Bet-hedging dispersal strategy of a specialist marine herbivore: a settlement dimorphism among sibling larvae of Alderia modesta

Abstract

Dispersal polymorphisms are known from many terrestrial organisms that inhabit fluctuating environments, but they are not well-recognized among marine invertebrates. An unusual form of variation was found in the settlement behavior of lecithotrophic larvae of the mollusc Alderia modesta (Lovén, 1844) that markedly altered the dispersal potential of sibling larvae. Most clutches contained, in variable proportions, larvae that spontaneously metamorphosed in the egg mass or within 2 d of hatching, and larvae that delayed metamorphosis until encountering the obligate adult food, the yellow-green alga Vaucheria longicaulis. The proportion of larvae undergoing spontaneous metamorphosis within a clutch was highly variable, ranging from 0 to 90%, and was unrelated to adult size. The proportion of intracapsular metamorphosis was also variable, ranging from 0 to 32%. The percentage of spontaneous metamorphosis per clutch was phenotypically plastic: when adults were starved, there was a significant tendency for each successive clutch to have a lower percentage of spontaneous metamorphosis, thus increasing the dispersal potential of the offspring. The decrease in spontaneous metamorphosis was significant after only 24 h of starvation. There was no significant increase in the cumulative level of spontaneous metamorphosis after the 2nd day post-hatching, but larval mortality increased as a linear function after the 5th day. Most larvae that did not spontaneously settle in the first 2 d delayed metamorphosis until they were exposed to the adult host alga, V. longicaulis. When 2 d old larvae were exposed to 17 species of macroalgae and sediment from the adult habitat, only V. longicaulis induced significant metamorphosis (93.3 ± 6.7%); all other species of algae and field sediment induced no metamorphosis or low levels (0-9%) that were not significantly higher than sea water controls. There was no difference in the settlement specificity of 2 and 9 d old larvae when tested against 2 different algae, nor in their ability to complete metamorphosis. The high initial percentage of spontaneous metamorphosis reduces the dispersal potential of some larvae in each clutch relative to their siblings that delay metamorphosis until stimulated by V. longicaulis; this settlement dimorphism represents a novel bet-hedging strategy among marine invertebrates.

Groups travel further: pelagic metamorphosis and polyp clustering allow higher dispersal potential in sun coral propagules

“…Species producing lecithotrophic offspring can apparently also control the pelagic larval duration, and thus dispersal potential, by manipulating resource allocation to individuals (Wendt 2000;Krug 2001;Marshall and Keough 2003;Gribben et al 2006;Stamps 2006). This regulation, however, is obviously limited by the constraints on the amount of resources that parents can transfer to eggs.…”

Variation in the dispersal potential of non-feeding invertebrate larvae: the desperate larva hypothesis and larval size

“…Larval settlement behaviour also has the potential to affect larval dispersal strongly. Larvae that settle relatively indiscriminately are likely to settle soon after becoming competent, while those using very specific settlement cues are likely to spend longer in the plankton before encountering the appropriate cue (Toonen & Pawlik 1994, Krug 2001. Any variation in settlement behaviour may, therefore, result in variation in the dispersal potential of larvae (Toonen & Pawlik 1994, Krug 2001.…”

“…Raimondi & Keough (1990) challenged this view and highlighted the existence of substantial intraspecific variation in the settlement behaviour of most larvae that had been studied. Since then, it has been suggested that this variation may be important and adaptive, particularly as a way of dealing with variation in the adult environment (Krug 2001, Toonen & Pawlik 2001a. Larval settlement behaviour also has the potential to affect larval dispersal strongly.…”

Larval metamorphosis of Phestilla spp. in response to waterborne cues from corals

“…Pawlik (1989) describes the trade off between settlement specificity and larval dispersal "…larvae appear to be selective enough to increase the likelihood of juvenile survival, but sufficiently broad in their response so as to minimize larval mortality." Some opisthobranchs have solved this trade off with a bet hedging strategy and have both lecithotrophic and planktotrophic larvae (Krug 2001;Smolensky et al, 2009). Settlement cues and metamorphic inducers are required for many marine larvae; however, even within the genus Phestilla there is a range of strategies for settling in the appropriate habitat for post-settlement survival.…”

“…Larvae of many marine molluscs can settle and metamorphose in response to chemical cues released by their prey, including sea hares (Switzer-Dunlap and Hadfield, 1977), the queen conch Strombus gigas (Boettcher and Targett, 1996), the dorid nudibranch Adalaria proxima (Lambert and Todd, 1994;Lambert et al, 1997), and the sacoglossan Alderia modesta (Krug, 2001;Krug and Manzi, 1999;Krug and Zimmer, 2000). Phestilla sibogae is a specialist aeolid nudibranch that has been studied for its larval ecology, physiology and behavior during the last 30 years (Hadfield, 1977;Hadfield and Paul, 2001).…”