Animal behaviour
rsbl.royalsocietypublishing.org
Predator odours attract other predators, creating an olfactory web of information Peter B. Banks, Andrew Daly and Jenna P. Bytheway
Research Cite this article: Banks PB, Daly A, Bytheway JP. 2016 Predator odours attract other predators, creating an olfactory web of information. Biol. Lett. 12: 20151053. http://dx.doi.org/10.1098/rsbl.2015.1053
Received: 16 December 2015 Accepted: 20 April 2016
Subject Areas: behaviour, ecology Keywords: eavesdropping, olfactory communication, predation risk, odour deterrent
Author for correspondence: Peter B. Banks e-mail: [email protected]
School of Life and Environmental Sciences, The University of Sydney, Sydney, New South Wales 2006, Australia PBB, 0000-0002-4340-6495; JPB, 0000-0003-4033-9538 Many studies have reported the aversive reactions of prey towards a predator’s odour signals (e.g. urine marks), a behaviour widely thought to reduce the risk of predation by the predator. However, because odour signals persist in the environment, they are vulnerable to exploitation and eavesdropping by predators, prey and conspecifics. As such, scent patches created by one species might attract other species interested in information about their enemies. We studied this phenomenon by examining red fox investigation of odours from conspecifics and competing species in order to understand what prey are responding to when avoiding the odours of a predator. Surprisingly, foxes showed limited interest in conspecific odours but were highly interested in the odours of their competitors (wild dogs and feral cats), suggesting that odours are likely to play an important role in mediating competitive interactions. Importantly, our results identify that simple, dyadic interpretations of prey responses to a predator odour (i.e. cat odour ¼ risk of cat encounter ¼ fear of cats) can no longer be assumed in ecological or psychology research. Instead, interactions mediated by olfactory cues are more complex than previously thought and are likely to form a complicated olfactory web of interactions.
1. Introduction The exploitation of signals (e.g. visual, auditory, olfactory) by predators, prey, competitors and conspecifics is a well-established phenomenon in ecology (reviewed in [1,2]). In particular, numerous studies have investigated the response of prey to predator odours, and prey behaviours such as avoidance and reduction in feeding, activity or reproduction are thought to reduce predation risk from the donor species [3,4]. Predator odours are also widely used in the psychology literature to understand fear, and many such studies also assume that fear responses in laboratory animals after exposure to a predator’s odour are owing to fear of that predator [4]. However, anti-predator responses to the odours of a predator species will only decrease predation risk if the odour represents a hotspot of that predator’s activity. This tight spatial association has been assumed in many studies, given that scent marks made to demarcate territory ownership will attract passing conspecifics [5], but it is rarely investigated. Olfactory communication in this way is traditionally considered to be a dyadic interaction, with one signaller (e.g. predator) and one receiver (e.g. prey). This simple approach is unlikely to hold however, given the properties of olfactory cues in terms of longevity, spatial association and the need for close inspection to receive specific information [1]. It is likely that olfactory signals are of interest not only to the intended receiver but also to an array of eavesdroppers in the community who seek to gain beneficial information, including predators, prey, competitors and conspecifics. Olfactory cues in particular are vulnerable to eavesdropping, as unlike acoustic and visual cues, odours typically persist in the environment long after the creator has departed [1]. This creates potential for a complex olfactory web of interactions whereby receivers (intended or otherwise) may not only be responding to the signaller, but also to many other potential receivers.
& 2016 The Author(s) Published by the Royal Society. All rights reserved.
% investigated
(a)
2
60 29
dog
cat
40 22 33 *
20
0 control
fox
(b) 4
no. investigations
5 3 8 2 6
5
control
fox
1
0 dog
cat
treatment
Figure 1. (a) The percentage of visited odour-treated plots that were investigated by foxes. The number of visits to each treatment is indicated above the bars. An asterisk indicates an ASR value . j2j. (b) The average number of times a visited plot was investigated. Error bars represent standard error of the mean. The sample size is indicated above the bars.
2. Material and methods This experiment was conducted in a 225 km2 area of the mallee wheatlands near Walpeup, Victoria, Australia where the mammalian predator community consists of foxes (density 0.9– 2.0 km22) [12], feral cats and feral dogs [13]. Roaming domestic farm dogs and cats may also interact with other predators in the area. Cat and dog urine was collected from domestic animals (both genders) during routine surgical patient management at a veterinary hospital. Fox urine was collected from the bladders of foxes (both genders) shot during pest control programmes well outside the study area. Urine was kept frozen at 2208C until use. Predator urine (1 ml; typical volume of a scent mark [5]) was dripped onto 10 30 cm pieces of cotton towel, each towel receiving odour from a different individual. Controls consisted of untreated towels. Forty sand plots (2 m wide and a minimum of 500 m apart (average 650 m) to maintain independence of fox visits [14]; nightly results from adjacent plots were independent; x 2 ¼ 3.12, p ¼ 0.08, n ¼ 112) were created across roads using in situ sand and randomly assigned to an odour treatment (cat, dog, fox or control; n ¼ 10). Odour-treated towels were fixed to the ground with a tent peg on road verges and alternated between road sides to avoid bias. A light coating of sand was sprinkled over the towel to reduce visual conspicuousness. Plots were checked for 6 days for predator tracks, and visitors were identified to species using track characteristics (with reference to [15]). An observer ( J.P.B.) who was blind to the treatment recorded the number of fox footprints within 1 m of the towel and the spatial arrangement of footprints. Investigation of the treatment towel was determined from 10 or more footprints within 1 m of the towel, scats or diggings present within 1 m of the towel, clear change in direction of footprints towards
the towel or obvious disturbance of the towel. All other fox records were considered to be incidental passings. Treatment towels were replaced daily with the same odour treatment.
(a) Statistical analyses We performed a x 2 test of independence using exact probability values to compare the percentage of investigation events by foxes between treatments. Adjusted standardized residuals (ASRs) were calculated to identify where significance could be attributed; ASRs . j2j indicate a lack of fit of the null hypothesis in that cell [16]. To compare the number of fox investigations at an odour plot among treatments, we conducted a one-way pffiffiffiffiffiffiffiffiffiffiffi analysis of variance (ANOVA). Data were transformed ( x þ 1) to meet the assumptions of ANOVA. All statistics were conducted in IBM SPSS STATISTICS v. 22. Only plots that received some form of visitation (incidental or investigation) were included.
3. Results Fox investigation of odour plots was significantly affected by treatment (Pearson’s x 2 ¼ 9.928, d.f. ¼ 3, p ¼ 0.018). Cat and dog odour plots received a high level of investigation, with 52% and 50% of visits respectively resulting in investigation by foxes (ASR ¼ 1.8 and 1.6, respectively; figure 1a). While control plots received some attention (32%, ASR ¼ 20.6), only 18% of fox-treated plots were investigated (ASR ¼ 22.7;
Biol. Lett. 12: 20151053
28
rsbl.royalsocietypublishing.org
The idea that olfactory information can have multiple users to create an olfactory web of interactions has received some theoretical consideration, albeit indirectly [6]. For example, infochemical webs and the ‘crying for help’ hypothesis are based on the direct signals produced by plants suffering herbivory (herbivore-induced plant volatiles) to attract their herbivores’ enemies ( predators or parasitoids) [6]. It is also known that some mammals use olfactory cues produced by competitors [7] as well as conspecifics [8] as cues of interaction with shared predators. Here we investigated the patterns of visitation by red foxes (Vulpes vulpes) to scent marks of two species of competitors: feral cats (Felis catus) and wild dogs (Canis lupus familiaris), as well as conspecifics, to assess the likely risk of fox encounter associated with these odours. Odours from red foxes, cats and dogs have all induced avoidance/fear responses in a wide range of mammalian prey, both in the field and in the laboratory (see review [4]). All of these predators use urine and faeces to maintain territories and are attracted to the odours of conspecifics within their territory to over-mark and signal their presence [5,9], so their odours should represent hotspots of conspecific activity. Like most predators, foxes live in a multi-predator community. There is dietary overlap among foxes, cats and dogs, who compete for food and possibly other resources [10], and likely use each others’ odours to mediate competitive interactions [11]. If foxes eavesdrop on the odour cues of their enemies, we predicted that fox visitation would be high not only at scent marks of unfamiliar foxes, but also at scent marks of cats and dogs, to create an olfactory web of information available for prey to assess their risk of fox encounter.
3
rsbl.royalsocietypublishing.org
apex predators e.g. dog/dingo
conspecific predators i.e. foxes
this study
mesopredator (fox) odour cue
intraguild competitors/predators e.g. cats and quolls
[12]
[12] [12]
conspecific prey
this study
[7,21]
prey individual
interspecific competing prey
Figure 2. An olfactory web of communication among a predator : prey assemblage. Thick lines are direct responses to fox odour cues; thin lines are indirect associations generated by direct responses to foxes by other members of the food web.
figure 1a). The number of investigations to an odour plot also appeared to be higher for dog- and cat-treated plots; although this was not significant (F3,20 ¼ 2.918, p ¼ 0.059; figure 1b), it is nonetheless indicative of a large effect size (h 2 ¼ 0.304). Foxes visited (incidental or investigation) almost all (3940) of the sand plots.
4. Discussion Foxes investigated cat and dog odour 62% and 56% more than untreated controls, respectively. This suggests that odours have a strong role in mediating competitive interactions among these predators. Foxes are likely to be competitively superior to cats (cat populations increase in the absence of foxes [17]) and occasionally kill them [10]. In Australia, wild dogs/dingoes harass and kill foxes [18], compete with them for food [19] and exclude them from other resources such as water [20]. Foxes exhibit small-scale avoidance of dogs [11], and our results suggest that this avoidance behaviour may be facilitated by olfactory cues, which require close investigation to retrieve specific information about competitors. Foxes were least interested in conspecific odour, which was surprising giving its purported use in social interactions, including territorial maintenance and mating [5,9]. We presented fox odours from unfamiliar individuals to represent interloping individuals, which we predicted to induce greater interest than would odours from local foxes [21]. However, foxes were as attracted to interloper scent marks as much as they were to the novelty in odours of an untreated towel. Fox investigation of one-third of the untreated controls suggests
some neophilic attraction to the novelty of the towel, even without the addition of a biologically significant odour. Given that foxes were highly attracted to odours of other predator species, what risk does a predator scent actually signal to eavesdropping prey? Cat and dog odours, in fact, had a higher probability of visitation by foxes than did fox odour. It is likely that fox odour would, in turn, attract other predators such as cats and dogs/dingoes. Thus, anti-predator responses induced by fox odour, e.g. [4], may be a tactic to avoid predation by other eavesdropping predators rather than only the foxes themselves. Predator–prey interactions mediated by olfactory cues are clearly more complex than previously thought and are likely to form a complicated web of interactions akin to a food web (figure 2). Decision-making on whether to visit a particular olfactory cue must take into consideration who else may be eavesdropping on that cue and the potential outcome of an encounter with either the cue creator or an eavesdropper. The concept of an olfactory web predicts that a suite of competitors and predators should all show varying degrees of attraction to and avoidance of each other’s odours, as these social signals are likely to be useful in mediating their interactions with their enemies. This concept undermines the traditional approach used in hundreds of studies examining prey responses to predator odours, which assumes that it is a simple dyadic interaction, with one signaller (predator) and one receiver ( prey) of the information. Before making inferences about the information encoded in the odours of a predator or indeed any species, future studies need to first untangle the potential olfactory web by quantifying visitation rates of all members of an interacting community to their own
Biol. Lett. 12: 20151053
this study
Ethics. This study was conducted in accordance with the Australian code of practice for the care and use of animals for scientific purposes. Research was approved by The University of Sydney Animal Ethics Committee (approval no. 2013/5743). Data accessibility. Data supporting this article are available at the University of Sydney’s eScholarship Repository at http://hdl.handle.net/ 2123/14727.
Authors’ contributions. All authors contributed to the study design and drafted the manuscript. J.P.B. and A.D. carried out the fieldwork. All authors gave approval for publication of the final version and agree to be held accountable for the content herein. Competing interests. We declare we have no competing interests.
Funding. This study was supported by an ARC Discovery grant DP140104413 awarded to P.B.B.
Acknowledgements. We thank the RSPCA and NSW National Parks and Wildlife Service for their assistance in collecting predator odours, and Paul Shanta for assistance in graphic design.
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3.
4.
5. 6.
7.
8.
Hughes NK, Kelley JL, Banks PB. 2012 Dangerous liaisons: the predation risks of receiving social signals. Ecol. Lett. 15, 1326 –1339. (doi:10.1111/j. 1461-0248.2012.01856.x) Stowe MK, Turlings T, Loughrin JH, Lewis WJ, Tumlinson JH. 1995 The chemistry of eavesdropping, alarm, and deceit. Proc. Natl Acad. Sci. USA 92, 23 –28. (doi:10.1073/pnas.92.1.23) Kats LB, Dill LM. 1998 The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5, 361– 394. Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS. 2005 The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci. Biobehav. Rev. 29, 1123–1144. (doi:10.1016/j.neubiorev.2005.05.005) Brown RE, Macdonald DW. 1985 Social odours in mammals. New York, NY: Clarendon Press. Vet LE. 1999 From chemical to population ecology: infochemical use in an evolutionary context. J. Chem. Ecol. 25, 31–49. (doi:10.1023/A:1020833015559) Hughes NK, Korpima¨ki E, Banks PB. 2010 The predation risks of interspecific eavesdropping: weasel –vole interactions. Oikos 119, 1210 –1216. (doi:10.1111/j.1600-0706.2010.18006.x) Hughes NK, Kelley JL, Banks PB. 2009 Receiving behaviour is sensitive to risks from eavesdropping
9.
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13.
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15.
predators. Oecologia 160, 609–617. (doi:10.1007/ s00442-009-1320-2) Macdonald D. 1979 Some observations and field experiments on the urine marking behaviour of the red fox, Vulpes vulpes L. Z. Tierpsychol. 51, 1 –22. (doi:10.1111/j.1439-0310.1979.tb00667.x) Glen AS, Dickman CR. 2005 Complex interactions among mammalian carnivores in Australia, and their implications for wildlife management. Biol. Rev. 80, 387–401. (doi:10.1017/S1464793105006718) Mitchell BD, Banks PB. 2005 Do wild dogs exclude foxes? Evidence for competition from dietary and spatial overlaps. Aust. Ecol. 30, 581 –591. (doi:10. 1111/j.1442-9993.2005.01473.x) Saunders G, Coman B, Kinnear J, Braysher M. 1995 Managing vertebrate pests: foxes. Canberra, Australia: Australian Government Publ. Service. Hughes NK, Price CJ, Banks PB. 2010 Predators are attracted to the olfactory signals of prey. PLoS ONE 5, e13114. (doi:10.1371/journal.pone.0013114) Mahon PS, Banks PB, Dickman CR. 1998 Population indices for wild carnivores: a critical study in sanddune habitat, south-western Queensland. Wildl. Res. 25, 11 –22. (doi:10.1071/WR97007) Tirggs B. 2004 Tracks, scats and other traces: a field guide to Australian mammals. South Melbourne, Australia: Oxford University Press.
16. Agresti A. 1992 A survey of exact inference for contingency tables. Stat. Sci. 7, 131–153. (doi:10. 1214/ss/1177011454) 17. Risbey DA, Calver MC, Short J, Bradley JS, Wright IW. 2000 The impact of cats and foxes on the small vertebrate fauna of Heirisson Prong, Western Australia. II. A field experiment. Wildl. Res. 27, 223–235. (doi:10.1071/WR98092) 18. Moseby KE, Neilly H, Read JL, Crisp HA. 2012 Interactions between a top order predator and exotic mesopredators in the Australian rangelands. Int. J. Ecol. 2012, 250352. (doi:10.1155/2012/ 250352) 19. Cupples JB, Crowther MS, Story G, Letnic M. 2011 Dietary overlap and prey selectivity among sympatric carnivores: could dingoes suppress foxes through competition for prey? J. Mammal. 92, 590–600. (doi:10.1644/10-MAMM-A-164.1) 20. Brawata RL, Neeman T. 2011 Is water the key? Dingo management, intraguild interactions and predator distribution around water points in arid Australia. Wildl. Res. 38, 426–436. (doi:10.1071/ WR10169) 21. Arnold J, Soulsbury C, Harris S. 2011 Spatial and behavioral changes by red foxes (Vulpes vulpes) in response to artificial territory intrusion. Can. J. Zool. 89, 808 –815. (doi:10.1139/z11-069)
Biol. Lett. 12: 20151053
References
4
rsbl.royalsocietypublishing.org
and each other’s olfactory cues. This is an essential step to provide clarity in our understanding of how eavesdroppers exploit odours in a landscape of risk signalled by olfactory cues.
rsbl.royalsocietypublishing.org
Predator odours attract other predators, creating an olfactory web of information Peter B. Banks, Andrew Daly and Jenna P. Bytheway
Research Cite this article: Banks PB, Daly A, Bytheway JP. 2016 Predator odours attract other predators, creating an olfactory web of information. Biol. Lett. 12: 20151053. http://dx.doi.org/10.1098/rsbl.2015.1053
Received: 16 December 2015 Accepted: 20 April 2016
Subject Areas: behaviour, ecology Keywords: eavesdropping, olfactory communication, predation risk, odour deterrent
Author for correspondence: Peter B. Banks e-mail: [email protected]
School of Life and Environmental Sciences, The University of Sydney, Sydney, New South Wales 2006, Australia PBB, 0000-0002-4340-6495; JPB, 0000-0003-4033-9538 Many studies have reported the aversive reactions of prey towards a predator’s odour signals (e.g. urine marks), a behaviour widely thought to reduce the risk of predation by the predator. However, because odour signals persist in the environment, they are vulnerable to exploitation and eavesdropping by predators, prey and conspecifics. As such, scent patches created by one species might attract other species interested in information about their enemies. We studied this phenomenon by examining red fox investigation of odours from conspecifics and competing species in order to understand what prey are responding to when avoiding the odours of a predator. Surprisingly, foxes showed limited interest in conspecific odours but were highly interested in the odours of their competitors (wild dogs and feral cats), suggesting that odours are likely to play an important role in mediating competitive interactions. Importantly, our results identify that simple, dyadic interpretations of prey responses to a predator odour (i.e. cat odour ¼ risk of cat encounter ¼ fear of cats) can no longer be assumed in ecological or psychology research. Instead, interactions mediated by olfactory cues are more complex than previously thought and are likely to form a complicated olfactory web of interactions.
1. Introduction The exploitation of signals (e.g. visual, auditory, olfactory) by predators, prey, competitors and conspecifics is a well-established phenomenon in ecology (reviewed in [1,2]). In particular, numerous studies have investigated the response of prey to predator odours, and prey behaviours such as avoidance and reduction in feeding, activity or reproduction are thought to reduce predation risk from the donor species [3,4]. Predator odours are also widely used in the psychology literature to understand fear, and many such studies also assume that fear responses in laboratory animals after exposure to a predator’s odour are owing to fear of that predator [4]. However, anti-predator responses to the odours of a predator species will only decrease predation risk if the odour represents a hotspot of that predator’s activity. This tight spatial association has been assumed in many studies, given that scent marks made to demarcate territory ownership will attract passing conspecifics [5], but it is rarely investigated. Olfactory communication in this way is traditionally considered to be a dyadic interaction, with one signaller (e.g. predator) and one receiver (e.g. prey). This simple approach is unlikely to hold however, given the properties of olfactory cues in terms of longevity, spatial association and the need for close inspection to receive specific information [1]. It is likely that olfactory signals are of interest not only to the intended receiver but also to an array of eavesdroppers in the community who seek to gain beneficial information, including predators, prey, competitors and conspecifics. Olfactory cues in particular are vulnerable to eavesdropping, as unlike acoustic and visual cues, odours typically persist in the environment long after the creator has departed [1]. This creates potential for a complex olfactory web of interactions whereby receivers (intended or otherwise) may not only be responding to the signaller, but also to many other potential receivers.
& 2016 The Author(s) Published by the Royal Society. All rights reserved.
% investigated
(a)
2
60 29
dog
cat
40 22 33 *
20
0 control
fox
(b) 4
no. investigations
5 3 8 2 6
5
control
fox
1
0 dog
cat
treatment
Figure 1. (a) The percentage of visited odour-treated plots that were investigated by foxes. The number of visits to each treatment is indicated above the bars. An asterisk indicates an ASR value . j2j. (b) The average number of times a visited plot was investigated. Error bars represent standard error of the mean. The sample size is indicated above the bars.
2. Material and methods This experiment was conducted in a 225 km2 area of the mallee wheatlands near Walpeup, Victoria, Australia where the mammalian predator community consists of foxes (density 0.9– 2.0 km22) [12], feral cats and feral dogs [13]. Roaming domestic farm dogs and cats may also interact with other predators in the area. Cat and dog urine was collected from domestic animals (both genders) during routine surgical patient management at a veterinary hospital. Fox urine was collected from the bladders of foxes (both genders) shot during pest control programmes well outside the study area. Urine was kept frozen at 2208C until use. Predator urine (1 ml; typical volume of a scent mark [5]) was dripped onto 10 30 cm pieces of cotton towel, each towel receiving odour from a different individual. Controls consisted of untreated towels. Forty sand plots (2 m wide and a minimum of 500 m apart (average 650 m) to maintain independence of fox visits [14]; nightly results from adjacent plots were independent; x 2 ¼ 3.12, p ¼ 0.08, n ¼ 112) were created across roads using in situ sand and randomly assigned to an odour treatment (cat, dog, fox or control; n ¼ 10). Odour-treated towels were fixed to the ground with a tent peg on road verges and alternated between road sides to avoid bias. A light coating of sand was sprinkled over the towel to reduce visual conspicuousness. Plots were checked for 6 days for predator tracks, and visitors were identified to species using track characteristics (with reference to [15]). An observer ( J.P.B.) who was blind to the treatment recorded the number of fox footprints within 1 m of the towel and the spatial arrangement of footprints. Investigation of the treatment towel was determined from 10 or more footprints within 1 m of the towel, scats or diggings present within 1 m of the towel, clear change in direction of footprints towards
the towel or obvious disturbance of the towel. All other fox records were considered to be incidental passings. Treatment towels were replaced daily with the same odour treatment.
(a) Statistical analyses We performed a x 2 test of independence using exact probability values to compare the percentage of investigation events by foxes between treatments. Adjusted standardized residuals (ASRs) were calculated to identify where significance could be attributed; ASRs . j2j indicate a lack of fit of the null hypothesis in that cell [16]. To compare the number of fox investigations at an odour plot among treatments, we conducted a one-way pffiffiffiffiffiffiffiffiffiffiffi analysis of variance (ANOVA). Data were transformed ( x þ 1) to meet the assumptions of ANOVA. All statistics were conducted in IBM SPSS STATISTICS v. 22. Only plots that received some form of visitation (incidental or investigation) were included.
3. Results Fox investigation of odour plots was significantly affected by treatment (Pearson’s x 2 ¼ 9.928, d.f. ¼ 3, p ¼ 0.018). Cat and dog odour plots received a high level of investigation, with 52% and 50% of visits respectively resulting in investigation by foxes (ASR ¼ 1.8 and 1.6, respectively; figure 1a). While control plots received some attention (32%, ASR ¼ 20.6), only 18% of fox-treated plots were investigated (ASR ¼ 22.7;
Biol. Lett. 12: 20151053
28
rsbl.royalsocietypublishing.org
The idea that olfactory information can have multiple users to create an olfactory web of interactions has received some theoretical consideration, albeit indirectly [6]. For example, infochemical webs and the ‘crying for help’ hypothesis are based on the direct signals produced by plants suffering herbivory (herbivore-induced plant volatiles) to attract their herbivores’ enemies ( predators or parasitoids) [6]. It is also known that some mammals use olfactory cues produced by competitors [7] as well as conspecifics [8] as cues of interaction with shared predators. Here we investigated the patterns of visitation by red foxes (Vulpes vulpes) to scent marks of two species of competitors: feral cats (Felis catus) and wild dogs (Canis lupus familiaris), as well as conspecifics, to assess the likely risk of fox encounter associated with these odours. Odours from red foxes, cats and dogs have all induced avoidance/fear responses in a wide range of mammalian prey, both in the field and in the laboratory (see review [4]). All of these predators use urine and faeces to maintain territories and are attracted to the odours of conspecifics within their territory to over-mark and signal their presence [5,9], so their odours should represent hotspots of conspecific activity. Like most predators, foxes live in a multi-predator community. There is dietary overlap among foxes, cats and dogs, who compete for food and possibly other resources [10], and likely use each others’ odours to mediate competitive interactions [11]. If foxes eavesdrop on the odour cues of their enemies, we predicted that fox visitation would be high not only at scent marks of unfamiliar foxes, but also at scent marks of cats and dogs, to create an olfactory web of information available for prey to assess their risk of fox encounter.
3
rsbl.royalsocietypublishing.org
apex predators e.g. dog/dingo
conspecific predators i.e. foxes
this study
mesopredator (fox) odour cue
intraguild competitors/predators e.g. cats and quolls
[12]
[12] [12]
conspecific prey
this study
[7,21]
prey individual
interspecific competing prey
Figure 2. An olfactory web of communication among a predator : prey assemblage. Thick lines are direct responses to fox odour cues; thin lines are indirect associations generated by direct responses to foxes by other members of the food web.
figure 1a). The number of investigations to an odour plot also appeared to be higher for dog- and cat-treated plots; although this was not significant (F3,20 ¼ 2.918, p ¼ 0.059; figure 1b), it is nonetheless indicative of a large effect size (h 2 ¼ 0.304). Foxes visited (incidental or investigation) almost all (3940) of the sand plots.
4. Discussion Foxes investigated cat and dog odour 62% and 56% more than untreated controls, respectively. This suggests that odours have a strong role in mediating competitive interactions among these predators. Foxes are likely to be competitively superior to cats (cat populations increase in the absence of foxes [17]) and occasionally kill them [10]. In Australia, wild dogs/dingoes harass and kill foxes [18], compete with them for food [19] and exclude them from other resources such as water [20]. Foxes exhibit small-scale avoidance of dogs [11], and our results suggest that this avoidance behaviour may be facilitated by olfactory cues, which require close investigation to retrieve specific information about competitors. Foxes were least interested in conspecific odour, which was surprising giving its purported use in social interactions, including territorial maintenance and mating [5,9]. We presented fox odours from unfamiliar individuals to represent interloping individuals, which we predicted to induce greater interest than would odours from local foxes [21]. However, foxes were as attracted to interloper scent marks as much as they were to the novelty in odours of an untreated towel. Fox investigation of one-third of the untreated controls suggests
some neophilic attraction to the novelty of the towel, even without the addition of a biologically significant odour. Given that foxes were highly attracted to odours of other predator species, what risk does a predator scent actually signal to eavesdropping prey? Cat and dog odours, in fact, had a higher probability of visitation by foxes than did fox odour. It is likely that fox odour would, in turn, attract other predators such as cats and dogs/dingoes. Thus, anti-predator responses induced by fox odour, e.g. [4], may be a tactic to avoid predation by other eavesdropping predators rather than only the foxes themselves. Predator–prey interactions mediated by olfactory cues are clearly more complex than previously thought and are likely to form a complicated web of interactions akin to a food web (figure 2). Decision-making on whether to visit a particular olfactory cue must take into consideration who else may be eavesdropping on that cue and the potential outcome of an encounter with either the cue creator or an eavesdropper. The concept of an olfactory web predicts that a suite of competitors and predators should all show varying degrees of attraction to and avoidance of each other’s odours, as these social signals are likely to be useful in mediating their interactions with their enemies. This concept undermines the traditional approach used in hundreds of studies examining prey responses to predator odours, which assumes that it is a simple dyadic interaction, with one signaller (predator) and one receiver ( prey) of the information. Before making inferences about the information encoded in the odours of a predator or indeed any species, future studies need to first untangle the potential olfactory web by quantifying visitation rates of all members of an interacting community to their own
Biol. Lett. 12: 20151053
this study
Ethics. This study was conducted in accordance with the Australian code of practice for the care and use of animals for scientific purposes. Research was approved by The University of Sydney Animal Ethics Committee (approval no. 2013/5743). Data accessibility. Data supporting this article are available at the University of Sydney’s eScholarship Repository at http://hdl.handle.net/ 2123/14727.
Authors’ contributions. All authors contributed to the study design and drafted the manuscript. J.P.B. and A.D. carried out the fieldwork. All authors gave approval for publication of the final version and agree to be held accountable for the content herein. Competing interests. We declare we have no competing interests.
Funding. This study was supported by an ARC Discovery grant DP140104413 awarded to P.B.B.
Acknowledgements. We thank the RSPCA and NSW National Parks and Wildlife Service for their assistance in collecting predator odours, and Paul Shanta for assistance in graphic design.
1.
2.
3.
4.
5. 6.
7.
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and each other’s olfactory cues. This is an essential step to provide clarity in our understanding of how eavesdroppers exploit odours in a landscape of risk signalled by olfactory cues.
