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Climate change effects on terrestrial parasitic nematodes: Where are the knowledge gaps?
Published online by Cambridge University Press: 04 December 2023
Abstract
Climate change is expected to affect parasitic nematodes and hence possibly parasite–host dynamics and may have far-reaching consequences for animal health, livestock production, and ecosystem functioning. However, there has been no recent overview of current knowledge to identify how studies could contribute to a better understanding of terrestrial parasitic nematodes under changing climates. Here we screened almost 1,400 papers to review 57 experimental studies on the effects of temperature and moisture on hatching, development, survival, and behaviour of the free-living stages of terrestrial parasitic nematodes with a direct life cycle in birds and terrestrial mammals. Two major knowledge gaps are apparent. First, research should study the temperature dependency curves for hatching, development, and survival under various moisture treatments to test the interactive effect of temperature and moisture. Second, we specifically advocate for more studies that investigate how temperature, and its interaction with moisture, affect both vertical and horizontal movement of parasitic nematodes to understand infection risks. Overall, we advocate for more field experiments that test environmental effects on life-history traits and behaviour of parasitic nematodes in their free-living stages under natural and realistic circumstances. We also encourage studies to expand the range of used hosts and parasitic nematodes because 66% of results described in the available studies use sheep and cattle as hosts and 32% involve just three nematode species. This new comprehension brings attention to understudied abiotic impacts on terrestrial parasitic nematodes and will have broader implications for livestock management, wildlife conservation, and ecosystem functioning in a rapidly warming climate.
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References
Aleuy, OA, Hoberg, EP, Paquette, C, Ruckstuhl, KE, and Kutz, S (2019) Adaptations and phenotypic plasticity in developmental traits of Marshallagia marshalli. International Journal for Parasitology 49, 789–796.10.1016/j.ijpara.2019.05.007CrossRefGoogle ScholarPubMed
Aleuy, OA and Kutz, S (2020) Adaptations, life-history traits and ecological mechanisms of parasites to survive extremes and environmental unpredictability in the face of climate change. International Journal for Parasitology: Parasites and Wildlife 12, 308–317.Google ScholarPubMed
Altizer, S, Dobson, A, Hosseini, P, Hudson, P, and Pascual, M (2006) Seasonality and the dynamics of infectious diseases. Ecology Letters 9, 467–484.10.1111/j.1461-0248.2005.00879.xCrossRefGoogle ScholarPubMed
Beltrame, L, Rose Vineer, H, Walker, JG, Morgan, ER, Vickerman, P, and Wagener, T (2021) Discovering environmental management opportunities for infectious disease control. Scientific Reports 11. https://doi.org/10.1038/s41598-021-85250-1CrossRefGoogle ScholarPubMed
Brooker, S, Clements, AC, and Bundy, DA (2006) Global epidemiology, ecology and control of soil-transmitted helminth infections. Advances in parasitology 62, 221–261.10.1016/S0065-308X(05)62007-6CrossRefGoogle ScholarPubMed
Bryant, AS and Hallem, EA (2018) Temperature-dependent behaviors of parasitic helminths. Neuroscience Letters 687, 290–303.10.1016/j.neulet.2018.10.023CrossRefGoogle ScholarPubMed
Charlier, J, Höglund, J, von Samson-Himmelstjerna, G, Dorny, P, and Vercruysse, J (2009) Gastrointestinal nematode infections in adult dairy cattle: impact on production, diagnosis and control. Veterinary Parasitology 164, 70–79.CrossRefGoogle ScholarPubMed
Chaudary, FR, Qayyum, M, and Miller, JE (2008) Development and survival of Haemonchus contortus infective larvae derived from sheep faeces under sub-tropical conditions in the Potohar region of Pakistan. Tropical Animal Health and Production 40, 85–92.10.1007/s11250-007-9037-xCrossRefGoogle ScholarPubMed
Chung, JA and Boeri, F (2012) Nematodes: morphology, functions and management strategies. New York: Nova Science Publishers, Incorporated.Google Scholar
Ciordia, H and Bizell, WE (1963) The effects of various constant temperatures on the development of the free living- stages of some nematode parasites of cattle. The Journal of Parasitology 49, 60–63.CrossRefGoogle ScholarPubMed
Cizauskas, CA, Carlson, CJ, Burgio, R, Clements, CF, Dougherty, ER, Harris, NC, and Phillips, AJ (2017) Parasite vulnerability to climate change: an evidence-based functional trait approach. Royal Society Open Science 4. https://doi.org/10.1098/rsos.160535CrossRefGoogle ScholarPubMed
Convey, P, Abbandonato, H, Bergan, F, Beumer, LT, Biersma, EM, Bråthen, VS, D’Imperio, L, Jensen, CK, Nilsen, S, Paquin, K, Stenkewitz, U, Svoen, ME, Winkler, J, Müller, E, and Coulson, SJ (2015) Survival of rapidly fluctuating natural low winter temperatures by High Arctic soil invertebrates. Journal of Thermal Biology 54, 111–117.10.1016/j.jtherbio.2014.07.009CrossRefGoogle ScholarPubMed
Crofton, HD (1965) Ecology and biological plasticity of sheep nematodes. I. The effect of temperature on the hatching of eggs of some nematode parasites of sheep. Cornell Veterinarian 55, 242–250.Google ScholarPubMed
Dobson, A, Molnár, PK, and Kutz, S (2015) Climate change and Arctic parasites. Trends in Parasitology 31, 181–188.10.1016/j.pt.2015.03.006CrossRefGoogle ScholarPubMed
Dulovic, A, Norman, M, Harbecke, D, and Streit, A (2022) Chemotactic and temperature-dependent responses of the Strongyloidoidea superfamily of nematodes. Parasitology 149, 116–123.CrossRefGoogle ScholarPubMed
Fox, NJ, Marion, G, Davidson, RS, White, PCL, and Hutchings, MR (2012) Livestock helminths in a changing climate: approaches and restrictions to meaningful predictions. Animals 2, 93–107.CrossRefGoogle Scholar
Gardner, MP, Gems, D, and Viney, ME (2004) Aging in a very short-lived nematode. Experimental Gerontology 39, 1267–1276.10.1016/j.exger.2004.06.011CrossRefGoogle Scholar
Grenfell, BT (1988) Gastrointestinal nematode parasites and the stability and productivity of intensive ruminant grazing systems. Philosophical Transactions of the Royal Society of London. B, Biological Sciences 321, 541–563.Google ScholarPubMed
Grenfell, BT (1992) Parasitism and the dynamics of ungulate grazing systems. The American Naturalist 139, 907–929.CrossRefGoogle Scholar
Grønvold, J and Høgh-Schmidt, K (1989) Factors influencing rain splash dispersal of infective larvae of Ostertagia ostertagi (Trichostrongylidae) from cow pats to the surroundings. Veterinary Parasitology, 57–70.CrossRefGoogle Scholar
Gyeltshen, T, Kahn, LP, and Laurenson, YCSM (2022) Ecology of the free-living stages of Trichostrongylid parasites of sheep. Veterinary Parasitology 303. https://doi.org/10.1016/j.vetpar.2022.109683CrossRefGoogle ScholarPubMed
Halvorsen, O (2012) Reindeer parasites, weather and warming of the Arctic. Polar Biology 35, 1749–1752.10.1007/s00300-012-1209-0CrossRefGoogle Scholar
Hamilton, KM, Waghorn, TS, de Waal, T, Keane, OM, Green, P, and Leathwick, DM (2022) In vitro evaluation of fitness parameters for isolates of Teladorsagia circumcincta resistant and susceptible to multiple anthelmintic classes. Veterinary Parasitology 310. https://doi.org/10.1016/j.vetpar.2022.109791CrossRefGoogle ScholarPubMed
Hatcher, MJ, Dick, JTA, and Dunn, AM (2006) How parasites affect interactions between competitors and predators. Ecology Letters 9, 1253–1271.CrossRefGoogle ScholarPubMed
Hayes, KS, Bancroft, AJ, Goldrick, M, Portsmouth, C, Roberts, IS, and Grencis, RK (2010) Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris. Science 328, 1391–1394.10.1126/science.1187703CrossRefGoogle ScholarPubMed
Hernandez, AD, Poole, A, and Cattadori, IM (2013) Climate changes influence free-living stages of soil-transmitted parasites of European rabbits. Global Change Biology 19, 1028–1042.CrossRefGoogle ScholarPubMed
Hoar, B (2012) Ecology and transmission dynamics of Ostertagia gruehneri in Barrenground Caribou. Calgary, AB: University of Calgary.Google ScholarPubMed
Holand, H, Jensen, H, Kvalnes, T, Tufto, J, Pärn, H, Sæther, BE, and Ringsby, TH (2019) Parasite prevalence increases with temperature in an avian metapopulation in northern Norway. Parasitology 146, 1030–1035.CrossRefGoogle Scholar
Hudson, PJ, Cattadori, IM, Boag, B, and Dobson, AP (2006) Climate disruption and parasite–host dynamics: patterns and processes associated with warming and the frequency of extreme climatic events. Journal of Helminthology 80, 175–182.CrossRefGoogle ScholarPubMed
Hudson, PJ, Dobson, AP, and Newborn, D (1992) Do parasites make prey vulnerable to predation? Red grouse and parasites. Journal of Animal Ecology 61, 681–692.10.2307/5623CrossRefGoogle Scholar
Hutchings, MR, Kyriazakis, I, Anderson, DH, Gordon, IJ, and Coop, RL (1998) Behavioural strategies used by parasitized and non-parasitized sheep to avoid ingestion of gastro-intestinal nematodes associated with faeces. Animal Science 67, 97–106.CrossRefGoogle Scholar
IPCC. (2021) Summary for policymakers. In Masson-Delmotte, VP, Zhai, P, Pirani, A, Connors, BZSL, Péan, C, Berger, S, Caud, N, Chen, Y, Goldfarb, L, Gomis, MI, Huang, M, Leitzell, K, Lonnoy, E, Matthews, JBR, Maycock, TK, Waterfield, T, Yelekçi, O, Yu, R (Eds), Climate change 2021: The physical science basis. Contribution of working group I to the sixth assessment report of the intergovernmental panel on climate change.Google Scholar
Jenkins, EJ, Veitch, AM, Kutz, SJ, Hoberg, EP, and Polley, L (2006) Climate change and the epidemiology of protostrongylid nematodes in northern ecosystems: Parelaphostrongylus odocoilei and Protostrongylus stilesi in Dall’s sheep (Ovis d. dalli). Parasitology 132, 387–401.CrossRefGoogle ScholarPubMed
Khadijah, S, Kahn, LP, Walkden-Brown, SW, Bailey, JN, and Bowers, SF (2013) Soil moisture influences the development of Haemonchus contortus and Trichostrongylus colubriformis to third stage larvae. Veterinary Parasitology 196, 161–171.10.1016/j.vetpar.2013.01.010CrossRefGoogle ScholarPubMed
Khadijah, S, Kahn, LP, Walkden-Brown, SW, Bailey, JN, and Bowers, SF (2013a) Effect of simulated rainfall timing on faecal moisture and development of Haemonchus contortus and Trichostrongylus colubriformis eggs to infective larvae. Veterinary Parasitology 192, 199–210.CrossRefGoogle ScholarPubMed
Khadijah, S, Kahn, LP, Walkden-Brown, SW, Bailey, JN, and Bowers, SF (2013b) Soil moisture modulates the effects of the timing and amount of rainfall on faecal moisture and development of Haemonchus contortus and Trichostrongylus colubriformis to infective third stage larvae. Veterinary Parasitology 196, 347–357.CrossRefGoogle ScholarPubMed
Khadijah, S, Kahn, LP, Walkden-Brown, SW, Bailey, JN, and Bowers, SF (2013c) Translation of Haemonchus contortus and Trichostrongylus colubriformis from egg to establishment in grazing sheep is unaffected by rainfall timing, rainfall amount and herbage height under conditions of high soil moisture in the Northern Tablelands of NSW. Veterinary Parasitology 197, 204–211.CrossRefGoogle ScholarPubMed
Khanyari, M, Milner-Gulland, EJ, Oyanedel, R, Vineer, HR, Singh, NJ, Robinson, S, Salemgareyev, A, and Morgan, ER (2022) Investigating parasite dynamics of migratory ungulates for sustaining healthy populations: application to critically endangered saiga antelopes Saiga tatarica. Biological Conservation 266. https://doi.org/10.1016/j.biocon.2022.109465CrossRefGoogle Scholar
Knapp-Lawitzke, F, von Samson-Himmelstjerna, G, and Demeler, J (2016) Elevated temperatures and long drought periods have a negative impact on survival and fitness of strongylid third stage larvae. International Journal for Parasitology 46, 229–237.CrossRefGoogle ScholarPubMed
Koltz, AM, Civitello, DJ, Becker, DJ, Deem, SL, Classen, AT, Barton, B, … and Ezenwa, VO (2022) Sublethal effects of parasitism on ruminants can have cascading consequences for ecosystems. Proceedings of the National Academy of Sciences 119, e2117381119.CrossRefGoogle ScholarPubMed
Kutz, SJ, Hoberg, EP, Molnár, PK, Dobson, A, and Verocai, GG (2014) A walk on the tundra: Host-parasite interactions in an extreme environment. International Journal for Parasitology: Parasites and Wildlife 3, 198–208.Google Scholar
Kutz, SJ, Jenkins, EJ, Veitch, AM, Ducrocq, J, Polley, L, Elkin, B, and Lair, S (2009) The Arctic as a model for anticipating, preventing, and mitigating climate change impacts on host-parasite interactions. Veterinary Parasitology 163, 217–228.CrossRefGoogle Scholar
Kuzmina, TA, Kuzmin, YI, and Kharchenko, VA (2006) Field study on the survival, migration and overwintering of infective larvae of horse strongyles on pasture in central Ukraine. Veterinary Parasitology 141, 264–272.CrossRefGoogle Scholar
Lafferty, KD, Dobson, AP, and Kuris, AM (2006) Parasites dominate food web links. Proceedings of the National Academy of Sciences of the United States of America 103, 11211–11216.CrossRefGoogle ScholarPubMed
Langrová, I, Jankovská, I, Borovský, M, and Fiala, T (2003). Effect of climatic influences on the migrations of infective larvae of Cyathostominae. Veterinarni Medicina 48, 18–24.CrossRefGoogle Scholar
Lembrechts, JJ, Hoogen, J, Aalto, J, Ashcroft, MB, de Frenne, P, Kemppinen, J, Kopecký, M, Luoto, M, Maclean, IMD, Crowther, TW, Bailey, JJ, Haesen, S, Klinges, DH, Niittynen, P, Scheffers, BR, van Meerbeek, K, Aartsma, P, Abdalaze, O, Abedi, M, … Lenoir, J (2022) Global maps of soil temperature. Global Change Biology 28, 3110–3144.CrossRefGoogle ScholarPubMed
May, K, Raue, K, Blazejak, K, Jordan, D, and Strube, C (2022) Pasture rewetting in the context of nature conservation shows no long-term impact on endoparasite infections in sheep and cattle. Parasites and Vectors 15. https://doi.org/10.1186/s13071-022-05155-4CrossRefGoogle ScholarPubMed
McCarthy, C, Vineer, HR, Morgan, ER, and van Dijk, J (2022) Predicting the unpredictable? A climate-based model of the timing of peak pasture infectivity for Dictyocaulus viviparus. Veterinary Parasitology 309. https://doi.org/10.1016/j.vetpar.2022.109770CrossRefGoogle ScholarPubMed
McFarland, C, Rose Vineer, H, Chesney, L, Henry, N, Brown, C, Airs, P, Nicholson, C, Scollan, N, Lively, F, Kyriazakis, I, and Morgan, ER (2022) Tracking gastrointestinal nematode risk on cattle farms through pasture contamination mapping. International Journal for Parasitology 52, 691–703.CrossRefGoogle ScholarPubMed
Mehlhorn, H (2016) Worms (Helminths). pp. 251–498 in Mehlhorn, H (Eds), Animal parasites. Cham: Springer International Publishing.CrossRefGoogle Scholar
Melville, LA, van Dijk, J, Mitchell, S, Innocent, G, and Bartley, DJ (2020) Variation in hatching responses of Nematodirus battus eggs to temperature experiences. Parasites & Vectors 13. https://doi.org/10.1186/s13071-020-04368-9CrossRefGoogle ScholarPubMed
Mendez, P, Walsh, B, and Hallem, EA (2022) Using newly optimized genetic tools to probe Strongyloides sensory behaviors. Molecular and Biochemical Parasitology 250. https://doi.org/10.1016/j.molbiopara.2022.111491CrossRefGoogle ScholarPubMed
Molnár, PK, Dobson, AP, and Kutz, SJ (2013) Gimme shelter – the relative sensitivity of parasitic nematodes with direct and indirect life cycles to climate change. Global Change Biology 19, 3291–3305.CrossRefGoogle ScholarPubMed
Molnár, PK, Kutz, SJ, Hoar, BM, and Dobson, AP (2013) Metabolic approaches to understanding climate change impacts on seasonal host-macroparasite dynamics. Ecology Letters 16, 9–21.CrossRefGoogle ScholarPubMed
Molnár, PK, Sckrabulis, JP, Altman, KA, and Raffel, TR (2017) Thermal performance curves and the metabolic theory of ecology – a practical guide to models and experiments for parasitologists. The Journal of Parasitology 103, 423–439.CrossRefGoogle ScholarPubMed
Morgan, ER, Aziz, NAA, Blanchard, A, Charlier, J, Charvet, C, Claerebout, E, Geldhof, P, Greer, AW, Hertzberg, H, Hodgkinson, J, Höglund, J, Hoste, H, Kaplan, RM, Martínez-Valladares, M, Mitchell, S, Ploeger, HW, Rinaldi, L, von Samson-Himmelstjerna, G, Sotiraki, S, … Vercruysse, J (2019) 100 questions in livestock helminthology research. Trends in Parasitology 35, 52–71.CrossRefGoogle ScholarPubMed
Morley, NJ and Lewis, JW (2014) Temperature stress and parasitism of endothermic hosts under climate change. Trends in Parasitology 30, 221–227.CrossRefGoogle ScholarPubMed
Navarre, CB (2020) Epidemiology and control of gastrointestinal nematodes of cattle in southern climates. Veterinary Clinics of North America – Food Animal Practice 36, 45–57.CrossRefGoogle ScholarPubMed
O’ Connor, LJ, Walkden-Brown, SW, and Kahn, LP (2006) Ecology of the free-living stages of major trichostrongylid parasites of sheep. Veterinary Parasitology 142, 1–15.CrossRefGoogle ScholarPubMed
O’Connor, LJ, Kahn, LP, and Walkden-Brown, SW (2007) Moisture requirements for the free-living development of Haemonchus contortus: quantitative and temporal effects under conditions of low evaporation. Veterinary Parasitology 150, 128–138.CrossRefGoogle ScholarPubMed
O’Connor, LJ, Kahn, LP, and Walkden-Brown, SW (2008) Interaction between the effects of evaporation rate and amount of simulated rainfall on development of the free-living stages of Haemonchus contortus. Veterinary Parasitology 155, 223–234.CrossRefGoogle ScholarPubMed
Ogdee, JL, Henke, SE, Wester, DB, and Fedynich, AM (2016) Permeability and viability of Baylisascaris procyonis eggs in Southern Texas soils. Journal of Parasitology 102, 608–612.CrossRefGoogle ScholarPubMed
Oliver, AB, Pomroy, WE, Ganesh, S, and Leathwick, DM (2016) Chilling requirements for hatching of a New Zealand isolate of Nematodirus filicollis. Veterinary Parasitology 226, 17–21.CrossRefGoogle ScholarPubMed
Peacock, SJ, Kutz, SJ, Hoar, BM, and Molnár, PK (2022) Behaviour is more important than thermal performance for an Arctic host-parasite system under climate change. Royal Society Open Science 9. https://doi.org/10.1098/rsos.220060CrossRefGoogle ScholarPubMed
Phillips, JA, Vargas Soto, JS, Pawar, S, Koprivnikar, J, Benesh, D, and Molnár, PK (2022) The effects of phylogeny, habitat, and host characteristics on the thermal sensitivity of helminth development. Proceedings of the Royal Society B 289. https://doi.org/10.1098/rspb.2021.1878Google ScholarPubMed
Rose, H, Caminade, C, Bolajoko, MB, Phelan, P, van Dijk, J, Baylis, M, Williams, D, and Morgan, ER (2016) Climate-driven changes to the spatio-temporal distribution of the parasitic nematode, Haemonchus contortus, in sheep in Europe. Global Change Biology 22, 1271–1285.CrossRefGoogle Scholar
Rossanigo, CE and Gruner, L (1995) Moisture and temperature requirements in faeces for the development of free-living stages of gastrointestinal nematodes of sheep, cattle and deer. Journal of Helminthology 69, 357–362.CrossRefGoogle ScholarPubMed
Rossanigo, CE and Gruner, L (1996) The length of strongylid nematode infective larvae as a reflection of developmental conditions in faeces and consequences on their viability. Parasitology Research 82, 304–311.CrossRefGoogle ScholarPubMed
Rossi, L, Interisano, M, Deksne, G, and Pozio, E (2019) The subnivium, a haven for Trichinella larvae in host carcasses. International Journal for Parasitology: Parasites and Wildlife 8, 229–233.Google ScholarPubMed
Salame, L and Glazer, I (2015) Stress avoidance: vertical movement of entomopathogenic nematodes in response to soil moisture gradient. Phytoparasitica 43, 647–655.CrossRefGoogle Scholar
Santos, MC, Silva, BF, and Amarante, AFT (2012) Environmental factors influencing the transmission of Haemonchus contortus. Veterinary Parasitology 188, 277–284.CrossRefGoogle ScholarPubMed
Saunders, LM, Tompkins, DM, and Hudson, PJ (2000a) Spatial aggregation and temporal migration of free-living stages of the parasitic nematode Trichostrongylus tenuis. Functional Ecology 14, 468–473.10.1046/j.1365-2435.2000.00432.xCrossRefGoogle Scholar
Saunders, LM, Tompkins, DM, and Hudson, PJ (2000b) The role of oxygen availability in the embryonation of Heterakis gallinarum eggs. International Journal for Parasitology 30, 1481–1485.CrossRefGoogle ScholarPubMed
Shearer, CL and Ezenwa, VO (2020) Rainfall as a driver of seasonality in parasitism. International Journal for Parasitology: Parasites and Wildlife 12, 8–12.Google ScholarPubMed
Shifaw, A, Feyera, T, Elliott, T, Sharpe, B, Ruhnke, I, and Walkden-Brown, SW (2022) Method optimisation for prolonged laboratory storage of Ascaridia galli eggs. Veterinary Parasitology 309. https://doi.org/10.1016/j.vetpar.2022.109758CrossRefGoogle ScholarPubMed
Silva, BF, Amarante, MRV, Kadri, SM, Carrijo-Mauad, JR, and Amarante, AFT (2008) Vertical migration of Haemonchus contortus third stage larvae on Brachiaria decumbens grass. Veterinary Parasitology 158, 85–92.CrossRefGoogle ScholarPubMed
Stankiewicz, M (1996) Observations on the biology of free-living stages of Parastrongyloides trichosuri [Nematoda, Rhabditoidea]. Acta Parasitologica 1, 38–42.Google Scholar
Stromberg, BE (1997) Environmental factors influencing transmission. Veterinary Parasitology 72, 247–264.CrossRefGoogle ScholarPubMed
Takeishi, A (2022) Environmental-temperature and internal-state dependent thermotaxis plasticity of nematodes. Current Opinion in Neurobiology 74. https://doi.org/10.1016/j.conb.2022.102541CrossRefGoogle ScholarPubMed
Tarbiat, B, Rahimian, S, Jansson, DS, Halvarsson, P, and Höglund, J (2018) Developmental capacity of Ascaridia galli eggs is preserved after anaerobic storage in faeces. Veterinary Parasitology 255, 38–42.CrossRefGoogle ScholarPubMed
Thomas, F, Bonsall, MB, and Dobson, AP (2005) Parasitism, biodiversity, and conservation. pp. 124–139 in Thomas, F, Renaud, F, and Guegan, J (Eds), Parasitism and ecosystems. Oxford: OUP Oxford.CrossRefGoogle Scholar
Thomas, F, Poulin, R, de Meeüs, T, Guégan, JF, and Renaud, F (1999) Parasites and ecosystem engineering: what roles could they play? Oikos 84, 167–171.CrossRefGoogle Scholar
Thompson, RCA, Lymbery, AJ, and Smith, A (2010) Parasites, emerging disease and wildlife conservation. International Journal for Parasitology 40, 1163–1170.CrossRefGoogle ScholarPubMed
Tompkins, DM, Dobson, AP, Arneberg, P, Begon, ME, Cattadori, IM, Greenman, JV, Heesterbeek, JAP, Hudson, PJ, Newborn, D, Pugliese, A, Rizzoli, AP, Rosa, R, Rosso, F, and Wilson, K (2002) Parasites and host population dynamics. pp. 45–62 in Hudson, PJ, Rizzoli, A, Grenfell, BT, Heesterbeek, H, and Dobson, AP (Eds), The ecology of wildlife diseases. Oxford: Oxford University Press.CrossRefGoogle Scholar
van der Wal, R, Irvine, J, Stien, A, Shepherd, N, and Albon, SD (2000) Faecal avoidance and the risk of infection by nematodes in a natural population of reindeer. Oecologia 124, 19–25.CrossRefGoogle Scholar
van Dijk, J, de Louw, MDE, Kalis, LPA, and Morgan, ER (2009) Ultraviolet light increases mortality of nematode larvae and can explain patterns of larval availability at pasture. International Journal for Parasitology 39, 1151–1156.CrossRefGoogle ScholarPubMed
van Dijk, J and Morgan, ER (2008) The influence of temperature on the development, hatching and survival of Nematodirus battus larvae. Parasitology 135, 269–283.10.1017/S0031182007003812CrossRefGoogle ScholarPubMed
van Dijk, J and Morgan, ER (2009) Hatching behaviour of Nematodirus filicollis in a flock co-infected with Nematodirus battus. Parasitology 136, 805–811.CrossRefGoogle Scholar
van Dijk, J and Morgan, ER (2011) The influence of water on the migration of infective trichostrongyloid larvae onto grass. Parasitology 138, 780–788.CrossRefGoogle ScholarPubMed
van Dijk, J and Morgan, ER (2012) The influence of water and humidity on the hatching of Nematodirus battus eggs. Journal of Helminthology 86, 287–292.CrossRefGoogle ScholarPubMed
van Dijk, J, Sargison, ND, Kenyon, F, and Skuce, PJ (2010) Climate change and infectious disease: helminthological challenges to farmed ruminants in temperate regions. Animal 4, 377–392.CrossRefGoogle ScholarPubMed
Vineer, HR, Steiner, J, Knapp-Lawitzke, F, Bull, K, Fernex, EVS, Bosco, A, Hertzberg, H, Demeler, J, Rinaldi, L, Morrison, AA, Skuce, P, Bartley, DJ, and Morgan, ER (2016) Implications of between-isolate variation for climate change impact modelling of Haemonchus contortus populations. Veterinary Parasitology 229, 144–149.CrossRefGoogle Scholar
Viney, ME (1996) Developmental switching in the parasitic nematode Strongyloides ratti. Biological Sciences 263, 201–208.Google ScholarPubMed
Waghorn, TS, Reynecke, DP, Oliver, AMB, Miller, CM, Vlassoff, A, Koolaard, JP, and Leathwick, DM (2011) Dynamics of the free-living stages of sheep intestinal parasites on pasture in the North Island of New Zealand. 1. Patterns of seasonal development. New Zealand Veterinary Journal 59, 279–286.CrossRefGoogle ScholarPubMed
Wang, T, van Wyk, JA, Morrison, A, and Morgan, ER (2014) Moisture requirements for the migration of Haemonchus contortus third stage larvae out of faeces. Veterinary Parasitology 204, 258–264.CrossRefGoogle ScholarPubMed
Wang, T, Vineer, HR, Morrison, A, van Wyk, JA, Bolajoko, MB, Bartley, DJ, and Morgan, ER (2018) Microclimate has a greater influence than macroclimate on the availability of infective Haemonchus contortus larvae on herbage in a warmed temperate environment. Agriculture, Ecosystems and Environment 265, 31–36.CrossRefGoogle Scholar
Wang, T, Vineer, HR, Redman, E, Morosetti, A, Chen, R, McFarland, C, Colwell, DD, Morgan, ER, and Gilleard, JS (2022) An improved model for the population dynamics of cattle gastrointestinal nematodes on pasture: parameterisation and field validation for Ostertagia ostertagi and Cooperia oncophora in northern temperate zones. Veterinary Parasitology 310. https://doi.org/10.1016/j.vetpar.2022.109777CrossRefGoogle ScholarPubMed
Weaver, HJ, Hawdon, JM, and Hoberg, EP (2010) Soil-transmitted helminthiases: implications of climate change and human behavior. Trends in parasitology 26, 574–581.CrossRefGoogle ScholarPubMed
Young, RR and Anderson, N (1981) The ecology of the free-living stages of Ostertagia ostertagi in a winter rainfall region. Australian Journal of Agricultural Research 32, 371–388.CrossRefGoogle Scholar
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