Skip to main content

Advertisement

Log in

Fluctuating asymmetry and blood parameters in three endangered gazelle species

  • Original Investigation
  • Published:
Mammalian Biology Aims and scope Submit manuscript

Abstract

There is currently no agreement about the suitability of fluctuating asymmetry (FA) as an estimate of individual quality. We investigated the relationship between FA and health, a proxy for individual quality, in captive populations of three endangered gazelle species: Gazella cuvieri, G. dama, and G. dorcas. FA indices including information from sexual (horns) and/or non-sexual ordinary traits were calculated for each individual. Health was assessed using 15 blood parameters, and inbreeding coefficient was also included in the analyses. In the three species, the FA index was significantly related to at least one blood parameter (platelets, mean platelet cell volume, albumin, and lactate dehydrogenase), with levels indicating unhealthy condition in more asymmetric individuals. The exception was the negative relationship between FA and aspartate aminotransferase in ordinary traits of G. cuvieri and G. dama. FA was related to different blood parameters in every species and type of trait. As a large number of diseases can cause abnormal blood parameter levels in humans, we assumed that this also might be the case in gazelles. In general, the results suggest that FA is related to health in the three gazelle species studied, and thus, we concluded that FA can provide useful information about individual quality.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abáigar, T., 1993. Hematology and plasma chemistry values for captive dama gazelles (Gazella dama mhorr) and cuvie’s gazelles (Gazella cuvieri): age, gender, and reproductive status differences. J. Zoo. Wildl. Med. 24, 177–184.

    Google Scholar 

  • Alados, C.L., Escós, J.M., Emlen, J.M., 1995. Fluctuating asymmetry and fractal dimension of the sagittal suture as indicators of inbreeding depression in dama and dorcas gazelles. Can. J. Zool. 73, 1967–1974.

    Article  Google Scholar 

  • Anderson, P.H., Berrett, S., Brush, P.J., Hebert, C.N., Parfitt, J.W., Patterson, D.S., 1977. Biochemical indicators of liver injury in calves with experimental fascioliasis. Vet. Rec. 100, 43–45.

    Article  CAS  PubMed  Google Scholar 

  • Atroshi, F., Parantainen, J., Sankari, S., Järvinen, M., Lindberg, L.A., Saloniemi, H., 1996. Changes in inflammation-related blood constituents of mastitic cows. Vet. Res. 27, 125–132.

    CAS  PubMed  Google Scholar 

  • Bani Ismail, Z.A., Dickinson, C., 2010. Alterations in coagulation parameters in dairy cows affected with acute mastitis caused by E. coli and S. aureus pathogens. Vet. Res. Commun. 34, 533–539.

    Article  Google Scholar 

  • Bath, P., Algert, C., Chapman, N., Neal, B., for the PROGRESS Collaborative Group, 2004. Association of mean platelet volume with risk of stroke among 3134 individuals with history of cerebrovascular disease. Stroke 35, 622–626.

    Article  PubMed  Google Scholar 

  • Bessman, J.D., Williams, L.J., Gilmer, P.R., 1982. Platelet size in health and hematologic disease. Am. J. Clin. Pathol. 78, 150–153.

    Article  CAS  PubMed  Google Scholar 

  • Brown, W.M., Price, M.E., Kang, J.S., Pound, N., Zhao, Y., Yu, H., 2008. Fluctuating asymmetry and preferences for sex-typical bodily characteristics. Proc. Natl. Acad. Sci. U.S.A. 105, 12938–12943.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buccheri, G., Ferrigno, D., 1994. Prognostic factors in lung-cancer: tables and comments. Eur. Respir. J. 7, 1350–1364.

    Article  CAS  PubMed  Google Scholar 

  • Burnham, K.P., Anderson, D.R., 2002. Model Selection and Multimodel Inference: A Practical Information-theoretic Approach, 2nd edition. Springer-Verlag, New York.

    Google Scholar 

  • Bush, M., Smith, E.E., Custer, R.S., 1981. Hematology and serum chemistry values for captive dorcas gazelles: variations with sex, age and health status. J. Wildl. Dis. 17, 135–143.

    Article  CAS  PubMed  Google Scholar 

  • Cassinello, J., 2005. Inbreeding depressionon reproductive performance and survival in captive gazelles of great conservation value. Biol. Conserv. 122, 453–464.

    Article  Google Scholar 

  • Cassinello, J., Gomendio, M., Roldan, E.R.S., 2001. Relationship between coefficient of inbreeding and parasite burden in endangered gazelles. Conserv. Biol. 15, 1171–1174.

    Article  Google Scholar 

  • Chandler, C.R., 1995. Practical considerations in the use of simultaneous inference for multiple tests. Anim. Behav. 49, 524–527.

    Article  Google Scholar 

  • Chapelle, J.P., Albert, A., Heusghem, C., Smeets, J.P., Kulbertus, H.E., 1980. Predictive value of serum enzyme determinations in acute myocardial-infarction. Clin. Chim. Acta 106, 29–38.

    Article  CAS  PubMed  Google Scholar 

  • Côté, S.D., Festa-Bianchet, M., 2001. Life-history correlates of horn asymmetry in mountain goats. J. Mammal. 82, 389–400.

    Article  Google Scholar 

  • Cuervo, J.J., Møller, A.P., 1999. Phenotypic variation and fluctuating asymmetry in sexually dimorphic feather ornaments in relation to sex and mating system. Biol. J. Linn. Soc. 68, 505–529.

    Article  Google Scholar 

  • Dailey, R.N., Montgomery, D.L., Ingram, J.T., Siemion, R., Vasquez, M., Raisbeck, M.F., 2008. Toxicity of the lichen secondary metabolite (+)-usnic acid in domestic sheep. Vet. Pathol. 45, 19–25.

    Article  CAS  PubMed  Google Scholar 

  • Day, R.D., Segars, A.L., Arendt, M.D., Lee, A.M., Peden-Adams, M.M., 2007. Relationship of blood mercury levels to health parameters in the loggerhead sea turtle (Caretta caretta). Environ. Health Perspect. 115, 1421–1428.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drevemo, S., Grootenhuis, J.G., Karstad, L., 1974. Blood parameters in wild ruminants in Kenya. J. Wildl. Dis. 10, 327–334.

    Article  CAS  PubMed  Google Scholar 

  • English, A.W., Lepherd, E.E., 1981. The hematology and serum biochemistry of wild fallow deer (Dama dama) in New South Wales. J. Wildl. Dis. 17, 289–295.

    Article  CAS  PubMed  Google Scholar 

  • Ferre, I., Barrio, J.P., González Gallego, J., Rojo Vázquez, F.A., 1994. Appetite depression in sheep experimentally infected with Fasciola hepatica L. Vet. Parasitol. 55, 71–79.

    Article  CAS  PubMed  Google Scholar 

  • Folstad, I., Arneberg, P., Karter, A.J., 1996. Antlers and parasites. Oecologia 105, 556–558.

    Article  PubMed  Google Scholar 

  • Gangestad, S.W., Thornhill, R., 1999. Individual differences in developmental precision and fluctuating asymmetry: a model and its implications. J. Evol. Biol. 12, 402–416.

    Article  Google Scholar 

  • Gökçe, H.I., Gökçe, G., Cihan, M., 2007. Alterations in coagulation profiles and biochemical and haematological parameters in cattle with traumatic reticuloperitonitis. Vet. Res. Commun. 31, 529–537.

    Article  PubMed  Google Scholar 

  • Goldwasser, P., Feldman, J., 1997. Association of serum albumin and mortality risk. J. Clin. Epidemiol. 50, 693–703.

    Article  CAS  PubMed  Google Scholar 

  • Gomendio, M., Cassinello, J., Roldan, E.R.S., 2000. A comparative study of ejaculate traits in three endangered ungulates with different levels of inbreeding: fluctuating asymmetry as an indicator of reproductive and genetic stress. Proc. R. Soc. Lond. B 267, 875–882.

    Article  CAS  Google Scholar 

  • Hammer, S., Hammer, C., Schulz, J., Wernery, U., Clauss, M., 2006. Biochemische serumparameter bei in gefangenschaft gehaltenen gazellen. Tierärztl. Prax. Grob. 34, 190–196.

    Article  Google Scholar 

  • IUCN, 2010. 1UCN Red List of Threatened Species. Version 2010.2, http://www.iucnredlist.org [accessed 13 August 2010].

  • Keller, S.L., Jefferson, B.J., Jacobs, R.M., Wood, R.D., 2006. Effects of noncytopathic type2 Bovine viral diarrhea virus on the proliferation of bone marrow progenitor cells. Can. J. Vet. Res. 70, 20–27.

    PubMed  PubMed Central  Google Scholar 

  • Kontaş Aşkar, T., Salmanoğlu, B., İriadam, M., Hişmioğullari, A., 2007. Serum biochemical values of Gazella subgutturosa in Ceylanpınar, Şanlıurfa, Turkey. J. Appl. Biol. Sci. 1, 77–79.

    Google Scholar 

  • Lagesen, K., Folstad, I., 1998. Antler asymmetry and immunity in reindeer. Behav. Ecol. Sociobiol. 44, 135–142.

    Article  Google Scholar 

  • Leamy, L., 1993. Morphological integration of fluctuating asymmetry in the mouse mandible. Genetica 89, 139–153.

    Article  Google Scholar 

  • Leary, R.F., Allendorf, F.W., 1989. Fluctuating asymmetry and indicator of stress: implications for conservation biology. Trends Ecol. Evol. 4, 214–217.

    Article  CAS  PubMed  Google Scholar 

  • Lessells, C.M., Boag, P.T., 1987. Unrepeatable repeatabilities: a common mistake. Auk 104, 116–121.

    Article  Google Scholar 

  • Leung, B., Forbes, M.R., 1996. Fluctuating asymmetry in relation to stress and fitness: effects of trait type as revealed by meta-analysis. Ecoscience 3, 400–413.

    Article  Google Scholar 

  • Leung, B., Forbes, M.R., Houle, D., 2000. Fluctuating asymmetry as a bioindicator of stress: comparing efficacy of analyses involving multiple traits. Am. Nat. 155, 101–115.

    Article  PubMed  Google Scholar 

  • Lilliehöök, I., Egenvall, A., Tvedten, H.W., 1998. Hematopathology in dogs experimentally infected with a Swedish granulocytic Ehrlichia species. Vet. Clin. Pathol. 27, 116–122.

    Article  Google Scholar 

  • Littleton-Kearney, M.T., Hurn, P.D., Kickler, T.S., Traystman, R.J., 1998. Incomplete global cerebral ischemia alters platelet biology in neonatal and adult sheep. Am. J. Physiol. Heart Circ. Physiol. 274, H1293–H1300.

    Article  CAS  Google Scholar 

  • Mateos, C., Alarcos, S., Carranza, J., Sánchez-Prieto, C.B., Valencia, J., 2008. Fluctuating asymmetry of red deer antlers negatively relates to individual condition and proximity to prime age. Anim. Behav. 75, 1629–1640.

    Article  Google Scholar 

  • Milner, J.M., Stien, A., Irvine, R.J., Albon, S.D., Langvatn, R., Ropstad, E., 2003. Body condition in Svalbard reindeer and the use of blood parameters as indicators of condition and fitness. Can. J. Zool. 81, 1566–1578.

    Article  Google Scholar 

  • Møller, A.P., 1996. Parasitism and developmental instability of hosts: a review. Oikos 77, 189–196.

    Article  Google Scholar 

  • Møller, A.P., 1997. Developmental stability and fitness: a review. Am. Nat. 149, 916–932.

    Article  PubMed  Google Scholar 

  • Møller, A.P., 1999. Asymmetry as a predictor of growth, fecundity and survival. Ecol. Lett. 2, 149–156.

    Article  Google Scholar 

  • Møller, A.P., 2006. A review of developmental instability, parasitism and disease: infection, genetics and evolution. Infect. Genet. Evol. 6, 133–140.

    Article  PubMed  Google Scholar 

  • Møller, A.P., Cuervo, J.J., Soler, J.J., Zamora-Muñoz, C., 1996. Horn asymmetry and fitness in gemsbok, Oryx g. gazella. Behav. Ecol. 7, 247–253.

    Article  Google Scholar 

  • Møller, A.P., Swaddle, J.P., 1997. Asymmetry, Developmental Stability and Evolution. Oxford University Press, Oxford.

    Google Scholar 

  • Newman, S.H., Anderson, D.W., Ziccardi, M.H., Trupkiewicz, J.G., Tseng, F.S., Christopher, M.M., Zinkl, J.G., 2000. An experimental soft-release of oil-spill rehabilitated American coots (Fulica americana): II. Effects on health and blood parameters. Environ. Pollut. 107, 295–304.

    Article  CAS  PubMed  Google Scholar 

  • O’Kelly, J.C., 1980. Parasitism and blood composition in genetically different types of cattle grazing in a tropical environment. Vet. Parasitol. 6, 381–390.

    Article  Google Scholar 

  • Omer, O.H., El-Malik, K.H., Mahmoud, O.M., Haroun, E.M., Hawas, A., Sweeney, D., Magzoub, M., 2002. Haematological profiles in pure bred cattle naturally infected with Theileria annulata in Saudi Arabia. Vet. Parasitol. 107, 161–168.

    Article  CAS  PubMed  Google Scholar 

  • Palmer, A.R., Strobeck, C., 1986. Fluctuating asymmetry: measurement, analysis, patterns. Annu. Rev. Ecol. Syst. 17, 391–421.

    Article  Google Scholar 

  • Palmer, A.R., Strobeck, C., 2003. Fluctuating asymmetry analyses revisited. In: Polak, M. (Ed.), Developmental Instability: Causes and Consequences. Oxford University Press, New York, pp. 279–319.

    Google Scholar 

  • Pardío, V.T., Ibarra, N.D., Waliszewski, K.N., López, K.M., 2007. Effect of coumaphos on cholinesterase activity, hematology, and biochemical blood parameters of bovines in tropical regions of Mexico. J. Environ. Sci. Health B 42, 359–366.

    Article  PubMed  CAS  Google Scholar 

  • Parsons, P.A., 1990. Fluctuating asymmetry: an epigenetic measure of stress. Biol. Rev. 65, 131–145.

    Article  CAS  PubMed  Google Scholar 

  • Peinado, V., Viscor, G., Palomeque, J., 1990. Hematology and blood chemistry in captive dorcas gazelles and blackbucks. Comp. Biochem. Physiol. A 97, 595–599.

    Article  Google Scholar 

  • Pélabon, C., Joly, P., 2000. What, if anything, does visual asymmetry in fallow deer antlers reveal? Anim. Behav. 59, 193–199.

    Article  Google Scholar 

  • Pérez, J.M., González, F.J., Serrano, E., Granados, J.E., Fandos, P., Carro, F., Soriguer, R.C., 2006. Is blood collected from shot Iberian ibex (Capra pyrenaica) useful for monitoring their physiological status? Eur. J. Wildl. Res. 52, 125–131.

    Article  Google Scholar 

  • Peters Jr., T., 1995. All About Albumin: Biochemistry, Genetics, and Medical Applications. Academic Press, San Diego.

    Google Scholar 

  • Polak, M. (Ed.), 2003. Developmental Instability: Causes and Consequences. Oxford University Press, New York.

    Google Scholar 

  • Polak, M., Møller, A.P., Gangestad, S., Manning, J., Thornhill, R., 2003. Does an individual asymmetry parameter exist? A meta-analysis. In: Polak, M. (Ed.), Developmental Instability: Causes and Consequences. Oxford University Press, New York, pp. 81–96.

    Google Scholar 

  • Putman, R.J., Sullivan, M.S., Langbein, J., 2000. Fluctuating asymmetry in antlers of fallow deer (Dama dama): the relative roles of environmental stress and sexual selection. Biol. J. Linn. Soc. 70, 27–36.

    Article  Google Scholar 

  • Rantala, M.J., Ahtiainen, J.J., Suhonen, J., 2004. Fluctuating asymmetry and immune function in a field cricket. Oikos 107, 479–484.

    Article  Google Scholar 

  • Rantala, M.J., Koskimäki, J., Taskinen, J., Tynkkynen, K., Suhonen, J., 2000. Immunocompetence, developmental stability and wingspot size in the damselfly Calopteryx splendens L. Proc. R. Soc. Lond. B 267, 2453–2457.

    Article  CAS  Google Scholar 

  • Rea, L.D., Castellini, M.A., Fadely, B.S., Loughlin, T.R., 1998. Health status of young Alaska Steller sea lion pups (Eumetopiasjubatus) as indicated by blood chemistry and hematology. Comp. Biochem. Physiol. A 120, 617–623.

    Article  CAS  Google Scholar 

  • Rice, W.R., 1989. Analyzing tables of statistical tests. Evolution 43, 223–225.

    Article  PubMed  Google Scholar 

  • Rietkerk, F.E., Delima, E.C., Mubarak, S.M., 1994. The hematological profile of the mountain gazelle (Gazella Gazella): variations with sex, age, capture method, season, and anesthesia. J. Wildl. Dis. 30, 69–76.

    Article  CAS  PubMed  Google Scholar 

  • Rissing, J.P., Newman, C., Moore, W.L., 1978. Artifactual depression of serumglutamic oxaloacetic transaminase by metronidazole. Antimicrob. Agents Chemother. 14, 636–638.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roldan, E.R.S., Cassinello, J., Abáigar, T., Gomendio, M., 1998. Inbreeding, fluctuating asymmetry, and ejaculate quality in an endangered ungulate. Proc. R. Soc. Lond. B 265, 243–248.

    Article  CAS  Google Scholar 

  • Rowlands, D., Clampitt, R.B., 1979. Plasma enzyme levels in ruminants infected with Fasciola hepatica. Vet. Parasitol. 5, 155–175.

    Article  Google Scholar 

  • Säkkinen, H., Tverdal, A., Eloranta, E., Dahl, E., Holand, Ø., Saarela, S., Ropstad, E., 2005. Variation of plasma protein parameters in four free-ranging reindeer herds and in captive reindeer under defined feeding conditions. Comp. Biochem. Physiol. A 142, 503–511.

    Article  CAS  Google Scholar 

  • Sams, M.G., Lochmiller, R.L., Qualls, C.W., Leslie, D.M., 1998. Sensitivity of condition indices to changing density in a white-tailed deer population. J. Wildl. Dis. 34, 110–125.

    Article  CAS  PubMed  Google Scholar 

  • Scaradavou, A., 2002. HIV-related thrombocytopenia. Blood Rev. 16, 73–76.

    Article  CAS  PubMed  Google Scholar 

  • Sobiech, P., Radwińska, J., Krystkiewicz, W., Snarska, A., Stopyra, A., 2008. Changes in the coagulation profile of cattle with left abomasal displacement. Pol. J. Vet. Sci. 11, 301–306.

    CAS  PubMed  Google Scholar 

  • Song, W.J., Sullivan, M.G., Legare, R.D., Hutchings, S., Tan, X.L., Kufrin, D., Ratajczak, J., Resende, I.C., Haworth, C., Hock, R., Loh, M., Felix, C., Roy, D.C., Busque, L., Kurnit, D., Willman, C., Gewirtz, A.M., Speck, N.A., Bushweller, J.H., Li, F.P., Gardiner, K., Poncz, M., Maris, J.M., Gilliland, D.G., 1999. Haploinsufficiency of CBFA2 causes familial thrombocytopenia with propensity to develop acute myelogenous leukaemia. Nat. Genet. 23, 166–175.

    Article  CAS  PubMed  Google Scholar 

  • StatSoft Inc., 2007. Statistica (Data Analysis Software System). Version 8.0., http://www.statsoft.com.

  • Thuita, J.K., Kagira, J.M., Mwangangi, D., Matovu, E., Turner, C.M.R., Masiga, D., 2008. Trypanosoma brucei rhodesiense transmitted by a single tsetse fly bite in vervet monkeys as a model of human African trypanosomiasis. PLoS Negl. Trop. Dis. 2 (5), e238.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tracy, M., Freeman, D.C., Duda, J.J., Miglia, KJ., Graham, J.H., Hough, R.A., 2003. Developmental instability: an appropriate indicator of plant fitness components. In: Polak, M. (Ed.), Developmental Instability: Causes and Consequences. Oxford University Press, New York, pp. 196–212.

    Google Scholar 

  • VanValen, L., 1962. Astudy of fluctuating asymmetry. Evolution 16, 125–142.

    Article  Google Scholar 

  • Vassart, M., Greth, A., de la Farge, F., Braun, J.P., 1994. Serum chemistry values for Arabian sand gazelles (Gazella subgutturosa marica). J. Wildl. Dis. 30, 426–428.

    Article  CAS  PubMed  Google Scholar 

  • Wiesner, H., Müller, P., 1998. On the reintroduction of the Mhorr gazelle in Tunisia and Morocco. Naturwissenschaften 85, 553–555.

    Article  CAS  PubMed  Google Scholar 

  • Wolkers, H., Wensing, T., Schonewille, J.T., 1994. Effect of undernutrition on hematological and serum biochemical characteristics in red deer (Cervus elaphus). Can. J. Zool. 72, 1291–1296.

    Article  Google Scholar 

  • Wood, R.D., Goens, S.D., Carman, P.S., Deregt, D., Jefferson, B., Jacobs, R.M., 2004. Effect on hematopoietic tissue of experimental infection of calves with noncytopathic type 2 bovine viral diarrhea virus. Can. J. Vet. Res. 68, 42–48.

    PubMed  PubMed Central  Google Scholar 

  • Wyckoff, J.H., Bradley, R.E., 1985. Diagnosis of Fasciola hepatica infection in beef calves by plasma enzyme analysis. Am. J. Vet. Res. 46, 1015–1019.

    CAS  PubMed  Google Scholar 

  • Yang, H.L., Jiang, X.C., Zhang, X.Y., Li, W.J., Hu, B.Y., Zhao, G.P., Guo, X.K., 2006. Thrombocytopenia in the experimental leptospirosis of guinea pig is not related to disseminated intravascular coagulation. BMC Infect. Dis. 6, 19.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang, Q., Mao, W.H., Ferre, I., Bayón, J.E., Mao, X.Z., González Gallego, J., 1998. Plasma aspartate aminotransferase (AST), glutamate dehydrogenase (GLDH) and gamma-glutamyl transpeptidase (GGT) activities in water buffaloes with experimental subclinical fasciolosis. Vet. Parasitol. 78, 129–136.

    Article  CAS  PubMed  Google Scholar 

  • Yaralıoğlu, S., Şahin, T., Şındak, N., Yürekli, U.F., 2004. Investigation of some hematologic and biochemical parameters in the serum of gazelles (Gazella subgutturosa) in Ceylanpınar, Şanlıurfa, Turkey. Turk. J. Vet. Anim. Sci. 28, 369–372.

    Google Scholar 

  • Zakharov, V.M., Cubinishvili, A.T., Baranov, A.S., Borisov, V.I., Chistyakova, E.K., Dmitriev, S.G., Kryazheva, N.G., Krysanov, E.Y., Pronin, A.V., Valetsky, A.V., 2001. The Health of the Environment: Experience of Assessment. Center for Russian Environmental Policy and Center for the Health of the Environment, Moscow.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to José Javier Cuervo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cuervo, J.J., Dhaoui, M. & Espeso, G. Fluctuating asymmetry and blood parameters in three endangered gazelle species. Mamm Biol 76, 498–505 (2011). https://doi.org/10.1016/j.mambio.2011.01.007

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1016/j.mambio.2011.01.007

Keywords

Navigation