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Tick infestation effects on haemoglobin levels of deer mice (Peromyscus maniculatus)

Published online by Cambridge University Press:  05 October 2021

Erica Fellin Open the ORCID record for Erica Fellin [Opens in a new window]  and
Albrecht Schulte-Hostedde
Erica Fellin*
Affiliation:
Department of Biology, Laurentian University, Sudbury, ON, Canada
Albrecht Schulte-Hostedde
Affiliation:
Department of Biology, Laurentian University, Sudbury, ON, Canada
*
Author for correspondence: Erica Fellin, E-mail: [email protected]
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Abstract

Deer mice (Peromyscus maniculatus) are hosts to ixodid ticks as well as the associated tick-borne pathogens they can spread. As the ranges of black-legged ticks (Ixodes scapularis) and American dog ticks (Dermacentor variabilis) expand northwards, naïve host populations of deer mice are likely to become infested by ticks and experience the physiological effects that ticks can have on them via blood-feeding. The prevalence of these haematophagous ticks can affect the haemoglobin levels of the mice they infest. Haemoglobin levels were compared and analysed in deer mice populations at three different sites with varying tick exposure. These results suggested that without confounding effects, the abundance of black-legged and American dog ticks on individual mice had a significant negative effect on the hosts' haemoglobin levels, but only in an area with high tick infestation. This was seen across the average haemoglobin levels between populations, where there was a significant difference between the source population with the longest established tick populations and the source population where neither black-legged nor American dog ticks were prevalent. As the ticks' ranges expand and they become more abundant, it is important to understand how their prevalence and intensity can alter host physiology, potentially affecting their own range expansion and the spread of the diseases they may carry.

Keywords

Dermacentor variabilishaemoglobinIxodes scapularisparasite−host interactionsPeromyscus
Type
Research Article
Information
Parasitology , Volume 149 , Issue 2 , February 2022 , pp. 209 - 217
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Anderson, J, Moore, I, Nagata, B, Ribeiro, J, Valenzuela, J and Sonenshine, D (2017) Ticks, Ixodes scapularis, feed repeatedly on white-footed mice despite strong inflammatory response: an expanding paradigm for understanding tick-host interactions. Frontiers in Immunology 8, 1–15.10.3389/fimmu.2017.01784CrossRefGoogle ScholarPubMed
Andrews, N (1997) Iron deficiency: lessons from anemic mice. Yale Journal of Biology and Medicine 70, 219–226.Google ScholarPubMed
Arsnoe, I, Hickling, G, Ginsberg, H, McElreath, R and Tsao, J (2015) Different populations of black-legged tick nymphs exhibit differences in questing behavior that have implications for human lyme disease risk. PLoS One 10, e0127450.10.1371/journal.pone.0127450CrossRefGoogle ScholarPubMed
Baggs, RB and Miller, SA (1973) Nutritional iron deficiency as a determinant of host resistance in the rat. The Journal of Nutrition 103, 1554–1560.10.1093/jn/103.11.1554CrossRefGoogle ScholarPubMed
Banfield, AW (1974) The mammals of Canada. 1st Edn. Toronto and Buffalo: University of Toronto Press.Google Scholar
Bedford, N and Hoekstra, H (2015) Peromyscus mice as a model for studying natural variation. eLife 4, e06813.10.7554/eLife.06813CrossRefGoogle ScholarPubMed
Bobbie, C, Schmidt, E, Foley, J and Schulte-Hostedde, A (2016) The presence of parasitic miteson small mammals in Algonquin provincial park, Ontario, Canada. Canadian Journal of Zoology 95, 61–65.10.1139/cjz-2016-0085CrossRefGoogle Scholar
Bordes, F, Blumstein, D and Morand, S (2007) Rodent sociality and parasite diversity. Biology Letters 3(6), 692–694.10.1098/rsbl.2007.0393CrossRefGoogle ScholarPubMed
Borggraefe, I, Yuan, J, Telford, SR, Menon, S, Hunter, R, Shah, S, Spielman, A, Gelfand, J, Wortis, H and Vannier, E (2006) Babesia microti primarily invades mature erythrocytes in mice. Infection and Immunity 74, 3204–3212.10.1128/IAI.01560-05CrossRefGoogle ScholarPubMed
Bouchard, C, Beauchamp, G, Nguon, S, Trudel, L, Milord, F, Lindsay, LR, Bélanger, D and Ogden, N (2011) Associations between Ixodes scapularis ticks and small mammal hosts in a newly endemic zone in southeastern Canada: implications for Borrelia burgdorferi transmission. Ticks and Tick-Borne Diseases 2, 183–190.10.1016/j.ttbdis.2011.03.005CrossRefGoogle Scholar
Breusch, TS and Pagan, AR (1979) A simple test for heteroscedasticity and random coefficient variation. Econometrica 47, 1287–1294.10.2307/1911963CrossRefGoogle Scholar
Brockhurst, M, Buckling, A, Poullain, V and Hochberg, M (2007) The impact of migration from parasite-free patches on antagonistic host-parasite coevolution. Evolution 61, 1238.10.1111/j.1558-5646.2007.00087.xCrossRefGoogle ScholarPubMed
Buchholz, M and Dick, C (2017) Ecology of rodent – ectoparasite associations in south-central Kentucky. Northeastern Naturalist 24, 97–109.10.1656/045.024.0201CrossRefGoogle Scholar
Bush, AO, Lafferty, KD, Lotz, JM, Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology 83, 575–583.10.2307/3284227CrossRefGoogle Scholar
Carleton, R (2008) Ectoparasites affect hemoglobin and percentages of immature erythrocytes but not hematocrit in nestling eastern bluebirds. Wilson Journal of Ornithology 120, 565–568.10.1676/07-158.1CrossRefGoogle Scholar
Clark, K and Durden, L (2002) Parasitic arthropods of small mammals in Mississippi. Journal of Mammalogy 83, 1039–1048.10.1644/1545-1542(2002)083<1039:PAOSMI>2.0.CO;22.0.CO;2>CrossRefGoogle Scholar
Clow, K, Ogden, N, Lindsay, LR, Michel, P, Pearl, D and Jardine, C (2016) Distribution of ticks and the risk of lyme disease and other tick-borne pathogens of public health significance in Ontario, Canada. Vector-Borne and Zoonotic Diseases 16(4), 215–222. doi: 10.1089/vbz.2015.1890CrossRefGoogle ScholarPubMed
Clow, K, Leighton, P, Ogden, N, Lindsay, LR, Michel, P, Pearl, D and Jardine, C (2017) Northward range expansion of Ixodes scapularis evident over a short timescale in Ontario, Canada. PLoS One 12, e0189393.10.1371/journal.pone.0189393CrossRefGoogle Scholar
Crins, W, Gray, P, Uhlig, P and Wester, M (2009) The ecosystems of Ontario, Part 1: Ecozones and Ecoregions. Ministry of Natural Resources – Science & Information Branch. Technical Report SIB TER IMA TR-01.Google Scholar
Dlugosz, E, Downs, C, Khokhlova, I, Degen, A and Krasnov, BR (2014) Ectoparasite performance when feeding on reproducing mammalian females: an unexpected decrease when on pregnant hosts. The Journal of Experimental Biology 217, 1058–1064.Google ScholarPubMed
Dryden, MW and Gaafar, SM (1991) Blood consumption by the cat flea, Ctenocephalides felis (Siphonaptera: Pulicidae). Journal of Medical Entomology 28, 394–400.10.1093/jmedent/28.3.394CrossRefGoogle Scholar
Dubie, T, Grantham, R, Coburn, L and Noden, B (2017) Pictorial key for identification of immature stages of common ixodid ticks found in pastures in Oklahoma. Southwestern Entomologist 42, 1–14.10.3958/059.042.0101CrossRefGoogle Scholar
Estrada-Peña, A and La Fuente, J (2014) The ecology of ticks and epidemiology of tick-borne viral diseases. Antiviral Research 108, 104–128.10.1016/j.antiviral.2014.05.016CrossRefGoogle ScholarPubMed
Falls, JB, Falls, EA and Fryxell, J (2007) Fluctuations of deer mice in Ontario in relation to seed crops. Ecological Monographs 77, 19–32.10.1890/05-1485CrossRefGoogle Scholar
Frost, J (2019) Regression Analysis (1st ed.). Statistics by Jim. [self-published]. Retrieved from https://www.statisticsbyjim.com.Google Scholar
Fryxell, J, Falls, JB, Falls, EA and Brooks, R (1998) Long-term dynamics of small-mammal populations in Ontario. Ecology 79, 213–225.10.1890/0012-9658(1998)079[0213:LTDOSM]2.0.CO;2CrossRefGoogle Scholar
Gaitan, J and Millien, V (2016) Stress level, parasite load, and movement pattern in a small mammal reservoir host for lyme disease. Canadian Journal of Zoology 94, 565–573.10.1139/cjz-2015-0225CrossRefGoogle Scholar
Godinho, L, Cripps, J, Coulson, G and Lumsden, L (2013) The effect of ectoparasites on the grooming behaviour of Gould's Wattled Bat (Chalinolobus gouldii): an experimental study. Acta Chiropterologica 15, 463–472.10.3161/150811013X679080CrossRefGoogle Scholar
Gómez-Rodríguez, R, Gutiérrez-Granados, G, Montiel-Parra, G, Rodríguez-Moreno, A and Sánchez-Cordero, V (2015) Diversity and coexistence of Ectoparasites in small rodents in a tropical dry forest. Biotropica 47(4), 484–490.10.1111/btp.12229CrossRefGoogle Scholar
Grimm, A, Gruber, B and Henle, K (2014) Reliability of different mark-recapture methods for population size estimation tested against reference population sizes constructed from field data. PLoS One 9, e98840.10.1371/journal.pone.0098840CrossRefGoogle ScholarPubMed
Hamer, S, Hickling, G, Walker, E and Tsao, J (2014) Increased diversity of zoonotic pathogens and Borrelia burgdorferi strains in established versus incipient Ixodes scapularis populations across the Midwestern United States. Infection, Genetics and Evolution 27, 531–542.10.1016/j.meegid.2014.06.003CrossRefGoogle ScholarPubMed
Harper, J and Austad, S (2001) Effect of capture and season on fecal glucocorticoid levels in deer mice (Peromyscus maniculatus) and Red-Backed Voles (Clethrionomys gapperi). General and Comparative Endocrinology 123, 337–344.10.1006/gcen.2001.7682CrossRefGoogle Scholar
Harrison, X, Donaldson, L, Correa-Cano, ME, Evans, J, Fisher, DN, Goodwin, CED, Robinson, BS, Hodgson, DJ and Inger, R (2018) A brief introduction to mixed-effects modelling and multi-model inference in ecology. PeerJ 6, e4794.10.7717/peerj.4794CrossRefGoogle ScholarPubMed
Hawlena, H, Krasnov, BR, Abramsky, Z, Khokhlova, IS, Saltz, D, Kam, M, Tamir, A and Degen, AA (2006). Flea infestation and energy requirements of rodent hosts: are there general rules? Functional Ecology 20, 1028–1036.10.1111/j.1365-2435.2006.01190.xCrossRefGoogle Scholar
Hersh, M, LaDeau, S, Previtali, M and Ostfeld, R (2014) When is a parasite not a parasite? Effects of larval tick burdens on white-footed mouse survival. Ecology 95, 1360–1369.10.1890/12-2156.1CrossRefGoogle Scholar
Huang, C, Kay, S, Davis, S, Tufts, D, Gaffett, K and Tefft, B (2019) High burdens of Ixodes scapularis larval ticks on white-tailed deer may limit lyme disease risk in a low biodiversity setting. Ticks and Tick-Borne Diseases 10, 258–268.10.1016/j.ttbdis.2018.10.013CrossRefGoogle Scholar
Jones, C, Brunner, J, Scoles, G and Owen, J (2015) Factors affecting larval tick feeding success: host, density and time. Parasites & Vectors 8, 340.10.1186/s13071-015-0955-6CrossRefGoogle ScholarPubMed
Jones, H, Pekins, P, Kantar, L, Sidor, I, Ellingwood, D, Lichtenwalner, A and O'Neal, M (2019) Mortality assessment of moose (Alces alces) calves during successive years of winter tick (Dermacentor albipictus) epizootics in New Hampshire and Maine (USA). Canadian Journal of Zoology 97, 22–30.10.1139/cjz-2018-0140CrossRefGoogle Scholar
Judy, H and Price, N (1958) Hemoglobin level and red blood cell count findings in normal women. JAMA 167, 563–566.10.1001/jama.1958.02990220033010CrossRefGoogle ScholarPubMed
Kaur, D, Jaiswal, K and Mishra, S (2017) Effect of tick infestation on parameters of calves. Journal of Entomology and Zoology Studies 5, 107–111.Google Scholar
Kennedy, MA (2010) A brief review of the basics of immunology: the innate and adaptive response. Veterinary Clinics of North America: Small Animal Practice 40, 369–379.10.1016/j.cvsm.2010.01.003CrossRefGoogle ScholarPubMed
Kim, H, Kim, S and Ryu, J (2017) Changes in the blood components caused by water intake. Korean Journal of Clinical Laboratory Science 49, 227–232.10.15324/kjcls.2017.49.3.227CrossRefGoogle Scholar
Kocan, K, de la Fuente, J and Coburn, L (2015) Insights into the development of Ixodes scapularis: a resource for research on a medically important tick species. Parasites & Vectors 8, 592.10.1186/s13071-015-1185-7CrossRefGoogle ScholarPubMed
Koch, H and Sauer, J (1984) Quantity of blood ingested by four species of hard ticks (Acari: Ixodidae) fed on domestic dogs. Annals of the Entomological Society of America 77, 142–146.10.1093/aesa/77.2.142CrossRefGoogle Scholar
Krogmann, L and Holstein, J (2010) Chapter 18: preserving and specimen handling: insects and other invertebrates. In Eymann, J, Degreef, J, Hauser, C, Monje, JC, Samyn, Y and VandenSpiegel, D (eds), Manual on Field Recording Techniques and Protocols for All Taxa Biodiversity Inventories. Brussels, Belgium: ABC Taxa, pp. 463–481.Google Scholar
Kutzer, M and Armitage, S (2016) Maximising fitness in the face of parasites: a review of host tolerance. Zoology 119, 281–289.10.1016/j.zool.2016.05.011CrossRefGoogle ScholarPubMed
Larson, SR, Lee, X and Paskewitz, SM (2018) Prevalence of tick-borne pathogens in two species of Peromyscus mice common in Northwestern Wisconsin. Journal of Medical Entomology 55, 1002–1010.10.1093/jme/tjy027CrossRefGoogle Scholar
Leighton, P, Koffl, J, Pelcat, Y and Ogden, N (2012) Predicting the speed of tickinvasion: an empirical model of range expansion for the lyme disease vector lxodes scapularis in Canada. Journal of Applied Ecology 49(2), 457–464.10.1111/j.1365-2664.2012.02112.xCrossRefGoogle Scholar
Lindquist, E, Galloway, T, Artsob, H, Lindsay, LR, Drebot, M, Wood, H and Robbins, R (2016) A Handbook to the Ticks of Canada (Ixodida: Ixodidae, Argasidae). Canada: Biological Survey of Canada.10.3752/9780968932186CrossRefGoogle Scholar
Lindsay, LR, Barker, IK, Surgeoner, GA, McEwen, SA, Elliott, LA and Kolar, J (1991) Apparent incompetence of Dermacentor variabilis (Acari: Ixodidae) and fleas (Insecta: Siphonaptera) as vectors of Borrelia burgdorferi in an Ixodes dammini endemic area of Ontario, Canada. Journal of Medical Entomology 28, 750–753.10.1093/jmedent/28.5.750CrossRefGoogle Scholar
Milnes, E, Thronton, G, Levéillé, A, Delnatte, P, Barta, J, Smith, D and Nemeth, N (2019) Babesia odocoilei and zoonotic pathogens identified from Ixodes scapularis ticks in Southern Ontario, Canada. Ticks and Tick-Borne Diseases 10, 670–676.10.1016/j.ttbdis.2019.02.016CrossRefGoogle ScholarPubMed
Minigan, J, Hager, H, Peregrine, A and Newman, J (2018) Current and potential future distribution of the American dog tick (Dermacentor variabilis, Say) in North America. Ticks and Tick-borne Diseases 9, 354–362.10.1016/j.ttbdis.2017.11.012CrossRefGoogle Scholar
Mize, E, Tsao, J and Maurer, B (2011) Habitat correlates with the spatial distribution of ectoparasites on Peromyscus leucopus in Southern Michigan. Journal of Vector Ecology 36, 308–320.10.1111/j.1948-7134.2011.00171.xCrossRefGoogle ScholarPubMed
Morshed, M, Scott, J, Fernando, K, Mann, R and Durden, L (2003) Lyme disease spirochaete, Borrelia burgdorferi endemic at the epicenter in rondeau provincial Park, Ontario. Journal of Medical Entomology 40, 91–94.10.1603/0022-2585-40.1.91CrossRefGoogle ScholarPubMed
National Research Council (US) Institute for Laboratory Animal Research (1996) Guide for the Care and Use of Laboratory Animals. Washington (DC): National Academies Press (US).Google Scholar
Nédélec, Y, Sanz, J, Baharian, G, Szpiech, Z, Pacis, A, Dumaine, A, Grenier, J, Freiman, A, Sams, A, Hebert, S, Sabourin, A, Luca, F, Blekhman, R, Hernandez, R, Pique-Regi, R, Tung, J, Yotova, V and Barreiro, L (2016) Genetic ancestry and natural selection drive population differences in immune responses to pathogens. Cell 167, 657–669.10.1016/j.cell.2016.09.025CrossRefGoogle ScholarPubMed
Nichols, J, Hines, J and Pollock, K (1984) Effects of permanent trap response in capture probability on Jolly-Seber capture-recapture model estimates. JSTOR 48, 289–294.Google Scholar
O'Brien, E, Morrison, B and Johnson, LS (2003) Assessing the effects of haematophagous ectoparasites on the health of nestling birds: haematocrit vs haemoglobin levels in house wrens parasitized by blow fly larvae. Journal of Avian Biology 32, 73–76.10.1034/j.1600-048X.2001.320110.xCrossRefGoogle Scholar
Ostfeld, R, Miller, M and Schnurr, J (1993) Ear tagging increases tick (Ixodes Dammini) infestation rates of white-footed mice (Peromyscus leucopus). Journal of Mammalogy 74, 651–655.10.2307/1382286CrossRefGoogle Scholar
Ostfeld, R, Miller, M and Hazler, K (1996) Causes and consequences of tick (Ixodes scapularis) burdens on white-footed mice (Peromyscus leucopus). Journal of Mammalogy 77, 166–273.10.2307/1382727CrossRefGoogle Scholar
Papkou, A, Gokhale, CS, Traulsen, A and Schulenburg, H (2016) Host-parasite coevolution: why changing population size matters. Zoology 119, 330–338.10.1016/j.zool.2016.02.001CrossRefGoogle ScholarPubMed
Parasuraman, S, Raveendran, R and Kesavan, R (2010) Blood sample collection in small laboratory animals. Journal of Pharmacology Pharmacotherapy 1, 87–93.10.4103/0976-500X.72350CrossRefGoogle ScholarPubMed
Patterson, JE, Neuhaus, P, Kutz, SJ and Ruckstuhl, KE (2013) Parasite removal improves reproductive success of female North American red squirrels (Tamiasciurus hudsonicus). PLoS One 8, e55779.10.1371/journal.pone.0055779CrossRefGoogle Scholar
Pfäffle, M, Petney, T, Elgas, M, Skuballa, J and Taraschewski, H (2009) Tick-induced blood loss leads to regenerative anaemia in the European hedgehog (Erinaceus europaeus). Parasitology 136, 443–452.10.1017/S0031182009005514CrossRefGoogle Scholar
Powell, R and Proulx, G (2003) Trapping and marking terrestrial mammals for research: integrating ethics, performance criteria, techniques, and common sense. ILAR Journal 44, 259–276.10.1093/ilar.44.4.259CrossRefGoogle ScholarPubMed
PREDICT One Health Consortium (2016) PREDICT Operating Procedures: Rodent Sampling Methods.Google Scholar
Public Health Ontario (2019) Ontario Lyme Disease Map 2019 Estimated Risk Areas. Ontario Agency for Health Protection and Promotion. Toronto, ON: Queen's Printer for Ontario.Google Scholar
Rahman, MM, Mostofa, M, Jahan, MS and Kamal, MAHM (2009) Comparative efficacy of neem leaves and ivermectin (ivomec®) against ectoparasites in calves. Journal of the Bangladesh Agricultural University 7, 73–78.10.3329/jbau.v7i1.4802CrossRefGoogle Scholar
Rand, P, Lacombe, E, Smith, R, Rich, S, Kilpatrick, W, Dragoni, C and Caporale, D (1993) Competence of Peromyscus maniculatus (Rodentia: Cricetidae) as a reservoir host for Borrelia burgdorferi (Spirochaetares: Spirochaetaceae) in the wild. Journal of Medical Entomology 30, 614–618.10.1093/jmedent/30.3.614CrossRefGoogle ScholarPubMed
Randolph, JC (1980) Daily energy metabolism of two rodents (Peromyscus leucopus and Tamias striatus) in their natural environment. Physiological Zoology 53, 70–81.10.1086/physzool.53.1.30155776CrossRefGoogle Scholar
R Core Team, (2019) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.Google Scholar
Reiczigel, J, Marozzi, M, Fabian, I and Rozsa, L (2019) Biostatistics for parasitologists – A primer to quantitative parasitology. Trends in Parasitology 35, 277–281.10.1016/j.pt.2019.01.003CrossRefGoogle ScholarPubMed
Rosales, F, Jang, J, Pinero, D, Erikson, K, Beard, J and Ross, C (1999) Iron deficiency in young rats alters the distribution of vitamin A between plasma and liver and between hepatic retinol and retinyl esters. The Journal of Nutrition 129, 1223–1228.CrossRefGoogle ScholarPubMed
Rózsa, L, Reiczigel, J and Majoros, G (2000) Quantifying parasites in samples of hosts. Journal of Parasitology 86, 228–232.CrossRefGoogle ScholarPubMed
Schmidt, E, Mykytczuk, N and Schulte-Hostedde, A (2019) Effects of the captive and wild environment on diversity of the gut microbiome of deer mice (Peromyscus maniculatus). ISME Journal 13, 1293–1305.10.1038/s41396-019-0345-8CrossRefGoogle Scholar
Shaw, M, Keesing, F, McGrail, R and Ostfeld, R (2003) Factors influencing the distribution of larval black-legged ticks on rodent hosts. American Journal of Tropical Medicine and Hygiene 68, 447–452.10.4269/ajtmh.2003.68.447CrossRefGoogle ScholarPubMed
Sonenshine, D (2018) Range expansion of tick disease vectors in North America: implications for the spread of tick-borne disease. International Journal of Environmental Research and Public Health 15, 478.10.3390/ijerph15030478CrossRefGoogle ScholarPubMed
Storz, JF, Sabatino, SJ, Hoffman, FG, Gering, EJ, Moriyama, H, Ferrand, N, Monterio, B and Nachman, MW (2007) The molecular basis of high-altitude adaptation in deer mice. Plos Genetis 3(e45), 448–459.Google ScholarPubMed
Torre, I, Freixas, L, Arrizabalaga, A and Diaz, M (2016) The efficiency of two widely used commercial live-traps to develop monitoring protocols for small mammal biodiversity. Ecological Indicators 66, 481–487.10.1016/j.ecolind.2016.02.017CrossRefGoogle Scholar
Tufts, D, Revsbech, I, Cheviron, Z, Weber, R, Fago, A and Storz, J (2013) Phenotypic plasticity in blood-oxygen transport in highland and lowland deer mice. Journal of Experimental Biology 216, 1167–1173.Google ScholarPubMed
Watson, TG and Anderson, RC (1976) Ixodes scapularis say on white-tailed deer (Odocoileus virginianus) from Long Point, Ontario. Journal of Wildlife Diseases 12, 66–71.10.7589/0090-3558-12.1.66CrossRefGoogle ScholarPubMed
Weber, M, Stevens, R, Diniz-Filho, JAF and Grelle, CEV (2016) Is there a correlation between abundance and environmental suitability derived from ecological niche modelling? A meta-analysis. Ecography 40, 817–828.10.1111/ecog.02125CrossRefGoogle Scholar
Weldon, L, Abolina, S, Lenzi, L, Bourne, C, Riley, E and Viney, M (2015) The gut microbiota of wild mice. PLoS One 10, e0134643.CrossRefGoogle ScholarPubMed
Westblade, L, Simon, M, Mathison, B and Kirkman, L (2017) Babesia microti: from mice to ticks to an increasing number of highly susceptible humans. Journal of Clinical Microbiology 55, 2903–2912.10.1128/JCM.00504-17CrossRefGoogle Scholar
Wickham, H (2016) ggplot2: Elegant Graphics for Data Analysis. New York: Springer-Verlag. ISBN 978-3-319-24277-4, https://ggplot2.tidyverse.org.10.1007/978-3-319-24277-4CrossRefGoogle Scholar
Wickham, H, Averick, M, Bryan, J, Chang, W, D'Agostino McGowan, L, Francois, R, Grolemund, G, Hayes, A, Henry, L, Hester, J, Kuhn, M, Pedersen, TL, Miller, E, Bache, SM, Muller, K, Ooms, J, Robinson, D, Seidel, DP, Spinu, V, Takahashi, K, Vaughan, D, Wilke, C, Woo, K and Yutani, H (2019) Welcome to the Tidyverse. Journal of Open Source Software 4, 1686.10.21105/joss.01686CrossRefGoogle Scholar
Wilde, L, Wolf, C, Porter, S, Stager, M, Cheviron, Z and Senner, N (2018) Botfly infections impair the aerobic performance and survival of montane populations of deer mice, Peromyscus maniculatus rufinus. Functional Ecology 33, 608–618.10.1111/1365-2435.13276CrossRefGoogle Scholar