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Strongylid infection varies with age, sex, movement and social factors in wild African elephants

Published online by Cambridge University Press:  09 January 2020

Jenna M. Parker Open the ORCID record for Jenna M. Parker [Opens in a new window] ,
Shifra Z. Goldenberg ,
David Letitiya  and
George Wittemyer
Jenna M. Parker*
Affiliation:
Graduate Degree Program in Ecology and Department of Fish, Wildlife and Conservation Biology, Colorado State University, 1474 Campus Delivery, Fort Collins, CO80523, USA Save the Elephants, Marula Manor, Marula Lane, Karen, Nairobi00200, Kenya
Shifra Z. Goldenberg
Affiliation:
Save the Elephants, Marula Manor, Marula Lane, Karen, Nairobi00200, Kenya Conservation Ecology Center, Smithsonian Conservation Biology Institute, 1500 Remount Road, Front Royal, VA22630, Kenya Institute for Conservation Research, San Diego Zoo Global, 15600 San Pasqual Valley Road, Escondido, CA92027, USA
David Letitiya
Affiliation:
Save the Elephants, Marula Manor, Marula Lane, Karen, Nairobi00200, Kenya
George Wittemyer
Affiliation:
Graduate Degree Program in Ecology and Department of Fish, Wildlife and Conservation Biology, Colorado State University, 1474 Campus Delivery, Fort Collins, CO80523, USA Save the Elephants, Marula Manor, Marula Lane, Karen, Nairobi00200, Kenya
*
Author for correspondence: Jenna M. Parker, E-mail: [email protected]
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Abstract

Comparing parasitic infection among individuals of wildlife populations can provide insight into factors that influence wildlife disease ecology. Strongylids are parasitic worms that infect the intestinal tract of vertebrates, and infection with strongylids can be approximated by counting strongylid eggs in dung samples. Here we tested for correlations between strongylid egg counts and 18 different individual characteristics, environmental and social factors in individually known wild African elephants. We counted more eggs in the dung samples of younger elephants and females relative to mature elephants and males. We also found that elephants spending more time outside reserves shed more strongylid eggs than elephants that were more often within reserves. Elephants that were less socially integrated, as measured by how much aggression they received from other elephants, shed fewer strongylid eggs; relatedly, socially isolated orphan elephants that had left their family shed fewer strongylid eggs than elephants that remained with their family. Our results suggest that landscapes altered by livestock grazing and social disruption caused by humans may impact parasitic infection in wildlife.

Keywords

Conservationdisease ecologyfaecal egg countsgastrointestinal nematodelivestock grazingLoxodonta africanaorphanparasitismpoachingsocial networks
Type
Research Article
Information
Parasitology , Volume 147 , Issue 3 , March 2020 , pp. 348 - 359
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Copyright
Copyright © Cambridge University Press 2019

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References

Akinyi, MY, Jansen, D, Habig, B, Gesquiere, LR, Susan, C, Archie, EA, Alberts, SC, Archie, EA (2019) Costs and drivers of helminth parasite infection in wild female baboons. Journal of Animal Ecology 88, 1029–1043. doi: 10.1111/1365-2656.12994.CrossRefGoogle Scholar
Albery, GF, Kenyon, F, Morris, A, Morris, S, Nussey, DH and Pemberton, JM (2018) Seasonality of helminth infection in wild red deer varies between individuals and between parasite taxa. Parasitology 145, 1410–1420.CrossRefGoogle Scholar
Allen, K, Follis, T and Kistner, T (1974) Ocurrence of Grammocephalus clathratus (Baird, 1868) Raillet and Henry, 1910 (Nematoda: Ancylostomatidae), in an African Elephant imported into the United States. Journal of Parasitology 60, 952.CrossRefGoogle Scholar
Arnold, TW (2010) Uninformative parameters and model selection using Akaike's information criterion. Journal of Wildlife Management 74, 1175–1178.CrossRefGoogle Scholar
Baines, L, Morgan, ER, Ofthile, M and Evans, K (2015) Occurrence and seasonality of internal parasite infection in elephants, Loxodonta africana, in the Okavango Delta, Botswana. International Journal for Parasitology: Parasites and Wildlife 4, 43–48.Google ScholarPubMed
Barrat, A, Barthélemy, M, Pastor-Satorras, R and Vespignani, A (2004) The architecture of complex weighted networks. Proceedings of the National Academy of Sciences 101, 3737–3752.CrossRefGoogle ScholarPubMed
Bates, D, Mächler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.CrossRefGoogle Scholar
Bivand, R and Lewin-Koh, N (2019) maptools: Tools for Handling Spatial Objects. R package version 0.9-5.Google Scholar
Bivand, RS, Pebesma, E and Gomez-Rubio, V (2013) Applied Statistical Analysis with R. New York: Springer.Google Scholar
Bivand, R, Keitt, T and Rowlingston, B (2019) Bindings for the ‘Geospatial’ Data Abstraction Library. R package version 1.3-9.Google Scholar
Buma, B (2015) Disturbance interactions: characterization, prediction, and the potential for cascading effects. Ecosphere 6, 1–15.CrossRefGoogle Scholar
Burnham, KP and Anderson, DR (2004) Multimodel inference. Sociological Methods & Research 33, 261–304.CrossRefGoogle Scholar
Cerling, TE, Wittemyer, G, Rasmussen, HB, Vollrath, F, Cerling, CE, Robinson, TJ and Douglas-Hamilton, I (2006) Stable isotopes in elephant hair document migration patterns and diet changes. Proceedings of the National Academy of Sciences 103, 371–373.CrossRefGoogle ScholarPubMed
Cizauskas, CA, Turner, WC, Pitts, N and Getz, WM (2015) Seasonal patterns of hormones, macroparasites, and microparasites in wild African ungulates: the interplay among stress, reproduction, and disease. PLoS ONE 10, e0120800–29.CrossRefGoogle Scholar
Condy, JB (1974) Observation on internal parasites in Rhodesian elephants, Loxodonta africana Blumenback 1797. Proceedings and Transactions of the Rhodesia Scientific Association 55, 67–99.Google Scholar
Côte, IM and Poulin, R (1995) Parasitism and group size in social animals: a meta-analysis. Behavioral Ecology 2, 159–165.CrossRefGoogle Scholar
Crompton, DWT and Nesheim, MC (2002) Nutritional impact of intestinal helminthiasis during the human life cycle. Annual Review of Nutrition 22, 35–59.CrossRefGoogle ScholarPubMed
Csárdi, G and Nepusz, T (2006) The igraph software package for complex network research. Interjournal Complex Systems, 1965. doi: 10.3724/SP.J.1087.2009.02191Google Scholar
Eloff, AK and van Hoven, W (1980) Intestinal Protozoa of the African Elephant Loxodonta Africana (Blumenbach). South African Journal of Zoology 15, 83–90.Google Scholar
ESRI (Environmental Systems Research Institute) (2017) ArcGIS Release 10.5. Redlands, CA.Google Scholar
Evans, KE and Harris, S (2008) Adolescence in male African elephants, Loxodonta africana, and the importance of sociality. Animal Behaviour 76, 779–787.CrossRefGoogle Scholar
Ezenwa, VO and Worsley-Tonks, KEL (2018) Social living simultaneously increases infection risk and decreases the cost of infection. Proceedings of the Royal Society B: Biological Sciences 285, 20182142. doi: 10.1098/rspb.2018.2142.CrossRefGoogle ScholarPubMed
Farine, DR and Whitehead, H (2015) Constructing, conducting and interpreting animal social network analysis. Journal of Animal Ecology 84, 1144–1163.CrossRefGoogle ScholarPubMed
Fournier, DA, Skaug, HJ, Ancheta, J, Ianelli, J, Magnusson, A, Maunder, MN, Nielsen, A and Sibert, J (2012) AD Model builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optimization Methods and Software 27, 233–249.CrossRefGoogle Scholar
Gibbons, L, Jacobs, DE, Fox, MT and Hansen, J (2004) The RVC/FAO guide to veterinary diagnostic parasitology. McMaster egg-counting technique. Available at http://www.rvc.ac.uk/review/Parasitology/EggCount/Purpose.htm (accessed March 2015).Google Scholar
Ginsberg, JR and Young, TP (1992) Measuring association between individuals or groups in behavioural studies. Animal Behaviour 44, 377–379.CrossRefGoogle Scholar
Goldenberg, SZ (2016) Ivory poaching, sociality, and the role of behavior in conservation. Colorado State U, PhD dissertation.Google Scholar
Goldenberg, SZ and Wittemyer, G (2017) Orphaned female elephant social bonds reflect lack of access to mature adults. Scientific Reports 7, 14408.CrossRefGoogle ScholarPubMed
Goldenberg, SZ and Wittemyer, G (2018) Orphaning and natal group dispersal are associated with social costs in female elephants. Animal Behaviour 143, 1–8.CrossRefGoogle Scholar
Goldenberg, SZ, Douglas-hamilton, I and Wittemyer, G (2018) Inter-generational change in African elephant range use is associated with poaching risk, primary productivity and adult mortality. Proceedings of the Royal Society B: Biological Sciences 285, 20180286. doi: 10.1098/rspb.2018.0286.CrossRefGoogle ScholarPubMed
González-Hernández, M, Rangel-Negrín, A, Schoof, VAM, Chapman, CA, Canales-Espinosa, D and Dias, PAD (2014) Transmission patterns of pinworms in two sympatric congeneric primate species. International Journal of Primatology 35, 445–462.CrossRefGoogle Scholar
Gorelick, N, Hancher, M, Dixon, M, Ilyushchenko, S, Thau, D and Moore, R (2017) Google earth engine: planetary-scale geospatial analysis for everyone. Remote Sensing of Environment 202, 18–27.CrossRefGoogle Scholar
Handcock, M, Hunter, D, Butts, C, Goodreau, S, Krivitsky, P and Morris, M (2018) ergm: Fit, Simulate and Diagnose Exponential-Family Models for Networks. The Statnet Project. R package version 3.9.4.Google Scholar
Hijmans, RJ (2019) Introduction to the ‘ Raster’ Package (Version 2. 8-19).Google Scholar
Hunter, D, Handcock, M, Butts, C, Goodreau, S and Morris, M (2008) Ergm: a package to fit, simulate and diagnose exponential-family models for networks. Journal of Statistical Software 24, 1–29.CrossRefGoogle ScholarPubMed
Ihwagi, FW, Wang, T, Wittemyer, G, Skidmore, AK, Toxopeus, AG, Ngene, S, King, J, Worden, J, Omondi, P and Douglas-Hamilton, I (2015) Using poaching levels and elephant distribution to assess the conservation efficacy of private, communal and government land in northern Kenya. PLoS ONE 10, e0139079. doi: 10.1371/journal.pone.0139079.CrossRefGoogle ScholarPubMed
IUCN (2019) The IUCN Red List of Threatened Species. Version 2019-3. http://www.iucnredlist.org (accessed September 2019).Google Scholar
Khan, MN, Sajid, MS, Khan, MK, Iqbal, Z and Hussain, A (2010) Gastrointestinal helminthiasis: prevalence and associated determinants in domestic ruminants of district Toba Tek Singh, Punjab, Pakistan. Parasitology Research 107, 787–794.CrossRefGoogle ScholarPubMed
Khan, MA, Roohi, N and Rana, MAA (2015) Strongylosis in equines: a review. Journal of Animal and Plant Sciences 25(1), 1–9.Google Scholar
Kim, M and Kyung, M (2017) Maximum likelihood estimation of logistic random effects model. Korean Journal of Applied Statistics 30, 957–981.Google Scholar
Krause, J, Croft, DP and James, R (2007) Social network theory in the behavioural sciences: potential applications. Behavioral Ecology and Sociobiology 62, 15–27.CrossRefGoogle Scholar
Lafferty, KD and Holt, RD (2003) How should environmental stress affect the population dynamics of disease? Ecology Letters 6, 654–664.CrossRefGoogle Scholar
Lester, HE and Matthews, JB (2014) Faecal worm egg count analysis for targeting anthelmintic treatment in horses: points to consider. Equine Veterinary Journal 46, 139–145.CrossRefGoogle ScholarPubMed
Leung, TLF and Koprivnikar, J (2019) Your infections are what you eat: how host ecology shapes the helminth parasite communities of lizards. Journal of Animal Ecology 88, 416–426.CrossRefGoogle ScholarPubMed
Levecke, B, Behnke, JM, Ajjampur, SSR, Albonico, M, Ame, SM, Charlier, J, Geiger, SM, Hoa, NTV, Ngassam, RIK, Kotze, AC, et al. (2011) A comparison of the sensitivity and fecal egg counts of the McMaster egg counting and Kato–Katz thick smear methods for soil-transmitted helminths. PLoS Neglected Tropical Diseases 5(6), e1201. doi: 10.1371/journal.pntd.0001201.CrossRefGoogle ScholarPubMed
Lynsdale, CL, dos Santos, DJF, Hayward, AD, Mar, KU, Htut, W, Aung, HH, Soe, AT and Lummaa, V (2015) A standardised faecal collection protocol for intestinal helminth egg counts in Asian elephants, Elephas maximus. International Journal for Parasitology: Parasites and Wildlife 4, 307–315.Google ScholarPubMed
Lynsdale, CL, Mumby, HS, Hayward, AD, Mar, KU and Lummaa, V (2017) Parasite-associated mortality in a long-lived mammal: variation with host age, sex, and reproduction. Ecology and Evolution 7, 10904–10915.CrossRefGoogle Scholar
MacIntosh, AJJ, Jacobs, A, Garcia, C, Shimizu, K, Mouri, K, Huffman, MA and Hernandez, AD (2012) Monkeys in the middle: parasite transmission through the social network of a wild primate. PLoS ONE 7, 15–21.CrossRefGoogle ScholarPubMed
Maizels, RM, Hewitson, JP and Smith, KA (2012) Susceptibility and immunity to helminth parasites. Current Opinion in Immunology 24, 459–466.CrossRefGoogle ScholarPubMed
Mclean, AER, Kinsella, JM, Chiyo, P, Obanda, V, Moss, C and Archie, A (2012) Genetic identification of five strongyle nematode parasites in wild African elephants (Loxodonta africana). Journal of Wildlife Diseases 48, 707–716.CrossRefGoogle Scholar
Moss, C (1988) Elephant Memories: Thirteen Years in the Life of an Elephant Family. Chicago: The University of Chicago Press.Google Scholar
Obanda, V, Iwaki, T, Mutinda, NM and Gakuya, F (2011) Gastrointestinal parasites and associated pathological lesions in starving free-ranging African elephants. South African Journal of Wildlife Research 41, 167–172.CrossRefGoogle Scholar
Pagano, AM and Arnold, TW (2009) Detection probabilities for ground-based breeding waterfowl surveys. Journal of Wildlife Management 73, 392–398.CrossRefGoogle Scholar
Pebesma, EJ and Bivand, RS (2005) Classes and methods for spatial data in R. R News 5(2). Available at https://cran.r-project.org/doc/Rnews/.Google Scholar
Pihl, TH, Nielsen, MK, Olsen, SN, Leifsson, PS and Jacobsen, S (2018) Nonstrangulating intestinal infarctions associated with Strongylus vulgaris: clinical presentation and treatment outcomes of 30 horses (2008–2016). Equine Veterinary Journal 50, 474–480.CrossRefGoogle Scholar
Prince, SD and Goward, SN (1995) Global primary production: a remote sensing approach. Journal of Biogeography 22, 815–835.CrossRefGoogle Scholar
Profousová, I, Mihaliková, K, Laho, T, Váradyová, Z, Petrželková, KJ, Modrý, D and Kišidayová, S (2011) The ciliate, Troglodytella abrassarti, contributes to polysaccharide hydrolytic activities in the chimpanzee colon. Folia Microbiologica 56, 339–343.CrossRefGoogle ScholarPubMed
Rifkin, JL, Nunn, CL and Garamszegi, LZ (2012) Do animals living in larger groups experience greater parasitism? A meta-analysis. American Naturalist 180, 70–82.CrossRefGoogle ScholarPubMed
Rimbach, R, Link, A, Bisanzio, D, Gillespie, TR, Galvis, N and Di Fiore, A (2015) Brown spider monkeys (Ateles hybridus): a model for differentiating the role of social networks and physical contact on parasite transmission dynamics. Philosophical Transactions of the Royal Society B: Biological Sciences 370, 20150179–20150179.CrossRefGoogle Scholar
Sánchez, CA, Becker, DJ, Teitelbaum, CS, Barriga, P, Brown, LM, Majewska, AA, Hall, RJ and Altizer, S (2018) On the relationship between body condition and parasite infection in wildlife: a review and meta-analysis. Ecology Letters 21, 1869–1884.CrossRefGoogle ScholarPubMed
Sapolsky, RM (2004) Why Zebras Don't Get Ulcers. New York: Owl Book/Henry Holt and Co.Google Scholar
Schley, PD and Field, CJ (2002) The immune-enhancing effects of dietary fibres and prebiotics. British Journal of Nutrition 87, S221–S230.CrossRefGoogle ScholarPubMed
Seivwright, LJ, Redpath, SM, Mougeot, F, Watt, L and Hudson, PJ (2004) Faecal egg counts provide a reliable measure of Trichostrongylus tenuis intensities in free-living red grouse Lagopus lagopus scoticus. Journal of Helminthology 78, 69–76.CrossRefGoogle ScholarPubMed
Skaug, H, Fournier, D, Bolker, B, Magnusson, A and Nielsen, A (2016) Generalized Linear Mixed Models using ‘AD Model Builder’. R package version 0.8.3.3.Google Scholar
Smyth, KN and Drea, CM (2015) Patterns of parasitism in the cooperatively breeding meerkat: a cost of dominance for females. Behavioral Ecology 27, 148–157.CrossRefGoogle Scholar
Sun, P, Wronski, T, Bariyanga, JD and Apio, A (2018) Gastro-intestinal parasite infections of Ankole cattle in an unhealthy landscape: an assessment of ecological predictors. Veterinary Parasitology 252, 107–116.CrossRefGoogle Scholar
Thurber, MI, O'Connell-Rodwell, CE, Turner, WC, Nambandi, K, Kinzley, C, Rodwell, TC, Faulkner, CT, Felt, SA and Bouley, DM (2011) Effects of rainfall, host demography, and musth on strongyle fecal egg counts in African elephants (Loxodonta africanna) in Namibia. Journal of Wildlife Diseases 47, 172–181.CrossRefGoogle Scholar
Vanderwaal, KL, Obanda, V, Omondi, GP, McCowan, B, Wang, H, Fushing, H and Isbell, LA (2016) The strength of weak ties and helminth parasitism in giraffe social networks. Behavioral Ecology 27, 1190–1197.CrossRefGoogle Scholar
Venables, WN and Ripley, BD (2002) Modern Applied Statistics with S. New York: Springer.CrossRefGoogle Scholar
Vidya, TNC and Sukumar, R (2002) The effect of some ecological factors on the intestinal parasite loads of the Asian elephant (Elephas maximus) in southern India. Journal of Biosciences 27, 521–528.CrossRefGoogle Scholar
Wickham, H (2007) Reshape_Rmanual.pdf. Journal of Statistical Software 21, 1–20.Google Scholar
Wijeyamohan, S, Treiber, K, Schmitt, D and Santiapillai, C (2014) A visual system for scoring body condition of Asian elephants (Elephas maximus). Zoo Biology 34, 53–59.CrossRefGoogle Scholar
Wilson, K, Bjørnstad, ON, Dobson, AP, Merler, S, Poglayen, G, Randolf, SE, Read, AF and Skorping, A (2002) Heterogeneities in macroparasite infections: patterns and processes. In The Ecology of Wildlife Diseases. New York City: Oxford University Press, pp. 6–44. doi: 10.1.1.17.8839Google Scholar
Wittemyer, G (2001) The elephant population of Samburu and Buffalo Springs National Reserves, Kenya. African Journal of Ecology 39, 357–369.CrossRefGoogle Scholar
Wittemyer, G, Daballen, D, Rasmussen, H, Kahindi, O and Douglas-Hamilton, I (2005a) Demographic status of elephants in the Samburu and Buffalo Springs National Reserves, Kenya. African Journal of Ecology 43, 44–47.CrossRefGoogle Scholar
Wittemyer, G, Douglas-Hamilton, I and Getz, WM (2005b) The socioecology of elephants: analysis of the processes creating multitiered social structures. Animal Behaviour 69, 1357–1371.CrossRefGoogle Scholar
Wittemyer, G, Barner Rasmussen, H and Douglas-Hamilton, I (2007a) Breeding phenology in relation to NDVI variability in free-ranging African elephant. Ecography 30, 42–50.CrossRefGoogle Scholar
Wittemyer, G, Getz, WM, Vollrath, F and Douglas-Hamilton, I (2007b) Social dominance, seasonal movements, and spatial segregation in African elephants: a contribution to conservation behavior. Behavioral Ecology and Sociobiology 61, 1919–1931.CrossRefGoogle Scholar
Wittemyer, G, Cerling, TE and Douglas-Hamilton, I (2009) Establishing chronologies from isotopic profiles in serially collected animal tissues: an example using tail hairs from African elephants. Chemical Geology 267, 3–11.CrossRefGoogle Scholar
Wittemyer, G, Daballen, D and Douglas-Hamilton, I (2013) Comparative demography of an at-risk African elephant population. PLoS ONE 8, e53726. doi: 10.1371/journal.pone.0053726.CrossRefGoogle ScholarPubMed
Wittemyer, G, Keating, LM, Vollrath, F and Douglas-Hamilton, I (2016) Graph theory illustrates spatial and temporal features that structure elephant rest locations and reflect risk perception. Ecography 40. doi: 10.1111/ecog.02379.Google Scholar
Zuk, M and McKean, KA (1996) Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 1009–1024.CrossRefGoogle ScholarPubMed
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