Chemical defenses in the sea hare Aplysia parvula: importance of diet and sequestration of algal secondary metabolites

Ginsburg, David W.; Paul, Valerie J.

doi:10.3354/meps215261

Cited by 50 publications

(30 citation statements)

References 57 publications

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“…Indiscriminate predation by fishes was reported for chemically rich versus poor juvenile A. californica (Pennings 1990a) and Stylocheilus longicauda (Pennings et al 2001). The lack of deterrence by A. parvula with D. pulchra or L. obtusa secondary metabolites indicates that these compounds are ineffective as general defences against some fishes, in contrast to evidence for A. parvula with acquired Portieria hornemannii metabolites (Ginsburg & Paul 2001). Thus, A. parvula gain no additional protection by accumulating high concentrations of D. pulchra metabolites, or for the higher cost in performance associated with a diet of D. pulchra.…”

Section: Predation By Fishesmentioning

confidence: 63%

“…Furthermore, high levels of some secondary metabolites from the cyanophyte Lyngbya majuscula have an inhibitory effect on feeding by Stylocheilus longicauda (Nagle et al 1998). Furanone 3 from D. pulchra may also reduce feeding by A. parvula, as do apakaochtodene A and B from the alga Portieria hornemannii in Guam (Ginsburg & Paul 2001). One possible explanation is that high sequestration of furanone 3 causes lower consumption because of physiological limitations on processing ingested metabolites.…”

Section: Effects Of Diet On Performancementioning

confidence: 99%

“…A. parvula also differentially accumulate high concentrations of the metabolites palisadin A and furanone 3 from these red algae (Rogers et al 2000a). Ginsburg & Paul (2001) found A. parvula fed the chemically rich red alga Portieria hornemannii were unpalatable to reef fishes, whereas conspecifics fed the chemically poor red alga Acanthophora spicifera were readily eaten. In contrast to this evidence for a defensive role for algal metabolites acquired by sea hares, Pennings (1994) found variable results when comparing the palatability of skin tissue, ink and opaline secretions from 4 species of sea hare against crabs and fishes, and suggested that acquired algal metabolites play no part in defence.…”

Section: Introductionmentioning

confidence: 99%

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Effects of algal diet on the performance and susceptibility to predation of the sea hare Aplysia parvula

Rogers¹,

Nys²,

Steinberg³

2002

Mar. Ecol. Prog. Ser.

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Although sea hares are well known for acquiring algal secondary metabolites from their diet, the effects of diet on fitness and the susceptibility of sea hares to predators are poorly understood. We examined the effects of diet on the performance of the sea hare Aplysia parvula, and measured predation by reef fishes on sea hares raised on different seaweeds. Diet-switching, body size, the presence of conspecifics, and the presence of epiphytes on dietary algae were also investigated experimentally. A. parvula were fed the chemically rich red algae Delisea pulchra or Laurencia obtusa in laboratory experiments, and consumption, growth, egg production, conversion efficiency, and survivorship were measured. Sea hares fed L. obtusa consumed more algae, grew faster, laid more eggs, and had higher survivorship compared to sea hares fed D. pulchra. Most other factors investigated -body size, the presence of conspecifics or epiphytes -were in general unimportant relative to the effects of diet. The disparity in fitness of A. parvula fed D. pulchra versus L. obtusa is primarily due to different levels of consumption of each seaweed, as conversion efficiencies were similar. Predation on sea hares raised on different diets and containing different types and levels of acquired secondary metabolites was measured in field experiments in which sea hares were exposed to mixed assemblages of reef fishes. A high proportion of both chemically rich (fed red algae) and chemically poor sea hares (fed the green alga Ulva sp.) were eaten by fishes (with predation rates of 25 to 55% over 1 to 2 h), although this sea hare was relatively unpalatable compared to squid tissue. Juvenile A. parvula were eaten at a significantly greater rate than adults. Sea hare ink did not deter some fishes, which consumed both de-inked and untreated sea hares. Predation by fishes was similar in adjacent habitats, but varied between sites, and was not restricted to A. parvula as reef fishes also ate juvenile A. dactylomela of equivalent size. The benefit A. parvula gain from acquiring algal secondary metabolites is unclear, as these compounds appear ineffective as defences against some fishes. A. parvula may sequester algal secondary metabolites as part of a broader defensive strategy that includes crypsis and escape movements.

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Section: Predation By Fishesmentioning

confidence: 63%

Section: Effects Of Diet On Performancementioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Effects of algal diet on the performance and susceptibility to predation of the sea hare Aplysia parvula

Rogers¹,

Nys²,

Steinberg³

2002

Mar. Ecol. Prog. Ser.

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“…Passive chemical defenses are present in the skin, thus producing a distasteful surface to would-be predators, and many of these deterrent compounds have been identified (Kinnel et al, 1979; reviewed by Carefoot, 1987;Faulkner, 1992;Yamada and Kigoshi, 1997;Johnson and Willows, 1999;Rogers et al, 2000;Ginsburg and Paul, 2001). Active chemical defenses are released only upon predatory attack, and they include the secretions from two separate glands.…”

Section: Introductionmentioning

confidence: 99%

Packaging of chemicals in the defensive secretory glands of the sea hareAplysia californica

Johnson

Kicklighter

Schmidt

et al. 2006

Journal of Experimental Biology

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SUMMARY Sea hares protect themselves from predatory attacks with several modes of chemical defenses. One of these is inking, which is an active release of a protective fluid upon predatory attack. In many sea hares including Aplysia californica and A. dactylomela, this fluid is a mixture of two secretions from two separate glands, usually co-released: ink,a purple fluid from the ink gland; and opaline, a white viscous secretion from the opaline gland. These two secretions are mixed in the mantle cavity and directed toward the attacking predator. Some of the chemicals in these secretions and their mechanism of action have been identified. In our study,we used western blots, immunocytochemistry, amino acid analysis, and bioassays to examine the distribution of these components: (1) an l-amino acid oxidase called escapin for A. californica and dactylomelin-P for A. dactylomela, which has antimicrobial activity but we believe its main function is in defending sea hares against predators that evoke its release; and (2) escapin's major amino acid substrates - l-lysine and l-arginine. Escapin is exclusively produced in the ink gland and is not present in any other tissues or secretions. Furthermore, escapin is only sequestered in the amber vesicles of the ink glandand not in the red-purple vesicles, which contain algal-derived chromophores that give ink its distinctive purple color. The concentration of escapin and dactylomelin-P in ink, both in the gland and after its release, is as high as 2 mg ml-1, or 30 μmol ml-1, which is well above its antimicrobial threshold. Lysine and arginine (and other amino acids) are packaged into vesicles in the ink and opaline glands, but arginine is present in ink and opaline at <1 mmol l-1 and lysine is present in ink at <1 mmol l-1 but in opaline at 65 mmol l-1. Our previous results showed that both lysine and arginine mediate escapin's bacteriostatic effects, but only lysine mediates its bactericidal effects. Given that escapin's antimicrobial effects require concentrations of lysine and/or arginine >1 mmol l-1, our data lead us to conclude that lysine in opaline is the primary natural substrate for escapin in ink. Furthermore, packaging of the enzyme escapin and its substrate lysine into two separate glands and their co-release and mixing at the time of predatory attack allows for the generation of bioactive defensive compounds from innocuous precursors at the precise time they are needed. Whether lysine and/or arginine are substrates for escapin's antipredatory functions remains to be determined.

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“…As a biologically relevant stimulus, we chose the defensive ink of the sea hare Aplysia californica (Nolen et al, 1995;Coelho et al, 1998;Ginsburg and Paul, 2001;Kicklighter et al, 2005). Sea hares possess a variety of compounds and mechanisms that enable them to escape predation (Derby et al, 2007;Derby and Aggio, 2011), and the principal deterrent components of the ink for both blue crabs and bluehead wrasses have been identified as aplysioviolin (APV) and phycoerythrobilin (PEB) (Kamio et al, 2010a).…”

Section: Introductionmentioning

confidence: 99%

Oesophageal chemoreceptors of blue crabs,Callinectes sapidus, sense chemical deterrents and can block ingestion of food

Aggio

Tieu

Wei

et al. 2012

Journal of Experimental Biology

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SUMMARYDecapod crustaceans such as blue crabs possess a variety of chemoreceptors that control different stages of the feeding process. All these chemoreceptors are putative targets for feeding deterrents that cause animals to avoid or reject otherwise palatable food. As a first step towards characterizing the chemoreceptors that mediate the effect of deterrents, we used a behavioral approach to investigate their precise location. Data presented here demonstrate that chemoreceptors located on the antennules, pereiopods and mouthparts do not mediate the food-rejection effects of a variety of deterrents, both natural and artificial to crabs. Crabs always searched for deterrent-laced food and took it to their oral region. The deterrent effect was manifested as either rejection or extensive manipulation, but in both cases crabs bit the food. The biting behavior is relevant because the introduction of food into the oral cavity ensured that the deterrents gained access to the oesophageal taste receptors, and so we conclude that they are the ones mediating rejection. Additional support comes from the fact that a variety of deterrent compounds evoked oesophageal dilatation, which is mediated by oesophageal receptors and has been linked to food rejection. Further, there is a positive correlation between a compoundʼs ability to elicit rejection and its ability to evoke oesophageal dilatation. The fact that deterrents do not act at a distance is in accordance with the limited solubility of most known feeding deterrents, and likely influences predator-prey interactions and their outcome: prey organisms will be attacked and bitten before deterrents become relevant.

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Chemical defenses in the sea hare Aplysia parvula: importance of diet and sequestration of algal secondary metabolites

Cited by 50 publications

References 57 publications

Effects of algal diet on the performance and susceptibility to predation of the sea hare Aplysia parvula

Effects of algal diet on the performance and susceptibility to predation of the sea hare Aplysia parvula

Packaging of chemicals in the defensive secretory glands of the sea hareAplysia californica

Oesophageal chemoreceptors of blue crabs,Callinectes sapidus, sense chemical deterrents and can block ingestion of food

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