Abstract
Neighbour-stranger discrimination is widespread in territorial animals, and depending on the relative threat posed by neighbours and strangers, residents commonly exhibit either the “dear enemy phenomenon” or the “nasty neighbour effect”. Different members of the same group may represent different threat levels, and the response of residents can be modified depending on, e.g. the sex and dominance status of the intruder. Neighbour-stranger discrimination is primarily investigated in neighbours with shared borders, and whether residents recognize their more distant neighbours remains unexplored. Here, using experimental scent marks, we investigated whether Eurasian beavers (Castor fiber) discriminate between distant neighbours (i.e. two territories away) and strangers (i.e. further away than the known dispersal distance). We tested the hypotheses that Eurasian beavers can discriminate between distant neighbours and strangers and that social status (i.e. sub-dominant or dominant) and sex of the intruder affect the responses of resident beavers. We predicted that resident beavers show the “dear enemy phenomenon” in response towards dominant distant neighbours due to their territory ownership and the “nasty neighbour effect” in response towards sub-dominants due to their likelihood to disperse. Sex of residents and social status of intruders were important in explaining territorial responses, with males exhibiting stronger responses to sub-dominant distant neighbours, especially males, than sub-dominant strangers. No such discrimination was found by females or between dominant distant neighbours and strangers. We suggest that the “nasty neighbour” response by male resident beavers towards sub-dominant distant neighbours relates to the relative threat levels due to repeated intrusions during dispersal attempts.
Significance statement
Territorial animals discriminate between neighbours and strangers to allocate aggressive behaviour to conspecific intruders. This neighbour-stranger discrimination has primarily been investigated between adjacent neighbours, but extraterritorial movements of residents into distant territories occur. Whether residents can discriminate between distant neighbours and strangers has only been studied in skylarks (Alauda arvensis), based on acoustic communication. Yet, it is unknown whether distant neighbours are perceived as neighbours or strangers based on olfactory recognition. Here we investigated whether Eurasian beavers (C. fiber) can discriminate between distant neighbours (i.e. two territories away) and strangers, based on olfactory scent samples including information on social status (i.e. dominant or sub-dominant) and sex of the intruder. Our results show that male residents showed a “nasty neighbour” response towards sub-dominant distant neighbours. These findings highlight the sensitivity of territorial mammals to the familiarity and social status of intruders.
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Data availability
The datasets generated and analysed during the current study are available in the USN repository, https://doi.org/10.23642/usn.11197736.v1.
References
Akçay C, Wood WE, Searcy WA, Templeton CN, Campbell SE, Beecher MD (2009) Good neighbour, bad neighbour: song sparrows retaliate against aggressive rivals. Anim Behav 78:97–102
Arnold TW (2010) Uninformative parameters and model selection using Akaike’s information criterion. J Wildl Manag 74:1175–1178
ASAB/ABS (2016) Guidelines for the treatment of animal in behavioural research and teaching. Anim Behav 111:I–IX. https://doi.org/10.1016/S0003-3472(15)00461-3
Barton K (2013) MuMIn: Multi-model inference. R package version 1(43):6 http://www2.uaem.mx/r-mirror/web/packages/MuMIn. Accessed 22 Sept 2019
Bates D, Maechler M, Bolker B, Walker S (2015) Linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135
Booksmythe I, Jennions MD, Backwell PRY (2010) Investigating the 'dear enemy' phenomenon in the territory defence of the fiddler crab, Uca mjoebergi. Anim Behav 7:419–423
Briefer E, Aubin T, Rybak F (2009) Response to displaced neighbours in a territorial songbird with a large repertoire. Naturwissenschaften 96:1067–1077
Briefer E, Rybak F, Aubin T (2010) Are unfamiliar neighbours considered to be dear-enemies? PLoS One 5:e12428
Campbell R (2010) Demography and life history of the Eurasian beaver Castor fiber. PhD thesis, Merton College, Oxford
Campbell RD, Rosell F, Nolet BA, Dijkstra VAA (2005) Territory and group sizes in Eurasian beavers (Castor fiber): echoes of settlement and reproduction? Behav Ecol Sociobiol 58:597–607
Campbell RD, Newman C, Macdonald DW, Rosell F (2013) Proximate weather patterns and spring green-up phenology effect Eurasian beaver (Castor fiber) body mass and reproductive success: the implications of climate change and topography. Glob Chang Biol 19:1311–1324
Carazo P, Font E, Desfilis E (2008) Beyond ‘nasty neighbours' and ‘dear enemies'? Individual recognition by scent marks in a lizard (Podarcis hispanica). Anim Behav 76:1953–1963
Christensen C, Kern JM, Bennitt E, Radford AN (2016) Rival group scent induces changes in dwarf mongoose immediate behavior and subsequent movement. Behav Ecol 27:1627–1634
Crawford JC, Liu Z, Nelson TA, Nielsen CK, Bloomquist CK (2008) Microsatellite analysis of mating and kinship in beavers (Castor canadensis). J Mammal 89:575–581
Crawley MJ (2007) The R book. Wiley, Chichester
Cross HB, Zedrosser A, Nevin O, Rosell F (2014) Sex discrimination via anal gland secretion in a territorial monogamous mammal. Ethology 120:1044–1052
delBarco-Trillo J, McPhee ME, Johnston RE (2011) Syrian hamster males below an age threshold do not elicit aggression from unfamiliar adult males. Aggress Behav 37:91–97
Eppley TM, Ganzhorn JU, Donati G (2016) Latrine behavior as a multimodal communicatory signal station in wild lemurs: the case of Hapalemur meridionalis. Anim Behav 111:57–67
Fawcett JK, Fawcett JM, Soulsbury CD (2013) Seasonal and sex differences in urine marking rates of wild red foxes Vulpes vulpes. J Ethol 31:41–47
Fisher RA (1954) Evolution and bird sociality. In: Huxley J, Hardy AC, Ford EB (eds) Evolution as a process. Allen & Unwin, London, pp 71–83
Gilchrist JS, Otali E (2002) The effects of refuse-feeding on home-range use, group size, and intergroup encounters in the banded mongoose. Can J Zool 80:1795–1802
Gosling L, Roberts S (2001) Scent marking by male mammal: cheat-proof signals to competitors and mates. Adv Study Behav 30:169–217
Graf PM, Wilson RP, Qasem L, Hackländer K, Rosell F (2015) The use of acceleration to code for animal behaviours: a case study in free-ranging Eurasian beavers Castor fiber. PLoS One 10:e0136751
Graf PM, Mayer M, Zedrosser A, Häcklander K, Rosell F (2016) Territory size and age explain movement patterns in the Eurasian beaver. Mamm Biol 81:587–594
Grafen A (1987) The logic of divisively asymmetric contests: respect for ownership and the desperado effect. Anim Behav 35:462–467
Haughland DL, Larsen KW (2004) Exploration correlates with settlement: red squirrel dispersal in contrasting habitats. J Anim Ecol 73:1024–1034
Havens RP (2006) Beaver home ranges and movement patterns on the Embarras River watershed in east Central Illinois. MSc thesis, Eastern Illinois University, Charleston
Herr J, Müller-Schwarze D, Rosell F (2006) Resident beavers (Castor canadensis) do not discriminate between castoreum scent marks from simulated adult and subadult male intruders. Can J Zool 84:615–622
Hohwieler K, Rosell F, Mayer M (2018) Scent-marking behavior by subordinate Eurasian beavers. Ethology 124:591–599
Kroodsma DE, Byers BE, Goodale E, Johnson S, Liu W-C (2001) Pseudoreplication in playback experiments, revisited a decade later. Anim Behav 61:1029–1033
Mayeaux DJ, Johnston RE (2002) Discrimination of individual odours by hamsters (Mesocricetus auratus) varies with the location of those odours. Anim Behav 64:269–281
Mayer M, Zedrosser A, Rosell F (2017a) When to leave: the timing of natal dispersal in a large, monogamous rodent, the Eurasian beaver. Anim Behav 123:375–382
Mayer M, Zedrosser A, Rosell F (2017b) Extra-territorial movements differ between territory holders and subordinates in a large, monogamous rodent. Sci Rep 7:15261
Mech LD, Boitani L (2010) Wolves: behavior, ecology, and conservation. University of Chicago Press, Chicago
Monclús R, Saavedra I, de Miguel J (2014) Context-dependent responses to neighbours and strangers in wild European rabbits (Oryctolagus cuniculus). Behav Process 106:17–21
Müller CA, Manser MB (2007) ‘Nasty neighbours’ rather than ‘dear enemies’ in a social carnivore. Proc R Soc Lond B 274:959–965
Nolet B, Rosell F (1994) Territoriality and time budgets in beavers during sequential settlement. Can J Zool 72:1227–1237
Noonan MJ, Markham A, Newman C, Trigoni N, Buesching CD, Ellwood SA, Macdonald DW (2014) Climate and the individual: inter-annual variation in the autumnal activity of the European badger (Meles meles). PLoS One 9:e83156
Piechocki R (1977) Ökologische Todesursachenforschung am Elbebiber (Castor fiber albicus). Beitr Jagd Wildforsch 10:332–341
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna https://www.R-project.org. Accessed 22 Sept 2019
Radford AN (2005) Group-specific vocal signatures and neighbour-stranger discrimination in the cooperatively breeding green wood hoopoe. Anim Behav 70:1227–1234
Ralls K (1971) Mammalian scent marking. Science 171:443–449
Rayor LS (1985) Effects of habitat quality on growth, age of first reproduction, and dispersal in Gunnison prairie dogs (Cynomys gunnisoni). Can J Zool 63:2835–2840
Rosell F, Bjørkøyli T (2002) A test of the dear enemy phenomenon in the Eurasian beaver. Anim Behav 63:1073–1078
Rosell F, Steifetten Ø (2004) Subspecies discrimination in the Scandinavian beaver (Castor fiber): combining behavioral and chemical evidence. Can J Zool 82:902–909
Rosell F, Sun L (1999) Use of anal gland secretion to distinguish the two beaver species Castor canadensis and Castor fiber. Wildl Biol 5:119–123
Rosell F, Sundsdal L (2001) Odorant source used in Eurasian beaver territory marking. J Chem Ecol 27:2471–2491
Rosell F, Thomsen LR (2006) Sexual dimorphism in territorial scent marking by adult Eurasian beavers (Castor fiber). J Chem Ecol 32:1301–1315
Rosell F, Bergan F, Parker H (1998) Scent-marking in the Eurasian beaver (Castor fiber) as a means of territory defense. J Chem Ecol 24:207–219
Rosell F, Johansen G, Parker H (2000) Eurasian beaver (Castor fiber) behavioral response to simulated territorial intruders. Can J Zool 78:931–935
Rosell F, Zedrosser A, Parker H (2010) Correlates of body measurements and age in Eurasian beaver from Norway. Eur J Wildl Res 56:43–48
Schradin C, Schneider C, Lindholm AK (2010) The nasty neighbour in the striped mouse (Rhabdomys pumilio) steals paternity and elicits aggression. Front Zool 7:19
Schulte B (1998) Scent marking and responses to male castor fluid by beavers. J Mammal 79:191–203
Sharpe F, Rosell F (2003) Time budgets and sex differences in the Eurasian beaver. Anim Behav 66:1059–1067
Soulsbury CD, Baker PJ, Iossa G, Harris S (2008) Fitness costs of dispersal in red foxes (Vulpes vulpes). Behav Ecol Sociobiol 62:1289–1298
Steyaert S, Zedrosser A, Rosell F (2015) Socio-ecological contexts other than sex affect resource selection in the obligate monogamous Eurasian beaver. Oecologia 179:1023–1032
Sun L, Müller-Schwarze D (1997) Sibling recognition in the beaver: a field test for phenotype matching. Anim Behav 54:493–502
Sun L, Müller-Schwarze D, Schulte B (2000) Dispersal pattern and effective population size of the beaver. Can J Zool 78:393–398
Svendsen GE (1989) Pair formation, duration of pair-bonds, and mate replacement in a population of beavers (Castor canadensis). Can J Zool 67:336–340
Temeles EJ (1994) The role of neighbours in territorial systems: when are they “dear enemies”? Anim Behav 47:339–350
Tinnesand HV, Jojola S, Zedrosser A, Rosell F (2013) The smell of desperadoes? Beavers distinguish between dominant and subordinate intruders. Behav Ecol Sociobiol 67:895–904
Tinnesand HV, Buesching CD, Noonan MJ, Newman C, Zedrosser A, Rosell F, Macdonald DW (2015) Will trespassers be prosecuted or assessed according to their merits? A consilient interpretation of territoriality in a group-living carnivore, the European badger (Meles meles). PLoS One 10:e0132432
White M, Swaisgood R, Zhang H (2003) Chemical communication in the giant panda (Ailuropoda melanoleuca): the role of age in the signaller and assessor. J Zool 259:171–178
Wilson EO (1975) Sociobiology: the new synthesis. Harvard University Press, Cambridge
Woodward RL Jr, Bartos K, Ferkin MH (2000) Meadow voles (Microtus pennsylvanicus) and prairie voles (M. ochrogaster) differ in their responses to over-marks from opposite-and same-sex conspecifics. Ethology 106:979–992
Ydenberg RC, Giraldeau L-A, Falls JB (1988) Neighbours, strangers, and the asymmetric war of attrition. Anim Behav 36:343–347
Young AJ, Monfort SL (2009) Stress and the cause of extra-territorial movement in a social carnivore. Biol Lett 5:439–441
Acknowledgments
We gratefully thank Christian A. Robstad, Patricia M. Graf and Yasmin Dawson for help in the field. We would also like to thank the anonymous reviewers for their valuable comments and suggestions to improve the quality of the paper.
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This study was funded by the University of South-Eastern Norway.
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All capture and handling procedures performed in this study involving animals were approved by the Norwegian Directorate for Nature Management (2012/1191 ART-VI-ORD) and the Norwegian Experimental Animal Board (ID 4387). The ASAB/ABS Guidelines for the treatment of animals in behavioural research and teaching were met (ASAB/ABS 2016). None of the animals captured for this study were injured, and all were successfully released at the site of capture after handling. No subsequent long-term effects of capture were observed.
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Benten, A., Cross, H.B., Tinnesand, H.V. et al. Distant neighbours: friends or foes? Eurasian beavers show context-dependent responses to simulated intruders. Behav Ecol Sociobiol 74, 17 (2020). https://doi.org/10.1007/s00265-019-2792-7
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DOI: https://doi.org/10.1007/s00265-019-2792-7