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.     

Native Australian frogs avoid the scent of invasive cane toads

Invasive species can affect the ecosystems they colonize by modifying the behaviour of native taxa; for example, avoidance of chemical cues from the invader may modify habitat use (shelter site selection) by native species. In laboratory trials, we show that metamorphs of most (but not all) native frog species on a tropical Australian floodplain avoid the scent of invasive cane toads (Bufo marinus Linnaeus 1758). Cane toads also avoid conspecific scent. This response might reduce vulnerability of metamorph frogs and toads to larger predatory toads. However, similar avoidance of one type of pungency control (garlic), and the presence of this avoidance behaviour in frogs at the toad invasion front (and hence, with no prior exposure to toads), suggest that this may not be an evolved toad‐specific response. Instead, our data support the simpler hypothesis that the metamorph anurans tend to avoid shelter sites that contain strong and unfamiliar scents. Temporal and spatial differences in activity of frogs versus toads, plus the abundance of suitable retreat sites during the wet season (the primary time of frog activity), suggest that avoiding toad scent will have only a minor impact on the behaviour of native frogs. However, this behavioural impact may be important when environmental conditions bring toads and frogs into closer contact.     

Avoidance and escape responses of the gastropod mollusc Olivella biplicata (Sowerby) to predatory asteroids

The sand-dwelling gastropod Olivella biplicata (Sowerby) gives two chemically-mediated defensive responses to predatory asteroids — an avoidance and an escape response. An avoidance response is triggered by water-borne chemicals diffusing from distant starfish. When snails on the surface of the sand sense a distant predatory starfish, they avoid the predator by burying themselves in the sand. Strong avoidance responses are given to the predatory asteroids Pisaster brevispinus (Stimpson), P. ochraceus (Brandt), and Pycnopodia helianthoides (Brandt). Little or no response is given to the omnivorous asteroid Patiria miniata (Brandt) or to the predatory gastropod Polinices lewisii (Gould). An escape response is given when a snail on the surface is contacted by the starfish Pisaster brevispinus. Upon contact, the snail immediately retracts the propodium, sometimes throwing the metapodium forward at the same time; the snail then turns sharply away from the point of contact, and buries itself. Both avoidance and escape responses can be observed in the field and laboratory.     

Factors affecting the behaviour of crown-of-thorns starfish (Acanthaster planci L.) on the Great Barrier Reef:: 1: Patterns of activity

The feeding, moving and cryptic behaviours of 5749 crown-of-thorns starfish, Acanthaster planci (L.), were studied on 15 reefs of the Great Barrier Reef between June 1986 and December 1987. Log-linear analyses of field data showed that these behaviours were influenced by complex interactions between a number of important physical and biological factors including the size of starfish, their depth and physical condition, time of day, and substratum type. For most of these factors, the patterns of behaviour were shown to be consistent across reefs. Irrespective of their size, starfish spent on average about 45% of their time feeding. However, there were strong diurnal effects with smaller starfish (<20 cm) strongly favouring nocturnal feeding. For larger starfish (>40 cm) this pattern was reversed, though the diurnal effects were not as strong. Diurnal variation was greater at shallower depths (<3 m). Larger starfish spent more time moving (∼20%), particularly during the day, compared to smaller starfish (∼5%), with the latter moving mainly at night. Motion increased with depth for all starfish. The density and degree of aggregation of starfish had no effect on behaviour. The cryptic behaviour of starfish decreased with size, from ∼60% for small starfish to less than 10% for large starfish. For starfish <30 cm in size, there were strong diurnal effects on cryptic behaviour, with smaller starfish being almost exclusively cryptic during the day. Cryptic behaviour was also influenced by the condition of starfish. Those in poor condition were 5 times more likely to be moving than those in good condition. Cryptic starfish were 10 times more likely to be in good condition than non-cryptic starfish. This may partly explain the relatively rapid breakdown in starfish aggregations which has been observed at the ends of outbreaks.     

Animal interactions and the emergence of territoriality

Inferring the role of interactions in territorial animals relies upon accurate recordings of the behaviour of neighbouring individuals. Such accurate recordings are rarely available from field studies. As a result, quantification of the interaction mechanisms has often relied upon theoretical approaches, which hitherto have been limited to comparisons of macroscopic population-level predictions from un-tested interaction models. Here we present a quantitative framework that possesses a microscopic testable hypothesis on the mechanism of conspecific avoidance mediated by olfactory signals in the form of scent marks. We find that the key parameters controlling territoriality are two: the average territory size, i.e. the inverse of the population density, and the time span during which animal scent marks remain active. Since permanent monitoring of a territorial border is not possible, scent marks need to function in the temporary absence of the resident. As chemical signals carried by the scent only last a finite amount of time, each animal needs to revisit territorial boundaries frequently and refresh its own scent marks in order to deter possible intruders. The size of the territory an animal can maintain is thus proportional to the time necessary for an animal to move between its own territorial boundaries. By using an agent-based model to take into account the possible spatio-temporal movement trajectories of individual animals, we show that the emerging territories are the result of a form of collective animal movement where, different to shoaling, flocking or herding, interactions are highly heterogeneous in space and time. The applicability of our hypothesis has been tested with a prototypical territorial animal, the red fox (Vulpes vulpes).     

Sex, age, and family differences in the chemical composition of owl monkey (Aotus nancymaae) subcaudal scent secretions

Numerous behavioral studies have shown that animals use olfactory cues as inbreeding avoidance or kin avoidance mechanisms, implying that scent is unique to families. However, few studies have analyzed the chemical profile of a scent and ascertained the messages that are conveyed in scent secretions. Owl monkeys (Aotus nancymaae) are socially monogamous primates that utilize scent when interacting with foreign conspecifics. This suggests there is a difference in the chemical composition of scent marks. We chemically analyzed sub-caudal gland samples from three families of captive owl monkeys (Aotus nancymaae). Samples were analyzed by capillary GC-MS and relative retention time and fragment pattern was compared with known standards. Gland samples were high in large plant-based shikikate metabolites and fatty ketones; alcohols, acids, and acetates were virtually absent. Gender, age, and family could be reliably classified using discriminant analysis (92.9, 100, and 100%, respectively). Female scent profiles were greater in concentration of aromatic plant metabolites, possibly the result of a different diet or physiological differences in female metabolism as compared to male. Offspring of adult age still living in their natal group showed a less complex chemical profile than their parents. Finally, each family had its own unique and complex chemical profile. The presence of family scent may play a role in mediating social interactions.     

Can protective attributes of artificial refuges offset predation risk in lizards?

Artificial refuges are often used to supplement habitat in areas where natural shelters have been degraded or removed. Although artificial refuges are intended to support particular species, they may be equally attractive and accessible to others, including predators. We explored the influence of snake predation risk and shelter attributes on the overnight use of different artificial refuges (timber, tiles, and iron) using the predator‐prey relationship between Boulenger's skink, Morethia boulengeri and the curl snake, Suta suta. We collected adult M. boulengeri from two bioregions in south‐eastern Australia: the Riverina, where the two species co‐occur, and the South Western Slopes, where S. suta does not occur. Two adult S. suta were collected for use as chemical donors. We conducted four experiments on overnight refuge choice to determine: (i) predator‐scent avoidance, (ii) artificial refuge preferences, (iii) a trade‐off between a preferred refuge and predator‐avoidance, and (iv) the effect of gap height on refuge preference. We found that skinks avoided predator‐scented refuges in favour of identical, but unscented refuges. Skinks preferred timber refuges, and most skinks maintained this preference when predator‐scent was added. However, when gap height was manipulated, skinks shifted to the refuge with the smallest gap. Skinks displayed complex regional variation in behaviour; skinks from both bioregions avoided predator‐scent, but in the trade‐off experiment, skinks from the South Western Slopes were less likely to avoid predator‐scented timber refuges than those from the Riverina. Our findings suggest that protective refuge attributes, such as small gap height, can offset the risk implied by predator‐scent within a refuge. This study highlights the need to consider predator‐prey interactions when designing and using artificial refuges for habitat restoration or biological monitoring.     

Central and peripheral action of testosterone propionate on scent gland morphology and marking behaviour in the Mongolian gerbil

Scent gland size and activity and frequency of marking under standard conditions were compared in five groups of male and female gerbils: (1) intact, sham-operated controls, (2) intact with scent glands excised, (3) gonadectomized, (4) gonadectomized injected with 1000 μg testosterone propionate (TP) on alternate days, and (5) gonadectomized with a low dose (25 μg) TP applied topically to the ventral scent gland on alternate days. The animals were housed in individual cages and tested for marking in an open field arena with plastic pegs.The scent gland is not required in either sex for the behavioural act of marking. Topical application of a dose of TP too low to exert a systematic effect restored the scent gland but not marking. Injection of sufficient TP to restore seminal vesicle weight restored marking, as well as the scent glands.It was concluded that in the male, both marking behaviour and scent gland size are controlled by the testes. The effect of androgens on marking is mediated directly through the central nervous system, and not through peripheral stimulation of the glands.Females have smaller glands and mark less than males. The ovaries appear to have little control over marking frequency, and some control over scent gland size. It is possible to stimulate marking behaviour to supernormal levels by TP injection, but not by topical application.     

Scent marking within and between groups of wild banded mongooses

Scent marking is commonly described as a territorial behaviour, and scent marks might deter potential intruders from entering occupied areas. Conspecific neighbours present both a reproductive and a territorial threat, thus, determining which, if any, of these threats shapes scent-marking behaviour is difficult. Banded mongooses Mungos mungo provide a rare clear separation between reproductive rivals (found within groups) and territorial rivals (neighbouring groups), because immigration into social groups is extremely rare, and mating occurs almost exclusively within groups. This situation offers an opportunity to assess the relative importance of territorial defence and intra-group competition for mates in shaping scent-marking behaviour. We combined detailed behavioural observations of scent marking, chemical analyses of scent composition and discrimination experiments in the field, and found little evidence for higher rates of scent marking in overlapping areas, a lack of group specificity of scents and a failure of individuals to discriminate between the scents of different groups. Although scent may fulfill some role in territorial demarcation and defence, these results suggest that scent marks and scent-marking patterns are also involved in communicating within social groups.     

Does human scent bias the survival of bird nests?

Human-scent contamination of bird nests and the human-made trails leading to them is suspected to influence nest survival by attracting or deterring predatory mammals. This paper (1) reviews studies in which human-scent contamination was suspected to have biased the survival of real and artificial nests by influencing the behaviour of predatory mammals, (2) summarizes the procedures used in attempts to mitigate human-scent contamination in nest-survival studies, and (3) describes procedures to enhance the design and interpretation of nest-survival experiments. The behaviour of various non-domesticated mammals is confirmed or suspected to be affected by human scent, so similar effects on nest predators are plausible. However, suggestions that human scent affects nest survival by influencing the behaviour of predatory mammals are poorly supported, due to a dearth of appropriately designed experiments. Some studies failed to include measures to reduce human-scent contamination, and the effectiveness of scent-mitigation methods used in other studies has seldom been verified. In addition, volatile compounds arising from soil and vegetation disturbed underfoot by field researchers may have confounded many nest-survival studies. Investigators have routinely inferred human-scent effects from post hoc predation patterns or have simply acknowledged possible human-scent effects among other potential influences of nest fate. Studies are needed of the effects of human scent using uniform methods of scent application and verified methods of scent mitigation, where the fates of different types of nests are examined under a range of field conditions. More fundamentally, studies of naïve and experienced mammals are needed to assess their responses to human scent and clarify its salience in wildlife disturbance.     

Understanding the toad code: Behavioural responses of cane toad (Chaunus marinus) larvae and metamorphs to chemical cues

Abstract Larvae of many anuran taxa display strong behavioural responses to chemical cues, including alarm signals from injured conspecific tadpoles. We exposed tadpoles and metamorphs from an Australian population of the invasive cane toad (Chaunus[Bufo] marinus) to a range of chemical stimuli and quantified their responses both in the laboratory and in the field. Filtered fluids containing scent cues from crushed conspecifics elicited strong avoidance from tadpoles, whereas other cues (e.g. scent of food, of native‐range fish or urodele predators, and thermal stimuli) did not. Apparent aggregation of tadpoles in response to scent cues proved to be an artifact of tank design, and was an indirect consequence of avoidance of those cues. Field trials confirmed that free‐ranging toad tadpoles and metamorphs avoided chemical cues from crushed conspecifics, suggesting that the chemicals inducing this response might provide an opportunity to develop targeted control methods for this invasive species.     

Responses of naïve and experienced European rabbits to predator odour

The response of prey species to predator scent has been investigated in many mammalian species; however, there is little information about the responses of European wild rabbits at the population level. Therefore, we conducted a simple experiment to investigate the behavioural response of a rabbit population to native predator cues in the wild. We compared the response to the scent of a predator (red fox) in a wild rabbit population bred in semi-natural conditions and naïve to terrestrial predators with the response of a population in a similar environment where terrestrial predators were present. The response to predators was based on rabbit abundance, inferred from pellet counts and measured by the defecation rate per day (DRD). Our results indicate that rabbits responded to the odour of fox faeces in the treatment warrens, resulting in a lower DRD. The main anti-predator behaviour observed was spatial avoidance (warren abandonment), which seemed to be more accentuated for rabbits who had not previously had contact with foxes in the plot where terrestrial predators were excluded. In both the fenced and the unfenced plot, the differences in the effect of the predator odour between the control and treatment warrens disappeared after cessation of treatment, suggesting a flexible and adaptive behaviour of rabbits to predator cues.

     

Differential endocrine responses to infant odors in common marmoset (Callithrix jacchus) fathers

Olfactory cues can exert priming effects on many mammalian species. Paternally experienced marmosets, Callithrix jacchus, exposed to direct isolated olfactory contact with their own infant's scent show rapid decreases in testosterone levels within 20 min, whereas paternally inexperienced males do not. The following study tests whether there is a differential steroid response to exposure of infant scent from dependent infants (own and novel) and independent infants (own and novel). We examined the serum levels of estradiol, estrone, testosterone, dihydrotestosterone (DHT), and combined estrogens and androgens in eight male marmosets 20 min after exposure to isolated infant scent. Testosterone and androgen levels combined were significantly lower with exposure to own infant scent than a novel infant scent when the infants were at a dependent age but not at an independent age. Estrogen levels elevated significantly in response to own infant scent when the infants were at a dependent age but not at an independent age. These results suggest that marmoset fathers are more responsive to priming cues from related infants and hormonal responses from fathers are greatest when the infant is at a dependent age.     

Biochemical investigation of two responses involved in the feeding behaviour of Acanthaster planci (L.). II. Isolation and characterization of chemical stimuli

Feeding behaviour is induced in the crown-of-thorns starfish, Acanthaster planet (L.), by two kinds of chemical stimulus originating in coral. One is macromolecular, and the other of low molecular weight, largely accounted for by small peptides and amino acids.It is found that, under experimental conditions, starfish rapidly habituate to a chemical stimulus which at first strongly induces feeding behaviour.The pronounced withdrawal response which occurs when a crude extract of coral is applied to the starfish (a response apparently identical with that evoked by contact with live coral) is caused by a component which corresponds closely in chromatographie behaviour with proline. Proline itself produces the response, but is present at too low a concentration in coral to account for the observed activity.     

MHC odours are not required or sufficient for recognition of individual scent owners

To provide information about specific depositors, scent marks need to encode a stable signal of individual ownership. The highly polymorphic major histocompatibility complex (MHC) influences scents and contributes to the recognition of close kin and avoidance of inbreeding when MHC haplotypes are shared. MHC diversity between individuals has also been proposed as a primary source of scents used in individual recognition. We tested this in the context of scent owner recognition among male mice, which scent mark their territories and countermark scents from other males. We examined responses towards urine scent according to the scent owner's genetic difference to the territory owner (MHC, genetic background, both and neither) or genetic match to a familiar neighbour. While urine of a different genetic background from the subject always stimulated greater scent marking than own, regardless of familiarity, MHC-associated odours were neither necessary nor sufficient for scent owner recognition and failed to stimulate countermarking. Urine of a different MHC type to the subject stimulated increased investigation only when this matched both the MHC and genetic background of a familiar neighbour. We propose an associative model of scent owner recognition in which volatile scent profiles, contributed by both fixed genetic and varying non-genetic factors, are learnt in association with a stable involatile ownership signal provided by other highly polymorphic urine components.     

Rib fabrication in Ostreoidea and Plicatuloidea (Bivalvia,Pteriomorphia) and its evolutionary significance

Ribs of Ostreoidea and Plicatuloidea are defined as antimarginal, that is, perpendicular to the margin throughout growth. Morphogenetically, these ribs are unique, since, unlike radial ribs, they are secreted by a homogeneous mantle margin. Based also on the reconstructed shell secretion cycle in Bivalvia, we propose that ribs of Ostreoidea and Plicatuloidea are formed by a mantle margin which, upon extension from the shell margin, stretches and folds by taking the preformed ribs as templates. In extending perpendicular to the margin (as in all Bivalvia growing isometrically), such a mantle extends the rib pattern antimarginally. Ribs of this kind are purely mechanical structures, as their arrangement depends on the mechanical properties of the mantle and on the environmental conditions. This explains the high irregularity of such ribbing patterns. The presence of antimarginal ribs in both the Ostreoidea and Plicatuloidea sheds light on their origin. The first known oyster, Actinostreon cristadifformis, probably derived from an antimarginally ribbed Prospondylidae gen. indet. in the Late Permian or Early Triassic. Antimarginally ribbed Triassic species formerly included in Placunopsis originated both the Dimyidae Atreta in the Late Triassic and Enantiostreon in the Mid Triassic, which was transitional to Plicatulidae. Therefore, Dimyidae and Plicatulidae are closely connected and grouped under Plicatuloidea, to which Ostreoidea is phylogenetically unrelated.     

Flexibility in starfish behavior by multi-layered mechanism of self-organization

Understanding animal behavior as a product of natural selection sometimes result in an underestimation of the animal's adaptability: lower animals with poor mental capabilities are usually considered to simply exhibit innate behavioral patterns. Self-organized behavior may exhibit both stability of certain behavioral patterns and flexibility in adopting those patterns. Thus, the self-organization processes of starfish arm and tube feet movements are investigated, by observing obstacle avoidance behavior and tube feet of moving starfish. As starfish have no central nervous systems, their behaviors are the result of certain self-organization processes. Starfish have hierarchically constructed motor organs consisting of arms and tube feet. The collective behavior of the tube feet does not function only as simple fluctuations in the arms' coordination. As a result, starfish seem to exhibit more versatile behavioral changes than expected from the original model of a self-organized behavior.     

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.     

Donning your enemy's cloak: ground squirrels exploit rattlesnake scent to reduce predation risk

Ground squirrels (Spermophilus spp.) have evolved a battery of defences against the rattlesnakes (Crotalus spp.) that have preyed on them for millions of years. The distinctive behavioural reactions by these squirrels to rattlesnakes have recently been shown to include self-application of rattlesnake scent-squirrels apply scent by vigorously licking their fur after chewing on shed rattlesnake skins. Here, we present evidence that this behaviour is a novel antipredator defence founded on exploitation of a foreign scent. We tested three functional hypotheses for snake scent application--antipredator, conspecific deterrence and ectoparasite defence--by examining reactions to rattlesnake scent by rattlesnakes, ground squirrels and ectoparasites (fleas). Rattlesnakes were more attracted to ground squirrel scent than to ground squirrel scent mixed with rattlesnake scent or rattlesnake scent alone. However, ground squirrel behaviour and flea host choice were not affected by rattlesnake scent. Thus, ground squirrels can reduce the risk of rattlesnake predation by applying rattlesnake scent to their bodies, potentially as a form of olfactory camouflage. Opportunistic exploitation of heterospecific scents may be widespread; many species self-apply foreign odours, but few such cases have been demonstrated to serve in antipredator defence.