Foot-thumping as an alarm signal in macropodoid marsupials: prevalence and hypotheses of function
TANIA A. ROSE*, ADAM J. MUNN†, DANIEL RAMP* and PETER B. BANKS*
*
School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW 2052 and
†
Institute of Wildlife Research, School of Biological Sciences, A08,
University of Sydney, NSW 2006, Australia
ABSTRACT1.
Alarm signalling as a means to reduce predation risk is an important component of thebehavioural repertoire of many species. It has previously been noted that many of themacropodoid marsupials (kangaroos, wallabies and rat-kangaroos) produce a foot-thump,an audible signal created by striking the ground with one or both feet, that is most likely analarm signal.
2.
The prevalence of foot-thumping within the macropodoids and hypotheses of its functionas an alarm signal have been poorly documented. To address this issue, we investigate theprevalence of foot-thumping in macropodoids and interpret possible function according tocurrent alarm signalling theory. Evidence for foot-thumping was found in almost allmacropodoids. In light of this, the behaviour appears to be a conservative trait that may havearisen alongside or followed the evolution of bipedal locomotion, and suggests that this traitcarries significant benefits that transcend ecological and predation differences among species.
3.
Nine alarm signal hypotheses were explored in order to determine the function of foot-thumping in macropodoid marsupials. However, the existing evidence for consistent functionremains inconclusive. Therefore, a series of predictions were developed to provide the foun-dation for future research to investigate more thoroughly the function of foot-thumping inmacropodoid marsupials.
Many prey animals have developed anti-predator strategies to mitigate the risk of predation;some reduce visibility using cryptic colouration or reduced activity, whereas others rely onthe dilution of risk through grouping or on the early detection of predators through behav-iours such as vigilance. In contrast, alarm signalling is a particularly conspicuous anti-predator strategy. Unlike concealment strategies, alarm signalling direct to predators or toneighbours may remove any chance of concealment. Alarm signals may be olfactory, visualor acoustic, and are found in a great variety of species (e.g. Hamilton, 1963; Maynard-Smith,1965; Estes & Goddard, 1967; Trivers, 1971; Hasson, 1991; Caro
et al
., 2004).Macropodoid marsupials (order: Diprotodontia; superfamily: Macropodoidea) are a
radiation of mammals that includes kangaroos, wallabies (family: Macropodidae) and
rat-kangaroos (family: Potoroidae). All extant macropodoids are exposed to the risk ofpredation at some stage of their lives and demonstrate various strategies of crypsis, conceal-ment, vigilance and grouping in order to reduce their risk of capture (Jarman & Coulson,1989). However, many macropodoid species also strike the ground with one or both hindfeet, producing an audible thump (Coulson, 1989), in response to a disturbance or approach-ing predator. This ‘foot-thumping’ by macropodoids is considered an acoustic form ofcommunication because it is visually inconspicuous, and it is considered by many to be adeliberate alarm signal (e.g. Croft, 1981; Blumstein
et al
., 2000, 2002a; Bender, 2005; reviewsby Coulson, 1989, 1996). Although a form of macropodoid foot-thumping may occur in othercontexts (e.g. in sexual contexts, see Coulson, 1989), most reports of the behaviour indicatethat it is more common in alarm contexts, and as such our specific interest in this review isto consider the behaviour within the framework of predator–prey interactions. Within thiscontext, it is unclear whether all species perform the behaviour and for whom the signal isintended: the predator, conspecifics, or both. Few studies have specifically investigated thefoot-thumping in macropodoids within a predator–prey context (but see Shepherd, 1981;Coulson, 1996; Blumstein
et al
., 2000, 2002a) and hence, it is not clear how macropodoidfoot-thumping fits with current alarm signal theories.
In this review, we investigate the occurrence of foot-thumping in the superfamilyMacropodoidea; exploring possible function in the context of other behavioural and ecolog-ical traits such as sociality, habitat and diets as they relate to predictions of the nine currenthypotheses on alarm signal function developed for other taxa. Each hypothesis is assessed inlight of documented studies of foot-thumping in macropodoid species, their varying ecologiesand relationships with key predators. Subsequently, a series of predictions are developed toenable the function of macropodoid foot-thumping to be explored experimentally, buildinga foundation for future research.
PREVALENCE AND ECOLOGY OF FOOT-THUMPING IN MACROPODOID MARSUPIALS
The superfamily Macropodoidea contains 50 Australian and 13 Papua New Guinean species(Strahan, 1995; Flannery, 1996). The macropodoids are distinguished from other marsupialsby their powerful hind limbs with elongated feet, weaker forelimbs and strong tail. Thesefeatures enable rapid economical locomotion via a distinctive hopping gait (Dawson, 1977),used by all but one monospecific genus, the musky rat-kangaroo
Hypsiprymnodon moschatus
(Burk, Westerman & Springer, 1998). There is considerable ecological diversity in the group,as their habitats vary from tropical rainforests to alpine tussock grasslands and arid inlandplains (Grigg, Jarman & Hume, 1989). Body sizes range from less than 500 g (musky rat-kangaroo) to over 85 kg (red kangaroo
Macropus rufus
) (Strahan, 1995). Diets also vary,from omnivorous to both browsing and grazing herbivores (Strahan, 1995). Somemacropodoids are strictly solitary, whereas others form tight social groups (Strahan, 1995).In other taxa, these factors (habitat, body size, diet, sociality) typically influence the functionof an alarm signal (e.g. see Taylor, Balph & Balph, 1990; Blumstein & Armitage, 1998).
Determining the prevalence of foot-thumping among the macropodoids is logisticallydifficult, largely because there are numerous species for which no documented behaviouralrepertoires exist, although Coulson (1989) reported foot-thumping in 18 species. Therefore,to assess its prevalence, 27 species specialists (research scientists and keepers of captivemacropodoids) were contacted to report on instances of foot-thumping in a given speciesbased upon our operational definition (see Tables 1–3). From these combined sources, foot-thumping was reported to occur in 46 macropodoid species and subspecies out of the 48 for
which information was available (Table 1). No information was available for the remaining15 species (Table 3), which predominantly comprise species occurring in remote areas ofPapua New Guinea, extremely rare species or those that have not been well studied. Althoughno observations of foot-thumping in free-living tree-kangaroos were reported, this may bedue to the difficulty of observing the behaviour of these animals in dense rainforest habitats(Flannery, 1996). In captivity, foot-thumping has been observed in three species of tree-kangaroo: the grizzled tree-kangaroo Dendrolagus inustus (U. Ganslosser, personal commu-nication; B. Smith, personal communication), Lumholtz tree-kangaroo D. lumholtzi (B.Smith, personal communication); and the Huon tree-kangaroo D. matschiei (J. Blessington,personal communication).
Of the macropodoid species for which enough information is available, only two specieshad not been observed foot-thumping, Goodfellow’s tree-kangaroo D. goodfellowi (C.Andrus, personal communication) and the musky rat-kangaroo (P. Johnson, personal com-munication) (Table 2). This is despite the respective species specialists having spent consider-able time with captive populations (13–14 years, Table 2). Notably, the musky rat-kangaroois the most primitive of the extant macropodoids (Flannery, 1984; Burk et al., 1998). Thisspecies has a quadrupedal, bounding gait, unlike the bipedal hopping of other macropodoids(Ganslosser, 1992; Strahan, 1995; Burk et al., 1998) and lacks several tarsal specialisationsof the hind foot that are adaptations for bipedal hopping (e.g. the calcaneofibular facet isabsent; see Burk et al., 1998). Burk et al. (1998) argued that bipedal hopping evolved onlyonce in the macropodoid radiations subsequent to Hypsiprymnodon. As macropodoidsusually foot-thump just prior to or during bipedal locomotion (Coulson, 1989), the presenceof foot-thumping in every macropodoid genus except Hypsiprymnodon suggests that it is ahighly conservative trait, and that foot-thumping has arisen alongside or following theevolution of bipedal locomotion in macropodoids, carrying fitness benefits irrespective ofspecies’ individual characteristics. Such behavioural consistency across so many species withdifferences in social structure (solitary and gregarious), habitats (open and dense) and life-history strategies is relatively unusual.
If foot-thumps are an alarm-call response to predation threat, predation must have influ-enced the evolution of macropodoid behaviour. Despite suggestions that predation has beengenerally insignificant in the evolution of marsupial behaviour (Flannery, 1984; Lee & Cock-burn, 1985; Burk et al., 1998), it does appear that over evolutionary time, macropodoids ofall sizes have been subject to predation at some stage of their life cycles (Jarman & Coulson,1989). There have been at least three genera of the now extinct leopard-sized marsupial lions(Thylacoleonidae) that, from their bone morphology, appear to have been cursorial huntersof macropodoids of all sizes (Jarman & Coulson, 1989). More recently, extinct thylacines(Thylacinidae) were a pursuit hunter of macropodoids, as were some large Dasyurid species(family: Dasyuridae, e.g. Sarcophilus), and ambush reptiles like the giant Maglania monitors(family: Varanidae), and giant crocodilians Quinkana spp. Extant predators of macropodoidsinclude the quolls Dasyurus spp. and an array of large ambush-hunting raptors (order:Falconiformes), both preying on small to medium-sized macropodoids. Larger raptors, suchas wedge-tailed eagles Aquila audax and white-bellied sea eagles Haliaeetus leucogaster, arealso known to attack larger macropodoids (see Jarman & Coulson, 1989). For the past4000 years, dingoes Canis familiaris dingo have preyed on all body sizes of macropodoids,hunting both in groups and alone (Shepherd, 1981; Jarman & Coulson, 1989), alteringmacropodoid population dynamics (Robertshaw & Harden, 1989). There has also beensubstantial hunting pressure on macropodoids by humans (Jarman & Coulson, 1989), andpredation pressure has increased via introduced predators such as the red fox Vulpes vulpes,
a hunting predator whose diet includes small to medium-sized macropodoids; and the feralcat Felis catus, an ambush predator whose diet includes small macropodoids (see Mitchell &Banks, 2005). Thus, good evidence exists that there has been a sustained suite of predators,notably with cosmopolitan distributions, diverse modes of attack and preying upon a widerange of body sizes of macropodoids (Jarman & Coulson, 1989; Wroe, Argot & Dickman,2004).
FOOT-THUMPING AS AN ALARM SIGNALFoot-thumping in alarm contexts is common in many mammalian taxa, although in no othermajor taxonomic unit is it as prevalent as in the superfamily Macropodoidea. As is the casewith many macropodoids (Coulson, 1989), some taxa that use foot-thumping strike theground with one or both feet to produce a single or double thump. This ‘foot-thumping’ isdistinguished here from ‘foot-drumming’, where the hind feed are drummed repeatedlyin rapid succession, such as the foot-drumming of kangaroo rats (Randall, 2001). Foot-drumming occurs in many small mammals, particularly rodents (see Randall, 2001). Foot-thumping, as opposed to foot-drumming, is more common in larger mammals, and, inaddition to the Macropodoidea, has been observed in some ungulates (Perissodactyla andArtiodactyla) and some rabbits (Lagomorpha) (Ewer, 1968; Randall, 2001).
Communication inherently involves a sender and a recipient. As an acoustic alarm signal,foot-thumps can be used when the sender and the recipient are not in visual contact such asby nocturnal species, grazers or animals living in dense cover. Similarly, as a vibrational alarmsignal, the acoustic thump may operate at low frequencies, causing ground vibrations iden-tifiable over large distances. The recipients of alarm signals are variously argued to beconspecifics, predators or both (e.g. Maynard-Smith, 1965; Woodland, Jaafar & Knight,1980). Generally, the type of alarm signal that an animal uses depends on which of the costsof signalling are outweighed by the benefits (Caro, 1986a; Taylor et al., 1990). Costs varyaccording to the type of signal and its function, and may include a metabolic expense, a timecost involved with execution of the signal, the foregoing of alternate activities, and anincreased predation risk from attracting the predator’s attention (Krebs & Davies, 1981; Caro,1986a; Johnstone, 1997; Randall, 2001). In macropodoids, the metabolic expense of foot-thumping is likely to be trivial when apportioned over the time and energy expense of bipedalflight. The time cost of executing a foot-thump while hopping may depend upon the animal’sflight speed: at high speeds, creating an audible thump with the hind feet rather than pushingoff from the ground may reduce stride length and so increase the time it takes to escape,whereas when the animal is stationary or moving at low speeds, the time cost of foot-thumping may be negligible. The risks associated with attracting a predator’s attention willvary according to the function of the signal and the attack mode of the predator. The benefitsare primarily a reduction in predation risk for the signaller or, if the signal acts as an altruisticwarning of danger, for the signaller’s conspecifics.
The numerous theories that describe the benefits of alarm signals fall broadly into two (notmutually exclusive) categories: signals directed towards conspecifics, and signals directedtowards predators. In an effort to discern the function of stotting in Thomson’s gazelles, Caro(1986a) developed an array of hypotheses. These hypotheses form the basis of the alarm signalhypotheses reviewed here; however, not all of Caro’s hypotheses were applicable to foot-thumping in macropodoids (e.g. attracting the mother’s attention and play). Furthermore,some alarm signalling hypotheses that were not considered by Caro (1986a) have beenincluded (warning conspecifics to decrease future risk and signalling to create havoc) becauseof their potential relevance to foot-thumping behaviour in macropodoids.
Signalling to conspecificsSignals directed to conspecifics may serve several functions. They may warn conspecifics ofpotential danger, improve social cohesion to reduce an individual’s immediate risk, or maycreate havoc to improve an individual’s chances of escape. In warning conspecifics, there isthe risk of attracting the attention of a predator (Maynard-Smith, 1965; Estes & Goddard,1967; Trivers, 1971; Sherman, 1977). Yet warning signals are argued not to function as purealtruism but to provide direct or indirect benefits to the signaller (Maynard-Smith, 1965;Trivers, 1971; Sherman, 1977). The signaller may benefit directly via decreased future preda-tion risk because an unsuccessful predation event may deter predators from that patch(Sherman, 1977) or indirectly from warning close relatives (kin-selected altruism: Maynard-Smith, 1965; Estes & Goddard, 1967) or by the potential of future reciprocation by others(reciprocal altruism: Trivers, 1971).
If macropodoids are signalling to conspecifics, then signalling will only occur when indi-viduals are in close proximity (groups); only one animal (usually the first animal to see apredator) should signal; and, if the signal functions as kin-selected altruism, signalling willoccur more frequently in groups of closely related individuals. Clear tests providinganswers to these predictions are lacking. Blumstein et al. (2000) suggested that foot-thumpswere conspecific signals because tammar wallabies M. eugenii responded to audio play-backs of foot-thumps by decreasing time spent foraging and increasing vigilance, althoughplaybacks did not affect locomotion. Similarly, playbacks of foot-thumps to red-neckedpademelons Thylogale thetis (Blumstein et al., 2002a) yielded a decrease in foraging and anincrease in vigilance behaviours, but so did a range of other sounds (including calls ofpredators and magpies). Blumstein et al. (2002a) proposed these interspecific differenceswere functionally different anti-predator strategies: both species aggregate when feeding,but red-necked pademelons assess predation risk independently of the presence of conspe-cifics. Notably, Strahan (1995) describes both species as essentially solitary, aggregatingonly occasionally and in small groups when feeding in clearings or along forest edges.Hence, tests of the ‘warning to conspecifics’ hypotheses in essentially solitary species maynot give the clearest evidence for alarm function, and a response to playback may merelyrepresent an eavesdropping phenomenon.
Observations of free-living social kangaroos similarly offer only limited insights into thewarnings hypotheses. Shepherd (1981) noted that red kangaroos showed little response to thefoot-thumps of conspecifics in response to dingoes. And foot-thumping in social western greykangaroos M. fuliginosus was observed when individuals were alone, in small groups(2.5 ± 0.3 individuals), and sometimes when they were more than 300 m from their nearestneighbour (Coulson, 1996). Gregarious eastern grey kangaroos M. gigantus are also knownto foot-thump when alone or when in groups (Bender, 2004). Furthermore, the prevalence offoot-thumping in both solitary and social macropodoids (Table 1) suggests that, althoughfoot-thumping may sometimes act as a communication to conspecifics, this may not be itsonly function.
Evidence for signals to kin is also weak as few species form social groups, mainlywith relatives; instead, grouping is often highly labile (Croft, 1989) and yet foot-thumping occurs in both types of social aggregations. Although some macropodoids candiscriminate between kin and non-kin (e.g. tammar wallabies: Blumstein et al., 2002b),thumping by adult males is common in western grey kangaroos (37% of observations)(Coulson, 1989) and eastern grey kangaroos (50% of observations) (Bender, 2004), eventhough males are the dispersing sex and are therefore unlikely to be related to signalrecipients.
That macropodoid foot-thumps signal conspecifics to create a social cohesion or grouphavoc response has some support because the signal often causes many individuals in a groupto flee. Social cohesion is thought to dilute the risk to any one individual (Malcolm & VanLawick, 1975; Treisman, 1975), as avoiding the periphery of a group lowers an animal’s riskof predation (Hamilton, 1971). But it is often difficult to assess whether social cohesion iscaused by the alarm signal or by a predator’s presence. Similarly, havoc is defined as disruptivechaos (Rooney, 1999) and may eventuate from a proportion of the group, such as 50% (Caro,1986b), simultaneously reacting to the signal by scattering or moving about erratically (Char-nov & Krebs, 1975). Havoc may confuse the predator and lessen its chance of a successfulattack (Hoogland & Sherman, 1976; Wittenberger, 1981). The presence of foot-thumping insolitary individuals and solitary species (Table 1) suggests that it is unlikely that the solefunction of foot-thumping is to act as a catalyst for either social cohesion or the generationof havoc, and that this hypothesis may not fully explain the function of foot-thumping inmacropodoids. Observations that a simultaneous chaotic reaction to foot-thumping occursin a substantial proportion of the group [Caro (1986b) suggests 50%] will more fully evaluatewhether foot-thumping does create havoc in some species.
Signalling to predatorsAlarm signals directed to predators may also function in several ways. They may act as apursuit-deterrent by communicating early detection of the predator or by advertising thesignaller’s body condition; they may invite the predator to prematurely initiate chase; orthey may confuse the predator and thus improve the chances of escape (see Caro, 1986a).The pursuit-deterrent hypothesis suggests that signals carry an implicit message that a chasewould be unsuccessful, causing the predator to abandon pursuit (Woodland et al., 1980;Hasson, 1991; Caro, 1995). Pursuit-deterrent signals may not always honestly communicatethe ability of the prey to escape. Prey may misjudge their ability to escape (juveniles, naiveanimals), or animals may ‘cheat’ and provide fake information (Bildstein, 1983; Caro, 1986a).Although this may be a successful strategy for some animals, it is likely that cheaters withinthe population will ensure that the honesty of the signal is frequently tested. If the numberof cheaters in a population becomes too high, predators may soon become aware that thesignal is no longer a reliable indicator of capture success, and the signal would eventuallylose its effectiveness. Therefore, for a condition advertisement signal to be maintained, cheat-ing would only be favoured in a small proportion of the population.
If foot-thumping in macropodoids acts as a pursuit-deterrent, signalling would occurregardless of whether the animals are alone or in groups, which is supported by observations(Table 1). To further support the pursuit-deterrent theory, experimental research is needed toprovide evidence that predators pursue individuals that foot-thump less often than individ-uals that do not foot-thump, that macropodoids do not foot thump when predators are closeenough that a successful attack is likely, and/or that foot-thumping does not occur once thepredator has initiated chase. Furthermore, if foot-thumping advertises that the signaller is ingood condition, it should occur less frequently in sick, injured, young or very old individuals(see FitzGibbon & Fanshawe, 1988).
In contrast, the pursuit-invitation hypothesis proposes that the alarm signal induces adetected predator to attack prematurely, before it is sufficiently close to capture the prey. Thismay cause it to depart after a failed attempt, and enable both the predator and the preyto resume activities that are more profitable than high-level vigilance or stalking a watchfulprey (Smythe, 1970, 1977). Macropodoid foot-thumping is likely to act as a pursuit-invitationif it occurs only when the thumper is far enough from the predator that escape is likely, but
should not occur once the predator has initiated chase, regardless of whether the animals arealone or in groups. Predators should respond to pursuit-invitation signals by preferentiallychasing individuals that foot-thump over individuals that do not, but there is little researchconducted on macropodoid–predator interactions, and no studies suggest that predatorspreferentially chase individuals that foot-thump. The distance from predators at which anindividual initiates flight varies according to the individual’s age and condition (Jarman &Wright, 1993), and although Coulson (1996) found that foot-thumping occurred at safedistances in western grey kangaroos, knowledge of the flight-initiation distances of individ-uals (or age classes) was lacking. A study involving the measurement of individuals’ flight-initiation distances would better determine whether thumps always occur at safe distancesfrom predators.
The predator-confusion hypothesis is an extension of the havoc hypothesis except thatmany individuals simultaneously signal to the predator, hindering its chances of capturingany individual prey (Humphries & Driver, 1967; Walther, 1969). This hypothesis was firstraised to explain erratic behaviour, such as stotting and zigzagging in Thomson’s gazelleswhile attempting to escape predators (Humphries & Driver, 1967). The predator-confusionhypothesis predicts that signalling will only occur in grouped animals, that more than oneanimal will signal, and that predators will become visibly confused after multiple animalshave signalled. The only evidence that suggests that the sole function of macropodoid foot-thumping may not be to confuse predators, is that foot-thumping occurs in both solitary andsocial animals (Table 1). Clearly, studies involving the measurement of the number of indi-viduals foot-thumping in response to a predator stimulus, along with observations of predatorresponses to multiple foot-thumps, would provide better support for this hypothesis.
Testing the alarm signal hypotheses against the predictions outlined above will exploremore thoroughly the function of foot-thumping in macropodoid marsupials. To test thevarious hypotheses critically, experiments could measure macropodoid reactions to con-trolled predator approaches and playbacks of foot-thump sounds. A summary of potentialobservations/manipulations that would test the predictions is provided in Tables 4 and 5. Thetiming (e.g. time after hearing a thump or proximity to predator stimuli), extent (e.g. howmany individual respond) and nature of responses (e.g. flight or foot-thumping) can be usedto distinguish among alarm-calling hypotheses. But because the same response can be pre-dicted under several different hypotheses, manipulation of group size, age class and related-ness will be needed to untangle the adaptive mechanism(s) behind foot-thump behaviour.
CONCLUSIONThe presence of foot-thumping in every extant macropodoid genus, with the notable excep-tion of the quadrupedal Hypsiprymnodon, suggests that foot-thumping is a conservative trait,having evolved alongside or following bipedal locomotion. The function of foot-thumpingmay vary between macropodoids; however, the prevalence of foot-thumping over a wide rangeof ecological conditions, and differences in historical and current predation pressure amongspecies, suggests that there may be some commonality to the foot-thump’s function.
Of the alarm signalling hypotheses proposed, some support is found for foot-thumping inmacropodoids acting to warn conspecifics, but the use of foot-thumping by solitary animalssuggests that this may not be its only function. It remains possible that the foot-thump actsas a communication to predators, and members of social species merely opportunisticallyreact to the sound of a foot-thump by conspecifics. Nonetheless, current knowledge ofmacropodoid foot-thumping does not provide conclusive support for any of the alarm sig-nalling hypotheses examined, and further research is needed to clarify the function(s) of this
Table 4. Predictions of macropodoid responses to predator approach and relationship to alarm signalling hypotheses
Manipulation: GroupingPredator approach to solitary and grouped macropods (gregarious species)Response Possible function of foot-thumpFoot-thumping will not occur when animals are solitary Warning conspecifics
Confusing predatorCreating havocSocial cohesion
Foot-thumping will occur when solitary or grouped Pursuit-invitationPursuit-deterrent (perception advertisement)Pursuit-deterrent (condition advertisement)
Manipulation: Response of conspecificsPlayback of foot-thump sound to grouped macropodoids (gregarious species)Response Possible function of foot-thumpMacropodoids react to the foot-thump sound by fleeing or
significantly increasing vigilance relative to a control soundWarning conspecifics
Macropodoids react to the foot-thump sound bydecreasing their space from one another
Social cohesion
Macropodoids react to the foot-thump sound by fleeing Warning conspecificsCreating havoc
Macropodoids react to the foot-thump sound by foot-thumping
Confusing predator
Macropodoids show no reaction to the foot-thump sound relative to a control sound
Manipulation: Condition-dependencePredator stimulus approaches solitary animals, varying age classes(NB assumes age class is an indicator of condition)Response Possible function of foot-thumpFoot-thumping occurs in animals of all age groups Pursuit-deterrent (perception advertisement)
Pursuit-invitationFoot-thumping does not occur in very young or old animals Pursuit-deterrent (condition advertisement)Foot-thumping does not occur in any animals Warning conspecifics
Social cohesionConfusing predator
Manipulation: Distance from threatControlled predator approach towards solitary animals, measuring distances at which foot-thumping occursResponse Possible function of foot-thumpFoot-thumping only occurs far from the threat Pursuit-invitationFoot-thumping occurs as soon as the animal perceives the
Strong (adult) animals foot-thump closer to the threat thanjuvenile or elderly animals
Pursuit-deterrent (condition advertisement)
Foot-thumping does not occur Warning conspecificsSocial cohesionConfusing predator
Manipulation: RelatednessTowards groups of related or unrelated animals (gregarious species)Response Possible function of foot-thumpFoot-thumping does not occur in unrelated group Warning conspecifics (kin selection)Foot-thumping occurs equally often in both related
and unrelated groupsWarning conspecifics (reciprocal altruism)Social cohesionConfusing predatorPursuit-invitationPursuit-deterrentCreating havoc
behaviour. Manipulations using various species of captive macropodoids, combined withobservations of interactions between macropodoids and predators in the wild, are necessaryto test the predictions generated by the alarm signalling hypotheses described here.
ACKNOWLEDGEMENTSThanks to the following keepers of captive macropodoids for providing information onfoot-thumping: M. Hawkins from Taronga Zoo, B. Smith from Currumbin Sanctuary, J.Blessington from Kansas City Zoo, J. Steenberg (co-author of the Tree-Kangaroo HusbandryManual), C. Andrus from San Diego Zoo, and C.De Alwis from Royal Melbourne Zoo.Thanks also to the research scientists who passed on their experiences with foot-thumping:D. Croft, T. Dawson, H. Bender, U. Ganslosser, L. Kazmeier, G. Newell, P. Johnson, P.Jarman, M. E., P. Christensen, D. Pearson, S. Ingleby, T. Flannery, A. Burbidge, A. Kabat,R. Rose, N. Noakes, D. Sigg, R. Teale, T. Pople and J. Nedved. Special thanks are given toC. Barclay, B. Mitchell and B. Russell for useful discussions.
Manipulation: Number of signallersPredator approach towards group (gregarious species)Response Possible function of foot-thumpMore than one individual will foot-thump, irrespective of age Confusing predatorMore than one individual will foot-thump, but not
very young or old individualsPursuit-deterrent (condition advertisement)
Only one individual will foot-thump Warning conspecificsCreating havocPursuit-deterrent (perception advertisement)Social cohesion
Observations of predators approaching macropodoidsResponse Possible function of foot-thumpFoot-thumping does not occur once the predator has initiated
Table 5. Predictions of predator responses to macropodoid foot-thumping and relationship to alarm signalling hypotheses
Observations of predators approaching macropodoids
Response Possible function of foot-thump
Predators chase individuals that foot-thump less often than Pursuit-deterrent (perception advertisement)individuals that do not foot-thump Pursuit-deterrent (condition advertisement)
Predators chase individuals that foot-thump more oftenthan individuals that do not foot-thump
Pursuit-invitation
Predators show no preference for chasing individuals that foot-thump or individuals that do not foot-thump
Warning conspecificsSocial cohesionCreating havoc
Predators should become visibly confused when attacking agroup of foot-thumpers
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Submitted 5 July 2005; returned for revision 5 September 2005; revision accepted 22 December 2005Editor: RM
