Individual variation in the dear enemy phenomenon via territorial vocalizations in red squirrels

in Behaviour
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?

Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.


Have Institutional Access?

Access content through your institution. Any other coaching guidance?



Territoriality arises when the benefits of resources exceed the costs of defending them. The dear enemy phenomenon, where familiar territorial neighbours refrain from intruding on one another and mutually reduce their defensive efforts, allows for reduction of these costs but requires discrimination between conspecifics. We hypothesized that territorial vocalizations in red squirrels (Tamiasciurus hudsonicus) are used for this discrimination. We performed a speaker replacement experiment where red squirrels (N=41) were temporarily removed from their territories and replaced with a speaker broadcasting their own call, an unfamiliar call, or silence. Contrary to our prediction, there were no differences in overall intrusion risk among our three playbacks, but the identity of intruders did vary. Existing variation in familiarity within territorial neighbourhoods should be considered, rather than the binary classification of familiar or stranger, when studying dear enemy effects. We also discuss the variable importance of silence in acoustic territorial populations.

Individual variation in the dear enemy phenomenon via territorial vocalizations in red squirrels

in Behaviour



  • AkçayÇ.WoodW.E.SearcyW.A.TempletonC.N.CampbellS.E. & BeecherM.D. (2009). Good neighbour, bad neighbour: song sparrows retaliate against aggressive rivals. — Anim. Behav. 78: 97-102.

  • AxelrodR. & HamiltonW.D. (1981). The evolution of cooperation. — Science 211: 1390-1396.

  • BerteauxD. & BoutinS. (2000). Breeding dispersal in female North American red squirrels. — Ecology 81: 1311-1326.

  • BooksmytheI.JennionsM.D. & BackwellP.R.Y. (2010). Investigating the “dear enemy” phenomenon in the territory defence of the fiddler crab, Uca mjoebergi. — Anim. Behav. 79: 419-423.

  • BoutinS. & SchweigerS. (1988). Manipulation of intruder pressure in red squirrels (Tamiasciurus hudsonicus): effects on territory size and acquisition. — Can. J. Zool. 66: 2270-2274.

  • BoutinS.WautersL.A.McAdamA.G.HumphriesM.M.TosiG. & DhondtA.A. (2006). Anticipatory reproduction and population growth in seed predators. — Science 314: 1928-1930.

  • BrehenyP. & BurchettW. (2017). visreg: visualization of regression models. R package version 2.4-1. — Available online at

  • BrieferE.AubinT.LehongreK. & RybakF. (2008a). How to identify dear enemies: the group signature in the complex song of the skylark Alauda arvensis. — J. Exp. Biol. 211: 317-326.

  • BrieferE.RybakF. & AubinT. (2008b). When to be a dear enemy: flexible acoustic relationships of neighbouring skylarks, Alauda arvensis. — Anim. Behav. 76: 1319-1325.

  • CarpenterF. & MacMillenR. (1976). Threshold model of feeding territoriality and test with a Hawaiian honeycreeper. — Science 194: 639-642.

  • DantzerB.BoutinS.HumphriesM.M. & McAdamA.G. (2012). Behavioral responses of territorial red squirrels to natural and experimental variation in population density. — Behav. Ecol. Sociobiol. 66: 865-878.

  • DantzerB.NewmanA.E.M.BoonstraR.PalmeR.BoutinS.HumphriesM.M. & McAdamA.G. (2013). Density triggers maternal hormones that increase adaptive offspring growth in a wild mammal. — Science 340: 1215-1217.

  • DigweedS.M.RendallD. & ImbeauT. (2012). Who’s your neighbor? Acoustic cues to individual identity in red squirrel Tamiasciurus hudsonicus rattle calls. — Curr. Zool. 58: 758-764.

  • DonaldJ.L. & BoutinS. (2011). Intraspecific cache pilferage by larder-hoarding red squirrels (Tamiasciurus hudsonicus). — J. Mammal. 92: 1013-1020.

  • FisherJ. (1954). Evolution and bird sociality. — In: Evolution as a process (HuxleyJ.HardyA. & FordE. eds). Allen & UnwinLondon p. 71-83.

  • HardouinL.A.TabelP. & BretagnolleV. (2006). Neighbour-stranger discrimination in the little owl, Athene noctua. — Anim. Behav. 72: 105-112.

  • HeinemannD. (1992). Resource use, energetic profitability, and behavioral decisions in migrant rufous hummingbirds. — Oecologia 90: 137-149.

  • JaegerR.G. (1981). Dear enemy recognition and the costs of aggression between salamanders. — Am. Nat. 117: 962-974.

  • KorenL. & GeffenE. (2011). Individual identity is communicated through multiple pathways in male rock hyrax (Procavia capensis) songs. — Behav. Ecol. Sociobiol. 65: 675-684.

  • KuznetsovaA.BrockhoffP.B. & ChristensenR.H.B. (2016). lmerTest: tests in linear mixed effects models. — R package version 2.0-33. Available online at

  • LamontagneJ.M. & BoutinS. (2007). Local-scale synchrony and variability in mast seed production patterns of Picea glauca. — J. Ecol. 95: 991-1000.

  • LarsenK.W. & BoutinS. (1995). Exploring territory quality in the North American red squirrel through removal experiments. — Can. J. Zool. 73: 1115-1122.

  • LeiserJ. & ItzkowitzM. (1999). The benefits of dear enemy recognition in three-contender convict cichlid (Cichlasoma nigrofasciatum) contests. — Behaviour 136: 983-1003.

  • McAdamA.G. & BoutinS. (2003). Variation in viability selection among cohorts of juvenile red squirrels (Tamiasciurus hudsonicus). — Evolution 57: 1689-1697.

  • McAdamA.G.BoutinS.SykesA.K. & HumphriesM.M. (2007). Life histories of female red squirrels and their contributions to population growth and lifetime fitness. — Ecoscience 14: 362.

  • MonclúsR.SaavedraI. & de MiguelJ. (2014). Context-dependent responses to neighbours and strangers in wild European rabbits (Oryctolagus cuniculus). — Behav. Process. 106: 17-21.

  • MüllerC.A. & ManserM.B. (2007). “Nasty neighbours” rather than “dear enemies” in a social carnivore. — Proc. Roy. Soc. Lond. B: Biol. Sci. 274: 959-965.

  • PriceK.BoutinS. & YdenbergR. (1990). Intensity of territorial defence in red squirrels: an experimental test of the asymmetric war of attrition. — Behav. Ecol. Sociobiol. 27: 348-350.

  • PriceK.BroughtonK.BoutinS. & SinclairA.R.E. (1986). Territory size and ownership in red squirrels: response to removals. — Can. J. Zool. 64: 1144-1147.

  • PuckettK.J. & DillL.M. (1985). The energetics of feeding territoriality in juvenile coho salmon (Oncorhynchus kisutch). — Behaviour 92: 97-111.

  • QuallsC.P. & JaegerR.G. (1991). Dear enemy recognition in Anolis carolinenis. — J. Herpetol. 25: 361-363.

  • R Core Team (2017). R: a language and environment for statistical computing. — R Foundation for Statistical ComputingViennaavailable online at

  • RandlerC. (2006). Red squirrels (Sciurus vulgaris) respond to alarm calls of Eurasian jays (Garrulus glandarius). — Ethology 112: 411-416.

  • RaynaudJ. & DobsonS.F. (2011). Scent communication by female Columbian ground squirrels, Urocitellus columbianus. — Behav. Ecol. Sociobiol. 65: 351-358.

  • RosellF. & BjørkøyliT. (2002). A test of the dear enemy phenomenon in the Eurasian beaver. — Anim. Behav. 63: 1073-1078.

  • RosellF.GundersenG. & Le GalliardJ.F. (2008). Territory ownership and familiarity status affect how much male root voles (Microtus oeconomus) invest in territory defence. — Behav. Ecol. Sociobiol. 62: 1559-1568.

  • ShonfieldJ.GorrellJ.C.ColtmanD.W.BoutinS.HumphriesM.M.WilsonD.R. & McAdamA.G. (2017). Using playback of territorial calls to investigate mechanisms of kin discrimination in red squirrels. — Behav. Ecol. 28: 382-390.

  • SiracusaE.R. (2018). Effects of the social environment on the behaviour and fitness of a territorial squirrel. — Ph.D. Thesis University of Guelph Guelph.

  • SiracusaE.BoutinS.HumphriesM.M.GorrellJ.C.ColtmanD.W.DantzerB.LaneJ.E. & McadamA.G. (2017a). Familiarity with neighbours affects intrusion risk in territorial red squirrels. — Anim. Behav. 133: 11-20.

  • SiracusaE.MorandiniM.BoutinS.HumphriesM.M.DantzerB.LaneJ.E. & McAdamA.G. (2017b). Red squirrel territorial vocalizations deter intrusions by conspecific rivals. — Behaviour 154: 1259-1273.

  • SmithC.C. (1968). The adaptive nature of social organization in the genus of tree squirrels Tamiasciurus. — Ecol. Monogr. 38: 31-64.

  • SmithC.C. (1978). Structure and function of the vocalizations of tree squirrels (Tamiasciurus). — J. Mammal. 59: 793-808.

  • Stuart-SmithA.K. & BoutinS. (1994). Costs of escalated territorial defence in red squirrels. — Can. J. Zool. 72: 1162-1167.

  • StuddE.K.BoutinS.McAdamA.G.KrebsC.J. & HumphriesM.M. (2015). Predators, energetics and fitness drive neonatal reproductive failure in red squirrels. — J. Anim. Ecol. 84: 249-259.

  • StuddE.K.BoutinS.McAdamA.G. & HumphriesM.M. (2016). Nest attendance of lactating red squirrels (Tamiasciurus hudsonicus): influences of biological and environmental correlates. — J. Mammal. 97: 806-814.

  • TemelesE.J. (1994). The role of neighbours in territorial systems: when are they “dear enemies”? — Anim. Behav. 47: 339-350.

  • TherneauT.M. (2015). coxme: mixed effects cox models. — R package version 2.2-5. Available online at

  • VachéM.FerronJ. & GouatP. (2001). The ability of red squirrels (Tamiasciurus hudsonicus) to discriminate conspecific olfactory signatures. — Can. J. Zool. 79: 1296-1300.

  • WeiM.LloydH. & ZhangY. (2011). Neighbour-stranger discrimination by yellow-bellied tit Parus venustulus: evidence for the “dear-enemy” effect. — J. Ornithol. 152: 431-438.

  • WilliamsC.T.WilstermanK.KelleyA.D.BretonA.R.StarkH.HumphriesM.M.McAdamA.G.BarnesB.M.BoutinS. & BuckC.L. (2014). Light loggers reveal weather-driven changes in the daily activity patterns of arboreal and semifossorial rodents. — J. Mammology 95: 1230-1239.

  • WilsonD.R.GobleA.R.BoutinS.HumphriesM.M.ColtmanD.W.GorrellJ.C.ShonfieldJ. & McAdamA.G. (2015). Red squirrels use territorial vocalizations for kin discrimination. — Anim. Behav. 107: 79-85.

  • ZenutoR.R. (2010). Dear enemy relationships in the subterranean rodent Ctenomys talarum: the role of memory of familiar odours. — Anim. Behav. 79: 1247-1255.


  • View in gallery

    Cox proportional hazard model of intrusion by neighbours, incorporating whether or not an intrusion occurred with the latency to that intrusion event. There were no differences in intrusion hazard between owner playback and silence (z=0.15, p=0.88) or owner and unfamiliar playbacks (z=1.48, p=0.14).

  • View in gallery

    Proportion of trials across three playback treatments where a neighbour (black) or non-neighbouring (grey) squirrel intruded during a 2-hour temporary removal. There were no significant differences between playbacks when considering all trials, only neighbour intrusions, or only non-neighbour intrusions.

  • View in gallery

    Relative hazard of intrusion by individual neighbouring squirrels during a temporary removal, under three audio treatments. Intrusion hazard is modelled using a mixed effects Cox proportional hazard model, accounting for the latency to an intrusion event and whether or not one occurred within the two-hour temporary removal; a high hazard corresponds to a shorter latency and higher probability of intrusion. There was a higher hazard of intrusion from relatively unfamiliar neighbours when broadcasting the owner’s rattle (β=1.05, z=2.82, p=0.005), whereas relative familiarity did not affect the hazard of intrusion during silence (β=0.16, z=0.49, p=0.63) or unfamiliar rattle playbacks (β=0.07, z=0.15, p=0.88).

  • View in gallery

    Standardized familiarity (z-scores, relative to neighbourhood) of intruding neighbours during temporary removals when broadcasting the owner’s call (N=9), silence (N=14), or an unfamiliar call (N=6). Standardized familiarity for intruders on the owner’s rattle was different from zero (t=2.85, df = 23, p=0.009), but this was not the case for either of the other two groups (silence: t=0.84, df = 23, p=0.41; unfamiliar: t=0.03, df = 23, p=0.97).

  • View in gallery

    Comparison of (a) local density and (b) familiarity within 130 m of focal squirrels used for temporary removal experiments in 2015 (N=55) and 2017 (N=41). With two further years of very low cone production since the 2014 mast event, population density has fallen with the lack of new food resources while average familiarity in 2017 has accrued as there was minimal recruitment of juveniles during this period.

Index Card

Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 116 116 14
Full Text Views 105 105 2
PDF Downloads 22 22 0
EPUB Downloads 0 0 0