Waterborne and Surface-Associated Carbohydrates as Settlement Cues for Larvae of the Specialist Marine Herbivore Alderia modesta

Krug, Patrick J.; Manzi, Adriana E.

doi:10.2307/1543000

Cited by 61 publications

(47 citation statements)

References 40 publications

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“…Patches of V. longicaulis from the Kendall-Frost Northern Wildlife Preserve (San Diego, CA, USA) were grown at 16°C under a 12h photoperiod and used to prepare a stock solution of the algal carbohydrates that induce metamorphosis (Krug and Manzi, 1999;Krug and Zimmer, 2004). Algal tissue (1.34g wet mass) was boiled in 50ml distilled water for 10min, and the resulting boiled V. longicaulis extract (BVE) was filtered through a 100μm Nitex mesh and centrifuged to clarity.…”

Section: Collection Of Specimens and Larvaementioning

confidence: 99%

Nitric oxide signaling differentially affects habitat choice by two larval morphs of the sea slugAlderia willowi: mechanistic insight into evolutionary transitions in dispersal strategies.

Romero

Phuong

Bishop

et al. 2012

Journal of Experimental Biology

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SUMMARYIn many marine animals, adult habitat is selected by lecithotrophic (non-feeding) larvae with a limited lifespan. In generalist species, larvae may increasingly accept sub-optimal habitat over time as energy stores are depleted (ʻdesperate larvaʼ hypothesis). If the fitness cost of suboptimal habitat is too high, larvae of specialists may prolong the searching phase until they encounter a high-quality patch or die (ʻdeath before dishonorʼ hypothesis). In generalists, starvation is hypothesized to lead to a decline in inhibitory nitric oxide (NO) signaling, thereby triggering metamorphosis. Here, we document alternative functions for identified signaling pathways in larvae having ʻdesperateʼ versus ʻdeath before dishonorʼ strategies in lecithotrophic clutches of a habitat specialist, the sea slug Alderia willowi. In an unusual dimorphism, each clutch of A. willowi hatches both non-selective larvae that settle soon after hatching and siblings that delay settlement in the absence of cues from the alga Vaucheria, the sole adult food. Pharmacological manipulation of NO signaling induced metamorphosis in non-selective but not selective stages. However, decreased NO signaling in selective larvae lowered the threshold for response to habitat cues, mimicking the effect of declining energy levels. Manipulation of cGMP or dopamine production induced metamorphosis in selective and non-selective larvae alike, highlighting a distinct role for the NO pathway in the two larval morphs. We propose a model in which NO production (1) links nitrogen metabolism with sensory receptor signaling, and (2) shifts from a regulatory role in ʻdesperate larvaʼ strategies to a modulatory role in ʻdeath before dishonorʼ strategies. This study provides new mechanistic insight into how the function of conserved signaling pathways may change in response to selection on larval habitat choice behaviors.

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Section: Collection Of Specimens and Larvaementioning

confidence: 99%

Nitric oxide signaling differentially affects habitat choice by two larval morphs of the sea slugAlderia willowi: mechanistic insight into evolutionary transitions in dispersal strategies.

Romero

Phuong

Bishop

et al. 2012

Journal of Experimental Biology

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“…A mean 93% of larvae metamorphosed on the obligate adult host alga Vaucheria longicaulis compared with 0 to 9% metamorphosis in response to 17 other species of algae and a natural biofilm. Larval metamorphosis is induced by both high-and low-molecular weight carbohydrates produced by V. longicaulis (Krug & Manzi 1999). Algal polysaccharides often have species-specific structural characteristics, which may account for the specificity of the settlement response in A. modesta.…”

Section: Variation In Dispersal Potential Among Sibling Larvaementioning

confidence: 99%

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

Krug¹

2001

Mar. Ecol. Prog. Ser.

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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.

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“…alga Vaucheria longicaulis (Krug and Manzi, 1999;Krug and Zimmer, 2000), older larvae do not metamorphose indiscriminately. Rather, older, starved larvae of Alderia sp.…”

Section: Introductionlarval Desperation and Histaminementioning

confidence: 99%

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

Swanson

Marshall

Steinberg

2007

Journal of Experimental Biology

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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.

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Waterborne and Surface-Associated Carbohydrates as Settlement Cues for Larvae of the Specialist Marine Herbivore Alderia modesta

Cited by 61 publications

References 40 publications

Nitric oxide signaling differentially affects habitat choice by two larval morphs of the sea slugAlderia willowi: mechanistic insight into evolutionary transitions in dispersal strategies.

Nitric oxide signaling differentially affects habitat choice by two larval morphs of the sea slugAlderia willowi: mechanistic insight into evolutionary transitions in dispersal strategies.

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

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

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