Associations between innate immune function and ectoparasites in wild rodent hosts

Parasitology Research

Volumn 112, Issue 4, 2013, Pages 1763-1770

  Rynkiewicz, Evelyn C ^a   Hawlena, Hadas ^b   Durden, Lance A ^c   Hastriter, Michael W ^d   Demas, Gregory E ^a   Clay, Keith ^a  

^a INDIANA UNIVERSITY   (United States)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^c GEORGIA SOUTHERN UNIVERSITY   (United States)

^d BRIGHAM YOUNG UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGE; ANDROLAELAPS FAHRENHOLZI; ANIMAL EXPERIMENT; ARTICLE; BACTERICIDAL ACTIVITY; CONTROLLED STUDY; CTENOPHTHALMUS PSEUDAGYRTES; DERMACENTOR VARIABILIS; ECTOPARASITE; ENERGY COST; EULAELAPS STABULARIS; EUTROMBICULA ALFREDDUGESI; EVOLUTION; FEMALE; FLEA; HAEMOGAMASUS LIPONYSSOIDES; HAEMOGAMASUS LONGITARSUS; HOST PARASITE INTERACTION; HOST RANGE; IMMUNOASSAY; INNATE IMMUNITY; IXODES SCAPULARIS; MALE; MICROTUS OCHROGASTER; MITE; NONHUMAN; ORCHOPEAS LEUCOPUS; PARASITE LOAD; PARASITE VECTOR; PEROMYSCUS; PEROMYSCUS LEUCOPUS; PRIORITY JOURNAL; RODENT; SEX DIFFERENCE; SPECIES DIFFERENCE; VOLE; WILD ANIMAL;

ANIMALS; ARVICOLINAE; BACTERIAL INFECTIONS; ECTOPARASITIC INFESTATIONS; FEMALE; MALE; MICE; PARASITE LOAD; PEROMYSCUS; RODENT DISEASES;

ACARI; BACTERIA (MICROORGANISMS); IXODIDA; MICROTUS; MICROTUS OCHROGASTER; PEROMYSCUS; PEROMYSCUS LEUCOPUS; RODENTIA; SIPHONAPTERA (FLEAS);

EID: 84876414548     PISSN: 09320113     EISSN: 14321955     Source Type: Journal    
DOI: 10.1007/s00436-013-3335-1     Document Type: Article

References (71)

1. Abbot P, Aviles AE, Eller L, Durden LA (2007) Mixed infections, cryptic diversity, and vector-borne pathogens: evidence from Polygenis fleas and Bartonella species. Appl Environ Microbiol 73:6045-6052
2. Allen JR (1994) Host resistance to ectoparasites. Rev Sci Tech Off Int Épiz 13:1287-1303
3. Amerault TE, Rose JE, Kuttler KL (1981) Comparative titration of Anaplasma marginale antibodies by card agglutination and complement-fixation tests. Am J Vet Res 42:1055-1056
4. Anderson JF, Johnson RC, Magnarelli LA, Hyde FW, Myers JE (1986) Peromyscus leucopus and Microtus pennsylvanicus simultaneously infected with Borrelia burgdorferi and Babesia microti. J Clin Microbiol 23:135-137
5. Baucom RS, de Roode JC (2011) Ecological immunology and tolerance in plants and animals. Funct Ecol 25:18-28
6. Bordes F, Ponlet N, de Bellocq JG, Ribas A, Krasnov BR, Morand S (2012) Is there sex-biased resistance and tolerance in Mediterranean wood mouse (Apodemus sylvaticus) populations facing multiple helminth infections? Oecologia 170:123-135
7. Boughton RK, Joop G, Armitage SAO (2011) Outdoor immunology: methodological considerations for ecologists. Funct Ecol 25:81-100
8. Bradley JE, Jackson JA (2008) Measuring immune system variation to help understand host-pathogen community dynamics. Parasitology 135:807-823
9. Brinkerhoff RJ, Martin AP, Jones RT, Collinge SK (2011) Population genetic structure of the prairie dog flea and plague vector, Oropsylla hirsuta. Parasitology 138:71-79
10. Brown SJ (1988) Highlights of contemporary research on host immune-responses to ticks. Vet Parasitol 28:321-334
11. Burkot TR, Schneider BS, Pieniazek NJ, Happ CM, Rutherford JS, Slemenda SB, Hoffmeister E, Maupin GO, Zeidner NS (2000) Babesia microti and Borrelia bissetii transmission by Ixodes spinipalpis ticks among prairie voles, Microtus ochrogaster, in Colorado. Parasitology 121:595-599
12. Calabrese JM, Brunner JL, Ostfeld RS (2011) Partitioning the aggregation of parasites on hosts into intrinsic and extrinsic components via an extended poisson-gamma mixture model. PLoS One 6:e29215
13. Chester EM, Bonu T, Demas GE (2010) Social defeat differentially affects immune responses in Siberian hamsters (Phodopus sungorus). Physiol Behav 101:53-58
14. Demas GE, Chefer V, Talan MI, Nelson RJ (1997) Metabolic costs of mounting an antigen-stimulated immune response in adult and aged C57BL/6 J mice. Am J Physiol Regul Integr Comp Physiol 273:R1631-R1637
15. Durden LA (1992) Ectoparasites of sympatric meadow voles and white footed mice at Fort Detrick, Maryland. J Med Entomol 29:761-766
16. Erickson DL, Anderson NE, Cromar LM, Jolley A (2009) Bacterial communities associated with flea vectors of plague. J Med Entomol 46:1532-1536
17. Ezenwa VO, Ekernas LS, Creel S (2011) Unravelling complex associations between testosterone and parasite infection in the wild. Funct Ecol 26:123-133
18. Fenton A, Viney ME, Lello J (2010) Detecting interspecific macroparasite interactions from ecological data: patterns and process. Ecol Lett 13:606-615
19. Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603-622
20. Folstad I, Nilssen AC, Halvorsen O, Andersen J (1989) Why do male reindeer (Rangifer-T tarandus) have higher abundance of 2nd and 3rd instar larvae of Hypoderma-tarandus tarandi Than Females. Oikos 55:87-92
21. Fornoni J, Nunez-Farfan J, Valverde PL, Rausher MD (2004) Evolution of mixed strategies of plant defense allocation against natural enemies. Evolution 58:1685-1695
22. Francis DH, Buening GM, Amerault TE (1980) Characterization of immune-responses of cattle to erythrocyte stroma, Anaplasma antigen, and dodecanoic acid-conjugated Anaplasma antigen: humoral immunity. Am J Vet Res 41:362-367
23. Fuxjager MJ, Foufopoulos J, Diaz-Uriarte R, Marler CA (2011) Functionally opposing effects of testosterone on two different types of parasite: implications for the immunocompetence handicap hypothesis. Funct Ecol 25:132-138
24. Gasparini J, McCoy KD, Haussy C, Tveraa T, Boulinier T (2001) Induced maternal response to the Lyme disease spirochaete Borrelia burgdorferi sensu lato in a colonial seabird, the kittiwake Rissa tridactyla. Proc R Soc Lond B Biol Sci 268:647-650
25. Ginsberg HS (2008) Potential effects of mixed infections in ticks on transmission dynamics of pathogens: comparative analysis of published records. Exp Appl Acarol 46:29-41
26. Gomez-Diaz E, Gonzalez-Solis J, Peinado MA, Page RDM (2007) Lack of host-dependent genetic structure in ectoparasites of Calonectris shearwaters. Mol Ecol 16:5204-5215
27. Graham AL, Hayward AD, Watt KA, Pilkington JG, Pemberton JM, Nussey DH (2010) Fitness correlates of heritable variation in antibody responsiveness in a wild mammal. Science 330:662-665
28. Graham AL, Shuker DM, Pollitt LC, Auld SKJR, Wilson AJ, Little TJ (2011) Fitness consequences of immune responses: strengthening the empirical framework for ecoimmunology. Funct Ecol 25:5-17
29. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds - a role for parasites. Science 218:384-387
30. Hawlena H, Rynkiewicz E, Toh E, Alfred A, Durden LA, Hastriter MW, Nelson DE, Rong R, Munro D, Dong Q, Fuqua C, Clay K (2013) The arthropod, but not the vertebrate host or its environment, dictates bacterial community composition of fleas and ticks. ISME J 7:221-223
31. Hawley DM, Altizer SM (2011) Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Funct Ecol 25:48-60
32. Hofmeister EK, Kolbert CP, Abdulkarim AS, Magera JMH, Hopkins MK, Uhl JR, Ambyaye A, Telford SR III, Cockerill FR III, Persing DH (1998) Cosegregation of a novel Bartonella species with Borrelia burgdorferi and Babesia microti in Peromyscus leucopus. J Infect Dis 177:409-416
33. Iwasa M, Kasuya S, Noda N, Hioki A, Ito A, Ohtomo H (1990) Trombiculid mites (Acari: Trombiculidae) and Rickettsia tsutsugamushi isolated from wild rodents in a new endemic area of Japan. J Med Entomol 27:501-508
34. Janeway CA, Travers P, Walport M, Shlomchik M (2007) Immunobiology, 7th edn. Garland Publishing, New York
35. Jones PH, Britten HB (2010) The absence of concordant population genetic structure in the black-tailed prairie dog and the flea, Oropsylla hirsuta, with implications for the spread of Yersinia pestis. Mol Ecol 19:2038-2049
36. Keil D, Luebke RW, Pruett SB (2001) Quantifying the relationship between multiple immunological parameters and host resistance: probing the limits of reductionism. J Immunol 167:4543-4552
37. Klompen JSH, Black WCV, Keirans JE, Oliver JH Jr (1996) Evolution of ticks. Annu Rev Entomol 41:141-161
38. Krasnov BR, Shenbrot GI, Khokhlova IS, Hawlena H, Degen AA (2006) Temporal variation in parasite infestation of a host individual: does a parasite-free host remain uninfested permanently? Parasitol Res 99:541-545
39. Krebs CJ (1970) Microtus population biology - behavioral changes associated with population cycle in M. ochrogaster and M. pennsylvanicus. Ecology 51:34-52
40. Lindstrom KM, Foufopoulos J, Parn H, Wikelski M (2004) Immunological investments reflect parasite abundance in island populations of Darwin's finches. Proc R Soc Lond B Biol Sci 271:1513-1519
41. LoGiudice K, Ostfeld RS, Schmidt KA, Keesing F (2003) The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. PNAS 100:567-571
42. Martin LB, Weil ZM, Nelson RJ (2007) Immune defense and reproductive pace of life in Peromyscus mice. Ecology 88:2516-2528
43. McAloon FM, Durden LA (2000) Attachment sites and frequency distribution of erythraeid mites, Leptus indianensis (Acari: Prostigmata), ectoparasitic on harvestmen, Leiobunum formosum (Opiliones). Exp Appl Acarol 24:561-567
44. Millet S, Bennett J, Lee KA, Hau M, Klasing KC (2007) Quantifying and comparing constitutive immunity across avian species. Dev Comp Immunol 31:188-201
45. Muehlenbein MP (2006) Intestinal parasite infections and fecal steroid levels in wild chimpanzees. Am J Phys Anthropol 130:546-550
46. Mumford RE, Whitaker JOJ (1982) Mammals of Indiana. Indiana University Press, Bloomington
47. Nelson RJ, Demas GE (1996) Seasonal changes in immune function. Q Rev Biol 71:511-548
48. Ostfeld RS, LoGiudice K (2003) Community disassembly, biodiversity loss, and the erosion of an ecosystem service. Ecology 84:1421-1427
49. Ostfeld RS, Cepeda OM, Hazler KR, Miller MC (1995) Ecology of Lyme disease: habitat associations of ticks (Ixodes scapularis) in a rural landscape. Ecol Appl 5:353-361
50. Pedersen AB, Fenton A (2007) Emphasizing the ecology in parasite community ecology. Trends Ecol Evol 22:133-139
51. Perkins SE, Ferrari MF, Hudson PJ (2008) The effects of social structure and sex-biased transmission on macroparasite infection. Parasitology 135:1561-1569
52. Petney TN, Vanark H, Spickett AM (1990) On sampling tick populations: the problem of overdispersion. Onderstepoort J Vet Res 57:123-127
53. Puustinen S, Koskela T, Mutikainen P (2004) Direct and ecological costs of resistance and tolerance in the stinging nettle. Oecologia 139:76-82
54. Råberg L, Sim D, Read AF (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318:812-814
55. Radovsky FJ (1985) Evolution of mammalian mesostigmate mites. In: Kim KC (ed) Coevolution of parasitic arthropods and mammals. Wiley, New York
56. Roberts ML, Buchanan KL, Evans MR (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68:227-239
57. Saino N, Moller AP, Bolzern AM (1995) Testosterone effects on the immune system and parasite infestations in the barn swallow (Hirundo rustica): an experimental test of the immunocompetence hypothesis. Behav Ecol 6:397-404
58. Schwanz LE, Voordouw MJ, Brisson D, Ostfeld RS (2011) Borrelia burgdorferi has minimal impact on the Lyme disease reservoir host Peromyscus leucopus. Vector-Borne Zoon Dis 11:117-124
59. Shaw DJ, Dobson AP (1995) Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111:S111-S133
60. Shaw DJ, Grenfell BT, Dobson AP (1998) Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117:597-610
61. Tieleman BI, Williams JB, Ricklefs RE, Klasing KC (2005) Constitutive innate immunity is a component of the pace-of-life syndrome in tropical birds. Proc Royal Soc B Biol Sci 272:1715-1720
62. Tilly K, Rosa PA, Stewart PE (2008) Biology of infection with Borrelia burgdorferi. Infect Dis Clin N Am 22:217-234
63. Traub R (1985) Coevolution of fleas and mammals. In: Kim KC (ed) Coevolution of parasitic arthropods and mammals. Wiley, New York, pp 295-437
64. Whitaker JO (1982) Ectoparasites of mammals of Indiana. Indiana Academy of Science, Indianapolis
65. Whitaker JO Jr., Walters BL, Castor LK, Ritzi CM, Wilson N (2007) Host and distribution lists of mites (Acari), parasitic and phoretic, in the hair or on the skin of North American wild mammals north of Mexico: records since 1974. Faculty Publications from the Harold W Manter Laboratory of Parasitology, University of Nebraska, Lincoln 1:1-173
66. Wikel SK (1999) Tick modulation of host immunity: an important factor in pathogen transmission. Int J Parasitol 29:851-859
67. Woolhouse MEJ, Dye C, Etard JF, Smith T, Charlwood JD, Garnett GP, Hagan P, Hii JLK, Ndhlovu PD, Quinnell RJ, Watts CH, Chandiwana SK, Anderson RM (1997) Heterogeneities in the transmission of infectious agents: implications for the design of control programs. PNAS 94:338-342
68. Zavala-Castro JE, Zavala-Velazquez JE, Peniche-Lara GF, Sulu Uicab JE (2009) Human rickettsialpox, Southeastern Mexico. Emerg Infect Dis 15:1665-1667
69. Zuk M, Johnson K, Thornhill R, Ligon JD (1990a) Parasites and male ornaments in free-ranging and captive red jungle fowl. Behaviour 114:232-248
70. Zuk M, Thornhill R, Ligon JD, Johnson K (1990b) Parasites and mate choice in red jungle fowl. Am Zool 30:235-244
71. Zysling DA, Garst AD, Demas GE (2009) Photoperiod and food restriction differentially affect reproductive and immune responses in Siberian hamsters Phodopus sungorus. Funct Ecol 23:1-10