The effect of a species-specific avoidance response to predatory starfish on the intertidal distribution of two gastropods

Summary The gastropodsAcmaea (Collisella) limatula andAcmaea (Notoacmea) scutum respond to water flowing over certain predatory starfish (i.e. to the scent of the starfish) by moving rapidly up a submerged, vertical surface. These limpets respond with upward movement to the scent ofPisaster ochraceus, Pisaster giganteus, Pycnopodia helianthoides, andLeptasterias aequalis. All of these starfish are predators on molluscs and at least occasionally inhabit the intertidal. In contrast, the limpets respond weakly or not at all to the scent ofPatiria miniata andPisaster brevispinus. Patiria is an omnivorous scavenger, andP. brevispinus is predaceous but strictly subtidal when it occurs on rocky shores. For the starfish tested, then, the limpets only give avoidance responses to starfish species naturally encountered as predators.The avoidance response ofA. limatula andA. scutum to predatory stafish can also be demonstrated in the field. When onePisaster ochraceus is placed beneath a population of limpets in the intertidal and confined so that contacts between the starfish and limpets are impossible, the limpet population is displaced significantly upward after one tidal cycle. In addition, the closer the limpets are to the starfish, the greater is their upward displacement.     

Behavioral responses of seven species of asteroids to the asteroid predator,Solaster dawsoni (responses of asteroids to the predator Solaster dawsoni)

Summary Seven asteroid species common to the northern California coast were studied for their defensive responses to the predator Solaster dawsoni. The presence or absence of an escape response was used to predict whether or not these species were susceptible to predation from Solaster. Strong escape responses were displayed by Patiria miniata, Henricia leviuscula, Leptasterias hexactis, Pycnopodia helianthoides, and small Pisaster ochraceus. Subsequent capture and consumption of Patiria, Henricia, Leptasterias and small P. ochraceus were observed. Solaster attacked all Pisaster spp. tested, but Pisaster brevispinus and larger P. ochraceus protected themselves from predation by utilizing their pedicellariae against Solaster whenever contact occurred. Dermasterias imbricata appeared to be immune to predation by Solaster. Contact between these two asteroids failed to elicit a defensive response in the former or an attack by the latter asteroid.     

Localization and electrical activity of the distance chemoreceptors that mediate predator avoidance behaviour in Acmaea limatula and Acmaea scutum (gastropoda, prosobranchia).

1. The marine gastropods Acmaea (Collisella) limatula and Acmaea (Notoacmea) scutum respond to distant predatory starfish (i.e. to starfish scent) by moving up a vertical surface. 2. The distance chemoreceptors that mediate this avoidance behaviour are located on the mantle margin. Heat cauterization of the limpets' mantle margin eliminates their responsiveness to Pisaster ochraceus scent, while a similar cauterization of the ctenidium and the osphradia does not diminish the avoidance behaviour. 3. Primary afferent electrical activity can be recorded from the chemoreceptors on the mantle margin that are responsive to starfish scent and also from other physiologically distinct receptors that are responsive to contact with starfish tube feet.     

Maintenance of the shore-level size gradient in the marine snail Tegula funebralis (A. Adams): Importance of behavioral responses to light and sea star predators

The intertidal gastropod, Tegula funebralis (A. Adams) exhibits a shore-level size gradient with mean shell size increasing in a down-shore direction. Snails transferred to zones where they do not usually occur migrated back towards their original zone, thus re-establishing a size gradient and implying differential movement among size classes. Both large (≥2.1 cm shell width) and small (≤ 1.77 cm) snails were photonegative on a horizontal surface and geonegative in the laboratory; there were no statistical differences between size classes. Light, however, inhibited upward, or caused downward, movement of large snails on vertical surfaces. Small snails were unaffected, ranging higher on illuminated vertical surfaces than large snails. Both sizes exhibited similar distributions in the dark. In an experimental chamber providing both emersed and immersed surfaces, T. funebralis established vertical size gradients when the chamber was illuminated from above. It is suggested that light is an important factor in the formation and maintenance of Tegula's shore-level size gradient.In response to water-borne chemicals derived from the sea star Pisaster ochraceus (Brandt), large snails moved up vertical surfaces in greater proportion than small. In response to contact with the predator, large snails moved away faster than small and individuals collected from crevices in the field moved away slower than those collected from open rock faces. Although predation may select for a size gradient in Tegulafunebralis, it is unlikely that responses to predatory sea stars directly and proximally cause or maintain them over the short term.     

The motile escape response of a sessile prey: A sponge-scallop mutualism

The association of the sponges Myxilla incrustans (Esper) and Mycale adhaerens (Lambe) with the scallops Chlamys hastata hericia Gould and C. rubida (Hines) is shown to be a mutualism, which protects the sponges from predatory sponge-rasping dorid nudibranchs and the scallops from predatory starfish. The sponge is protected by scallop motility (also shown for the Suberites ficus-hermit crab association). The sponge helps to protect the scallops by altering the surface texture of the shell so increasing the efficacy of the swimming escape response by decreasing the adhesive abilities of asteroid tube-feet. The sponge also provides tactile camouflage against certain predatory starfish. There was no evidence that either component chemically deceived or repelled the predators of the other component. Predation pressure on both components of the association appears to be the major force leading to the mutualism.     

Interpopulation and context-related differences in responses of a marine gastropod to predation risk

We conducted laboratory experiments to investigate interpopulation differences in the behavioural responses of the whelk Buccinum undatum to the predatory lobster Homarus americanus and the asteroid Leptasterias polaris, both in the absence and presence of feeding opportunities. Whelks from three populations in the eastern North Atlantic (1) responded to lobsters by displaying avoidance behaviours (burrowing in the sediments or retreating inside their shell), (2) responded to asteroids by displaying escape responses (rapid crawling, shell rocking behaviour or foot contortions), and (3) more often refrained from feeding in the presence of a lobster than in the presence of an asteroid. Although whelks from the three populations responded similarly to lobsters and asteroids, interpopulation differences were evident. Thus, whelks from populations sympatric with a given predator more frequently displayed 'appropriate' antipredator behaviours (i.e. avoidance in the presence of a lobster, and escape in the presence of an asteroid) than did whelks allopatric with that predator. Also, whelks from a population sympatric with both predators fed less readily in the presence of a given predator than did whelks allopatric with that predator. However, the presence of a lobster or an asteroid had the same impact on the feeding response of whelks from two populations with contrasting predator fields, one sympatric with lobsters, but allopatric with asteroids, and one sympatric with asteroids, but allopatric with lobsters. The results of our study indicate that coexistence (over evolutionary or ecological time) with lobsters and asteroids increases the propensity of the whelk to display avoidance and escape behaviours in the presence of lobsters and asteroids, respectively, but has a less predictable effect on how whelks trade off predation risk and food acquisition. Studies are needed to investigate the roles of inheritance and experience on the development of antipredator behaviours and decision making by prey animals when predation risk conflicts with other fitness-related activities such as the acquisition of food or reproductive opportunities. Copyright 1999 The Association for the Study of Animal Behaviour.     

Length of pelagic period in echinoderms with feeding larvae from the Northeast Pacific

Minimum and maximum times from fertilization to settling are reported for larvae reared in the laboratory from 12 species of echinoderms representing four classes. For the holothuroid Parastichopus californicus (Stimpson) the maximum time observed was 13 weeks; for the asteroids Luidia foliolata Grube, Pisaster ochraceus (Brandt), and Pycnopodia helianthoides (Brandt) the maxima were 20, 32, and 21 weeks, respectively; for the ophiuroid Ophiopholis aculeata (Linnaeus) the maximum was 31 weeks; for the echinoids Brisaster latifrons (A. Agassiz), Dendraster excentricus (Eschscholtz), Allocentrotus fragilis (Jackson), and Strongylocentrotus droebachiensis (O. F. Müller) maxima were 24, 23, 36, and 21 weeks, respectively. The maximum pelagic periods in each class of echinoderms were approximately double other estimates based on cultured larvae. The pelagic periods in these cultures suggest a capacity for extensive dispersal in nature.     

Chemoreception by the asteroid Cross aster papposus (L.)

Chemoreception abilities were demonstrated in the solasterid asteroid Crossaster papposus (L.) from a level substratum in the current-swept Crouch Estuary, England. C. papposus showed wide variability of positive and negative responses to crude extracts of prey species and (unattractive) conspecifics. C. papposus has an olfactory (distance chemoreception) ability to whole, live potential prey and conspecifics. This was confirmed by contact chemoreception responses, which are stronger, to the same stimuli. The olfaction tests in the Y-maze yielded variable results in which the initial (rheopositive or rheonegative) responses demonstrated that conspecifics and prey species were avoided yet subsequent arm choices of rheopositive individuals showed significant selection for prey over controls and no avoidance of conspecifics. The arm choices for prey relate to a priority of orientation to food and feeding over intraspecific avoidance in hungry asteroids. Intraspecific avoidance functions more in dispersion than prevention of cannibalism and is less important than feeding to hungry asteroids. Interpretation of chemically-mediated responses of asteroids requires appreciation of their innate behavioural variability which has led to confusion in the literature. This is the first experimental study of contact and distance chemoreception among solasterids. Their chemosensory abilities have previously been contradictory which may be due to intraspecific avoidance in satiated individuals of some species.     

Excito-Repellent Responses between <Emphasis Type="Italic">Culex quinquefasciatus</Emphasis> Permethrin Susceptible and Resistant Mosquitoes

The behavioral responses exhibited between four permethrin-resistant field-derived populations and a long-established, permethrin susceptible colony population of Culex quinquefasciatus mosquitoes was assessed for behavioral responses to permethrin in an excito-repellency (ER) test system. After a 30-min exposure to two different insecticide concentrations (200 and 500 mg/m²) in paired contact and noncontact test designs, the initial knockdown and escape (exit) responses were recorded followed by mortality after 24-h. All five test populations rapidly escaped from the chambers treated with permethrin regardless of background insecticide susceptibility status or chemical concentration. The greatest contact escape response was seen from the colonized population with 88 % of specimens escaping the chamber within 30-min. Contact irritancy was the predominant response compared to relatively weak noncontact spatial repellency in all test populations at both low and high concentrations. At the lower concentration, the contact escape responses did not appear influenced by background susceptibility status, whereas at the higher concentration the permethrin-resistant field populations exhibited significantly reduced avoidance behavior compared to the laboratory susceptible strain.     

Predator regime influences innate anti-predator behaviour in the freshwater gastropod Lymnaea stagnalis

1. Predation incurs high fitness costs in aquatic organisms either through direct consumption or through avoidance responses that reduce time for activities such as feeding and reproduction. Hence, avoidance responses of aquatic organisms should vary to match closely the predation threat in their environment.
2. The freshwater gastropod Lymnaea stagnalis occurs in a variety of environments which vary in the presence or absence of predatory fish. We used naïve snails reared from six populations of this species experiencing different predator regimes (three co-occurring with molluscivorous fish and three without) to assess whether populations differed in the type and degree of their avoidance behaviours. Innate behavioural responses to four treatments (control, conspecific alarm cues, fish kairomones and fish kairomones paired with alarm cue) were compared in laboratory trials.
3. The primary anti-predator behaviour of L. stagnalis in response to fish kairomones was to crawl out of the water rather than seek refuge under water. This response was strongest when fish kairomones were paired with alarm cues, and varied depending on population origin; snails reared from populations co-occurring with predatory fish showed a stronger response than those raised from populations not experiencing such predators. In addition, populations co-occurring with predatory fish responded to the fish kairomones presented alone.
4. Our findings suggest that the degree of innate anti-predator behaviour shown by L. stagnalis , in terms of both the level of risk to which it responds and the degree of response, varies depending on the predator regime experienced by field populations. Together with previous work on cue association, this demonstrates that this gastropod is able to match its avoidance behaviour very closely to short and long term predation threats within its habitat.     

Contrsating anti-predator defenses of sympatric marine gastropods (family Trochidae)

Three of four sympatric gastropods found in southern California waters, Tegula aureotincta Forbes, Norrisia norrisi (Sowerby), and Astraea undosa (Wood), display behavioral flight responses to predatory asteroids and a gastropod. The fourth species, Tegula eiseni Jordan, lacks this behavior but does have morphological features that deter predators. The shell of T. eiseni is thicker and the tissue more difficult to acid hydrolyze than that of its sympatric congener, T. aureotincta. Juvenile seastars fed T. aureotincta grew three times faster than those reared on T. eiseni. The dissimilarity in growth rates is not attributed to differences in nutritive value of the two Tegula species, but is due to differences in the rate at which the seastars can consume the snails. Laboratory choice tests demonstrate that the anti-predator defense of T. eiseni reduces its acceptability as food. In contrast, the behavioral flight defense of the three remaining gastropods decreases the probability of their capture by certain predators.     

Mantle defensive response of marine pulmonate Trimusculusperuvianus

The marine pulmonate Trimusculusperuvianus (Sowerby, 1835) which is found in caves or narrow crevices along the Chilean coast was studied to determine a possible chemical defense against the intertidal key predator Heliasterhelianthus. T.peruvianus releases a white secretion through the extended mantle animal covers, to contact with the tube feet of starfish. This behaviour significantly decreases predation of gastropod and it has not been described previously for members of the Trimusculidae family.     

Plasticity of Escape Responses: Prior Predator Experience Enhances Escape Performance in a Coral Reef Fish

Teleost and amphibian prey undertake fast-start escape responses during a predatory attack in an attempt to avoid being captured. Although previously viewed as a reflex reaction controlled by the autonomic nervous system, the escape responses of individuals when repeatedly startled are highly variable in their characteristics, suggesting some behavioural mediation of the response. Previous studies have shown that fishes are able to learn from past experiences, but few studies have assessed how past experience with predators affect the fast-start response. Here we determined whether prior experience with the smell or sight of a predator (the Dottyback, Pseudochromis fuscus) affected the escape response of juveniles of the Spiny Chromis (Acanthochromis polyacanthus). Results show that individuals exposed to any of the predator cues prior to being startled exhibited a stronger escape response (i.e., reduced latency, increased escape distance, mean response speed, maximum response speed and maximum acceleration) when compared with controls. This study demonstrates the plasticity of escape responses and highlights the potential for naïve reef fish to take into account both visual and olfactory threat cues simultaneously to optimise the amplitude of their kinematic responses to perceived risk.     

Pyrethroid susceptibility and behavioral avoidance in Anopheles epiroticus,a malaria vector in Thailand

The physiological susceptibility to insecticides and the behavioral responses of four wild‐caught populations of female Anopheles epiroticus to synthetic pyrethroids (deltamethrin, permethrin, and alpha‐cypermethrin) were assessed. Test populations were collected from different localities along the eastern coast, Trat (TR), Songkhla (SK), and Surat Thani (ST) and one population from the western coast, Phang Nga (PN). Results showed that all four populations of An. epiroticus were susceptible to all three synthetic pyrethroids tested. Behavioral responses to test compounds were characterized for all four populations using an excito‐repellency test system. TR displayed the strongest contact excitation (‘irritancy’) escape response (76.8% exposed to deltamethrin, 74.1% permethrin, and 78.4% alpha‐cypermethrin), followed by the PN population (24.4% deltamethrin, 35% permethrin, and 34.4% for alpha‐cypermethrin) by rapidly escaping test chambers after direct contact with surfaces treated with each active ingredient compared with match‐paired untreated controls. Moderate non‐contact repellency responses to all three compounds were observed in the TR population but were comparatively weaker than paired contact tests. Few mosquitoes from the SK and ST populations escaped from test chambers, regardless of insecticide tested or type of trial. We conclude that contact excitation was a major behavioral response in two populations of An. epiroticus, whereas two other populations showed virtually no escape response following exposure to the three pyrethroids. The explanation for these large unexpected differences in avoidance responses between pyrethroid‐susceptible populations of the same species is unclear and warrants further investigation.     

Biochemical investigation of two responses involved in the feeding behaviour of Acanthaster planci (L). I. Assay methods and preliminary results

Material obtained by simple biochemical fractionation of aqueous extracts of coral has been tested for its ability to induce responses normally associated with feeding on live corals in the crown-of-thorns starfish, Acanthaster planci (L.) With the use of a new assay method, it has been shown that both dialysable and non-dialysable components of aqueous coral extract cause cessation of movement, settlement, and eversion of the stomach as if over a whole coral. A second response, apparently of avoidance, seen as a starfish approaches a coral prior to feeding, has also been examined; it is evoked by the dialysable fraction of coral extract.     

Chemo-tactile predator avoidance responses of the common Antarctic limpet Nacella concinna

The Antarctic limpet, Nacella concinna, has the ability to escape predation by the predatory sea star, Neosmilaster georgianus. When the sea star comes into contact with the limpet, the limpet undergoes characteristic behaviors that include extension of its pallial tentacles, raising its shell in a mushroom-like fashion, rotation, and flight. These behaviors were not observed until the sea star physically contacted the limpets and were not induced by the omnivorous sea star, Odontaster validus, which occupies the same habitats as Ne. georgianus. Crude hydrophilic extracts from Ne. georgianus, but not from O. validus, induced the escape behaviors, indicating that this response is chemical as well as tactile. These putative escape behaviors displayed by Na. concinna may contribute to avoidance of predation by Ne. georgianus.     

Behavioral responses of Aedes aegypti,Aedes albopictus,Culex quinquefasciatus,and Anopheles minimus against various synthetic and natural repellent compounds

The behavioral responses of colony populations of Aedes aegypti, Aedes albopictus, Culex quinquefasciatus, and Anopheles minimus to four essential oils (citronella, hairy basil, catnip, and vetiver), two standard repellents (DEET and picaridin), and two synthetic pyrethroids (deltamethrin and permethrin) were conducted in the laboratory using an excito‐repellency test system. Results revealed that Cx. quinquefasciatus and An. minimus exhibited much stronger behavioral responses to all test compounds (65–98% escape for contact, 21.4–94.4% escape for non‐contact) compared to Ae. aegypti (3.7–72.2% escape (contact), 0–31.7% (non‐contact)) and Ae. albopictus (3.5–94.4% escape (contact), 11.2–63.7% (non‐contact)). In brief, essential oil from vetiver elicited the greatest irritant responses in Cx. quinquefasciatus (96.6%) and An. minimus (96.5%) compared to the other compounds tested. The synthetic pyrethroids caused a stronger contact irritant response (65–97.8% escape) than non‐contact repellents (0–50.8% escape for non‐contact) across all four mosquito species. Picaridin had the least effect on all mosquito species. Findings from the current study continue to support the screening of essential oils from various plant sources for protective properties against field mosquitoes.     

Effects of the toxic dinoflagellate Alexandrium catenella on histopathogical and escape responses of the Northern scallop Argopecten purpuratus

Juvenile Northern scallops Argopecten purpuratus were exposed to cultures of the paralytic shellfish toxin (PST) producing dinoflagellate, Alexandrium catenella, or a non-toxic microalga as a control, T-iso. After 3 and 6 days of exposure to either A. catenella or T-iso, scallops were stimulated to elicit an escape response by exposing them to the predatory sea star Meyenaster gelatinosus. We monitored the escape response of the scallops in terms of reaction time after first contact with the sea star, number of claps (burst of rapid valve closures) until exhaustion, clapping time, clapping rate, the time scallops spent closed when exhausted, and recovery from the initial number of claps, clapping time and clapping rate. Additionally, histopathological and stress responses (through heat-shock protein [hsp70] induction), as well as accumulation of Paralytic Shellfish Poisoning (PSP) toxins, were monitored on scallops after 3 and 6 days of exposure to A. catenella. After 6 days of exposure, scallops exposed to A. catenella accumulated PSTs and reacted more rapidly with a higher clapping rate, however the duration of their escape response was shorter than controls, when exposed to M. gelatinosus. Additionally, scallops exposed to A. catenella showed histopathological features, especially after 6 days of exposure, including increased melanization of the tissues and myopathy, with high levels of degeneration of the muscle fibers. A six-day exposure to A. catenella also caused an increase in prevalence of rickettsiales-like organisms within scallop tissues. This study suggests that PST accumulation can affect the interaction between the Northern scallop and both pathogens and predators, potentially increasing their susceptibility to either of them.     

Locomotor performance of sand lizards (Lacerta agilis): effects of predatory pressure and parasite load

Locomotor performance affects foraging efficiency, predator avoidance and consequently fitness. Agility and speed determine the animal's social status and reflect its condition. In this study, we test how predatory pressure and parasite load influences locomotor performance of wild specimens of the sand lizard Lacerta agilis. Animals were chased on a 2-metre racetrack. Lizards with autotomy ran significantly faster than lizards with an intact tail, but there was no significant difference in running speed between individuals with fresh caudal autotomy and regenerated tails. Parasite presence and load, age and sex had no significant effect on speed. Our results indicate that autotomy either alters locomotory behaviour or that individuals with autotomised tails were those that previously survived contact with predators, and therefore represented a subgroup of the fastest individuals. Therefore, in general, predatory pressure but not parasites affected locomotor performance in lizards.     

Escape tactics by a neotropical montane lizard: a comparison of flight responses against natural and nonnatural predators

Prey must judge the level of threat related to a given predator attack to employ the most efficient escape strategy at a low cost. In this context, the capacity of prey to correctly assess the threat from predators might optimise their decision on the strategy employed to flee. We examined the escape behaviour of the montane lizard Tropidurus montanus in response to different types of predatory stimuli. Lizards stimulated by a model of a natural predator ran shorter distances straight towards shelter and spent less time in flight. On the other hand, when exposed to a model of a nonnatural predator, T. montanus performed longer flights in distance and time, running across open and exposed substrates in the view of predators. These results showed that the lizard T. montanus made different escape decisions according to the type of predatory stimulus.