Alarm behaviour in Eciton army ants

The effective communication of alarm can be critical for social animals so that they are able to deal with threats posed by predators and competitors. In the case of many of the most ecologically dominant, large‐colony ant species, these alarm responses are aggressive and coordinated by alarm pheromones, produced generally from the mandibular glands. In the present study, the alarm behaviour of two Neotropical army ant species is examined, the swarm raiding Eciton burchellii (Westwood) and the column raiding Eciton hamatum (Fabricius). Both species exhibit aggressive alarm responses in response to crushed heads, suggesting that the alarm pheromone is indeed produced by the mandibular glands in these ants. The most abundant component of the mandibular gland secretion, 4‐methyl‐3‐heptanone (10 µL on a rubber septum), stimulates a substantial alarm response, although this is less than the response to a single crushed head. This suggests that 4‐methyl‐3‐heptanone may be an alarm‐stimulating compound in Eciton. The alarm response of E. burchellii involves more workers than that of E. hamatum, although major workers play a much greater role in the response of the latter species. The differences in the alarm response of the two closely‐related species may relate to their foraging strategies, with E. burchellii relying more on quantity rather than the caste of ants responding and possibly using alarm pheromones for offensive as well as defensive functions.     

The Response of the Tidepool Sculpin,Oligocottus maculosus,to Chemical Stimuli from Injured Conspecifics,Alarm Signalling in the Cottidae (Pisces)

The tidepool sculpin, Oligocottus maculosus, a small, cottiid fish of the Pacific coast of North America, shows reduced movement, less feeding activity, a greater tendency to attach itself to the substrate, and a shift from exposed areas to shelters and crevices when presented with water that has contained injured conspecifics. This alarm reaction does not occur in response to water that has contained uninjured, but disturbed, O. maculosus, or injured guppies, Poecilia reticulata, O. maculosus are not toxic or distasteful to piscine predators. They do possess large, epidermal sacciform cells that may contain the active chemical(s) released by injured individuals. This is the first report of chemical alarm signalling in Cottidae.     

Predator-induced diapause in Daphnia magna may require two chemical cues

The production of diapausing eggs by Daphnia magna stimulated by fish exudates can be explained as an anti-predator defence ensuring genome protection in periods of high risk from fish predation. The combined effects on the induction of D. magna diapause of an “alarm” chemical originating from injured conspecific prey and fish kairomones were tested. The results of the experiment showed that the cues when present together promote both the production of ephippial eggs and male formation, indicating their role in the synchronization of the entire mode of Daphnia sexual reproduction. Ephippial eggs were only produced in the presence of both fish kairomone and conspecific alarm chemicals, while male offspring occurred in the treatments where both, one or none of the cues were present. However, production of males was the highest when both cues were provided. D. magna responded similarly to the tested cues whether or not the hypothetical alarm substance associated with predator odour came from Daphnia specimens actually eaten by fish or from crushed conspecific individuals. However, chemicals from crushed chironomid larvae combined with fish kairomones did not induce a similar response in D. magna. The relative advantage of utilization of alarm cues or predator kairomones in the induction of defence responses in prey organisms is discussed. Received: 8 June 1998 / Accepted: 11 January 1999     

Influence of Body Size on the Responses of Fathead Minnows, Pimephales promelas, to Damselfly Alarm Cues

A wide diversity of aquatic organisms release chemical alarm cues upon encountering or being attacked by a predator. These alarm cues can be used by nearby individuals to assess local predation risk. Receivers warned by chemical alarm cues gain a survival benefit when encountering predators. Animals that are in the same prey guild (i.e. that co‐occur and share the same predators) may learn to recognize each others’ chemical alarm cues. This ability may confer an adaptive advantage if the prey animals are vulnerable to the same predators. However, if the prey grow to different sizes and as a consequence are no longer vulnerable to the same suite of predators, then there should no longer be an advantage for the prey to respond to each others’ alarm cues. In this study, we exposed small and large fathead minnows (Pimephales promelas) to cues from syntopic injured damselfly larvae (Enallagma boreale), cues from injured mealworm larvae (Tenebrio molitor) and to distilled water. Small minnows exhibited antipredatory behaviour and increased shelter use in response to injured damselfly cues but not to the controls of injured mealworm or distilled water. On the contrary, large minnows exhibited no significant change in shelter use in response to any of the injured cues. These data demonstrate that fathead minnows exhibit an antipredator response to damselfly alarm cues, but only when minnows are small and members of the same prey guild as damselfly larvae. These results demonstrate the considerable flexibility in the responses to heterospecific alarm cues.     

Responses to injured conspecifics and heterospecifics by water fleas,Chydorus sphaericus

Cladocerans have been shown to exhibit a variety of responses to chemical stimuli associated with predation risk, including those from predators and injured conspecifics. In this study, we tested the hypothesis that individuals of Chydorus sphaericus would respond with avoidance behavior to chemical cues from both injured conspecifics and injured heterospecifics. Avoidance behavior was seen in response to cues from C. sphaericus and Daphnia magna. Responses to cues from Daphnia pulex were intermediate between those of the other cues and the water control. We propose that a concentration effect may be responsible for the mixed responses to heterospecific cues and speculate that responses to a broad range of cues may help explain the expansive range of C. sphaericus.     

Assessment of Predation Risk by Juvenile Yellow Perch, Perca flavescens: Responses to Alarm Cues from Conspecifics and Prey Guild Members

In two laboratory experiments we tested juvenile yellow perch, Perca flavescens, for behavioural responses to alarm cues of injured conspecifics and several prey guild members: adult perch, Iowa darters, Etheostoma exile and spottail shiners, Notropis hudsonius. Spottail shiners are phylogenetically distant to yellow perch whereas Iowa darters and perch are both members of the Family Percidae. Groups of juvenile yellow perch increased shoal cohesion and movement towards the substrate after detecting conspecific alarm cues when compared to cues of injured swordtails, Xiphophorus helleri, a species phylogenetically distant from perch. Individual juvenile perch increased shelter use and froze more when exposed to chemical alarm cues from both juvenile and adult perch, shiners and darters compared to exposure to injured swordtail cues or distilled water. The response to cues of darters may indicate that alarm cues are evolutionarily conserved within percid fishes or that perch had learned to recognize darter cues. The response to spot tail shiners likely represents learned recognition of the cues of a prey guild member.     

A note on alarm cues in juvenile African catfish, Clarias gariepinus Burchell: Indications for opposing behavioural strategies

Following exposure of African catfish to alarm cues, a relationship (r_p = 0.60, N = 10, P = 0.07) between feed efficiency (measured as residual feed intake) and the change in percentage of time spent swimming in response to damage-released alarm cues was observed. Feed-efficient animals responded with a decrease in percentage of time spent swimming (P < 0.05) whereas feed-inefficient animals responded with an increase in percentage of time spent swimming (P < 0.05). This study shows opposing behavioural strategies in African catfish in response to damage-released alarm cues being related to feeding efficiency.     

A cross-phyla response to Daphnia chemical alarm substances by an aquatic oligochaete

Although chemical alarm substances from damaged heterospecifics have been well documented to induce defense mechanisms in potential prey, data about antipredator responses to alarm cues from prey organisms of a distinct phylum are scarce. In this study, we analyze the response of an oligochaete to chemical alarm substances from distantly related cladocerans. We conducted laboratory experiments to investigate whether the aquatic oligochaete Stylaria lacustris detects and responds to alarm substances from Daphnia. The oligochaetes were exposed to alarm substances from Daphnia magna, which is a member of the same prey guild, and D. hyalina, which is vulnerable to different predators. S. lacustris increased the fission rate in response to cues from conspecifics and the heterospecific D. magna. These species share common predators, especially damselfly larvae and hydras. In contrast, chemical cues released from D. hyalina did not induce an increase in the reproductive rate of the oligochaetes. D. hyalina is a pelagic species and is not included in the diet of predators preying upon S. lacustris. Our results indicate cross-phyla responses among invertebrates (Annelida and Arthropoda), and suggest strong selection pressures to respond to heterospecific alarm substances. The oligochaete S. lacustris is able to differentiate chemical substances released from damaged Daphnia of two different species. These results show that alarm cues released from damaged Daphnia may be species-specific. However, further studies on the chemical structure of alarm substances in cladocerans are needed to support this hypothesis.     

Alarm in a wasp-wasp nesting association: Do members signal cross-specifically?

Summary We studied interspecific alarm communication between two species of social wasps in a nesting association in northwestern Costa Rica by testing the alarm responses ofPolybia occidentalis andMischocyttarus immarginatus to venom of both species. This is the first investigation of alarm pheromone in the genusMischocyttarus. M. immarginatus did not respond with alarm behavior to the venom of either species.P. occidentalis, which responds to its own venom with alarm behavior (Jeanne, 1981), also responded with alarm behavior to the venom ofM. immarginatus, but with much less intensity. Since heterospecific venoms did not release species-typical levels of alarm behavior, we conclude that interspecific alarm signalling plays no role in the nesting association.     

Die Schreckstoffzellen von Phoxinus phoxinus und Morulius chrysophakedion (Cyprinidae,Ostariophysi, Pisces)

Zusammenfassung Die Untersuchung der Histochemie und der Ultrastruktur der Schreckstoffzellen von Phoxinus phoxinus und Morulius chrysophakedion (Cyprininae, Cyprinidae, Cypriniformes, Ostariophysi) führte zu übereinstimmenden Ergebnissen. Unmittelbar perinucleär sind Ribosomen, Mitochondrien und ein Golgikomplex nachweisbar, von dem ein Netzwerk tubulärer Systeme ausgeht. Histochemisch sind in unmittelbarer Kernnähe gelegentlich Glykogengranula, stets ein deutlicher RNS-Gehalt und die Aktivitäten der Succinatdehydrogenase, der Lactatdehydrogenase, in einigen Zellen der Glucose-6-phosphat-dehydrogenase darstellbar. Im gesamten Cytoplasma der Schreckstoffzelle ist die Aktivität der Leucinaminopeptidase vorhanden, deren Maximum ebenfalls in Kernnähe vorliegt. Nur im kernfernen Cytoplasma wurden Proteine und diastaseresistente Polysaccharide nachgewiesen. Aus den Ergebnissen geht hervor, daß die Schreckstoffzellen sekretorisch tätig sind; vermutlich handelt es sich bei dem spezifischen Sekret um ein kleinmolekulares Protein.

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The alarm substance cells of Phoxinus phoxinus and Morulius chrysophakedion (Cyprinidae, Ostariophysi, Pisces)Histochemical and electron microscopical study

Summary The histochemical studies of the alarm substance cells from Phoxinus phoxinus and Morulius chrysophakedion (Cyprininae, Cyprinidae, Cypriniformes, Ostariophysi) are in total agreement with the results of the ultrastructural investigations. Perinuclear ribosomes, mitochondria, and a golgi complex are demonstrated. A tubular network radiates from the golgi complex. Histochemically, glycogen granula can occasionally be demonstrated in proximity to the nucleus. Consistently a strong RNA reaction as well as succinic-dehydrogenase activity, lactic-dehydrogenase activity, and in some cells glucose-6-phosphatedehydrogenase activity can be shown. In the cytoplasm of the alarm substance cell leucyl-aminopeptidase activity exists; its maximum lies in vicinity of the nucleus. Proteins and diastase-resistant polysaccharides are found only in cytoplasm not directly adjacent to the nucleus. The results indicate that the alarm substance cells show a secretory activity. It is assumed that the specific secrete is a protein of low molecular weight.

Mit Unterstützung durch die Deutsche Forschungsgemeinschaft.     

The response of grass-cutting ants to natural and synthetic versions of their alarm pheromone

The responses of the grass‐cutting ants Atta bisphaerica (Forel) and Atta capiguara (Gonçalves) to the main components of their alarm pheromones were examined in simple field bioassays. Both species react most strongly to 4‐methyl‐3‐heptanone, which causes the full range of alarm behaviour and a large increase in the number of individuals near the sources. In later experiments with A. capiguara, this increase was found to be due primarily to attraction, with some arrestment also occurring. The ant response to 4‐methyl‐3‐heptanone was compared with that to crushed heads and to that with whole ants with crushed heads. The pheromone 4‐methyl‐3‐heptanone by itself stimulates the same level of attraction as crushed heads, but results in far less alarm behaviour and arrests fewer ants. Whole ants with crushed heads attract a greater number of ants than the other sources and also cause more alarm behaviour. Bodies alone attract ants, but do not result in alarm behaviour. The main component in both species is the same, supporting the view that alarm pheromones lack species specificity. However, it appears that other components may also be important either as synergists of the main compound, or by stimulating behaviours that would not be observed in its absence.     

Field observations of the alarm response to crushed conspecifics in the freshwater snail Pomacea canaliculata: effects of habitat,vegetation, and body size

The freshwater snail Pomacea canaliculata shows alarm responses to chemical cues released from injured conspecifics, but its behavioural responses in the field are unknown. We investigated effects of habitat (canals or paddy fields), vegetation, and body size on alarm responses in the field. Snails responded to crushed conspecifics within 4 min by burying themselves, but the proportions of self-buried snails were generally lower (0–28% depending on experiments) than those reported in the laboratory. Snails not only showed the alarm response, but also frequently fed on crushed conspecifics. There were no influences of habitat or body size on the proportions of individuals showing the alarm response. Nevertheless, in paddy fields with high-density vegetation a higher proportion of snails showed the alarm response than in paddy fields with low-density vegetation.     

Damage released prey alarm substances or predator odours? Risk assessment by an aquatic oligochaete

Although the abilities of prey to detect and respond to chemical substances associated with a predator have been widely reported, the factors promoting the evolution of responses to prey alarm cues vs. predator odours are still vague. In this article, we combined field research with laboratory experiments to explore which chemical substance associated with predator activity (predator odour, conspecific or heterospecific alarm substances) induces defence responses in the aquatic oligochaete Stylaria lacustris, which is vulnerable to common littoral predators. The field results indicated that predators injure the oligochaetes and a great proportion, up to 45% of individuals in the population, were found to be damaged. The results of the laboratory experiments revealed that chemical odours from damselfly larvae feeding on S. lacustris did not induce the defence response in the oligochaetes. On the contrary, oligochaetes detected and responded to alarm substances from damaged conspecifics alone and substances from damaged cladoceran Daphnia magna. We discussed conditions favouring the responses to damage released prey alarm cues instead of predator odours in Stylaria lacustris. Our data suggest that the selection of responses to alarm cues from damaged prey vs. predator odours may be dependent on three factors: (1) non-species-specific predation, (2) divergence of food niche of the different stages of the predator and (3) complex food web with multiple predators. Handling editor: S. Declerk     

Field verification of the use of chemical alarm cues in a coral reef fish

Chemical alarm cues function as early indicators of a predation threat and influence the outcome of predator–prey interactions in the favour of the prey animal. The tropical goby, Asterropteryx semipunctatus, responded with a stereotypical alarm response, including reduced movement and feeding, following exposure to water that contained chemical cues from injured conspecifics under natural field conditions. Gobies did not exhibit an alarm response when challenged with extracts from damaged fish from a different taxonomic family. The behavioural response in the field was similar to that observed in laboratory experiments. This study verifies the use of chemical alarm cues in a marine fish in their natural environment.     

Antipredator Behaviour and Suppressed Aggression by Convict Cichlids in response to Injury-released Chemical Cues of Conspecifics but not to those of an Allopatric Heterospecific

In aquatic environments, chemical cues serve as an important source of information for the detection of predation risk. Here, we investigate the response of convict cichlids, Cichlasoma nigrofasciatum, to injury-released chemical cues. We exposed pairs of juvenile convict cichlids first to dechlorinated tap water (control), then later to one of two test stimuli: 1. chemical cues from injured convict cichlids; or 2. chemical cues from injured mosquito fish, Gambusia affinis. Gambusia are allopatric and phylogenetically unrelated to convict cichlids. Gambusia skin was used to control for a general response to injured fish. In response to conspecific cues, convict cichlids significantly increased time spent near the bottom of test aquaria and time under a shelter object. In response to Gambusia skin, convict cichlids tended to increase time spent near the tank bottom but did not increase use of the shelter object. There was a trade-off between antipredator and agonistic behaviours. In response to convict cichlid cues, there was a significant reduction in the frequency of approaches and bites. Gambusia skin extract had no significant effect on aggressive behaviour. These data suggest a species-specific antipredator response to conspecific alarm pheromones in a New World cichlid fish and demonstrate a trade-off between predator avoidance and intraspecific aggression. Further, the presence of an alarm response in this model species sets the stage for the use of chemical cues as a research tool to manipulate predation risk in studies of the interaction between predation risk and reproductive behaviour.     

Chemical alarm and defence in the oribatid mite Collohmannia gigantea (Acari: Oribatida)

The multicomponent oil gland secretion of Collohmannia gigantea, a middle-derivative mixonomatan oribatid mite, is demonstrated to possess alarm pheromonal and allomonal properties. Four components of the secretion, namely the monoterpenes neryl formate, neral, geranial and the aromatic 2-hydroxy- 6-methyl-benzaldehyde (2,6-HMBD), showed moderate to strong alarm pheromonal activity in adult mites. Naturally elicited response is due to neral (about 50% of the secretion) and probably 2,6-HMBD (only 5% of the secretion, but strong alarm pheromonal activity). This is the second report of an alarm pheromone in Oribatida. Tridecane and pentadecane (=the hydrocarbon fraction of the secretion) did not evoke evident behavioural reactions, and most likely serve as solvents and spreading agents for the pheromonal-active components. Alarm reactions were characterized by a short recognition phase (waving movements with legs I), followed by shrinking back and panic escape from the scent source. In addition, all six components of the oil gland secretion, including the hydrocarbons, exhibited strong allomonal properties against a model oribatid predator, the scydmaenid beetle, Euconnus (Tetramelus) oblongus. Considering the widespread semiochemical properties of oil gland secretions in astigmatid mites (=a highly derivative oribatid group), these results furnish evidence for a phylogenetically early origin of defensive and communicative roles of oil gland secretions in oribatids. These roles include alarm communication, defence and the production of anti-fungal compounds.     

Chemical Alarm Signalling in Terrestrial Salamanders: Intra- and Interspecific Responses

Chemical alarm cues are known to be important in mediating predator avoidance in a variety of taxonomic groups. The purpose of this study was to test whether three species of salamanders that co-occur in the coastal mountains of Oregon utilize chemical alarm cues in predator avoidance. In laboratory experiments, Western redback salamanders, Plethodon vehiculum, and Southern torrent salamanders, Rhyacotriton variegatus, exhibited an avoidance response to stimuli from injured conspecifics, while Dunn's salamanders, Plethodon dunni did not. Additional experiments demonstrated interspecific alarm responses. P. vehiculum and R. variegatus responded to each other's alarm cues but did not respond to the alarm cues of allotopic long-toed salamanders, Ambystoma macrodactylum. For R. variegatus, this is despite the fact that they are more closely related to the allotopic species (A. macrodactylum) than to the syntopic species (P. vehiculum). Thus phylogeny alone may not explain patterns of cross-species alarm responses. Instead, interspecific alarm responses may occur between syntopic species that belong to the same prey guild (i.e. those species that co-occur spatially and temporally and are exposed to the same suite of predators).     

Embryonic substances induce alarm response in adult zebrafish (Danio rerio)

Many aquatic animals rely on chemicals released by injured individuals of the same species to assess predation risk. Among these chemical cues, alarm substances released from the injured skin of ostariophysan fishes have been extensively examined. In most fish species examined, these cues appear to be released by all injured individuals (including larvae, juveniles and adults) and elicit alarm responses in conspecifics. Adult alarm cues also affect development and physiology of embryos. Nonetheless, whether embryos produce alarm cues that affect adults is not known. This study reports that extracts of zebrafish (Danio rerio) embryos at 36 h post-fertilization or later induce antipredator behaviours reminiscent of those induced by skin alarm substances. At an equivalent of 10⁻⁶ g embryo per millilitre, the extract induced bottom-dwelling and freezing in adults. These behaviours are consistent with those induced by adult alarm substances. This study concludes that zebrafish embryos produce alarm substances.     

Behavioural response of aphids to the alarm pheromone component (E )-β-farnesene in the field

The alarm response of aphids to (E)‐β‐farnesene was examined for 59 species in the subfamilies Aphididae, Callaphididae, Chaitophoridae and Lachnidae, in the field. Forty‐one aphid species responded to (E)‐β‐farnesene at a dosage of 1 ng and/or 10 ng; however, 18 species did not. Myrmecophilous aphids did not react as extensively or strongly as non‐myrmecophilous aphids. The response of aphids to (E)‐β‐farnesene was related to host‐plant species.