期刊论文详细信息
Parasite
Ruminant self-medication against gastrointestinal nematodes: evidence, mechanism, and origins
and John Glendinning2  Serge Y. Landau1  Eugene D. Ungar1  James Miller3  Juan J. Villalba4 
[1] Department of Natural Resources, Institute of Plant Sciences, Agricultural Research Organization, the Volcani Center,Bet Dagan50250,Israel;Department of Biology, Barnard College, Columbia University,3009 Broadway,New York,NY,USA;Department of Pathobiological Sciences, School of Veterinary Medicine, Louisiana State University,70803Baton Rouge,USA;Department of Wildland Resources, Utah State University,5230 Old Main Hill,Logan,Utah84322-5230,USA
关键词: Learning;    Condensed tannins;    Foraging behavior;    Diet selection;   
Others  :  808294
DOI  :  doi:10.1051/parasite/2014032
 received in 2014-01-10, accepted in 2014-06-17,  发布年份 2014
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【 摘 要 】

Gastrointestinal helminths challenge ruminants in ways that reduce their fitness. In turn, ruminants have evolved physiological and behavioral adaptations that counteract this challenge. Ruminants display anorexia and avoidance behaviors, which tend to reduce the incidence of parasitism. In addition, ruminants appear to learn to self-medicate against gastrointestinal parasites by increasing consumption of plant secondary compounds with antiparasitic actions. This selective feeding improves health and fitness. Here, we review the evidence for self-medication in ruminants, propose a hypothesis to explain self-medicative behaviors (based on post-ingestive consequences), and discuss mechanisms (e.g., enhanced neophilia, social transmission) that may underlie the ontogeny and spread of self-medicative behaviors in social groups. A better understanding of the mechanisms that underlie and trigger self-medication in parasitized animals will help scientists devise innovative and more sustainable management strategies for improving ruminant health and well-being.

【 授权许可】

   
© J.J. Villalba et al., published by EDP Sciences, 2014

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【 参考文献 】
  • [1]Albers GAA, Gray GD, Piper LR, Barber JSF, LeJambre LF, Barger IA. 1987. The genetics of resistance and resilience to Haemonchus contortus infection in young Merino sheep. International Journal of Parasitology, 17, 1355–1367.
  • [2]Amit A, Cohen I, Marcovics A, Muklada H, Glasser TA, Ungar ED, Landau SY. 2013. Self-medication with tannin-rich browse in goats infectedwith gastro-intestinal nematodes. Veterinary Parasitology, 198, 305–311. [PubMed]
  • [3]Athanasiadou S, Arsenos G, Kyriazakis I. 2002. Animal health and welfare issues arising in organic ruminant production systems, in Organic Meat and Milk from Ruminants. Kyriazakis I, Zervas G, Editors. Wageningen Academic Publishers. p. 39–56.
  • [4]Azaizeh H, Halahleh F, Abbas N, Markovics A, Muklada H, Ungar ED, Landau SY. 2012. Polyphenols from Pistacia lentiscus and Phillyrea latifolia impair the exsheathment of gastro-intestinal nematode larvae. Veterinary Parasitology, 191, 44–50. [PubMed]
  • [5]Barroso FG, Alados CL, Boza J. 2000. Social hierarchy in the domestic goat: effect on food habits and production. Applied Animal Behaviour Science, 69, 35–53. [PubMed]
  • [6]Bell WJ. 1991. Searching behaviour. The behavioral ecology of finding resources. Cambridge University Press: Cambridge.
  • [7]Bernays EA, Singer MS. 2005. Taste alteration and endoparasites. Nature, 436, 476. [PubMed]
  • [8]Bown MD, Poppi DP, Sykes AR. 1991. The effect of post-ruminal infusion of protein or energy on the pathophysiology of Trichostrongylus colubriformis infection and body composition in lambs. Australian Journal of Agricultural Research, 42, 253–267.
  • [9]Brown JS. 1988. Patch use as an indicator of habitat preference, predation risk, and competition. Behavioral Ecology and Sociobiology, 22, 37–47.
  • [10]Burritt EA, Provenza FD. 1991. Ability of lambs to learn with a delay between food ingestion and consequences given meals containing novel and familiar foods. Applied Animal Behaviour Science, 32, 179–189.
  • [11]Caraco T, Blanckenhorn WU, Gregory GM, Newman JA, Recer GM, Zwicker SM. 1990. Risk-sensitivity: ambient temperature affects foraging choice. Animal Behaviour, 39, 338–345.
  • [12]Catoni C, Peters A, Schaefer M. 2008. Life history trade-offs are influenced by the diversity, availability and interactions of dietary antioxidants. Animal Behaviour, 76, 1107–1119.
  • [13]Coop RL, Kyriazakis I. 1999. Nutrition-parasite interactions. Veterinary Parasitology, 84, 187–204. [PubMed]
  • [14]Cooper J, Gordon IJ, Pike AW. 2000. Strategies for the avoidance of faeces by grazing sheep. Applied Animal Behaviour Science, 69, 15–33. [PubMed]
  • [15]Dunn AM. 1978. Veterinary Helminthology. William Heinemann Medical Books LTD: London. p. 173–185.
  • [16]Forbes AB, Huckle CA, Gibb MJ. 2004. Impact of eprinomectin on grazing behavior and performance in dairy cattle with sub-clinical gastrointestinal nematode infections under continuous stocking management. Veterinary Parasitology, 125, 353–364. [PubMed]
  • [17]Forbes AB, Huckle CA, Gibb MJ. 2007. Evaluation of the effect of eprinomectin in young dairy heifers sub-clinically infected with gastrointestinal nematodes on grazing behaviour and diet selection. Veterinary Parasitology, 150, 321–332. [PubMed]
  • [18]Fox NJ, Marion G, Davidson RS, White PCL, Hutchings MR. 2013. Modelling parasite transmission in a grazing system: the importance of host behaviour and immunity. PLoS ONE, 8(11), e77996. [PubMed]
  • [19]Ferreira AM, Araujo SS, Sales-Baptista E, Almeida AM. 2012. Identification of novel genes for bitter taste receptors in sheep (Ovis aries). Animal, 7, 547–554. [PubMed]
  • [20]Galef BG, Jr. 1991. Social factors in diet selection and poison avoidance by Norway Rats: A brief review, in Appetite and Nutrition. Friedman MI, Tordoff MG, Kare MR, Editors. Marcel Deckker: New York. p. 177–194.
  • [21]Garcia J, Hankins WG. 1975. The evolution of bitter and the acquisition of toxiphobia, in Olfaction and Taste, in V. Proceedings of the 5th International Symposium in Melbourne Australia. Denton DA, Coghlan JP, Editors. Academic Press: New York. p. 39–45.
  • [22]Garcia-Gonzalez R, Cuartas P. 1989. A comparison of the diets of the wild goat (Capra pyrenaica), domestic goat (Capra hircus), mouflon (Ovis musimon) and domestic sheep (Ovis aries) in the Cazorla mountain range. Acta Biologica Montana, 9, 123–132.
  • [23]Gardiner MR. 1966. Pathological Changes and Vitamin B12 Metabolism in Sheep Parasitised by Haemonchus contortus, Ostertagia spp. and Trichostrongylus colubriformis. Journal of Helminthology, 40, 63–76. [PubMed]
  • [24]Glasser TA, Ungar ED, Landau SY, Perevolotsky A, Muklada H, Walker JW. 2009. Breed and maternal effects on the intake of tannin-rich browse by juvenile domestic goats (Capra hircus). Applied Animal Behaviour Science, 119, 71–77.
  • [25]Glasser TA, Landau SY, Ungar ED, Perevolotsky A, Dvash L, Muklada H, Kababya D, Walker JW. 2012. Foraging selectivity of three goat breeds in a Mediterranean shrubland. Small Ruminant Research, 102, 7–12.
  • [26]Glendinning JI. 1992. Effect of salivary proline-rich proteins on ingestive responses to tannic acid in mice. Chemical Senses, 17, 1–12.
  • [27]Glendinning JI. 1994. Is the bitter rejection response always adaptive? Physiology & Behavior, 56, 1217–1227. [PubMed]
  • [28]Glendinning JI. 2007. How do predators cope with chemically defended foods? Biological Bulletin, 213, 252–266.
  • [29]Glendinning JI, Yiin YM, Ackroff K, Sclafani A. 2008. Intragastric infusion of denatonium conditions flavor aversions and delays gastric emptying in rodents. Physiology & Behavior, 93, 757–765. [PubMed]
  • [30]Gradé JT, Tabuti JRS, Van Damme P. 2009. Four footed pharmacists: indications of self-medicating livestock in Karamoja, Uganda. Economic Botany, 63, 29–42.
  • [31]Hart BL. 1988. Biological basis of the behavior of sick animals. Neuroscience & Biobehavioral Reviews, 12, 123–137.
  • [32]Hart BL. 2005. The evolution of herbal medicine: behavioural perspectives. Animal Behaviour, 70, 975–989.
  • [33]Huffman MA. 1997. Current evidence for self-medication in primates: a multidisciplinary perspective. Yearbook of Physical Anthropology, 40, 171–200.
  • [34]Huffman MA, Ohigashi H, Kawanaka M, Page JE, Kirby GC, Gasquet M, Murakami A, Koshimizu K. 1998. African great ape self-medication: A new paradigm for treating parasite disease with natural medicines? in Towards Natural Medicine Research in the 21st Century. Ageta H, Aimi N, Ebizuka Y, Fujita T, Honda G, Editors. Elsevier Science B.V: Amsterdam. p. 113–123.
  • [35]Huffman MA, Seifu M. 1989. Observations on the illness and consumption of a possibly medicinal plant Vernonia amygdalina by a wild chimpanzee in the Mahale Mountains National Park, Tanzania. Primates, 30, 51–63.
  • [36]Huffman MA. 2001. Self-medicative behavior in the African great apes: An evolutionary perspective into the origins of human traditional medicine. BioScience, 51, 651–661.
  • [37]Huffman MA. 2007. Primate self-medication, in Primates in Perspective. Campbell CJ, Fuentes A, MacKinnon KC, Panger M, Bearder SK, Editors. Oxford University Press: Oxford. p. 677–690.
  • [38]Huffman MA, Spiezio C, Sgaravatti A, Leca JB. 2010. Leaf swallowing behavior in chimpanzees (Pan troglodytes): Biased learning and the emergence of group level cultural differences. Animal Cognition, 13, 871–880. [PubMed]
  • [39]Hutchings MR, Gordon IJ, Kyriazakis I, Robertson E, Jackson F. 2002. Grazing in heterogeneous environments: infra- and supra- parasite distributions determine herbivore grazing decisions. Oecolagia, 132, 453–460.
  • [40]Hutchings MR, Athanasiadou S, Kyriazakis I, Gordon I. 2003. Can animals use foraging behaviour to combat parasites? Proceedings of the Nutrition Society, 62, 361–370.
  • [41]Jackson F, Miller J. 2006. Alternative approaches to control-quo vadit? Veterinary Parasitology, 139, 371–384. [PubMed]
  • [42]Jackson F, Varady M, Bartley DJ. 2012. Managing anthelmintic resistance in goats – Can we learn lessons from sheep? Small Ruminant Research, 103, 3–9.
  • [43]Janzen J. 1978. Complications in interpreting the chemical defenses of trees against tropical arboreal plant-eating vertebrates, in The Ecology of Arboreal Folivores. Montgomery G, Editor. Smithsonian Institution Press: Washington, D.C., USA. p. 73–84.
  • [44]Juhnke J, Miller J, Hall JO, Provenza FD, Villalba JJ. 2012. Preference for condensed tannins by sheep in response to challenge infection with Haemonchus contortus. Veterinary Parasitology, 188, 104–114. [PubMed]
  • [45]Kababya D, Perevolotsky A, Bruckental I, Landau S. 1998. Selection of diets by dual-purpose Mamber goats in Mediterranean woodland. Journal of Agricultural Science (Cambridge), 131, 221–228.
  • [46]Kalat JW. 1974. Taste salience depends on novelty, not concentration, in taste-aversion learning in the rat. Journal of Comparative and Physiological Psychology, 86, 47–50. [PubMed]
  • [47]Kidane A, Houdijk J, Athanasiadou S, Tolkamp B, Kyriazakis I. 2013. Nutritional sensitivity of periparturient resistance to nematode parasites in two breeds of sheep with different nutrient demands. British Journal of Nutrition, 104, 1477–1486.
  • [48]Knox MR, Torres-Acosta JFJ, Aguilar-Caballero AJ. 2006. Exploiting the effect of dietary supplementation of small ruminants on resilience and resistance against gastrointestinal nematodes. Veterinary Parasitology, 139, 385–393. [PubMed]
  • [49]Koshimizu K, Ohigashi H, Huffman M. 1994. Use of Vernonia amygdalina by wild chimpanzee: Possible roles of its bitter and related constituents. Physiology & Behavior, 56, 1209–1216. [PubMed]
  • [50]Kyriazakis I, Tolkamp BJ, Hutchings MR. 1998. Towards a functional explanation for the occurrence of anorexia during parasitic infections. Animal Behaviour, 56, 265–274. [PubMed]
  • [51]Kyriazakis I, Oldham JD, Coop RL, Jackson F. 1994. The effect of subclinical intestinal nematode infection on the diet selection of growing sheep. British Journal of Nutrition, 72, 665–677.
  • [52]Kyriazakis I, Anderson DH, Oldham JD, Coop RL, Jackson F. 1996. Long-term subclinical infection with Trichostrongylus colubriformis: effects on food intake, diet selection and performance of growing lambs. Veterinary Parasitology, 61, 297–313. [PubMed]
  • [53]Kyriazakis I, Tolkamp BJ, Hutchings MR. 1998. Towards a functional explanation for the occurrence of anorexia during parasitic infection. Animal Behaviour, 56, 265–274. [PubMed]
  • [54]Kyriazakis I. 2010. Is anorexia during infection in animals affected by food composition? Animal Feed Science and Technology, 156, 1–9.
  • [55]Lamoot I, Callebaut J, Degezelle T, Demeulenaere E, Laquière J, Vandenberghe C, Hoffmann M. 2004. Eliminative behaviour of free-ranging horses: Do they show latrine behaviour or do they defecate where they graze? Applied Animal Behavior Science, 86, 105–121.
  • [56]Landau SY, Azaizeh H, Muklada H, Glasser T, Ungar ED, Baram H, Abbas N, Markovics A. 2010. Anthelmintic activity of Pistacia lentiscus foliage in two Middle Eastern breeds of goats differing in their propensity to consume tannin-rich browse. Veterinary Parasitology, 173, 280–286. [PubMed]
  • [57]Langhans W. 2000. Anorexia of infection: current prospects. Nutrition, 16, 996–1005. [PubMed]
  • [58]Lefèvre T, Oliver L, Hunter MD, De Roode JC. 2010. Evidence for transgenerational medication in nature. Ecology Letters, 13, 1485–1493. [PubMed]
  • [59]Lisonbee LD, Villalba JJ, Provenza FD, Hall JO. 2009. Tannins and self-medication: Implications for sustainable parasite control in herbivores. Behavioural Processes, 82, 184–189. [PubMed]
  • [60]Martínez-Ortiz de-Montellano C, Vargas-Magaña JJ, Canul-Ku HL, Miranda-Soberanis R, Capetillo-Leal C, Sandoval-Castro CA, Hoste H, Torres-Acosta JFJ. 2010. Effect of a tropical tannin-rich plant Lysiloma latisiliquum on adult populations of Haemonchus contortus in sheep. Veterinary Parasitology, 172, 283–290. [PubMed]
  • [61]Min BR, Hart SP. 2003. Tannins for suppression of internal parasites. Journal of Animal Science, 81, E102–E109.
  • [62]Mirza SN, Provenza FD. 1990. Preference of the mother affects selection and avoidance of foods by lambs differing in age. Applied Animal Behaviour Science, 28, 255–263.
  • [63]Mirza SN, Provenza FD. 1992. Effects of age and conditions of exposure on maternally mediated food selection by lambs. Applied Animal Behaviour Science, 33, 35–42.
  • [64]Mueller-Harvey I. 2006. Unravelling the conundrum of tannins in animal nutrition and health. Journal of the Science of Food and Agriculture, 86, 2010–2037.
  • [65]Osoro K, Mateos-Sanz A, Frutos P, Garcia U, Ortega-Mora LM, Ferreira LMM, Celaya R, Ferre I. 2007. Anthelmintic and nutritional effects of heather supplementation on Cashmere goats grazing perennial ryegrass-white clover pastures. Journal of Animal Science, 85, 861–870. [PubMed]
  • [66]Palo RT, Robbins CT. 1991. Plant defenses against mammalian herbivory. CRC Press: Boca Raton.
  • [67]Pelchat ML, Grill HJ, Rozin P, Jacobs J. 1983. Quality of acquired responses to tastes by Rattus norvegicus depends on type of associated discomfort. Journal of Comparative Psychology, 97, 140–153. [PubMed]
  • [68]Poppi DP, Sykes AR, Dynes RA. 1990. The effect of endoparasitism on host nutrition: the implications for nutrient manipulation. Proceedings of the New Zealand Society of Animal Production, 50, 237–243.
  • [69]Provenza FD. 1995. Postingestive feedback as an elementary determinant of food preference and intake in ruminants. Journal of Range Management, 48, 2–17.
  • [70]Provenza FD, Villalba JJ, Cheney CD, Werner SJ. 1998. Self-organization of foraging behavior: from simplicity to complexity without goals. Nutrition Research Reviews, 11, 199–222. [PubMed]
  • [71]Provenza FD, Villalba JJ. 2006. Foraging in domestic herbivores: Linking the Internal and External Milieu, in Feeding in Domestic Vertebrates: From Structure to Function. Bels VL, Editor. CABI Publ: Oxfordshire. p. 210–240.
  • [72]Sanga U, Provenza FD, Villalba JJ. 2011. Transmission of self-medicative behaviour from mother to offspring in sheep. Animal Behaviour, 82, 219–227.
  • [73]Shrader AM, Kerley GIH, Kotler BP, Brown JS. 2007. Social information, social feeding, and competition in group-living goats (Capra hircus). Behavioral Ecology, 18, 103–107.
  • [74]Singer MS, Mace KC, Bernays EA. 2009. Self-medication as adaptive plasticity: increased ingestion of plant toxins by parasitized caterpillars. PLoS ONE, 4(3), e4796. [PubMed]
  • [75]Sykes AR. 1983. Effects of parasitism on metabolism in the sheep, in Sheep Production. Haresign W, Editor. Butterworths: London. p. 317–334.
  • [76]Sykes AR. 1987. Endoparasites and herbivore nutrition, in The Nutrition of Herbivores. Hacker JB, Ternouth JH, Editors. Academic Press: Sydney. p. 211–232.
  • [77]Symons LEA. 1985. Anorexia: occurrence, pathophysiology and possible causes in parasitic infections. Advances in Parasitology, 24, 103–133. [PubMed]
  • [78]Szyszka O, Tolkamp BJ, Edwards SA, Kyriazakis I. 2013. Do the changes in the behaviours of cattle during parasitism with Ostertagia ostertagi have a potential diagnostic value? Veterinary Parasitology, 193, 214–222. [PubMed]
  • [79]Thorhallsdottir AG, Provenza FD, Balph DF. 1990. Ability of lambs to learn about novel foods while observing or participating with social models. Applied Animal Behaviour Science, 25, 25–33.
  • [80]Torregosa AM, Dearing MD. 2009. Nutritional toxicology of mammals: regulated intake of plant secondary compounds. Functional Ecology, 23, 48–56.
  • [81]Vargas-Magaña JJ, Aguilar-Caballero AJ, Torres-Acosta JF, Sandoval-Castro CA, Hoste H, Capetillo-Leal CM. 2013. Tropical tannin-rich fodder intake modifies saliva-binding capacity in growing sheep. Animal, 7, 1921–1924. [PubMed]
  • [82]Villalba JJ, Provenza FD. 1996. Preference for flavored wheat straw by lambs conditioned with intraruminal administrations of sodium propionate. Journal of Animal Science, 74, 2362–2368. [PubMed]
  • [83]Villalba JJ, Provenza FD. 1997a. Preference for wheat straw by lambs conditioned with intraruminal infusions of starch. British Journal of Nutrition, 77, 287–297.
  • [84]Villalba JJ, Provenza FD. 1997b. Preference for flavored foods by lambs conditioned with intraruminal administrations of nitrogen. British Journal of Nutrition, 78, 545–561.
  • [85]Villalba JJ, Provenza FD. 1997c. Preference for flavored wheat straw by lambs conditioned with intraruminal infusions of acetate and propionate. Journal of Animal Science, 75, 2905–2914.
  • [86]Villalba JJ, Provenza FD, Rogosic J. 1999. Preference for flavored wheat straw by lambs conditioned with intraruminal infusions of starch administered at different times after straw ingestion. Journal of Animal Science, 77, 3185–3190. [PubMed]
  • [87]Villalba JJ, Provenza FD, Hall JO, Lisonbee LD. 2010. Selection of tannins by sheep in response to gastrointestinal nematode infection. Journal of Animal Science, 88, 2189–2198. [PubMed]
  • [88]Villalba JJ, Landau SY. 2012. Host behaviour, environment and ability to self-medicate. Small Ruminant Research, 103, 50–59.
  • [89]Villalba JJ, Miller J, Hall JO, Clemensen AK, Stott R, Snyder D, Provenza FD. 2013. Preference for tanniferous (Onobrychis viciifolia) and non-tanniferous (Astragalus cicer) forage plants by sheep in response to challenge infection with Haemonchus contortus. Small Ruminant Research, 112, 199–207.
  • [90]Vitazkova SK, Long E, Paul A, Glendinning JI. 2001. Mice suppress malaria infection by sampling a “bitter” chemotherapy agent. Animal Behaviour, 61, 887–894.
  • [91]Zahorik DM, Houpt KA, Swartzman-Andert J. 1990. Taste-aversion learning in three species of ruminants. Applied Animal Behaviour Science, 26, 27–39.
  • [92]Zhu X, He L, McCluskey LP. 2014. Ingestion of bacterial lipopolysaccharide inhibits peripheral taste responses to sucrose in mice. Neuroscience, 258, 47–61. [PubMed]
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