Larval desperation and histamine: how simple responses can lead to complex changes in larval behaviour

Abstract

SUMMARY Some marine invertebrate larvae expand the range of settlement cues to which they will respond as they age. How do relatively simple larvae achieve such complex changes in behaviour? Larvae of the Australian sea urchin Holopneustes purpurascens settle and metamorphose specifically in response to a settlement cue, dissolved histamine, produced by the host alga Delisea pulchra. Older H. purpurascens larvae appear to accept a wider range of host algae, which contain far less histamine than D. pulchra, than newly competent larvae. We tested the hypothesis that older H. purpurascens larvae accept a greater range of host algae by metamorphosing in response to lower concentrations of histamine. We compared the response of newly competent and older larvae to a range of histamine concentrations in settlement assays. Larval age strongly affected the minimum concentration of histamine that induced metamorphosis in H. purpurascens, with older larvae responding to lower concentrations of histamine than newly competent larvae. Older larvae were more sensitive to lower concentrations of histamine yet still maintained a stringent requirement for exposure to histamine in order to metamorphose. In addition, older larvae metamorphosed after shorter exposure periods to histamine than did younger larvae. By using histamine concentration as a proxy for specific habitat cues, H. purpurascens larvae appear to expand their range of settlement preferences with age by simply changing their sensitivity to a single settlement cue. Overall, our results show that marine invertebrate larvae can exhibit surprisingly complex changes in behaviour via simple changes in their response to a single cue.

Extrinsic and intrinsic factors affecting the metamorphic rate of Tripneustes gratilla (Echinodermata: Echinoidea)

“…Moreover, the effect of larval age and its interaction with habitat-associated cues has received little attention. Consistent with the expectations of the original desperate larva hypothesis (DLH), older larvae of the Australian sea urchin Holopneustes purpurascens, a specialized herbivore with lecithotrophic larvae, metamorphosed at lower concentrations of -and shorter exposure to -histamine produced by an alga (Swanson et al 2007). Studies on sea urchins, which are generalists with planktotrophic larvae, may provide insights on the predictions of the modified DLH, which considers the effects of larval energy intake (feeding or non-feeding), planktonic mortality and post-settled habitat specificity (generalist and specialist) on decreasing selectivity with age (Elkin & Marshall 2007).…”

Causes of decoupling between larval supply and settlement and consequences for understanding recruitment and population connectivity

“…Competency can be defined as 14 "the capacity of a developing individual to initiate settlement and complete morphogenic 15 transformation associated with metamorphosis" (Bishop et al, 2006). Competent larvae can also 16 include those larvae that delay metamorphosis although they are developmentally ready to 17 metamorphose (Swanson et al 2007). We would expect that larval settlement would be more 18 tightly coupled with supply of competent larvae than to a mixture including non-competent 19 larval stages.…”

Behavioral responses of invertebrate larvae to water column cues

“…This is supported by my observations of oyster swimming behavior over the full competency period (Chapter 6). An alternate, equally valid interpretation of the hypothesis is that larvae become more sensitive to settlement cues with age, so that older larvae detect lower cue concentrations than younger larvae [155,161,165]. One may consider the desperate larva hypothesis in the following framework: two larval behavioral regimes, classified as "non-settlement" and "settlement", are mediated by larval age and the concentration of the chemical cue ( Fig.…”

“…Finally, body size [163], plankton mortality [164], and prior exposure to settlement cues [39,165] appear to be factors influencing changes in larval responses to cues with age.…”