Avian predation on a parasitic fly of cervids during winter: Can host-related cues increase the predation risk?

Biological Journal of the Linnean Society

Volumn 106, Issue 2, 2012, Pages 275-286

  Kaunisto, Sirpa ^a   Välimäki, Panu ^b   Kortet, Raine ^a   Koskimäki, Jani ^b   Härkönen, Sauli ^c   Kaitala, Arja ^b   Laaksonen, Sauli ^d   Härkönen, Laura ^b   Ylönen, Hannu ^e  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b UNIVERSITY OF OULU   (Finland)

^c Finnish Wildlife Agency   (Finland)

^d UNIVERSITY OF HELSINKI   (Finland)

^e UNIVERSITY OF JYVÄSKYLÄ   (Finland)

Author keywords

Bedding sites; Blood feeding; Ectoparasite; Hippoboscidae; Invasive species; Moose; Parasitism; Tits

Indexed keywords

BEDDING PLANE; BEHAVIORAL RESPONSE; BIOTIC FACTOR; DEER; ECTOPARASITE; FLY; GEOGRAPHICAL REGION; HEMOPHAGY; INVASIVE SPECIES; PARASITE INFESTATION; PARASITE PREVALENCE; PARASITISM; POPULATION DISTRIBUTION; POPULATION DYNAMICS; PREDATION; PREDATION RISK; PUPA; SONGBIRD;

FINLAND; NORTHERN EUROPE;

AVES; CERVIDAE; HIPPOBOSCIDAE; LIPOPTENA CERVI; TACHINIDAE;

EID: 84859917973     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2012.01869.x     Document Type: Article

References (67)

1. Aitchison CW. 1987. Review of winter trophic relations of soricine shrews. Mammal Review 17: 1-24.
2. Alatalo RV. 1980. Seasonal dynamics of resource partitioning among foliage-gleaning passerines in northern Finland. Oecologia 45: 190-196.
3. Alatalo RV. 1982. Multidimensional foraging niche organization of foliage-gleaning birds in northern Finland. Ornis Scandinavica 13: 56-71.
4. Allen JA, Anderson KP. 1984. Selection by passerine birds is anti-apostatic at high prey density. Biological Journal of the Linnean Society 23: 237-246.
5. Barbaro L, Battisti A. 2011. Birds as predators of the pine processionary moth (Lepidoptera: Notodontidae). Biological Control 56: 107-114.
6. Barber NA, Marquis RJ, Tori WP. 2008. Invasive prey impacts the abundance and distribution of native predators. Ecology 89: 2678-2683.
7. Bates D, Maechler M. 2009. lme4. Linear mixed-effects models using S4 classes. R Package, Version 0.999375-32. Available at:
8. Bennett ATD, Cuthill IC. 1994. Ultraviolet vision in birds: what is its function? Vision Research 34: 1471-1478.
9. Bequaert JC. 1953. The Hippoboscidae or louse-flies (Diptera) of mammals and birds. Part I. Structure, physiology and natural history. Entomologica Americana 32: 1-209.
10. Brotons L. 1997. Changes in foraging behaviour of the coal tit Parus ater due to snow cover. Ardea 85: 249-257.
11. Brotons L, Herrando S. 2003. Effect of increased food abundance near forest edges on flocking patterns of coal tit Parus ater winter groups in mountain coniferous forests. Bird Study 50: 106-111.
12. Carlsson NOL, Sarnelle O, Strayer DL. 2009. Native predators and exotic prey - an acquired taste? Frontiers in Ecology and the Environment 7: 525-532.
13. Church SC, Bennett ATD, Cuthill IC, Partridge JC. 1998. Ultraviolet cues affect the foraging behaviour of blue tits. Proceedings of the Royal Society B: Biological Sciences 265: 1509-1514.
14. Coulson RN, Witter JA. 1984. Forest entomology: ecology and management. New York: John Wiley & Sons, Inc.
15. Dehio C, Sauder U, Hiestand R. 2004. Isolation of Bartonella schoenbuchensis from Lipoptena cervi, a blood-sucking arthropod causing deer ked dermatitis. Journal of Clinical Microbiology 42: 5320-5323.
16. Dolby AS, Grubb TC. 2000. Social context affects risk taking by a satellite species in a mixed-species foraging group. Behavioral Ecology 11: 110-114.
17. Forsman JT, Hjernquist MB, Gustafsson L. 2009. Experimental evidence for the use of density based interspecific social information in forest birds. Ecography 32: 539-545.
18. Fowler AC, Knight RL, George TL, McEwen LC. 1991. Effects of avian predation on grasshopper populations in North Dakota grasslands. Ecology 72: 1775-1781.
19. Frank JH. 1967. The effect of pupal predators on a population of winter moth, Operophtera brumata (L.) (Hydriomenidae). Journal of Animal Ecology 36: 611-621.
20. Haarløv N. 1964. Life cycle and distribution pattern of Lipoptena cervi (L.) (Dipt., Hippobosc.) on Danish deer. Oikos 15: 93-129.
21. Hackman W, Rantanen T, Vuojolahti P. 1983. Immigration of Lipoptena cervi (Diptera, Hippoboscidae) in Finland, with notes on its biology and medical significance. Notulae Entomologicae 63: 53-59.
22. Hansson L, Henttonen H. 1985. Gradients in density variations of small rodents: the importance of latitude and snow cover. Oecologia 67: 394-402.
23. Härkönen L, Härkönen S, Kaitala A, Kaunisto S, Kortet R, Laaksonen S, Ylönen H. 2010. Predicting range expansion of an ectoparasite - the effect of spring and summer temperatures on deer ked Lipoptena cervi (Diptera: Hippoboscidae) performance along a latitudinal gradient. Ecography 33: 906-912.
24. Hastings FL, Hain FP, Smith HR, Cook SP, Monahan JF. 2002. Predation of gypsy moth (Lepidoptera: Lymantriidae) pupae in three ecosystems along the southern edge of infestation. Environmental Entomology 31: 668-675.
25. Heinrich B, Collins SL. 1983. Caterpillar leaf damage, and the game of hide-and-seek with birds. Ecology 64: 592-602.
26. Jansson C, von Brömssen A. 1981. Winter decline of spiders and insects in spruce Picea abies and its relation to predation by birds. Ecography 4: 82-93.
27. Kaunisto S, Härkönen L, Niemelä P, Roininen H, Ylönen H. 2011. Northward invasion of the parasitic deer ked (Lipoptena cervi), is there geographical variation in pupal size and development duration? Parasitology 138: 354-363.
28. Kaunisto S, Kortet R, Härkönen L, Härkönen S, Ylönen H, Laaksonen S. 2009. New bedding site examination-based method to analyse deer ked (Lipoptena cervi) infection in cervids. Parasitology Research 104: 919-925.
29. Koivula K, Rytkönen S, Orell M. 1995. Hunger-dependency of hiding behaviour after a predator attack in dominant and subordinate willow tits. Ardea 83: 397-404.
30. Koivula M, Korpimäki E. 2001. Do scent marks increase predation risk of microtine rodents? Oikos 95: 275-281.
31. Kortet R, Härkönen L, Hokkanen P, Härkönen S, Kaitala A, Kaunisto S, Laaksonen S, Kekäläinen J, Ylönen H. 2010. Experiments on the ectoparasitic deer ked that often attacks humans: preferences for body parts, colour and temperature. Bulletin of Entomological Research 100: 279-285.
32. Kotiaho JS, Sulkava P. 2007. Effects of isolation, area and predators on invasion: a field experiment with artificial islands. Applied Soil Ecology 35: 256-259.
33. Krebs JR, Davies NB. 1993. An introduction to behavioural ecology, 3rd edn. Oxford: Blackwell Science Ltd.
34. Krebs JR, Erichsen JT, Webber MI, Charnov EL. 1977. Optimal prey selection in the great tit (Parus major). Animal Behaviour 25: 30-38.
35. Kynkäänniemi SM, Kortet R, Härkönen L, Kaitala A, Paakkonen T, Mustonen AM, Nieminen P, Härkönen S, Ylönen H, Laaksonen S. 2010. Threat of an invasive parasitic fly, the deer ked (Lipoptena cervi), to the reindeer (Rangifer tarandus tarandus): experimental infection and treatment. Annales Zoologici Fennici 47: 28-36.
36. Lahti K, Orell M, Rytkönen S, Koivula K. 1998. Time and food dependence in willow tit winter survival. Ecology 79: 2904-2916.
37. Lockwood JL, Hoopes MF, Marchetti MP. 2007. Invasion ecology. Oxford: Blackwell Publishing.
38. Maa TC. 1969. A revised checklist and concise host index of Hippoboscidae (Diptera). Pacific Insects Monograph 20: 261-299.
39. Mäntylä E, Alessio GA, Blande JD, Heijari J, Holopainen JK, Laaksonen T, Piirtola P, Klemola T. 2008. From plants to birds: higher avian predation rates in trees responding to insect herbivory. PLoS ONE 3: 2832.
40. Matsumoto K, Berrada ZL, Klinger E, Goethert HK, Telford SR III. 2008. Molecular detection of Bartonella schoenbuchensis from ectoparasites of deer in Massachusetts. Vector-Borne and Zoonotic Diseases 8: 549-554.
41. Menke SB, Fisher RN, Jetz W, Holway DA. 2007. Biotic and abiotic controls of Argentine ant invasion success at local and landscape scales. Ecology 88: 3164 -3173.
42. Montgomerie R, Weatherhead PJ. 1997. How robins find worms? Animal Behaviour 54: 143-151.
43. Murakami M. 1999. Effect of avian predation on survival of leaf-rolling lepidopterous larvae. Researches on Population Ecology 41: 135-138.
44. Naef-Daenzer L, Naef-Daenzer B, Nager RG. 2000. Prey selection and foraging performance of breeding great tits Parus major in relation to food availability. Journal of Avian Biology 31: 206-214.
45. Nevitt GA, Losekoot M, Weimerskirch H. 2008. Evidence for olfactory search in wandering albatross, Diomedea exulans. Proceedings of the National Academy of Sciences of the United States of America 105: 4576-4581.
46. Paakkonen T, Mustonen AM, Roininen H, Niemelä P, Ruusila V, Nieminen P. 2010. Parasitism of the deer ked, Lipoptena cervi, on the moose, Alces alces, in eastern Finland. Medical and Veterinary Entomology 24: 411-417.
47. Pimentel C, Nilsson JÅ. 2007. Response of great tits Parus major to an irruption of a pine processionary moth Thaumetopoea pityocampa population with a shifted phenology. Ardea 95: 191-199.
48. Popov AV. [????? A?] 1965. The life cycle of louse-flies Lipoptena cervi L. and Stenepteryx hirundinis L. (Diptera, Hippoboscidae). Revue d'Entomologie de l'URSS XLIV: 573-583. (in Russian).
49. R Development Core Team. 2009. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at:
50. Rajchard J. 2009. Ultraviolet (UV) light perception by birds: a review. Veterinarni Medicina 54: 351-359.
51. Rantanen T, Reunala T, Vuojolahti P, Hackman W. 1982. Persistent pruritic papules from deer ked bites. Acta Dermato-Venereologica 62: 307-311.
52. Roland J, Hannon SJ, Smith MA. 1986. Foraging pattern of pine siskins and its influence on winter moth survival in an apple orchard. Oecologia 69: 47-52.
53. Samuel WM, Mooring MS, Aalangdong OI. 2000. Adaptations of winter ticks (Dermacentor albipictus) to invade moose and moose to evade ticks. Alces 36: 183-195.
54. Schoener TW, Spiller DA. 1995. Effect of predators and area on invasion: an experiment with island spiders. Science 267: 1811-1813.
55. Schultz TD. 1983. Opportunistic foraging of Western kingbirds on aggregations of tiger beetles. Auk 100: 496-497.
56. Shwartz A, Strubbe D, Butler CJ, Matthysen E, Kark S. 2009. The effect of enemy-release and climate conditions on invasive birds: a regional test using the rose-ringed parakeet (Psittacula krameri) as a case study. A Journal of Conservation Biogeography 15: 310-318.
57. Steiger SS, Fidler AE, Valcu M, Kempenaers B. 2008. Avian olfactory receptor gene repertoires: evidence for a well-developed sense of smell in birds? Proceedings of the Royal Society B: Biological Sciences 275: 2309-2317.
58. Suhonen J. 1993. Predation risk influences the use of foraging sites by tits. Ecology 74: 1197-1203.
59. Suhonen J, Alatalo RV, Gustafsson L. 1994. Evolution of foraging ecology in Fennoscandian tits (Parus spp.). Proceedings of the Royal Society B: Biological Sciences 258: 127-131.
60. Tanhuanpää M, Ruohomäki K, Kaitaniemi P, Klemola T. 1999. Different impact of pupal predation on populations of Epirrita autumnata (Lepidoptera; Geometridae) within and outside the outbreak range. Journal of Animal Ecology 68: 562-570.
61. Välimäki P, Kaitala A, Madslien K, Härkönen L, Várkonyi G, Heikkilä J, Jaakola M, Ylönen H, Kortet R, Ytrehus B. 2011. Geographical variation in host use of a blood-feeding ectoparasitic fly: implications for population invasiveness. Oecologia 166: 985-995.
62. Välimäki P, Madslien K, Malmsten J, Härkönen L, Härkönen S, Kaitala A, Kortet R, Laaksonen S, Mehl R, Redford L, Ylönen H, Ytrehus B. 2010. Fennoscandian distribution of an important parasite of cervids, the deer ked (Lipoptena cervi), revisited. Parasitology Research 107: 117-125.
63. Van Ballenberghe V, Miquelle DG. 1990. Activity of moose during spring and summer in interior Alaska. The Journal of Wildlife Management 54: 391-396.
64. Vaughan TA, Ryan JM, Czaplewski NJ. 2011. Mammalogy, 5th edn. Ontario: Jones and Bartlett Publishers.
65. Vermeij GJ. 1996. An agenda for invasion biology. Biological Conservation 78: 3-9.
66. Viitala J, Korpimäki E, Palokangas P, Koivula M. 1995. Attraction of kestrels to vole scent marks visible in ultraviolet light. Nature 373: 425-427.
67. Williamson M. 1996. Biological Invasions. London: Chapman & Hall.