Changes in behavioural and physiological parameters associated with Taenia pisiformis infection in rabbits (Oryctolagus cuniculus) that may improve early detection of sick rabbits

Authors

  • Miguel Angel Betancourt-Alonso Universidad Autónoma del Estado de Morelos
  • Agustín Orihuela Universidad Autónoma del Estado de Morelos
  • Virginio Aguirre Universidad Autónoma del Estado de Morelos
  • Reyes Vázquez Universidad Autónoma del Estado de Morelos
  • Fernando Iván Flores-Pérez Universidad Autónoma del Estado de Morelos

DOI:

https://doi.org/10.4995/wrs.2011.801

Keywords:

Taenia pisiformis, behavior of sick animals, parasite infection, rabbits, hepatic function

Abstract

The purpose of the present experiment was to describe rabbits´ early behavioral responses to illness, and its relation with physiological changes to help improve early detection of infection, particularly those induced by Taenia pisiformis in rabbits. Twenty adult female New Zealand rabbits were randomly allocated in two groups, to determine whether changes in behavior and some physiological parameters can be induced in rabbits after a T. pisiformis infection. Infected animals were orally inoculated with 3,000 eggs of T. pisiformis, while controls only received saline solution. Behavioral activity was recorded daily from 19:00 to 21:00 h starting two days before infection. Mate choice and rank status were assessed, and blood samples were collected at -2, 7, 14 and 25 days post infection (dpi) for hematological and hepatic function determinations. All animals were observed for clinical signs every other day from the beginning of the experiment and euthanized 25 dpi after last sampling. Infected animals spent more (P<0.01) time lying down (87 vs. 17%) and less (P<0.05) time grooming (43 vs. 57%) and drinking (26 vs. 74%) than controls. These differences were noticeable 6 dpi and remained until the end of the experiment. No changes (P>0.05) were observed in the time spent at the feeder, rank status or mate choice. Leucocyte and lymphocyte concentrations increased (P<0.05) while heterophil counts decreased in infected rabbits as the experiment progressed. Furthermore, infected animals had larger concentrations of alkaline phosphatase as soon as 7 dpi. No clinical signs of the disease were detected. Necropsy findings corroborate hepatic lesions and presence of the parasite in all infected animals. It was concluded that an infection with 3,000 eggs of T. pisiformis induced changes in behavioral patterns, supported by some changes in hematological and hepatic parameters that could improve early detection of illness, regardless of clinical signs.

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References

Adams E.S. 2005. Bayesian analysis of linear dominance hierarchies. Anim. Behav. 69: 1191-1201. doi:10.1016/j.anbehav.2004.08.011.

Alzaga V., Vicente J., Villauna D., Acevedo P., Casas F., Gortazar C. 2008. Body condition and parasite intensity correlates with escape capacity in Iberian hares (Lepus granatensis). Behav. Ecol. Sociobiol., 62: 769-775. doi: 10.1007/s00265-007-0502-3.

American Veterinary Medical Association, 2001. Report of the AVMA panel on euthanasia. J. Am.Vet. Med. Assoc., 218: 669-696. doi: 10.2460/javma.2001.218.669

Anderson P.H., Mathews J.G., Berret S., Brush P.J., Patterson D.S. 1981. Change in plasma enzyme activities and other blood components in response to acute and chronic liver damage in cattle. Res. Vet. Sci., 31: 1-4.

Arnott M.A., Casella J.P., Aitken P.P., Hay J. 1990. Social interactions of mice with congenital Toxoplasma gondii infection. Ann. Trop. Med. Parasit., 84: 149-56.

Borderas F.T., Passillé A.M., Rushen J.P. 2007. Behavioural correlates of induced fever in dairy calves. In Proc.: 41st International Congress of the International Society for Applied Ethology. Mérida, Yuc., México.

Bortolotti A., Castelli D., Bonati M. 1989. Hematology and serum chemistry values of adult, pregnant and newborn New Zealand rabbits (Oryctolagus cuniculus). Lab. Anim. Sci., 39: 437-439.

Bowman D.D. 1999. Georgis´ Parasitology for Veterinarians, 7th Ed. WB. Saunder Company, Philadelphia, USA.

Conboy G.A., Stromberg B.E. 1991. Hematology and clinical pathology of experimental Fascioloides magna infection in cattle and guinea pigs. Vet. Parasitol., 40: 241-255.

Erhard H.W., Fábrega E., Stanworth G., Elston D.A., 2004. Assessing dominance in sheep in a competitive situation: level of motivation and test duration. Appl. Anim. Behav. Sci., 85: 277-292. doi: 10.1016/j.applanim.2003.09.013.

Flatt R.E., Cambell W.W. 1974. Cysticercosis in rabbits: incidence and lesions of the naturally occurring disease in young domestic rabbits. Lab. Anim. Sci., 24: 914-918.

Flatt R.E., Moses R.W. 1975. Lesions of experimental cysticercosis in domestic rabbits. Lab. Anim. Sci., 25: 162-167.

Flower F.C., Weary D.M. 2006. Effect of hoof pathologies on subjective assessments of dairy cow gait. J. Dairy Sci. 89: 139-46. doi:10.3168/jds.S0022-0302(06)72077-X.

Forbes A.B., Huckle C.A., Gibb M.J., Rook A.J., Nuthall R. 2000. Evaluation of the effects of nematode parasitism on grazing behavior, herbage intake and growth in young grazing cattle. Vet. Parasitol., 90: 111-118. doi:10.1016/S0304-4017(00)00218-1.

Fuentes G.C., Newgren J. 2008. Physiology and clinical pathology of laboratory New Zealand White rabbits housed individually and in groups. J. Am. Assoc. Lab. Anim., 47: 35-38.

García-Allan C., Martínez N., Flisser A., Aluja A., Allan J.C., Craig P.S. 1996. Immunocharacterization of Taenia solium oncosphere and metacestode antigens. J. Helmithol., 70: 271-280. doi: 10.1017/ S0022149X00015558.

Gonzalez G., Melo A.I., Zavala A., Beyer C. 1990. Variations in chinmarking behavior of New Zealand female rabbits throughout the whole reproductive cycle. Physiol. Behav., 48: 361-365. doi: 10.1016/0031-9384(90)90328-2.

Gonzalez G., Melo A.I., Zavala A., Chirino R., Beyer C. 1993. Sex steroid regulation of chin-marking behavior in male New Zealand rabbits. Physiol. Behav., 54: 1035-1040. doi: 10.1016/00319384(93)90321-6.

Gonzalez R., 2004. Cunicultura: La Ciencia del Conejo, 1st. Ed. Universidad Autónoma de Baja California Sur, Baja California Sur, Mexico.

Gourbal B.E., Gabrion C. 2004. A study of mate choice in mice with experimental Taenia crassiceps cisticercosis: Can males chose? Can. J. Zoolg. 82: 635-643. doi:.10.1139/z04-038.

Gunn D., Morton D.B. 1995. Inventory of the behavior of New Zealand White rabbits in laboratory cages. Appl. Anim. Behav. Sci. 45: 277292. doi:10.1016/0168-1591(95)00627-5.

Hansen L.T., Berthelsen H. 2000. The effect of environmental enrichment on the behaviour of caged rabbits (Oryctolagus cuniculus). Appl. Anim. Behav. Sci. 68: 163-178. doi: 10.1016/ S0168-1591(00)00093-9.

Hart B.L. 1988. Biological basis of the behavior of sick animals. Neurosci. Biobehav. R., 12: 123-137. doi: 10.1016/S0149-7634(88) 80004-6.

Huzzey J.M., Veira D.M., Weary D.M., Von Keyserlingk M.A. 2007. Prepartum behavior and dry matter intake identify dairy cows at risk for metritis. J. Dairy Sci., 90: 3220-3233. doi: 10.3168/ jds.2006-807.

Jain N.C. 1993. Essentials of Veterinary Hematology. 1st Ed. WilleyBlackwell, Philadelphia, USA.

Klein S.L. 2003. Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates. Physiol. Behav. 79: 441449. doi: 10.1016/S0031-9384(03)00163-X.

Kraft H., Schillinger D. 1989. Klinische labormethoden der Veterinärmedizin bei haussäugetieren. 3rd Ed. Ferdinand Enke Verlag Stuttgart.

Kristennson K., Mhalanga J.D.M., Bentivoglio M. 2002. Parasites and the brain: neuroinvasion, immunopathogenesis and neural dysfunction. Curr. Top. Microbiol., 265: 227-257.

Krohn T.C., Ritskes-Hoitinga J., Svendsen P. 1999. The effects of feeding and housing on the behaviour of the laboratory rabbit. Lab. Anim.-UK, 33: 101-107. doi: 10.1258/002367799780578327.

Krueger J.M., Majde J.A. 1994. Microbial products and cytokines in sleep and fever regulation. Crit. Rev. Immunol. 14: 355-379.

Krueger J.M., Majde J.A., Obal F. 2003. Sleep in host defense. Brain Behav. Immun. 17: 41-47. doi: 10.1016/S0889-1591(02)00065-X.

Kyriazakis I., Oldham J.D., Coop R.L., Jackson F. 1994. The effect of subclinical intestinal nematode infection on the diet selection of growing sheep. Brit. J. Nutr. 72: 665-677. doi: 10.1079/ BJN19940070.

Laye S., Parnet P., Goujon E., Dantzer R., 1994. Peripheral administration of lipopolysaccharide induces the expression of cytokine transcripts in the brain and pituitary of mice. Mol. Brain Res., 27: 157-162. doi:10.1016/0169-328X(94)90197-X.

Madsen T.N., Kristensen A.R. 2005. A model for monitoring the condition of young pigs by their drinking behavior. Comput. Electron. Agr., 48: 138-154. doi: 10.1016/j.compag.2005.02.014.

Matanović K., Servin K., Martinković F., Simpraga M., Janicki Z., Barisić J. 2007. Hematological and biochemical changes in organically farmed sheep naturally infected with Fasciola hepatica. Parasitol. Res., 101: 1657-1661. doi: 10.1007/s00436-007-0709-2.

Melman S.A. 1987. Mast cells and their mediators, emphasis on their role in type I immediate hypersensitivity in canines. Int. J. Dermatol. 26: 335-343. doi: 10.1111/j.1365-4362.1987.tb00553.x.

Orihuela A., Vázquez-Prats V.M. 2008. Behavioral strategies in hostparasite relationships. Review. Tec. Pecu. Mex., 46: 259-285.

Pastell M.E., Kujala M. 2007. A probabilistic neural network model for lameness detection. J. Dairy Sci. 90: 2283-2292. doi:10.3168/ jds.2006-267.

Pérez-Torres A., Ustarroz M., Constantino F., Villalobos De Aluja A. 2002. Taenia solium cisticercosis: lymphocites in the inflammatory reaction in naturally infected pigs. Parasitol. Res., 88: 150-152. doi: 10.1007/s00436-001-0510-6.

Presidente P.J., Mcbraw B.M., Lumsden J.H. 1975. Experimentally induced Fasciola hepatica infection in white-tailed deer. I. Clinicopathological and parasitological features. Can. J. Comp. Med., 39: 155-165.

Proudfoot K.L., Veira D.M., Weary D.M., Von Keyserlingk M.A.G. 2007. Changes in feeding and standing behavior of transition cows predict risk of sole hemorrhages and ulcers. J. Dairy Sci. 90 Suppl 1: 126 (abstract).

Rau M.E. 1983. The open–field behavior of mice infected with Trichinella spiralis. Parasitol., 86: 311-318. doi: 10.1017/ S0031182000050472.

Royo R. 1986. Hemogram in pigs inoculated experimentally with eggs of Taenia solium. Under graduate thesis Veterinary Faculty, National Autonomous University. Mexico.

Rushen J.P., Borderas F.T., De Passillé A.M.B., Von Keyserlingk M.A.G., Weary D.M. 2007. Using knowledge of animal behavior to improve animal health. In Proc.: 41st International Congress of the International Society for Applied Ethology. Mérida, Yuc, Mexico. SAS. 1988.

SAS/STAT User´s Guide (Release 6.03). SAS Inst. Inc., Cary, N.C. USA.

Snedecor G.W., Cochran W.G. 1989. Statistical Methods. Iowa State Univ. Press, Ames I.A., USA.

Steel J.W., Symons L.E.A., Jones W.O. 1980. Effects of level of larval intake on the productivity and physiological and metabolic responses of lambs infected with Trichostrongylus colubriformis. Aust. J. Agric. Res. 31: 821-838. doi: 10.1071/AR9800821.

Svensson C., Jensen M.B. 2007. Short Communication: Identification of diseased calves by use of data from automatic milk feeders. J. Dairy Sci. 90: 994-997. doi: 10.3168/jds.S0022-0302(07)71584-9.

Sykes A.R., Greer A.W. 2003. Effects of parasitism on the nutrient economy of sheep. Aust. J. Exp. Agric., 43: 1393-1398. doi: 10.1071/EA02228.

Trocino A., Xiccato G. 2006. Animal welfare in reared rabbits: a review with emphasis on housing systems. World Rabbit Sci. 14: 77-93.

Vengust G., Klinkon M., Bidovec A., Vengust A. 2003. Fasciola hepatica: effects on blood constituents and liver minerals in fallow deer (Dama dama). Vet. Parasitol., 112: 51-61. doi: 10.1016/ S0304-4017(02)00413-2.

Verga M. 2005. The impact of the current housing and husbandry systems on the health and welfare of farmed domestic rabbits. EFSA J., 267: 1-31. doi: 10.2903/j.efsa.2005.267.

Wang C.I., Ma X.Y., Kuo K.C., Fan C.P. 1997. A comparative study on egg hatching methods and oncosphera viability deterrmination for Taenia solium eggs. Int. J. Parasitol., 27: 1311-1314. doi: 10.1016/ S0020-7519(97)00087-8.

Webster J.P. 1994. The effect of Toxoplasma gondii and other parasites on activity levels in wild and hybrid Rattus norvergicus. Parasitol., 109: 583-589. doi: 10.1017/S0031182000076460.

Worley D.E. 1974. Quantitative studies on the migration and development of Taenia pisiformis larvae in laboratory rabbits. Lab. Anim. Sci., 2: 517-22..

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