Auditory and olfactory abilities of pre-settlement larvae and post-settlement juveniles of a coral reef damselfish (Pisces: Pomacentridae)

The propagules of most species of reef fish are advected from the reef, necessitating a return to reef habitats at the end of the pelagic stage. There is increasing evidence of active attraction to the reef but the sensory abilities of reef fish larvae have not been characterized well enough to fully identify cues. The electrophysiological methods of auditory brainstem response (ABR) and electroolfactogram (EOG) were used to investigate auditory and olfactory abilities of preand post-settlement stages of a damselfish, Pomacentrus nagasakiensis (Pisces, Pomacentridae). Audiograms of the two ontogenetic stages were similar. Pre-settlement larvae heard as well as their post-settlement counterparts at all but two of the tested frequencies between 100 Hz and 2,000 Hz. At 100 and 600 Hz, pre-settlement larvae had ABR thresholds 8 dB higher than those of post-settlement juveniles. Both stages were able to detect locally recorded reef sounds. Similarly, no difference in olfactory ability was found between the two ontogenetic stages. Both stages showed olfactory responses to conspecifics as well as L-alanine. Therefore, the auditory and olfactory senses have similar capabilities in both ontogenetic stages. Settlement stage larvae of P. nagasakiensis can hear and smell reef cues but it is unclear as to what extent larvae use these sounds or smells, or both, as cues for locating settlement sites. Introduction Coral reef fish have a bipartite lifecycle, wherein the first few days to months of life are spent as a larva in the pelagic environment, feeding, developing and growing before it is necessary to locate a suitable reef habitat for settlement (Leis 1991; Leis and McCormick 2002). Once a suitable benthic settlement habitat is located, a larva must metamorphose, thus changing both habitat and morphology over a short time period. Knowledge of the key processes and behaviours over this transition period are vital for understanding the life history of reef fishes and for the management of populations. Many gaps that had previously existed in our knowledge of behaviour and processes over this time are only recently being filled and this paper continues by investigating two sensory abilities of a pomacentrid damselfish over the settlement transition. The dispersal of reef fish larvae was long believed to be passive, with settlement thought to occur wherever currents took the larvae (Roberts 1997). These assumptions of passive dispersal are being revised, and strong evidence now exists to dispel the hypothesis of coral reef fish larvae as being only passive. Settlementstage larvae have strong swimming abilities, are able to swim at speeds greater than ambient currents, can swim long distances and can change both their horizontal and vertical trajectories (Leis et al. 1996; Leis and Carson-Ewart 1997, 2003; Stobutzki and Bellwood 1997). Larvae are also able to orientate in the pelagic environment (Stobutzki and Bellwood 1998; Leis and Carson-Ewart 1999, 2003) and return of larvae to natal reefs is now known to occur, in some cases accounting for as much as 60% of all new recruits (Jones et al. 1999; Swearer et al. 1999; Taylor and Hellberg 2003). Thus, larvae are far from passive and sensory abilities may play a vital role in their dispersal and settlement location. The sensory abilities of coral reef fish larvae were previously assumed to be poor, being developed suffiCommunicated by M. S. Johnson, Crawley K. J. Wright (&) School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia E-mail: [email protected] D. M. Higgs Æ A. J. Belanger Department of Biology, University of Windsor, Windsor, ON N9B3P4, Canada J. M. Leis Æ K. J. Wright Ichthyology and Division of Aquatic Zoology, Australian Museum, 6 College St, Sydney, NSW 2010, Australia Marine Biology (2005) 147: 1425–1434 DOI 10.1007/s00227-005-0028-z ciently for feeding and little else (Myrberg Jr and Fuiman 2002). We now know that this is not the case. Light traps deployed at night with a speaker broadcasting nocturnal reef noise attract more larvae than light traps that are quiet (Tolimieri et al. 2000; Leis et al. 2003) and the behaviour of larvae is altered in the presence of broadcast nocturnal reef noise (Leis et al. 2002). Further, larvae are able to distinguish between artificial sounds (pure tones) and natural sounds (reef noise) (Leis et al. 2002) and have the ability to localize a sound source (Tolimieri et al. 2004; Leis and Lockett 2005). In addition, the hearing sensitivity of post-settlement juveniles of two damselfishes showed converse changes with size—auditory thresholds of Stegastes partitus decreased with increasing size (Kenyon 1996) whilst thresholds of Abudefduf saxatilis increased with increasing size (Egner and Mann 2005), although no data exist on either species responses prior to settlement. The sense of smell has also been shown to be functional and utilised by settlement-stage reef-fish larvae. Apogonid larvae are capable of distinguishing between lagoon water and oceanic water by olfaction (Atema et al. 2002), and larval anemonefish use olfaction to locate a host anemone (Elliot et al. 1995; Arvedlund et al. 1999). All of these studies, however, are behavioural and not physiological and none have examined sensory abilities during the pelagic to benthic transition. The present study aimed to determine electrophysiologically, the auditory and olfactory abilities of a coral reef damselfish, Pomacentrus nagasakiensis, at settlement stage to identify potentially relevant cues for reef attraction. We also examine if the sensitivity of these senses changed with settlement and concomitant metamorphosis. Pomacentrids are a dominant feature of coral reef communities—they are one of the most speciose of fish families on coral reefs and account for a large proportion of the individual and fish biomass on coral reefs (Leis and Carson-Ewart 2002). Like most species of damselfishes (Allen 1991), P. nagasakiensis has a bipartite life cycle, with a pelagic larval stage followed by settlement on suitable reef habitat for the adult benthic phase of the life cycle (McCormick et al. 2002). To test auditory and olfactory abilities across the settlement transition, we employed two physiological methods previously used in auditory and olfactory tests in fish—auditory brainstem response (ABR) (Kenyon et al. 1998; Yan and Curtsinger 2000; Higgs et al. 2003; Wysocki and Ladich 2003) and electroolfactogram (EOG) (Caprio 1978). Both techniques measure electrical responses evoked by the sensory stimuli of sound and smell, and are a direct evaluation of auditory and olfactory ability, respectively. This is the first study to use ABR to test the hearing sensitivity of coral reef fish larvae, with previous work being confined to freshwater species or benthic juveniles and adults. It is also the first to use the EOG technique for the larvae of a marine fish. Using physiological techniques allow us to ascertain whether natural reef stimuli are a viable cue for orientation to settlement habitats and begin to quantify minimal stimulus levels required to drive such