Temporal shift in the presence of a chemical cue contributes to a diel shift in sociality

Spatial and temporal variation in animal aggregations may be due to variation in the presence of cues for aggregation (or disaggregation) or to variation in the receptivity of the animal to a particular cue or suite of cues. Spiny lobsters, Panulirus argus, forage solitarily but are often found aggregated in their diurnal shelters. An important proximate cause of aggregation among spiny lobsters is a scent they produce that influences shelter choice by conspecifics. We examined how variability in the presence of, or response to, such a chemical cue may contribute to diel shifts in sociality among spiny lobsters. We conducted a series of Y-maze shelter choice experiments using lobsters that were either maintained under altered dark:light schedules in the experimental arena or under natural lighting in the head tanks. Lobsters that were maintained on a light schedule 8 h later than normal chose shelters at their dawn (corresponding to the middle of the night for lobsters in the head tanks); however, their choices of shelter were not influenced by scents of conspecifics. Lobsters that were maintained on a schedule 8 h earlier than normal chose shelters in the middle of their night (corresponding to dawn for the lobsters in the head tanks). Their choices of shelter were significantly influenced by conspecific scents. These results suggest that the chemical cues for aggregation, released by spiny lobsters, are present discontinuously, that spiny lobsters are influenced by conspecific odours continuously, and that aggregation is controlled by temporal variation in the presence of a chemical cue. Copyright 2000 The Association for the Study of Animal Behaviour.     

Source and specificity of chemical cues mediating shelter preference of Caribbean spiny lobsters (Panulirus argus)

Caribbean spiny lobsters display a diversity of social behaviors, one of the most prevalent of which is gregarious diurnal sheltering. Previous research has demonstrated that shelter selection is chemically mediated, but the source of release and the identity of the aggregation signal are unknown. In this study, we investigated the source and specificity of the aggregation signal in Caribbean spiny lobsters, Panulirus argus. We developed a relatively rapid test of shelter choice in a 5000-l laboratory flume that simulated flow conditions in the spiny lobster's natural environment, and used it to examine the shelter preference of the animals in response to a variety of odorants. We found that both males and females associated preferentially with shelters emanating conspecific urine of either sex, but not with shelters emanating seawater, food odors, or the scent of a predatory octopus. These results demonstrate specificity in the cues mediating sheltering behavior and show that urine is at least one source of the aggregation signal.     

Death-associated odors induce stress in zebrafish

Living animals exploit information released from dead animals to conduct adaptive biological responses. For instance, a recently published study has shown that avoidance behavior is triggered by death-associated odors in zebrafish. Stress can clearly act as an adaptive response that allows an organism to deal with an imminent threat. However, it has not been demonstrated whether these chemical cues are stressful for fish. Here, we confirmed that dead zebrafish scents induce defensive behavior in live conspecifics. Additionally, we show for the first time in fish that these scents increase cortisol in conspecifics. To reach this conclusion, firstly, we exposed zebrafish to multi-sensorial cues (e.g., visual, tactile, chemical cues) from dead conspecifics that displayed defensive behaviors and increased cortisol. Also, when we limited zebrafish to chemical cues from dead conspecifics, similar responses arose. These responses coincide with the decaying destruction of epidermal cells, indicating that defensive and stress responses could take place as an effect of substances emanating from decaying flesh, as well as alarm substance released due to rupture of epidermal cells. Taken together, these results illustrate that living zebrafish utilize cues from dead conspecific to avoid or to cope with danger and ensure survival.     

Prevalence of Panulirus argus Virus 1 (PaV1) and habitation patterns of healthy and diseased Caribbean spiny lobsters in shelter-limited habitats

Caribbean spiny lobsters Panulirus argus are socially gregarious, preferring shelters harboring conspecifics over empty shelters. In laboratory trials, however, healthy lobsters strongly avoided shelters harboring lobsters infected with the highly pathogenic Panulirus argus Virus 1 (PaV1). Because PaV1 is transmitted by contact, this behavior may thwart its spread in wild lobsters. In a field experiment conducted from 1998 to 2002 in a shelter-poor reef lagoon (Puerto Morelos, Mexico), densities of juvenile P. argus increased significantly on sites enhanced with artificial shelters (casitas) but not on control sites. Because PaV1 emerged in this location during 2000, we reexamined these data to assess whether casitas could potentially increase transmission of PaV1. In 2001, PaV1 prevalence was 2.5% and the cohabitation level (percentage of healthy lobsters cohabiting with diseased lobsters) was similar between natural shelters (3.5%) and casitas (2.4 %). The relative lobster densities in casita sites and control sites did not change significantly before (1998-1999) or after (2001-2002) the disease emergence. In late 2006, data from casita sites showed a significant increase in prevalence (10.9%) and cohabitation level (29.4%), but no significant changes in lobster density. In May 2006, casitas were deployed on shelter-poor sites within Chinchorro Bank, 260 km south of Puerto Morelos. In late 2006, prevalence and cohabitation level were 7.4 and 21.7%, respectively. Our results are inconclusive as to whether or not casitas increase PaV1 transmission, but suggest that across shelter-poor habitats, lobsters make a trade-off between avoiding diseased conspecifics and avoiding predation risk.     

Anemonefishes rely on visual and chemical cues to correctly identify conspecifics

Organisms rely on sensory cues to interpret their environment and make important life-history decisions. Accurate recognition is of particular importance in diverse reef environments. Most evidence on the use of sensory cues focuses on those used in predator avoidance or habitat recognition, with little information on their role in conspecific recognition. Yet conspecific recognition is essential for life-history decisions including settlement, mate choice, and dominance interactions. Using a sensory manipulated tank and a two-chamber choice flume, anemonefish conspecific response was measured in the presence and absence of chemical and/or visual cues. Experiments were then repeated in the presence or absence of two heterospecific species to evaluate whether a heterospecific fish altered the conspecific response. Anemonefishes responded to both the visual and chemical cues of conspecifics, but relied on the combination of the two cues to recognize conspecifics inside the sensory manipulated tank. These results contrast previous studies focusing on predator detection where anemonefishes were found to compensate for the loss of one sensory cue (chemical) by utilizing a second cue (visual). This lack of sensory compensation may impact the ability of anemonefishes to acclimate to changing reef environments in the future.

     

Avoidance behavior in two sympatric planaria species: effects of conspecific and heterospecific chemical alarm cues

In many aquatic animals, predator avoidance can be stimulated by chemical cues, including those released by injured prey (alarm cues). Alarm cues of both conspecific and heterospecific origin have been identified within several fish taxa, where phylogenetic conservation of the cue-response complex is common. Turbellarian flatworms (planaria) are among the simplest animals known to respond to chemical cues released by injured conspecifics. We examined how two locally sympatric planaria species respond to conspecific and heterospecific chemical cues using macerated tissue suspensions. Brown (Girardia tigrina) and black (Dugesia dorotocephala) planaria both exhibited avoidance behavior when presented conspecific cues. Despite a significant twofold difference in body size (black > brown), stimulus prepared from a single (1×) individual of either species elicited avoidance. Increasing brown planaria cue concentration by macerating two individuals (2×) produced a significant increase in conspecific avoidance. Heterospecific stimuli produced asymmetric results. Black planaria avoided the brown planaria stimulus, but only in the higher concentration (2×) trials. Brown planaria did not consistently exhibit avoidance of the black planaria stimulus and some brown subjects approached and consumed black planarian tissues. Our results expand the demonstrated occurrence of alarm cues among planaria and suggest that avoidance behavior can be mediated by multiple environmental and intrinsic factors in freshwater Turbellaria.     

The olfactory pathway mediates sheltering behavior of Caribbean spiny lobsters, <Emphasis Type="Italic">Panulirus </Emphasis><Emphasis Type="Italic">argus</Emphasis>, to conspecific urine signals

The “noses” of diverse taxa are organized into different subsystems whose functions are often not well understood. The “nose” of decapod crustaceans is organized into two parallel pathways that originate in different populations of antennular sensilla and project to specific neuropils in the brain—the aesthetasc/olfactory lobe pathway and the non-aesthetasc/lateral antennular neuropil pathway. In this study, we investigated the role of these pathways in mediating shelter selection of Caribbean spiny lobsters, Panulirus argus, in response to conspecific urine signals. We compared the behavior of ablated animals and intact controls. Our results show that control and non-aesthetasc ablated lobsters have a significant overall preference for shelters emanating urine over control shelters. Thus the non-aesthetasc pathway does not play a critical role in shelter selection. In contrast, spiny lobsters with aesthetascs ablated did not show a preference for either shelter, suggesting that the aesthetasc/olfactory pathway is important for processing social odors. Our results show a difference in the function of these dual chemosensory pathways in responding to social cues, with the aesthetasc/olfactory lobe pathway playing a major role. We discuss our results in the context of why the noses of many animals contain multiple parallel chemosensory systems.     

Coexistence of congeneric spiny lobsters on coral reefs: differences in conspecific aggregation patterns and their potential antipredator benefits

Den sharing by conspecific spiny lobsters (aggregation) is modulated by chemical attraction but may confer several, not necessarily mutually exclusive, antipredator byproduct benefits: a “guide effect”, which only benefits the individual attracted to a sheltered conspecific; a “dilution effect”, which reduces per-capita risk of predation simply through aggregation; or active “group defense”. Each potential benefit has a different set of predictors (relationships between aggregation and conspecific or predator densities), but conflicting results could suggest the simultaneous operation of more than one benefit. These predictions were tested for coexisting Panulirus guttatus (a reef-obligate) and Panulirus argus (a temporary reef-dweller) using data collected during 11 surveys on fixed sites over a coral reef in Mexico. P. guttatus greatly outnumbered P. argus, but P. argus showed a greater tendency to aggregate. All three benefits of den sharing operated for the more social P. argus, with “group defense” being of the most benefit for larger individuals, and the “guide” and “dilution” effects for smaller individuals recently immigrating into the reef habitat and sharing dens with larger conspecifics. P. guttatus did not display “group defense” and its aggregations appeared to be modulated by the interplay between attraction and aggressive behaviors. This species relied more on solitary crypticity, especially at larger sizes, but appeared to benefit from a “guide effect” at high conspecific densities. In experimental tanks, each species tended to aggregate when tested separately, but when tested jointly, aggregation among P. guttatus was significantly reduced. The experimental results reflect the differential patterns of aggregation between the fore-reef, where P. guttatus dominated, and the back-reef, where coexistence of both species was greater.     

Smell, learn and live: The role of chemical alarm cues in predator learning during early life history in a marine fish

The speed with which individuals can learn to identify and react appropriately to predation threats when transitioning to new life history stages and habitats will influence their survival. This study investigated the role of chemical alarm cues in both anti-predator responses and predator identification during a transitional period in a newly settled coral reef damselfish, Pomacentrus amboinensis. Individuals were tested for changes in seven behavioural traits in response to conspecific and heterospecific skin extracts. Additionally, we tested whether fish could learn to associate a previously novel chemical cue (i.e. simulated predator scent) with danger, after previously being exposed to a paired cue combining the conspecific skin extract with the novel scent. Fish exposed to conspecific skin extracts were found to significantly decreased their feeding rate whilst those exposed to heterospecific and control cues showed no change. Individuals were also able to associate a previously novel scent with danger after only a single previous exposure to the paired conspecific skin extract/novel scent cue. Our results indicate that chemical alarm cues play a large role in both threat detection and learned predator recognition during the early post-settlement period in coral reef fishes.     

Innate responses to conspecific and heterospecific alarm cues in the endangered eastern cape redfin Pseudobarbus afer

We examined innate responses to conspecific and heterospecific alarm cues in a small cyprinid minnow, the Eastern Cape redfin Pseudobarbus afer. We found that redfins respond to conspecific skin extract, which contains alarm chemicals, and showed that their preferred response is to hide in refugia. Redfins also respond to skin extract from an allopatric, distantly related minnow species, the chubbyhead barb Enteromius anoplus indicating that neither sympatry nor close phylogenetic relationships are necessary for recognition of heterospecific alarm cues. Although both conspecific and heterospecific alarm cues induced similar responses, the response to heterospecific cues was less intense. This may be explained by a trade-off between selection to maximise threat recognition and selection to avoid the costs of responding to irrelevant cues, or by differences in chemical structures of alarm cues between species. These findings have implications for the conservation of this Endangered fish species and for freshwater fishes throughout Africa.     

Interspecific social interactions and behavioral responses of <Emphasis Type="Italic">Apodemus agrarius</Emphasis> and <Emphasis Type="Italic">Apodemus flavicollis</Emphasis> to conspecific and heterospecific odors

The social interactions between Apodemus agrarius and A. flavicollis, and their behavioral responses to conspecific and heterospecific odors, were studied in male–male and female–female interspecific dyadic encounters, and an attraction–avoidance test was used in order to clarify the behavioral mechanisms which control their relationships in wild populations. The experiments were carried out at the beginning and at the end of the breeding season—in spring and in autumn. In spring the aggressiveness was higher than in autumn. Males of both species showed attraction to conspecific odors from the opposite sex, while the females were indifferent. In autumn both males and females displayed attraction to conspecific odors from the same sex. However, mice of both species showed avoidance to heterospecific odors from the same and the opposite sex in spring, and indifference to heterospecific odors from the same and the opposite sex in autumn. Based on these findings, it could be assumed that the patterns of social interactions and responses to conspecific and heterospecific odors undergo seasonal changes in their life cycle. Probably the avoidance response to heterospecific odors could serve as a spacing mechanism to avoid aggressive encounters between A. agrarius and A. flavicollis in syntopic habitats during the breeding period.     

Avoidance of Chemical Alarm Cues Released from Autotomized Tails of Ravine Salamanders (Plethodon richmondi)

The ability of animals to detect and avoid areas containing chemical alarm cues from conspecifics is well documented in aquatic species. The ability to detect chemical alarm cues in terrestrial organisms has not been tested until recently. In this study, we tested the ability of the ravine salamander ( Plethodon richmondi ) to detect and avoid areas containing chemicals released from the autotomized tails of conspecifics and sympatric zigzag salamanders ( P. dorsalis ). We also ascertained whether any avoidance response could be attributed to the size or sex of the animal. Our results suggest that ravine salamanders avoid substrates containing odors released from the autotomized tails of conspecifics, but not of heterospecific salamanders and that this response occurs independent of the size and/or sex of the animal. By avoiding areas where a conspecific has recently been injured, an organism could reduce its chances of encountering a predator and thus increase its chances of survival.     

Migratory‐stage sea lamprey Petromyzon marinus stop responding to conspecific damage‐released alarm cues after 4 h of continuous exposure in laboratory conditions

This study investigated the length of avoidance response of migratory‐stage sea lamprey Petromyzon marinus exposed continuously to conspecific damage‐released alarm cues for varying lengths of time in laboratory stream channels. Ten replicate groups of P. marinus, separated by sex, were exposed to either deionized water control or to P. marinus extract for 0, 2 or 4 h continuously. Petromyzon marinus maintained their avoidance response to the conspecific damage‐released alarm cue after continuous exposure to the alarm cue for 0 and 2 h but not 4 h. Beyond being one of the first studies in regards to sensory–olfactory adaptation–acclimation of fishes to alarm cues of any kind, these results have important implications for use of conspecific alarm cues in P. marinus control. For example, continuous application of conspecific alarm cue during the day, when P. marinus are inactive and hiding, may result in sensory adaptation to the odour by nightfall when they migrate upstream.     

Transmission of Panulirus argus virus 1 (PaV1) and its effect on the survival of juvenile Caribbean spiny lobster

The Caribbean spiny lobster Panulirus argus, an important fisheries species, is host to Panulirus argus virus 1 (PaV1), a lethal, unclassified virus--the first found in any species of lobster--prevalent in juvenile lobsters. We describe a series of laboratory experiments aimed at assessing the likely modes of disease transmission, determining the survival of lobsters relative to each transmission pathway and identifying potential alternate hosts. Given evidence for lower prevalence of PaV1 in large lobsters, the effect of lobster size on susceptibility was also examined. Results demonstrated that PaV1 can be transmitted to juvenile lobsters via inoculation, ingestion of diseased tissue, contact with diseased lobsters and--among the smallest juveniles--through water over distances of a few meters. Contact and waterborne transmission, the most likely modes of transmission in the wild, were less efficient than inoculation or ingestion. Nevertheless, about half of the smallest lobsters in contact and waterborne trials contracted the disease and died within 3 mo. Other decapods that co-occur with P. argus (e.g. spotted lobster P. guttatus, stone crab Menippe mercenaria, channel crab Mithrax spinosissimus) did not acquire the disease after inoculation with PaV1-infected hemolymph. Our results confirmed that PaV1 is highly infectious and lethal to juvenile P. argus, particularly early benthic juveniles in the wild, and, hence, is a threat to mariculture.     

The behavioural response of adult Petromyzon marinus to damage‐released alarm and predator cues

Using semi‐natural enclosures, this study investigated (1) whether adult sea lamprey Petromyzon marinus show avoidance of damage‐released conspecific cues, damage‐released heterospecific cues and predator cues and (2) whether this is a general response to injured heterospecific fishes or a specific response to injured P. marinus. Ten replicate groups of 10 adult P. marinus, separated by sex, were exposed to one of the following nine stimuli: deionized water (control), extracts prepared from adult P. marinus, decayed adult P. marinus (conspecific stimuli), sympatric white sucker Catostomus commersonii, Amazon sailfin catfish Pterygoplichthys pardalis (heterospecific stimuli), 2‐phenylethylamine (PEA HCl) solution, northern water snake Nerodia sipedon washing, human saliva (predator cues) and an adult P. marinus extract and human saliva combination (a damage‐released conspecific cue and a predator cue). Adult P. marinus showed a significant avoidance response to the adult P. marinus extract as well as to C. commersonii, human saliva, PEA and the adult P. marinus extract and human saliva combination. For mobile P. marinus, the N. sipedon washing induced behaviour consistent with predator inspection. Exposure to the P. pardalis extract did not induce a significant avoidance response during the stimulus release period. Mobile adult female P. marinus showed a stronger avoidance behaviour than mobile adult male P. marinus in response to the adult P. marinus extract and the adult P. marinus extract and human saliva combination. The findings support the continued investigation of natural damage‐released alarm cue and predator‐based repellents for the behavioural manipulation of P. marinus populations in the Laurentian Great Lakes.     

Information use by an Invading Species: Do Invaders Respond More to Alarm Odors than Native Species?

Two species of crayfish were tested in the laboratory to evaluate the hypothesis that successful invaders use a broader range of chemical information than do displaced native species. The invasive species Orconectes rusticus reduced responses to food odors just as strongly when heterospecific (O. propinquus, O. virilis) alarm odors were introduced with food odors as they did when conspecific alarm odors were introduced at the same time as food odors. Individuals of the displaced native species, O. propinquus, did not reduce feeding responses as strongly when O. virilis alarm odor was introduced as with conspecific alarm odor or O. rusticus alarm odor. These results are consistent with the hypothesis that successful invaders use a wider range of information about their environment than do displaced native species.     

Opercular beat rate for rainbow darters Etheostoma caeruleum exposed to chemical stimuli from conspecific and heterospecific fishes

Opercular beat rates of rainbow darters Etheostoma caeruleum were used as a measure of a physiological response to chemical stimulation. Rainbow darters responded significantly to some chemical cues (active and ambush predators, competitors, novel stimuli and to conspecific and heterospecific alarm cues) with increases in opercular movements; neutral cues and novel alarm cues did not elicit significant changes. Changes in opercular movements may be a good bioassay for determining detection of chemical stimuli by rainbow darters.     

Chemical Communication in the Gregarious Psocid Cerastipsocus sivorii (Psocoptera: Psocidae)

The objectives of this study were: (1) to test the existence of an aggregation pheromone in the gregarious psocid Cerastipsocus sivorii; (2) to compare the attractiveness of odors from different aggregations; (3) to test whether nymphs are able to chemically recognize damage-released alarm signals. In a choice experiment conducted in the laboratory, we showed that psocids are able to detect chemical cues from groups of conspecifics. Laboratory experiments also showed that nymphs are capable of chemically recognizing the aggregations where they came from. Finally, in a field experiment, most aggregations dispersed when exposed to the body fluids of a crushed conspecific, but no aggregations dispersed upon exposure to a crushed termite. The implications of these results for the evolution of sociality in psocopterans are discussed.     

Habitat degradation disrupts neophobia in juvenile coral reef fish

Habitat degradation not only disrupts habitat‐forming species, but alters the sensory landscape within which most species must balance behavioural activities against predation risk. Rapidly developing a cautious behavioural phenotype, a condition known as neophobia, is advantageous when entering a novel risky habitat. Many aquatic organisms rely on damage‐released conspecific cues (i.e. alarm cues) as an indicator of impending danger and use them to assess general risk and develop neophobia. This study tested whether settlement‐stage damselfish associated with degraded coral reef habitats were able to use alarm cues as an indicator of risk and, in turn, develop a neophobic response at the end of their larval phase. Our results indicate that fish in live coral habitats that were exposed to alarm cues developed neophobia, and, in situ, were found to be more cautious, more closely associated with their coral shelters and survived four‐times better than non‐neophobic control fish. In contrast, fish that settled onto degraded coral habitats did not exhibit neophobia and consequently suffered much greater mortality on the reef, regardless of their history of exposure to alarm cues. Our results show that habitat degradation alters the efficacy of alarm cues with phenotypic and survival consequences for newly settled recruits.     

A death in the family: Sea lamprey (Petromyzon marinus) avoidance of confamilial alarm cues diminishes with phylogenetic distance

Alarm signals released after predator attack function as reliable public information revealing areas of high risk. The utility of this information can extend beyond species boundaries, benefiting heterospecifics capable of recognizing and responding appropriately to the signal. Nonmutually exclusive hypotheses explaining the acquisition of heterospecific reactivity to cues suggest it could be conserved phylogenetically following its evolution in a common ancestor (a species‐level effect) and/or learned during periods of shared risk (a population‐level effect; e.g., shared predators). Using a laboratory‐based space‐use behavioral assay, we tested the response of sea lamprey (Petromyzon marinus) to the damage‐released alarm cues of five confamilial (sympatric and allopatric) species and two distantly related out‐groups: a sympatric teleost (white sucker Catostomus commersonii) and an allopatric agnathan (Atlantic hagfish Myxine glutinosa). We found that sea lamprey differed in their response to conspecific and heterospecific odors; exhibiting progressively weaker avoidance of cues derived from more phylogenetically distant confamilials regardless of current overlap in distribution. Odors from out‐groups elicited no response. These findings suggest that a damage‐released alarm cue is at least partially conserved within the Petromyzontidae and that sea lamprey perceives predator attacks directed to closely related taxa. These findings are consistent with similar observations from gastropod, amphibian and bony fish taxa, and we discuss this in an eco‐evo context to provide a plausible explanation for the acquisition and maintenance of the response in sea lamprey.