Effect of plasticity in hatching on duration as a precompetent swimming larva in the nudibranch Phestilla sibogae

Plasticity in hatching can balance risks of benthic and pelagic development and thereby affect the extent of larval dispersal. Veligers of the nudibranch Phestilla sibogae hatched from their individual capsules if the encapsulated embryos were scattered from a torn gelatinous egg ribbon. Hatching occurred as early as day 4 at 231–251C. The early hatchlings lacked a propodium, swam, and were not yet competent to settle andmetamorphose. Hatchingmay be induced by predation: crabs consumed egg ribbons, and a portunid crab, caught in the act of tearing an egg ribbon, scattered encapsulated embryos. Undisturbed egg masses hatched as late as 9–11d at 231–251C, or as early as 8 d in a trial at 261C. Late hatchlings had a well-developed propodium, and 20–100% metamorphosed within a day of exposure to the inducer from the nudibranch’s coral prey. A few metamorphosed nudibranchs were found within hatching egg masses. Thus, the veligers can hatch so late that many are competent to metamorphose or so early that the obligate planktonic period can last 4 or more days. An attack by a predator means the benthic habitat is dangerous for the embryos, and swimming is presumably the safer option. In the absence of disturbance, the veligers hatch when ready or nearly ready to settle. Additional key words: metamorphosis, planktonic, risk, settlement Many animals protect embryos in aggregations, but the aggregations may also be attacked by predators. Hatching in response to an attack can adjust the risks of aggregated development in an egg mass or capsule versus solitary development as a hatched larva or juvenile (Warkentin 2000; Gomez-Mestre et al. 2008; Miner et al. 2010). For benthic animals with swimming larvae, plasticity in hatching could affect dispersal as well as mortality. Precompetent larvae have not yet developed the capacity to settle and metamorphose in response to stimuli that indicate favorable benthic sites. If adults are sedentary and if hatching at an earlier stage of development greatly extends the duration of precompetent pelagic development, then hatching in response to predation or other disturbance could greatly increase the distance that hatchlings travel from parents and siblings. Here, we examine the extent to which plasticity in hatching extends the duration of precompetent swimming for a benthic marine invertebrate. The veligers of the nudibranch gastropod Phestilla sibogae BERGH, 1874, can develop to metamorphic competence without food (Kempf & Hadfield 1985). As far as nutritional requirements are concerned, these nudibranchs could potentially hatch as metamorphosed crawling juveniles. The precompetent period of obligate swimming and dispersal of the larvae do not depend on an obligate period of feeding and growth for the development of metamorphic competence. Nevertheless, they have been observed to hatch as swimming veligers. Because a planktonic precompetent period does not result from a requirement for larval feeding and growth, the minimum period of larval swimming may be an indication of an adaptation for dispersal (Strathmann 2007). Timing of hatching is flexible, however, and affects more than dispersal. Plasticity in stage at hatching may also indicate a capacity to become planktonic when benthic development becomes dangerous (Hadfield & Strathmann 1996). The adults of P. sibogae lay gelatinous egg ribbons with a tough outer envelope (Fig. 1). Each embryo is in a separate capsule within the gel of the egg ribbon (Harris 1975). When the egg ribbon is torn, the capsules are scattered, and the Invertebrate Biology ]](]]): 1–10. r 2010, The American Microscopical Society, Inc. DOI: 10.1111/j.1744-7410.2010.00212.x Author for correspondence. E-mail: [email protected] veliger larvae hatch from their capsules, but hatching occurs later when ribbons are undisturbed (Miller & Hadfield 1986; Hadfield et al. 2000). Thus, the hatching of P. sibogae provides information about swimming larval stages as an adaptation for dispersal and as a migration to a habitat with benefits and risks different from that of the sea floor. Two other aspects of the veligers’ behavior also affect their dispersal. One is habituation to the metamorphic stimulus before hatching. The adults eat the coral Porites compressa DANA, 1846, and deposit their egg ribbons on the lower part of branches of the coral. The larvae settle and metamorphose in response to a chemical stimulus released into the water by the coral (Harris 1975; Hadfield 1977; Hadfield & Scheuer 1985; Hadfield & Pennington 1990; Koehl & Hadfield 2004; Koehl et al. 2007; Ritson-Williams et al. 2009). Veligers within an egg ribbon can become habituated to the metamorphic stimulus before hatching, and after hatching do not respond to the inducer until they have been in water free of the stimulus for 1–5h (Hadfield & Scheuer 1985). Thus, hatching veligers may be dispersed from the coral head occupied by the parents for a period of hours before they are capable of responding to the inducer. One interpretation is that enforced and obligate dispersal of a few hours is adaptive. Another is that habituation is an incidental consequence of exposure to the inducer. Dispersal may also be enhanced by a positive phototaxis in swimming of young hatched veligers (at 5–7d postfertilization at 261C) (Miller & Hadfield 1986). The positive phototaxis decreases with age. The effect of this age-dependent phototaxis on dispersal presumably depends on the age at hatching. The duration of obligate larval swimming of P. sibogae is the greatest, however, when egg ribbons are damaged. For experiments on larval behavior, egg ribbons can be artificially hatched by tearing (Hadfield & Scheuer 1985; Miller & Hadfield 1986; Pechenik et al. 1995). One interpretation is that hatching in response to damage of the egg ribbon is an adaptation in which veligers change habitat in response to risk. If damage to an egg ribbon is from a predator, unhatched veligers may soon be eaten. Even if the damage is from other causes, embryos that are scattered on the seafloor in capsules that are o350mm in length may be at a greater risk than embryos in an egg ribbon at a site selected by the mother. Hatching induced by damage to an egg mass increases the duration of precompetent swimming and thus increases larval dispersal, but the increased dispersal may be incidental to avoiding risk on the sea floor. Our objective in this study was to observe the range of stages and ages at which hatching can occur, vulnerability of egg ribbons to predation, and the consequences for the period of larval swimming before competence to settle. The minimum duration Fig. 1. Egg ribbons of Phestilla sibogae. A. Four egg ribbons on a coral fragment. Scale bar5 1 cm. B. Layers between a developing veliger and the sea. Arrows indicate the veliger surrounded by intracapsular fluid, the capsule wall, gel of the egg ribbon, and the envelope of the egg ribbon. Scale bar5 200 mm. C. A suspension of ink particles (dark) excluded by a fragment of gel (light) that was cut from an egg ribbon with included capsules and embryos. Scale bar5 400 mm. 2 Strathmann, Strathmann, Ruiz-Jones, & Hadfield Invertebrate Biology vol. ]], no. ]], ]] 2010 of precompetent larval swimming may indicate the extent of larval dispersal that is adaptive for these nudibranchs. The maximum duration of precompetent larval swimming indicates their maximum flexibility in avoiding risks of benthic development.