Cookies Notification

We use cookies to improve your website experience. To learn about our use of cookies and how you can manage your cookie settings, please see our Cookie Policy.
×

Effects of parasitism on antipredatory responses and defensive behaviors in the subterranean rodent Ctenomys talarum

Publication: Canadian Journal of Zoology
23 November 2021

Abstract

Predation represents an important evolutionary force shaping specific adaptations. Prey organisms present behavioral adaptations that allow them to recognize, avoid, and defend themselves from their predators. In addition to predation, there is a growing consensus about the role of parasitism in the structuring of biological communities. In vertebrates, the effects on hosts include changes in daily activity, feeding, mate selection, reproduction, and modifications in responses to environmental stimuli. These behavioral variations can benefit the parasite (parasitic manipulation), benefit the host, or appear as a side effect of the infection. We evaluated the influence of parasitism on the behavioral and physiological responses of the tuco-tucos of the Talas (Ctenomys talarum Thomas, 1898) to predator cues. We found that individuals exposed to cat odors and immobilization entered less often and spent less time in the transparent arms of elevated maze, exhibiting a preference for protected areas (anxiogenic response). Additionally, we evaluated if the presence of parasites affected antipredatory behaviors in C. talarum (naturally parasitized, deparasitized, or inoculated with Eimeria sp.). We did not find differences among the groups with regards to responses to predator cues. Therefore, while exposure to predator cues triggered a stress response, the manipulation of parasite loads did not modify homeostasis under these experimental conditions.

Résumé

La prédation constitue un important facteur d’évolution modulant différentes adaptations. Les organismes proies présentent des adaptations comportementales qui leur permettent de reconnaître, éviter et se défendre contre leurs prédateurs. Outre la prédation, il existe un consensus croissant concernant le rôle du parasitisme dans la structuration de communautés biologiques. Chez les vertébrés, les effets sur les hôtes comprennent des modifications de l’activité quotidienne, de l’alimentation, de la sélection de compagnons, de la reproduction et des réactions aux stimuli ambiants. Ces variations comportementales peuvent avantager le parasite (manipulation parasitique) ou l’hôte ou représenter un effet secondaire de l’infection. Nous avons évalué l’influence du parasitisme sur la réaction comportementale et physiologique du tuco-tuco des Talas (Ctenomys talarum Thomas, 1898) à des signaux de prédateurs. Nous avons constaté que les spécimens exposés à des odeurs et à l’immobilisation de chats entraient moins souvent et demeuraient moins longtemps dans des embranchements transparents de labyrinthes surélevés, montrant une préférence pour les endroits protégés (réaction anxiogène). Nous avons aussi tenté de déterminer si la présence de parasites avait une incidence sur les comportements antiprédateurs chez C. talarum (naturellement parasités, déparasités ou inoculés avec Eimeria sp.). Nous n’avons relevé aucune différence sur le plan des réactions aux signaux de prédateurs entre ces groupes. Donc, si l’exposition à des signaux de prédateurs a déclenché une réaction de stress, la manipulation des charges parasitaires n’a pas modifié l’homéostasie dans ces conditions expérimentales. [Traduit par la Rédaction]

Get full access to this article

View all available purchase options and get full access to this article.

References

Adelman J.S., Mayer C., and Hawley D.M. 2017. Infection reduces anti-predator behaviors in house finches. J. Avian Biol. 48: 519–528.
Allen P.C. and Jenkins M.C. 2010. Observations on the gross pathology of Eimeria praecox infections in chickens. Avian Dis. 54: 834–840.
Amoroso C.R. 2021. Integrating concepts of physiological and behavioral resistance to parasites. Front. Ecol. Evol. 9: 635607.
Armario A. 2006. The hypothalamic–pituitary–adrenal axis: what can it tell us about stressors? CNS Neurol. Disord. Drug Targets, 5: 485–501.
Belzung C. and Griebel G. 2001. Measuring normal and pathological anxiety-like behaviour in mice: a review. Behav. Brain Res. 125: 141–149.
Berdoy M., Webster J.P., and Macdonald D.W. 2000. Fatal attraction in rats infected with Toxoplasma gondii. Proc. R Soc. B Biol. Sci. 267(1452): 1591–1594.
Blanchard, R.J., and Blanchard, D.C. 1990. An ethoexperimental analysis of defense, fear and anxiety. In Anxiety. Edited by N. McNaughton and G. Andrews. Otago University Press, Dunedin, N.Z. pp. 124–133.
Brachetta V., Schleich C.E., and Zenuto R.R. 2014. Effects of acute and chronic exposure to predatory cues on spatial learning capabilities in the subterranean rodent Ctenomys talarum (Rodentia: Ctenomyidae). Ethology, 120: 563–576.
Brachetta V., Schleich C.E., and Zenuto R.R. 2015. Short-term anxiety response of the subterranean rodent Ctenomys talarum to odors from a predator. Physiol. Behav. 151: 596–603.
Brachetta V., Schleich C.E., and Zenuto R.R. 2016. Source odor, intensity, and exposure pattern affect antipredatory responses in the subterranean rodent Ctenomys talarum. Ethology, 122: 923–936.
Brachetta V., Schleich C.E., Cutrera A.P., Merlo J.L., Kittlein M.J., and Zenuto R.R. 2018. Prenatal predatory stress in a wild species of subterranean rodent: do ecological stressors always have a negative effect on the offspring? Dev. Psychobiol. 60(5): 567–581.
Brachetta V., Schleich C.E., and Zenuto R.R. 2020. Differential antipredatory responses in the tuco-tuco (Ctenomys talarum) in relation to endogenous and exogenous changes in glucocorticoids. J. Comp. Physiol. A, 206(1): 33–44.
Busch, C., Antinuchi, D., Del Valle, J., Kittlein, M., Malizia, A., Vassallo, A., and Zenuto, R. 2000. Population ecology of subterranean rodents. In Life underground: the biology of subterranean rodents. Edited by E. Lacey, J. Patton, and G. Cameron. University of Chicago Press, Chicago, Ill. pp. 183–226.
Canepuccia, A. 2005. Efectos del incremento de las precipitaciones sobre la estructura comunitaria de un pastizal del Sudeste de la region Pampeana, Argentina. Doctoral thesis, Universidad Nacional de Mar del Plata, Argentina.
Clinchy M., Sheriff M.J., and Zanette L.Y. 2013. Predator-induced stress and the ecology of fear. Funct. Ecol. 27: 56–65.
Coulson G., Cripps J.K., Garnick S., Bristow V., and Beveridge I. 2018. Parasite insight: assessing fitness costs, infection risks and foraging benefits relating to gastrointestinal nematodes in wild mammalian herbivores. Philos. Trans. R Soc. B Biol. Sci. 373: 20170197.
Cutrera A.P., Zenuto R.R., Luna F., and Antenucci C.D. 2010. Mounting a specific immune response increases energy expenditure of the subterranean rodent Ctenomys talarum (tuco-tuco): implications for intra and interspecific variation in immunological traits. J. Exp. Biol. 213: 715–724.
Cutrera A.P., Zenuto R.R., and Lacey E. 2011. MHC variation, multiple simultaneous infections and physiological condition in the subterranean rodent Ctenomys talarum. Infect. Genet. Evol. 11: 1023–1036.
Dielenberg R.A. and McGregor I.S. 1999. Habituation of the hiding response to cat odor in rats (Rattus norvegicus). J. Comp. Psychol. 113: 376–387.
Hatcher M.J., Dick J.T.A., and Dunn A.M. 2014. Parasites that change predator or prey behaviour can have keystone effects on community composition. Biol. Lett. 10: 20130879.
Hegab I.M., Shang G., Ye M., Jin Y., Wang A., Yin B., et al. 2014. Defensive responses of Brandt’s voles (Lasiopodomys brandtii) to chronic predatory stress. Physiol. Behav. 126: 1–7.
Holmes A., Parmigiani S., Ferrari P.F., Palanza P., and Rodgers R.J. 2000. Behavioral profile of wild mice in the elevated plus-maze test for anxiety. Physiol. Behav. 71(5): 509–516.
Hume M.E., Clemente-Hernández S., and Oviedo-Rondón E.O. 2006. Effects of feed additives and mixed Eimeria species infection on intestinal microbial ecology of broilers. Poult. Sci. 85: 2106–2111.
Johnstone C.P., Reina R.D., and Lill A. 2012. Interpreting indices of physiological stress in free-living vertebrates: a review. J. Comp. Physiol. B, 182: 861–879.
Kavaliers M. and Choleris E. 2001. Antipredator responses and defensive behavior: Ecological and ethological approaches for the neurosciences. Neurosci. Biobehav. Rev. 25: 577–586.
Kavaliers M. and Colwell D.D. 1992. Exposure to the scent of male mice infected with the protozoan parasite, Eimeria vermiformis, induces opioid- and nonopioid-mediated analgesia in female mice. Physiol. Behav. 52(2): 373–377.
Kavaliers M. and Colwell D.D. 1994. Parasite infection attenuates non-opioid mediated predator-induced analgesia. Physiol. Behav. 55: 505–510.
Kavaliers M. and Colwell D.D. 1995. Decreased predator avoidance in parasitized mice: neuromodulatory correlates. Parasitology, 111: 257–263.
Kavaliers M., Colwell D.D., and Perrot-Sinal T.S. 1997. Opioid and non-opioid NMDA-mediated predator-induced analgesia in mice and the effects of parasitic infection. Brain Res. 766(1-2): 11–18.
Kavaliers M., Colwell D., and Choleris E. 1999. Parasites and behavior: an ethopharmacological analysis and biomedical implications. Neurosci. Biobehav. Rev. 23: 1037–1045.
Kavaliers M., Colwell D.D., and Choleris E. 2000. Parasites and behaviour: an ethopharmacological perspective. Parasitol. Today, 16: 464–468.
Labaude S., Cézilly F., De Marco L., and Rigaud T. 2020. Increased temperature has no consequence for behavioral manipulation despite effects on both partners in the interaction between a crustacean host and a manipulative parasite. Sci. Rep. 10: 11670.
Malizia A.I. and Busch C. 1991. Reproductive parameters and growth in the fossorial rodent Ctenomys talarum (Rodentia: Octodontidae). Mammalia, 55 (2): 293–305.
Mastrángelo M., Schleich C.E., and Zenuto R.R. 2009. Short term effects of an acute exposure to predatory cues on the spatial memory performance in a subterranean rodent. Anim. Behav. 77: 685–692.
Merlo J.L., Cutrera A.P., and Zenuto R.R. 2016. Food restriction affects inflammatory response and nutritional state in tuco-tucos (Ctenomys talarum). J. Exp. Zool. 325: 675–687.
Moore J. 2013. An overview of parasite-induced behavioral alterations — and some lessons from bats. J. Exp. Biol. 216: 11–17.
Nerissa Ramnath K.M. 2009. Behavioral effects of parasitism in animals. J. Exotic Pet Med. 18: 254–265.
Pellow S., Chopin P., File S.E., and Briley M. 1985. Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods, 14(3): 149–167.
Poulin R. 1994. The evolution of parasite manipulation of host behaviour: a theoretical analysis. Parasitology, 109: S109–S118.
Poulin, R. 2010. Chapter 5: Parasite manipulation of host behavior: an update and frequently asked questions. In Advances in the study of behavior. Edited by H.J. Brockmann. Vol. 41. ScienceDirect. pp. 151–186.
Poulin R. and Maure F. 2015. Host manipulation by parasites: a look back before moving forward. Trends Parasitol. 31(11): 563–570.
Preston D. and Johnson P. 2010. Ecological consequences of parasitism. Nat. Educ. Knowl. 1(8): 39.
Quinn S.C., Brooks R.J., and Cawthorn R.J. 1987. Effects of the protozoan parasite Sarcocystis rauschorum on open-field behaviour of its intermediate vertebrate host, Dicrostonyx richardsoni. J. Parasitol. 73(2): 265–271.
Rodgers R.J. and Dalvi A. 1997. Anxiety, defence and the elevated plus-maze. Neurosci. Biobehav. Rev. 21(6): 801–810.
Romeo C., Wauters L.A., Santicchia F., Dantzer B., Palme R., Martinoli A., and Ferrari N. 2020. Complex relationships between physiological stress and endoparasite infections in natural populations. Curr. Zool. 66(5): 449–457.
Rossin M.A., Malizia A.I., Timi J.T., and Poulin R. 2010. Parasitism underground: determinants of helminth infections in two species of subterranean rodents (Octodontidae). Parasitology, 137: 1569–1575.
Schleich C.E., Zenuto R.R., and Cutrera A.P. 2015. Immune challenge but not dietary restriction affects spatial learning in the wild subterranean rodent Ctenomys talarum. Physiol. Behav. 139: 150–156.
Sheather A.L. 1923. The detection of intestinal protozoa and mange parasites by a floatation technique. J. Comp. Pathol. Therapeut. 36: 266–275.
Sikes R.S., and The Animal Care and Use Committee of the American Society of Mammalogists. 2016. 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J. Mammal. 97(3): 663–688.
Soghigian J., Valsdottir L.R., and Livdahl T.P. 2017. A parasite’s modification of host behavior reduces predation on its host. Ecol. Evol. 7: 1453–1461.
Thomas F., Adamo S., and Moore J. 2005. Parasitic manipulation: where are we and where should we go? Behav. Processes, 68(3): 185–199.
Thomas F., Poulin R., and Brodeur J. 2010. Host manipulation by parasites: a multidimensional phenomenon. Oikos, 119: 1217–1223.
Thomas O. 1898. Description of two Argentine rodents. Ann. Mag. Nat. Hist. 1: 283–286.
Thompson S.N. and Kavaliers M.I. 1994. Physiological bases for parasite-induced alterations of host behaviour. Parasitology, 109(Suppl.): S119–S139.
Vassallo A., Kittlein M., and Busch C. 1994. Owl predation on two sympatric species of tuco-tucos (Rodentia: Octodontidae). J. Mammal. 75: 725–732.
Vera F., Zenuto R., and Antenucci D. 2008. Decreased glucose tolerance but normal blood glucose levels in the field in the caviomorph rodent Ctenomys talarum: the role of stress and physical activity. Comp. Biochem. Physiol. A, 151: 232–238.
Vera F., Antenucci C.D., and Zenuto R.R. 2011. Cortisol and corticosterone exhibit different seasonal variation and responses to acute stress and captivity in tuco-tucos (Ctenomys talarum). Gen. Comp. Endocrinol. 170: 550–557.
Vera F., Antenucci C.D., and Zenuto R.R. 2019. Different regulation of cortisol and corticosterone in the subterranean rodent Ctenomys talarum: responses to dexamethasone, angiotensin II, potassium, and diet. Gen. Comp. Endocrinol. 273: 108–117.
Vyas A., Kim S.K., Giacomini N., Boothroyd J.C., and Sapolsky R.M. 2007. Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. Proc. Natl. Acad. Sci. U.S.A. 104: 6442–6447.
Walf A.A. and Frye C.A. 2007. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat. Protoc. 2: 322–328.
Windsor D.A. 1998. Most of the species on earth are parasites. Int. J. Parasitol. 28: 1939–1941.
Yun C.H., Lillehoj H.S., and Lillehoj E.P. 2000. Intestinal immune responses to coccidiosis. Dev. Comp. Immunol. 24: 303–324.

Information & Authors

Information

Published In

cover image Canadian Journal of Zoology
Canadian Journal of Zoology
Volume 100Number 2February 2022
Pages: 98 - 105

History

Received: 12 May 2021
Accepted: 22 October 2021
Accepted manuscript online: 23 November 2021
Version of record online: 23 November 2021

Permissions

Request permissions for this article.

Key Words

  1. predation risk
  2. parasitism
  3. parasitic manipulation
  4. subterranean rodent
  5. Ctenomys talarum
  6. tuco-tucos of the Talas
  7. antipredatory behaviors

Mots-clés

  1. risque de prédation
  2. parasitisme
  3. manipulation parasitique
  4. rongeur souterrain
  5. Ctenomys talarum
  6. tuco-tucos des Talas
  7. comportements antiprédateurs

Authors

Affiliations

V. Brachetta [email protected]
Laboratorio de Ecología Fisiológica y del Comportamiento, Instituto de Investigaciones Marinas y Costeras (IIMyC), Universidad Nacional de Mar del Plata – CONICET, C.C. 1260, Argentina.
C.E. Schleich
Laboratorio de Ecología Fisiológica y del Comportamiento, Instituto de Investigaciones Marinas y Costeras (IIMyC), Universidad Nacional de Mar del Plata – CONICET, C.C. 1260, Argentina.
R.R. Zenuto
Laboratorio de Ecología Fisiológica y del Comportamiento, Instituto de Investigaciones Marinas y Costeras (IIMyC), Universidad Nacional de Mar del Plata – CONICET, C.C. 1260, Argentina.

Funding Information

The research was supported by funds from Agencia Nacional de Promoción Científica y Tecnológica (PICT 2349) and Consejo Nacional de Investigaciones Científicas y Técnicas (PIP 0292).

Metrics & Citations

Metrics

Other Metrics

Citations

Cite As

Export Citations

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.

There are no citations for this item

View Options

Get Access

Login options

Check if you access through your login credentials or your institution to get full access on this article.

Subscribe

Click on the button below to subscribe to Canadian Journal of Zoology

Purchase options

Purchase this article to get full access to it.

Restore your content access

Enter your email address to restore your content access:

Note: This functionality works only for purchases done as a guest. If you already have an account, log in to access the content to which you are entitled.

View options

PDF

View PDF

Full Text

View Full Text

Media

Media

Other

Tables

Share Options

Share

Share the article link

Share on social media