between shaded and unshaded substrates (Maldonado & Young 1996; Maldonado & Uriz 1998). Settlement site preferences could be mediated by phototactic larval swimming. There is significant diversity among sponge species in phototactic behavior: of the 88 species with documented phototaxis, 25 display positive phototaxis, 41 show no clear response to light, and 22 are negatively phototactic (Table 1; Wapstra & Van Soest 1987). In addition, phototaxic behavior can change during the larval lifespan. For example, larvae of the dictyoceratid Cacospongia mollior SCHMIDT 1862 are positively phototactic when they are released from the parent, but become negatively phototactic after 4–6h (Maldonado et al. 2003). The mechanisms underlying phototaxis in sponge larvae, which lack neural networks and gap junctions, are not fully understood (Leys & Degnan 2001; Invertebrate Biology 129(2): 121–128. r 2010, The Authors Journal compilation r 2010, The American Microscopical Society, Inc. DOI: 10.1111/j.1744-7410.2010.00196.x Author for correspondence. E-mail: [email protected] Maldonado et al. 2003). Negative phototaxis in the larvae of Amphimedon queenslandica HOOPER & VAN SOEST 2006 (identified as Reneira sp. in Leys & Degnan (2001)) is thought to be conferred by a shadow response in which the long posterior cilia (LPC) straighten in response to an increase in the light intensity and bend in response to a decrease in the light intensity. The negatively phototactic larvae of Ircinia oros (SCHMIDT 1864) and C. mollior show the opposite response: the LPC fold inwards clockwise when exposed to sudden increases in light and flare outwards when the light is reduced below 50mmol photons m s 1 (Maldonado et al. 2003). The prevailing hypothesis, based on these observations, is that when light is directed from one side of the larva, the LPC bend in response to shading, resulting in an angle between the ciliary tuft and the body axis of the larva. Drag from this displacement of the LPC, combined with the clockwise rotation of the larva, causes the larva to turn away from the light (‘‘Maldonado Table 1. A summary of phototaxis (1, none, or ) and ciliary responses to increased light intensity in sponge larvae. These data are from studies published subsequent to the compilation of similar data by Wapstra & Van Soest (1987). Of these 28 species, seven display positive phototaxis, seven show no clear phototactic response, and 14 are negatively phototactic. Wapstra & Van Soest (1987) provided phototactic response data for an additional 60 taxa; when considering all 88 species, 25 display positive phototaxis, 41 show no clear response, and 22 are negatively phototactic. NA5not available. Species Phototaxis Ciliary response References Dendroceratida Chelonaplysilla noevus NA Mariani et al. (2005) Dictyoceratida Cacospongia mollior 1/ Extend then fold Maldonado et al. (2003) Dysidea avara 1 NA Mariani et al. (2005) Hippospongia lachne NA Kaye & Reiswig (1991) Ircinia oros Fold Maldonado et al. (2003) Luffariella variabilis None/ NA Ettinger-Epstein et al. (2008) Pleraplysilla spinifera 1 NA Mariani et al. (2005) Rhopaloeides odorabile 1 NA Whalan et al. (2008) Spongia (Spongia) barbara NA Kaye & Reiswig (1991) Spongia (Spongia) graminea NA Kaye & Reiswig (1991) Spongia (Spongia) officinalis NA Gaino et al. (2007) Hadromerida Cliona viridis None NA Mariani et al. (2005) Halichondrida Halichondria magniconulosa NA Maldonado & Young (1996) Halichondria melanodocia 1 NA Woollacott (1990) Scopalina lophyropoda None NA Mariani et al. (2005) Haplosclerida Amphimedon queenslandica Extend Leys & Degnan (2001) Haliclona sp. 1 NA Mariani et al. (2005) Haliclona (Reniera) tubifera NA Maldonado & Young (1996) Haliclona (Soestella) caerulea Extend Maldonado & Young (1996), Maldonado et al. (2003) Neopetrosia proxima 1 Extend then fold This study Niphates digitalis NA Lindquist et al. (1997) Xestospongia bocatorensis Fold This study Homosclerophorida Oscarella sp. None NA Mariani et al. (2005) Poecilosclerida Clathria (Thalysias) jolicoeuri None NA Mariani et al. (2005) Crambe crambe None NA Mariani et al. (2005) Phorbas tenacior NA Mariani et al. (2005) Tedania (Tedania) ignis NA Maldonado & Young (1996)