Annals of Occupational and Environmental Medicine | |
Differential behavioural and endocrine responses of common voles (Microtus arvalis) to nest predators and resource competitors | |
Monique Liesenjohann2  Thilo Liesenjohann2  Rupert Palme1  Jana Anja Eccard2  | |
[1] Department of Natural Sciences – Biochemistry, University of Veterinary Medicine, Veterinaer-Platz 1, A-1210 Vienna, Austria | |
[2] Department of Animal Ecology, University of Potsdam, Maulbeerallee 1, D-14469 Potsdam, Germany | |
关键词: Voles; Shrews; Burrow system; Faecal corticosterone metabolites; Stress response; Nest predation; Interspecific interactions; Small mammals; Behavioural adaptations; | |
Others : 1085189 DOI : 10.1186/1472-6785-13-33 |
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received in 2013-04-12, accepted in 2013-09-04, 发布年份 2013 | |
【 摘 要 】
Background
Adaptive behavioural strategies promoting co-occurrence of competing species are known to result from a sympatric evolutionary past. Strategies should be different for indirect resource competition (exploitation, e.g., foraging and avoidance behaviour) than for direct interspecific interference (e.g., aggression, vigilance, and nest guarding). We studied the effects of resource competition and nest predation in sympatric small mammal species using semi-fossorial voles and shrews, which prey on vole offspring during their sensitive nestling phase. Experiments were conducted in caged outdoor enclosures. Focus common vole mothers (Microtus arvalis) were either caged with a greater white-toothed shrew (Crocidura russula) as a potential nest predator, with an herbivorous field vole (Microtus agrestis) as a heterospecific resource competitor, or with a conspecific resource competitor.
Results
We studied behavioural adaptations of vole mothers during pregnancy, parturition, and early lactation, specifically modifications of the burrow architecture and activity at burrow entrances. Further, we measured pre- and postpartum faecal corticosterone metabolites (FCMs) of mothers to test for elevated stress hormone levels. Only in the presence of the nest predator were prepartum FCMs elevated, but we found no loss of vole nestlings and no differences in nestling body weight in the presence of the nest predator or the heterospecific resource competitor. Although the presence of both the shrew and the field vole induced prepartum modifications to the burrow architecture, only nest predators caused an increase in vigilance time at burrow entrances during the sensitive nestling phase.
Conclusion
Voles displayed an adequate behavioural response for both resource competitors and nest predators. They modified burrow architecture to improve nest guarding and increased their vigilance at burrow entrances to enhance offspring survival chances. Our study revealed differential behavioural adaptations to resource competitors and nest predators.
【 授权许可】
2013 Liesenjohann et al.; licensee BioMed Central Ltd.
【 预 览 】
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Figure 1. | 47KB | Image | download |
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【 参考文献 】
- [1]Connell J: Diversity and the coevolution of competitors, or the ghost of competition past. Oikos 1980, 35(2):131-138.
- [2]Mitchell WA, Abramsky Z, Kotler BP, Pinshow B, Brown JS: The effect of competition on foraging activity in desert rodents - theory and experiments. Ecology 1990, 71(3):844-854.
- [3]Amarasekare P: Interference competition and species coexistence. Proc Royal Soc 2002, 269(1509):2541-2550.
- [4]Peiman KS, Robinson BW: Ecology and evolution of resource-related heterospecific aggression. Q Rev Biol 2010, 85(2):133-158.
- [5]Eccard JA, Ylönen H: Direct interference or indirect exploitation? An experimental study of fitness costs of interspecific competition in voles. Oikos 2002, 99(3):580-590.
- [6]Eccard JA, Ylönen H: Interspecific competition in small rodents: from populations to individuals. Evol Ecol 2003, 17(4):423-440.
- [7]Martin TE: Fitness costs of resource overlap among coexisting bird species. Nature 1996, 380(6572):338-340.
- [8]Archer J: The behavioural biology of aggression. Cambridge: Cambridge University Press; 1988.
- [9]Palomares F, Caro TM: Interspecific killing among mammalian carnivores. Am Nat 1999, 153(5):492-508.
- [10]Martin TE: Avian life-history evolution in relation to nest sites, nest predation, and food. Ecol Monogr 1995, 65(1):101-127.
- [11]Martin TE: Avian life-history evolution has an eminent past: Does it have a bright future? Auk 2004, 121(2):289-301.
- [12]Martin TE, Li PJ: Life-history traits of open-nesting vs cavity-nesting birds. Ecology 1992, 73(2):579-592.
- [13]Montgomerie RD, Weatherhead PJ: Risks and rewards of nest defense by parent birds. Q Rev Biol 1988, 63(2):167-187.
- [14]Ricklefs RE: Natural selection and development of mortality rates in young birds. Nature 1969, 223(5209):922.
- [15]Martin TE: Nest predation and nest sites - new perspectives on old patterns. Bioscience 1993, 43(8):523-532.
- [16]Sih A, Crowley P, Mcpeek M, Petranka J, Strohmeier K: Predation, competition, and prey communities - a review of field experiments. Annu Rev Ecol Evol Syst 1985, 16:269-311.
- [17]Hansell M: Bird nests and construction behaviour. Cambridge, U.K.: Cambridge University Press; 2000.
- [18]Lima SL: Predators and the breeding bird: behavioral and reproductive flexibility under the risk of predation. Biol Rev 2009, 84(3):485-513.
- [19]Martin TE, Roper JJ: Nest predation and nest-site selection of a western population of the hermit thrush. Condor 1988, 90(1):51-57.
- [20]Lima SL: Stress and decision making under the risk of predation: Recent developments from behavioral, reproductive, and ecological perspectives. Stress and Behavior 1998, 27:215-290.
- [21]Schoener TW: Field experiments on interspecific competition. Am Nat 1983, 122(2):240-285.
- [22]Ziv Y, Abramsky Z, Kotler BP, Subach A: Interference competition and temporal and habitat partitioning in 2 gerbil species. Oikos 1993, 66(2):237-246.
- [23]Wolff JO: Why are female small mammals territorial. Oikos 1993, 68(2):364-370.
- [24]Kinlaw A: A review of burrowing by semi-fossorial vertebrates in arid environments. J Arid Environ 1999, 41(2):127-145.
- [25]Andersson M, Wiklund CG, Rundgren H: Parental defense of offspring - a model and an example. Anim Behav 1980, 28(May):536-542.
- [26]Clutton-Brock: The evolution of parental care. Princeton: Princeton University Press; 1991.
- [27]Trivers RL: Mother-offspring conflict. Am Zool 1972, 12(4):648-648.
- [28]Lima SL, Valone TJ, Caraco T: Foraging-efficiency predation-risk trade-off in the Grey squirrel. Anim Behav 1985, 33(Feb):155-165.
- [29]Stearns SC: Trade-offs in life-history evolution. Funct Ecol 1989, 3(3):259-268.
- [30]Magnhagen C: Conflicting demands in gobies - when to eat, reproduce, and avoid predators. Mar Behav Physiol 1993, 23(1–4):79-90.
- [31]Swaisgood RR, Rowe MP, Owings DH: Antipredator responses of California ground squirrels to rattlesnakes and rattling sounds: the roles of sex, reproductive parity, and offspring age in assessment and decision-making rules. Behav Ecol Sociobiol 2004, 55(4):410-413.
- [32]Ylönen H, Horne T: Infanticide and effectiveness of pup protection in bank voles: does the mother recognise a killer? Acta ethologica 2002, 4(2):97-101.
- [33]Koskela E, Juutistenaho P, Mappes T, Oksanen TA: Offspring defence in relation to litter size and age: Experiment in the bank vole Clethrionomys glareolus. Evol Ecol 2000, 14(2):99-109.
- [34]Monclus R, Rödel HG: Influence of different individual traits on vigilance behaviour in European rabbits. Ethology 2009, 115(8):758-766.
- [35]Wolff RJ: Mating behavior and female choice - their relation to social-structure in wild caught house mice (Mus musculus) housed in a semi-natural environment. J Zool 1985, 207(Sep):43-51.
- [36]Dale S, Gustavsen R, Slagsvold T: Risk taking during parental care: A test of three hypotheses applied to the pied flycatcher. Behav Ecol Sociobiol 1996, 39(1):31-42.
- [37]Listoen C, Karlsen RF, Slagsvold T: Risk taking during parental care: a test of the harm-to-offspring hypothesis. Behav Ecol 2000, 11(1):40-43.
- [38]Getz L, Larson C, Lindstrom K: Blarina brevicauda as a predator on nestling voles. J Mammal 1992, 73(3):591-596.
- [39]Fulk G: Effect of shrews on space utilization of voles. J Mammal 1972, 53(3):461.
- [40]Hawlena D, Schmitz OJ: Physiological stress as a fundamental mechanism linking predation to ecosystem functioning. Am Nat 2010, 176(5):537-556.
- [41]Cresswell W: Nest predation: The relative effects of nest characteristics, clutch size and parental behaviour. Anim Behav 1997, 53:93-103.
- [42]Lomascolo SB, Monmany AC, Malizia A, Martin TE: Flexibility in nest-site choice and nesting success of Turdus rufiventris (Turdidae) in a montane forest in Northwestern Argentina. Wilson J Ornithol 2010, 122(4):674-680.
- [43]Smith AP, Quin DG: Patterns and causes of extinction and decline in Australian conilurine rodents. Biol Conserv 1996, 77(2–3):243-267.
- [44]Bronner GN: Burrow system characteristics of seven small mammal species (Mammalia: Insectivora; Rodentia; Carnivora). Koedoe 1992, 35(1):125-128.
- [45]Harper S, Batzli G: Effects of predators on structure of the burrows of voles. J Mammal 1996, 77(4):1114-1121.
- [46]Rödel HG, Starkloff A, Seltmann MW, Prager G, von Holst D: Causes and predictors of nest mortality in a European rabbit population. Mamm Biol 2009, 74(3):200-211.
- [47]Monclus R, Rödel HG, von Holst D: Fox odour increases vigilance in European rabbits: A study under semi-natural conditions. Ethology 2006, 112(12):1186-1193.
- [48]Monclus R, Rödel HG, Von Holst D, De Miguel J: Behavioural and physiological responses of naive European rabbits to predator odour. Anim Behav 2005, 70:753-761.
- [49]Reynolds TD, Wakkinen WL: Characteristics of the burrows of 4 species of rodents in undisturbed soils in southeastern Idaho. Am Midl Nat 1987, 118(2):245-250.
- [50]Eilam D, Dayan T, Ben-Eliyahu S, Schulman I, Shefer G, Hendrie CA: Differential behavioural and hormonal responses of voles and spiny mice to owl calls. Anim Behav 1999, 58:1085-1093.
- [51]Wingfield JC, Ramenofsky M: Hormones and the behavioral ecology of stress. Sheffield: Sheffield Academic; 1999.
- [52]Blanchard RJ, Nikulina JN, Sakai RR, McKittrick C, McEwen B, Blanchard DC: Behavioral and endocrine change following chronic predatory stress. Physiol Behav 1998, 63(4):561-569.
- [53]Monclus R, Rödel HG, Palme R, Von Holst D, de Miguel J: Non-invasive measurement of the physiological stress response of wild rabbits to the odour of a predator. Chemoecology 2006, 16(1):25-29.
- [54]Sheriff MJ, Dantzer B, Delehanty B, Palme R, Boonstra R: Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 2011, 166(4):869-887.
- [55]Ylönen H, Eccard JA, Jokinen I, Sundell J: Is the antipredatory response in behaviour reflected in stress measured in faecal corticosteroids in a small rodent? Behav Ecol Sociobiol 2006, 60(3):350-358.
- [56]Bajkowska U, Chetnicki W, Fedyk S: Breeding of the common shrew, Sorex araneus, under laboratory conditions. Folia Zool 2009, 58(1):1-8.
- [57]Churchfield S: The natural history of shrews. London: Christopher Helm (Publishers) Ltd; 1990.
- [58]Niethammer J, Krapp F: Handbuch der Säugetiere Europas - Rodentia II. 2/I, 1 edition. Wiesbaden: Akademische Verlagsgesellschaft; 1982.
- [59]Churchfield S: Subterranean foraging and burrowing activity of the common shrew. Acta Theriol 1980, 25(32–4):451-459.
- [60]Ruzic A: Spitzmäuse als Räuber der Feldmaus Microtus arvalis (Pallas, 1779). Säugetierkundliche Mitteilungen 1971, 19:366-370.
- [61]Liesenjohann M, Liesenjohann T, Trebaticka L, Haapakoski M, Sundell J, Ylonen H, Eccard JA: From interference to predation: type and effects of direct interspecific interactions of small mammals. Behav Ecol Sociobiol 2011, 65(11):2079-2089.
- [62]Mayer AD: Maternal responsiveness and nest defense during the prepartum period in laboratory rats. Ann N Y Acad Sci 1986, 474:216-225.
- [63]Mclean IG: Plugging of nest burrows by female Spermophilus columbianus. J Mammal 1978, 59(2):437-439.
- [64]Caine NG, Weldon PJ: Responses by red-bellied tamarins (Saguinus labiatus) to fecal scents of predatory and non-predatory neotropical mammals. Biotropica 1989, 21(2):186-189.
- [65]Roberts SC: Social influences on vigilance in rabbits. Anim Behav 1988, 36:905-913.
- [66]Laundre JW, Hernandez L, Altendorf KB: Wolves, elk, and bison: reestablishing the “landscape of fear” in Yellowstone National Park, USA. Canadian Journal of Zoology-Revue Canadienne De Zoologie 2001, 79(8):1401-1409.
- [67]Murray DL: Differential body condition and vulnerability to predation in snowshoe hares. J Anim Ecol 2002, 71(4):614-625.
- [68]Winnie J, Creel S: Sex-specific behavioural responses of elk to spatial and temporal variation in the threat of wolf predation. Anim Behav 2007, 73:215-225.
- [69]Jones M, Dayan T: Foraging behavior and microhabitat use by spiny mice, Acomys cahirinus and A. russatus, in the presence of Blanford’s fox (Vulpes cana) odor. J Chem Ecol 2000, 26(2):455-469.
- [70]Connell JH: On the prevalence and relative importance of interspecific competition - evidence from field experiments. Am Nat 1983, 122(5):661-696.
- [71]Harper J, Austad S: Effect of capture and season on fecal glucocorticoid levels in deer mice (Peromyscus maniculatus) and red-backed voles (Clethrionomys gapperi). Gen Comp Endocrinol 2001, 123(3):337-344.
- [72]Touma C, Palme R, Sachser N: Analyzing corticosterone metabolites in fecal samples of mice: a noninvasive technique to monitor stress hormones. Horm Behav 2004, 45(1):10-22.
- [73]Touma C, Sachser N, Mostl E, Palme R: Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. Gen Comp Endocrinol 2003, 130(3):267-278.
- [74]Eccard JA, Liesenjohann T: Foraging decisions in risk-uniform landscapes. PLoS One 2008., 3(10) doi:10.1371/journal.pone.0003438