Cambridge Unversity Press, United Kingdom, pp 1342, Butterworth EW, Beverleyburton M (1981) Observations on the prevalence and intensity of Capillaria spp. Springer-Science + Business Media, B.V, Dordrecht, Book F., Bonsall, M. B. et al. 2003). 2016; Cybulska et al. https://doi.org/10.1016/j.biocon.2010.05.012, Raffel TR, Hoverman JT, Halstead NT, Michel PJ, Rohr JR (2010) Parasitism in a community context: trait-mediated interactions with competition and predation. Home; Products. (New York: Oxford University Press, 2005): 124-139. in ecological interactions. https://doi.org/10.1007/s00436-007-0520-0, Riba L, Tena J (1999) La marmotte (Marmota marmota) en principaut dandorre. https://doi.org/10.1016/j.vetpar.2018.03.007, Daskalaki AA, Ionica AM, Deak G, Gherman CM, DAmico G, Pastrav IR, Matei IA, Domsa C, Mihalca AD (2018) Environmental factors influencing the distribution of Theileria annae in red foxes, Vulpes vulpes in Romania. Many of them are discussed in the presented review, which should facilitate the planning of parasitological research of wild animals. https://doi.org/10.1016/j.ijppaw.2014.04.002, Machnicka-Rowiska B, Rocki B, Dziemian E, Koodziej-Sobociska M (2002) Raccoon dog (Nyctereutes procyonoides) - the new host of Echinococcus multilocularis in Poland. Sukhdeo, https://doi.org/10.1016/j.ijppaw.2016.04.002, Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Parasite mediation https://doi.org/10.1016/j.ijppaw.2018.02.001, Turner WC, Getz WM (2010) Seasonal and demographic factors influencing gastrointestinal parasitism in ungulates of Etosha National Park. An emerging area is the impact of parasites on intraguild predation (IGP). A. M., Briggs, C. J. et al. Parasitology 135(7):767781. Such migratory escape has been proposed as a driver of post-calving migration in reindeer (Rangifer tarandus tarandus) in Norway (Folstad et al. Oxford University Press, Oxford, Schmidt K, Kuijper DPJ (2015) A death trap in the landscape of fear. Parasitol Res 89(1):7778. https://doi.org/10.1016/s0065-308x(08)60503-5, Rohr JR, Civitello DJ, Crumrine PW, Halstead NT, Miller AD, Schotthoefer AM, Stenoien C, Johnson LB, Beasley VR (2015) Predator diversity, intraguild predation, and indirect effects drive parasite transmission. Conserv Biol 21(5):12691279. https://doi.org/10.1079/JOH2006364, Teitelbaum CS, Huang S, Hall RJ, Altizer S (2018) Migratory behaviour predicts greater parasite diversity in ungulates. Recent efforts to include parasites in food webs have revealed sharp changes in the topology of food webs, including species richness, the total number of links, food chain length (the number of trophic levels in a web), and connectance (Lafferty. Proceedings of the National Academy of Science, USA, 98, 4822-4824 (2001). This article has been posted to your Facebook page via Scitable LearnCast. Philos Trans R Soc Lond Ser B Biol Sci 372(1719):20160088. https://doi.org/10.1098/rstb.2016.0088, Cattadori IM, Boag B, Bjornstad ON, Cornell SJ, Hudson PJ (2005) Peak shift and epidemiology in a seasonal host-nematode system. 2012). A recent study revealed that following American mink introduction to an invaded range, parasite abundance in the invasive mammal increased significantly for only 20years (Koodziej-Sobociska et al. To better illustrate the complexity of the reviewed topic, the network of hostparasite associations and factors influencing their coexistence are presented in Fig. Philos Trans R Soc B-Biol Sci 373:20170095. https://doi.org/10.1098/rstb.2017.0095, Bruinskait-Schmidhalter R, arknas M, Malakauskas A, Mathis A, Torgerson P, Deplazes P (2011) Helminths of red foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procyonoides) in Lithuania. 2014; Chen et al. 2015). ), alariosis (Alaria spp. For example, a higher temperature increases parasite growth and infectivity; however, if too high, it may also increase parasite mortality (Lafferty 2009; Studer et al. The true Annu Rev Entomol 34:139161. perspective. https://doi.org/10.1016/0169-4758(88)90077-4, Article Table 1 STH prevalence values (any infection) in infected source villages used in simulations. as predators: Unifying natural enemy ecology. Predators also inadvertently consume parasites during the consumption of infected hosts (Johnson et al. Sex differences in parasite prevalence or intensity are commonly observed (Poulin 1996). Sarcoptic mange is an example of a disease whose spread depends on host sociality and behavior. Then I describe a number of experiments, some of which are very simple and are suitable for courses in experimental parasitology and ecology. For example, treating wild reindeer with anthelmintics increased their body condition, revealing negative relationships between parasitic load and body mass, fat deposition, and fecundity (Stien et al. The experiment section has two parts. Parasitol Res 88(3):259260. 2009, 2014; Duscher et al. Many factors, ecological, biological, and anthropogenic, form a complex network of interdependencies that shape this pattern. The structure and changes over time. ultimate missing links. Polis, G.A. An annual survey of parasite eggs and oocyst excretion from European bison dung showed an increase in their prevalence and abundance during winter months, when supplementary feeding is provided (Koodziej-Sobociska et al. Another trematode endoparasite, Ribeiroia ondatrae, causes amphibians to develop severe limb deformities, including extra or missing limbs (Johnson et al. https://doi.org/10.1086/523943, Bohm M, Palphramand KL, Newton-Cross G, Hutchings MR, White PCL (2008) The spatial distribution of badgers, setts and latrines: the risk for intra-specific and badger-livestock disease transmission. Eur J Wildl Res 58:515. I would also like to thank Anita Michalak for English language correction. https://doi.org/10.1016/j.parint.2017.12.006, Herbison R, Lagrue C, Poulin R (2018) The missing link in parasite manipulation of host behaviour. https://doi.org/10.2307/3933, Anderson RM, May RM (1979) Population biology of infectious diseases. Do you want to LearnCast this session? 2004; Lee et al. Anyone you share the following link with will be able to read this content: Sorry, a shareable link is not currently available for this article. The deterioration of the body condition may be accelerated because individuals in poor condition are unable to control parasitic infection by mounting sufficient immune defenses (Martin et al. Mills, K. E. & Bever, J. D. Oja et al. Vet Parasitol 252:2228. 2004; Torchin and Mitchell 2004). However, parasites may negatively influence the body condition of their hosts (Turgeon et al. (Courtesy of D. Herasimtschuk & P. Johnson), Considering the prominent roles played by parasites in trophic interactions, we might expect parasites to strongly influence food web characteristics. 2011; Kiffner et al. https://doi.org/10.1038/nature06536, Kanchev K, Kamenov Y, Atanassova I, Davidova R, Tomov R (2012) Parasitic alien terrestrial arthropods on small mammals in northeastern and South Bulgaria. 2017). 2012; Gaither et al. Among the variety of studies, the following three main research directions have been proven to be most promising: (i) parasites as accumulation indicators for selected pollutants, (ii) parasites as effect indicators in the broadest sense, and (iii) parasites interfering with the health of their hosts and with established monitoring or effect stu. The introduction of Asian sika deer (Cervus nippon) has led to rapid spread of the alien invasive blood-sucking nematode Ashworthius sidemi in European bison (Bison bonasus) populations in Poland (Drd et al. (2017) showed that the effects of supplementary feeding on gastrointestinal parasite infections in wild boar depend on the life cycle of the parasite species, as well as on environmental factors that affect survival and accumulation of oocysts and eggs at feeding sites. Trans R Soc Trop Med Hyg 101(11):10721074. supports high secondary productivity on small islands and coastal land 2013). In addition behavioural adaptations may also affect parasite population structure, thereby potentially reducing parasite intensity , and ultimately their evolutionary potential, classically defined as the ability to incorporate genotypes able to outcompete those put forward by the opponent . This pattern has been shown in studies of sarcoptic mange in carnivore communities inhabiting Biaowiea Primeval Forest (BPF), Poland (Koodziej-Sobociska et al. https://doi.org/10.1111/j.1365-2907.2006.00078.x, Holmes CJ, Dobrotka CJ, Farrow DW, Rosendale AJ, Benoit JB, Pekins PJ, Yoder JA (2018) Low and high thermal tolerance characteristics for unfed larvae of the winter tick Dermacentor albipictus (Acari: Ixodidae) with special reference to moose. When parasites become prey: https://doi.org/10.1890/09-1697.1, Reiterov K, Dziemian E, Miterpkov M, Antolov D, Koodziej-Sobociska M, Machnicka B, Dubinsky P (2006) Occurrence of Echinococcus multilocularis in red foxes from the Carpathian regions of Slovakia and Poland. 2003; Koodziej-Sobociska et al. Over the last 20 years, three main research directions have been shown to be highly promising and relevant, namely parasites as accumulation indicators for selected pollutants, parasites as effect indicators, and the role of parasites interacting with established bioindicators. 2016c). 1. macroalgal cover and increases abundance of juvenile corals on a Caribbean https://doi.org/10.1644/10-mamm-a-020.1, Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. 1. https://doi.org/10.1007/s00436-015-4742-2, Oivanen L, Kapel CMO, Pozio E, La Rosa G, Mikkonen T, Sukura A (2002) Associations between Trichinella species and host species in Finland. Oikos 88(2):380394. In addition, during the dry season, hosts shed far fewer parasite propagules into the environment than during the wet season (Holmes et al. Here I 2008), and examination of how parasitism changes with host age can provide insight into the existence of host-acquired immunity and age-dependent variation in host exposure to parasites (Woolhouse 1998). https://doi.org/10.1016/j.tree.2004.05.002, Price PW, Westoby M, Rice B, Atsatt PR, Fritz RS, Thompson JN, Mobley K (1986) Parasite mediation in ecological interactions. 1993). (New York: Oxford University Press, 2005): 54-67. Acta Parasitol 59(3):372379. Parasites are known to directly affect their hosts at both the individual and population level. Host population size is important in the context of hostparasite interactions because the spread of parasites is able to persist only if the number of hosts is above critical threshold (Anderson and May 1979). Biol Invasions 17(1):115122. Patterns of increased disease emergence in wildlife, with potential implications for human health and wellbeing, make it an especially relevant time to further integrate parasitism into community ecology and improve our understanding of the roles of parasites in nature. It has been suggested that individuals in poor condition could be a bad choice for parasites due to the lack of available resources (Bize et al. Nature 280(5721):361367. PubMed Mammal Research Institute, Polish Academy of Sciences, Stoczek 1, 17-230, Biaowiea, Poland, You can also search for this author in In some grasslands, fungal pathogens can control productivity and biomass more strongly than herbivorous insects, suggesting that parasites play important roles in ecosystem energetics. Biol Invasions 19(4):11211125. Philos Trans R Soc of Lond B Biol Sci 370(1665):20130553. https://doi.org/10.1098/rstb.2013.0553, Holmala K, Kauhala K (2006) Ecology of wildlife rabies in Europe. 2007; Pyziel et al. 2018a; Laurimaa et al. 2003). Vet Immunol Immunopathol 4(12):153176. Parasitol Res 112(10):35953600. (B) A Minnesota grassland ecosystem. Factors affecting the spread of parasites in populations of wild European terrestrial mammals, https://doi.org/10.1007/s13364-019-00423-8, Host-parasite relationships in invasive species: macroecological framework, Environmental variation mediates the prevalence and co-occurrence of parasites in the common lizard, Zootoca vivipara, Parasite counts or parasite incidences? links. In particular, trophically transmitted parasites may manipulate the behavior https://doi.org/10.1645/18-42, Dobson AP (1988) Restoring island ecosystems: the potential of parasites to control introduced mammals. Theor Popul Biol 120:2941. 6, 147-155 (2003). Parasitol Res 116(4):14111416. This content is currently under construction. F. Keith Barker and Marlene Zuk Published: 14 November 2018 https://doi.org/10.1098/rspb.2018.2147 Abstract Parasites have long been thought to influence the evolution of migration, but precisely determining the conditions under which this occurs by quantifying costs of infection remains a challenge. Oikos 60(3):391395. W., Westoby, M. et al. Prev Vet Med 113(4):356363. Acta Theriol 59(1):4959. https://doi.org/10.9734/ARRB/2015/10263, Sorensen A, van Beest FM, Brook RK (2014) Impacts of wildlife baiting and supplemental feeding on infectious disease transmission risk: a synthesis of knowledge. One of the main problems concerning characterization and systematization of wild mammals parasitofauna is the diversification of mammalian hosts. https://doi.org/10.1016/j.vetpar.2016.08.001, Koodziej-Sobociska M, Pyziel AM, Demiaszkiewicz AW, Borowik T, Kowalczyk R (2016d) Pattern of parasite egg shedding by European bison (Bison bonasus) in the Biaowiea Primeval Forest, Poland. https://doi.org/10.1002/ecy.1953, Kern P, Bardonnet K, Renner E, Auer H, Pawlowski Z, Ammann RW, Vuitton DA (2003) European echinococcosis registry: human alveolar echinococcosis, Europe, 19822000. (Craft et al. Correspondence to https://doi.org/10.1098/rspb.2008.1732, Beldomenico PM, Telfer S, Gebert S, Lukomski L, Bennett M, Begon M (2008) Poor condition and infection: a vicious circle in natural populations. 2001; Cornell et al. A. R. E. The eruption of the ruminants. https://doi.org/10.1111/j.1461-0248.2005.00879.x, Altizer S, Bartel R, Han BA (2011) Animal migration and infectious disease risk. https://doi.org/10.1016/j.jtbi.2009.08.022, Prenter J, MacNeil C, Dick JTA, Dunn AM (2004) Roles of parasites in animal invasions. Indeed, parasites can have variable effects on host morphology, fecundity, reproduction, behaviour and survival (Marcogliese, 2004), indirectly extending their impact to host populations,. Ecology 77, 1390-1397 (1996). This suggests that INNS escape from parasite pressure for a shorter duration than expected (Gendron et al. Am Nat 131(4):544555. Long dry seasons or very low temperatures limit development and survival of parasites in the environment and, as a result, host contact and parasite transmission. In Serengetti: PLoS One:e56940. Parasitol Res 113(9):32813285. Wiad Parazytol 48(1):6568, Mackenstedt U, Jenkins D, Romig T (2015) The role of wildlife in the transmission of parasitic zoonoses in peri-urban and urban areas. The following sections address some of the most relevant aspects and examples in detail. https://doi.org/10.1016/j.biocon.2016.10.034, Mysterud A, Qviller L, Meisingset EL, Viljugrein H (2016) Parasite load and seasonal migration in red deer. 2013). https://doi.org/10.1016/j.meegid.2018.02.005, Rogers WP, Sommerville RI (1963) The infective stage of nematode parasites and its significance in parasitism. Also population density may strongly increase risk of disease transmission through close contact between mating pairs or group members (Sugiura et al. London, UK: survival. 1991) and for non-native invasive American mink (Neovison vison) colonizing new territories in Poland (Koodziej-Sobociska et al. 2010). Oecologia 179(1):201207. Philos Trans R Soc B-Biol Sci 373(1751). J Mammal 92(1):221226. reef. https://doi.org/10.1016/S0020-7519(96)80001-4. Wild animals are subject to strong selection from parasites and other infectious agents. Ann Rev Ecol Systematics 17:487505, Price PW, Westoby M, Rice B (1988) Parasite-mediated competition - some predictions and tests. The emergence of the amphibian fungal pathogen, Batrachochytrium dendrobatidis (Bd), for example, represents a case of a parasite causing mass population declines, and even extinctions of frogs, on a global scale (Kilpatrick et al. Intra-guild predation observed among wolves (Canis lupus) and lynxes (Lynx lynx) preying upon medium-sized carnivores like the red foxes (Vulpes vulpes) or raccoon dogs (Nyctereutes procyonoides) was one of the behavioral traits affecting sarcoptic mange occurrence (Koodziej-Sobociska et al. Parasites include single-celled protozoans such as the agents of malaria . https://doi.org/10.1890/08-0079.1, Lassen B, Janson M, Viltrop A, Neare K, Hutt P, Golovljova I, Tummeleht L, Jokelainen P (2016) Serological evidence of exposure to globally relevant zoonotic parasites in the Estonian population. https://doi.org/10.1079/joh2006357, Hudson PJ, Dobson AP, Lafferty KD (2006b) Is a healthy ecosystem one that is rich in parasites? PubMed Environmental conditions must be permissive for parasite transmission to occur. https://doi.org/10.1089/vbz.2012.1283, Polley L (2005) Navigating parasite webs and parasite flow: emerging and re-emerging parasitic zoonoses of wildlife origin. Contact rate between individuals may be also accelerated by host behavior and sociality. Veterinary Science 8, 118-128 (1967). Biol Conserv 204:163174. volume64,pages 301318 (2019)Cite this article. Density- independent factor: Any factor in the environment that does not depend on the number of members in a population per unit area. https://doi.org/10.1111/j.1523-1739.1988.tb00334.x, Serrano-Moliner M, Morales-Suarez-Varela M, Valero MA (2018) Epidemiology and management of foodborne nematodiasis in the European Union, systematic review 20002016. https://doi.org/10.1371/journal.pntd.0001986, Napoli E, Anile S, Arrabito C, Scornavacca D, Mazzamuto MV, Gaglio G, Otranto D, Giannetto S, Brianti E (2016) Survey on parasitic infections in wildcat (Felis silvestris silvestris Schreber, 1777) by scat collection. Lafferty, https://doi.org/10.1016/i.trstmh.2007.05.014, Snchez CA, Becker DJ, Teitelbaum CS, Barriga P, Brown LM, Majewska AA, Hall RJ, Altizer S (2018) On the relationship between body condition and parasite infection in wildlife: a review and meta-analysis. https://doi.org/10.2307/3545084, Lymbery AJ, Morine M, Kanani HG, Beatty SJ, Morgan DL (2014) Co-invaders: the effects of alien parasites on native hosts. Most density-dependent factors make the per capita growth rate go down as the population increases. https://doi.org/10.1111/j.0141-9838.2004.00710.x, Koodziej-Sobociska M, Miniuk M (2018) Sparganosis neglected zoonosis and its reservoir in wildlife. Google Scholar, Chaneton EJ, Bonsall MB (2000) Enemy-mediated apparent competition: empirical patterns and the evidence. It can be assumed that comprehensive studies are only feasible through the combination of parasitological data with knowledge about the ecology and biology of mammalian hosts, their responses to infection, the history and range of non-native invasive species, or the methods of species management. J Wildl Dis 28:4250, Thomas F, Renaud F, Mees T, Czilly F (1995) Parasites, age and the Hamilton-Zuk hypothesis: inferential fallacy? A recent meta-analytical synthesis of parasite induced mortality of nestlings showed an overall small effect (12% mean parasite-induced mortality, range 0-89%, n = 117), with parasite-induced mortality determined by latitude, nesting site, probability of host survival and parasite prevalence (Mller et al., 2009). Academic Press, Cambridge, pp 219308, Walker SM, Demiaszkiewicz AW, Kozak M, Wdrychowicz H, Teofanova D, Prodohl P, Brennan G, Fairweather I, Hoey EM, Trudgett A (2013) Mitochondrial DNA haplotype analysis of liver fluke in bison from Biaowiea Primeval Forest indicates domestic cattle as the likely source of infection. This results in behavioral adaptations that help potential hosts avoid falling prey to parasites (Sarabian et al. The entomologist E. O. Wilson has characterised parasites as "predators that eat prey in units of less than one". Why are parasites ecologically important? https://doi.org/10.1016/j.biocon.2006.04.011, Milinski M (1984) Parasites determine a predators optimal feeding strategy. Oxford University Press, Oxford, pp 4353, Chapter Biol Invasions 18(10):30473061. https://doi.org/10.1007/s10530-011-0083-y, Grski P, Zalewski A, akomy M (2006) Parasites of carnivorous mammals in Biaowiea Primeval Forest. https://doi.org/10.1007/s00436-018-5819-5, Reperant LA, Hegglin D, Fischer C, Kohler L, Weber JM, Deplazes P (2007) Influence of urbanization on the epidemiology of intestinal helminths of the red fox (Vulpes vulpes) in Geneva, Switzerland. 2000; Koodziej-Sobociska et al. The parasite can infect one or both of the involved species . https://doi.org/10.1371/journal.pone.0026365, Article Jaenike, J. Yet we have only begun to dissect the complex roles played by parasites in community ecology. Social carnivores are more susceptible to mange than solitary ones (Koodziej-Sobociska et al. PubMed 2016). 2016a, d; Pyziel et al. 2009). Parasites live in other host organisms and depend on them for survival. Bulg J Agricult Sci 18(6):965970, Karamon J, Kochanowski M, Sroka J, Cencek T, Rycki M, Chmurzyska E, Bilska-Zajc E (2014) The prevalence of Echinococcus multilocularis in red foxes in Poland current results (20092013). Parasites that infect new hosts via trophic transmission frequently alter their host's behavior or morphology in ways that increase predation risk, thereby aiding the parasite in reaching the next host in its life cycle (Poulin et al. 2000; Jones et al. International Marmot Network, Lyon, France, pp 2732, Rocchigiani G, Ebani VV, Nardoni S, Bertelloni F, Bascherini A, Leoni A, Mancianti F, Poli A (2018) Molecular survey on the occurrence of arthropod-borne pathogens in wild brown hares (Lepus europaeus) from Central Italy. 2006; Viggers et al. J Parasitol 104(5):557559. Proc R Soc B-Biol Sci 275(1634):511518. Mammal Rev 36(1):1736. https://doi.org/10.1111/j.1461-0248.2012.01833.x, Faria PJ, van Oosterhout C, Cable J (2010) Optimal release strategies for captive-bred animals in reintroduction programs: experimental infections using the guppy as a model organism. M. V. K. & Hernandez, A. D. Food web patterns and the parasite's Elton, C. https://doi.org/10.1016/j.tree.2006.04.007, Hurley WL, Theil PK (2011) Perspectives on immunoglobulins in colostrum and milk. 2008). Moreover, infected wild terrestrial mammals could have an important influence on human health, as they are reservoirs for many zoonotic diseases including echinococossis (Echinococcus spp. 2010). PLoS One 9(5):e96358. Tradeoffs between disease risk and foraging drive animal activity around raccoon latrines. Thus, there are four possible combinations: (1) both filters are closedthe hostparasite association cannot exist; (2) the encounter filter is opened, but the compatibility filter is closedthe parasitehost association does not exist, but selective pressure on the parasite may allow some individuals of the parasite (e.g., selected mutants) to open the compatibility filter; (3) the encounter filter is closed, but the compatibility filter is openthe parasitehost association also does not exist, although a change in composition of the ecosystem or in host behavior may open the filter and result in association; (4) both the encounter and compatibility filters are open and the hostparasite association may exist (Combes 2001). ecology and impact of chytridiomycosis: An emerging disease of amphibians. Ecol Lett 7(8):721733. 2002). https://doi.org/10.1016/j.vetpar.2003.09.017, Smith MJ, Telfer S, Kallio ER, Burthe S, Cook AR, Lambin X, Begon M (2009) Host-pathogen time series data in wildlife support a transmission function between density and frequency dependence. 2009). 2011); (2) behavior (Herbison et al. Med Mycol 44(1):5160. https://doi.org/10.1016/j.biocon.2009.06.002, Figueiredo A, Oliveira L, Madeira de Carvalho L, Fonseca C, Torres T (2016) Parasite species of the endangered Iberian wolf (Canis lupus signatus) and a sympatric widespread carnivore. In fact parasitism is more common than traditional predation as a consumer lifestyle (De Mees & Renaud 2002), and arguably represents the most widespread life-history strategy in nature (Price 1980). 2006). https://doi.org/10.1073/pnas.0809145106, Solomon NU, James IM, Alphonsus NO, Nkiruka RU (2015) A review of host-parasite relationships. 2018a). Ecology Letters 6, 189-196 (2003). Ecography 41:12831294. https://doi.org/10.1890/04-0232, Schweiger A, Ammann RW, Candinas D, Clavien PA, Eckert J, Gottstein B, Halkic N, Muellhaupt B, Prinz BM, Reichen J, Tarr PE, Torgerson PR, Deplazes P (2007) Human alveolar echinococcosis after fox population increase, Switzerland. Parasitol Res 87(9):790791. Vet Parasitol 191(12):161164. 2016; Laurimaa et al. Understanding how both anticipated and cryptic changes in a system might affect parasite transmission at an individual, local 2023 Springer Nature Switzerland AG. 2002; Nahorski et al. 2000; Taraschewski 2006). Am Nat 123(4):572577. Vet Parasitol 231:106109. W. & Taylor, W. P. Long term The level of infection is associated with a hosts age (Bush et al. Parasites have been shown to reduce host density and to induce host population extinction in some cases but not in others. Both lizards host a malarial parasite, Plasmodium azurophilum, but the two lizards co-occur only where A. gingivinus is heavily parasitized (Figure 4). Proc Natl Acad Sci U S A 112(10):30083013. https://doi.org/10.1007/s10530-014-0709-y, Shimalov VV (2002) Helminth fauna of the striped field mouse (Apodemus agrarius Pallas, 1778) in ecosystems of Belorussian Polesie transformed as a result of reclamation. On the other hand, treatment of animals prior to release may not be beneficial because it may reduce their levels of immunity to disease (Faria et al. 2010; Demiaszkiewicz et al. https://doi.org/10.1111/j.1365-2656.2010.01742.x, Torchin ME, Mitchell CE (2004) Parasites, pathogens, and invasions by plants and animals. 19, 371-393 (1988). Population size often depends on population health status; the size of the weakened population with higher mortality rates will be smaller, which should slow down pathogen transmission. 1998; Koodziej-Sobociska et al. 2017). Int J Parasitol 43(1213):10791088. https://doi.org/10.1007/s13364-016-0270-4, Koodziej-Sobociska M, Brzeziski M, Niemczynowicz A, Zalewski A (2018a) High parasite infection level in non-native invasive species: it is just a matter of time. Apart from reproductive status, host immunity may also vary seasonally in relation to stress, food availability, photoperiod, etc. 1993). in Eurasian badger (Meles meles). You have authorized LearnCasting of your reading list in Scitable. Mammal Res 61(3):179186. Mitchell, 2008; Kethineni et al. Mn-Fr: 8am - 4pm. & Carpenter, R. C. https://doi.org/10.2478/s11686-014-0214-6, Article (2014), alien parasites can be divided into two groups: cointroduced parasites which have been transported with an alien host to a new territory and coinvading parasites which have been cointroduced and then spread to new, native hosts. The virus infects both species, but native red squirrels are highly susceptible, whereas invasive grey squirrels experience relatively minor negative effects. https://doi.org/10.1111/j.1523-1739.2007.00776.x, Pence DB, Ueckermann E (2002) Sarcoptic mange in wildlife. Proc R Soc B-Biol Sci 275(1644):17531759. 2008). 2014; Turner and Getz 2010). The prevalence values are achieved by setting the basic reproductive number R 0 and k (the shape parameter of the negative binomial distribution that describes the aggregation of parasites among hosts). Annual Review of Ecology and Systematics Google Scholar, Barger IA, Siale K, Banks DJD, Lejambre LF (1994) Rotational grazing for control of gastrointestinal nematodes of goats in a wet tropical environment. However, the lower A. sidemi infection intensity observed in European bison bulls (Koodziej-Sobociska et al. Oecologia 92, 58-64 (1992). 2018a). Emerg Infect Dis 13(6):878882. Annu Res Rev Biol 5:372385. In reality, though, populations of one species are rarelyif ever!isolated from populations of other species. https://doi.org/10.1007/s00436-015-4466-3, Rook GAW (2007) The hygiene hypothesis and the increasing prevalence of chronic inflammatory disorders. 2008; Turgeon et al. Science 330(6001):243246. For example. Ecosystem energetic implications of parasite and free-living biomass in three A) tundra B) deciduous forests C) tropics D) grasslands E) islands., We should care about loss in biodiversity in the populations of other species because of A) biophilia. https://doi.org/10.1016/j.ecolmodel.2015.11.021, Watve MG, Sukumar R (1995) Parasite abundance and diversity in mammals - correlates with host ecology. https://doi.org/10.1016/j.biocon.2010.02.032, Dmitric M, Vidanovic D, Vaskovic N, Matovic K, Sekler M, Debeljak Z, Karabasil N (2017) Trichinella infections in red foxes (Vulpes vulpes) and golden jackals (Canis aureus) in six districts of Serbia. 2018). 2014; Lempp et al. Parasitol Res 87(8):680681. biodiversity and conservation. https://doi.org/10.2307/3285395, Oja R, Velstrom K, Moks E, Jokelainen P, Lassen B (2017) How does supplementary feeding affect endoparasite infection in wild boar? 2011); on the other, migratory hosts may escape parasitism. Can J Zool 86(12):13891396. This method, however, has limitations, including the seasonality of parasite egg shedding and difficulty in their proper identification (Hines et al. Breastfed, young mammals should be better protected against diseases because they get maternal antibodies with milk. A parasite is a plant or an animal that lives on, or with, or inside a larger species extracting nutrients. This sometimes leads to a relatively stable relationship tending toward a parasitehost balance, as it is in the evolutionary interest of the parasite that its host survives (Rook 2007). The study by Cornell et al. A novel approach is using contact networks to explore and understand the dynamics of disease transmission; for example, data on African lion (Panthera leo) behavior and movement provide sophisticated evidence that outbreaks of canine distemper virus are partly driven by interspecific interactions among lions, spotted hyenas (Crocuta crocuta), and jackals (Canis spp.) J Parasitol 94(4):981984. J Theor Biol 261(4):561569. Ecography 36(12):12631275. Science 359(6381):12131214. Biol Conserv 143(6):13291341. Vet Parasitol 231:115117. 2008; Koodziej-Sobociska et al. In some studies of parasitewildlife interactions, experimental manipulations are needed to confirm directional relationships and point to underlying mechanisms (Snchez et al. and biomass by pathogens. 2012; Daszak et al. Parasite and predator avoidance strategies sometimes have mutual effects, e.g., avoiding predator feces protects prey against both predators and their parasites (Weinstein et al. Funct Ecol 25(1):132138. https://doi.org/10.1371/journal.pone.0096358, Sutor A, Schwarz S, Conraths FJ (2014) The biological potential of the raccoon dog (Nyctereutes procyonoides, Gray 1834) as an invasive species in Europe - new risks for disease spread? https://doi.org/10.1098/rspb.2007.1415, Craft ME, Hawthorne PL, Packer C, Dobson AP (2008) Dynamics of a multihost pathogen in a carnivore community. https://doi.org/10.1007/bf00310212, Mller AP (2005) Parasitism and the regulation of host populations. Mighty Mutualisms: The Nature of Plant-pollinator Interactions, Explaining General Patterns in Species Abundance and Distributions, Species with a Large Impact on Community Structure, Effects of Biogeography on Community Diversity, Trophic Cascades Across Diverse Plant Ecosystems, Causes and Consequences of Biodiversity Declines, Environmental Context Influences the Outcomes of Predator-prey Interactions and Degree of Top-down Control, Abiotically-Mediated Direct and Indirect Effects, Disturbance and Diversity: An Ecological Chicken and Egg Problem, Omnivorous Insects: Evolution and Ecology in Natural and Agricultural Ecosystems. https://doi.org/10.1111/j.1523-1739.1988.tb00333.x, Drd J, Demiaszkiewicz AW, Lachowicz J (1998) Ashworthius sidemi (Nematoda, Trichostrongylidae) a new parasite of the European bison Bison bonasus (L.) and the question of independence of A. gagarini. Vet Parasitol 246:14. https://doi.org/10.1016/j.ijppaw.2014.01.002, Lafferty KD (2009) The ecology of climate change and infectious diseases. Many live their lives secretively, in intimate contact with their host, but invisible to the outside world. It should be emphasized that human activity and natural factors are very important. Parasit Vectors 10:609. https://doi.org/10.1186/s13071-017-2571-0, Kavaliers M, Choleris E (2018) The role of social cognition in parasite and pathogen avoidance. 1997). Nature 451(7181):990993. https://doi.org/10.1093/jmammal/gyv043, Fuxjager MJ, Foufopoulos J, Diaz-Uriarte R, Marler CA (2011) Functionally opposing effects of testosterone on two different types of parasite: implications for the immunocompetence handicap hypothesis. 2002). 2016a) stands in opposition to the widely observed patterns of the higher susceptibility of males to parasitosis (Alexander and Stimson 1988; Klein 2004; Zuk and McKean 1996). Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. https://doi.org/10.1007/s10530-016-1199-x, Ostfeld RS, Holt RD (2004) Are predators good for your health? https://doi.org/10.1007/s12639-016-0847-5, Shimalov VV, Shimalov VT (2000) Helminth fauna of the wolf (Canis lupus Linnaeus, 1758) in Belorussian Polesie. All these interdependencies work bidirectionally as pathogens have an impact on animal populations, but population status, size, and density influence the speed and efficiency of disease transmission and spread (Scott 1988; Tompkins et al. Adv Parasitol 1:109177. The effects of parasitism on ecological communities can be particularly pronounced when the hosts are keystone or dominant species with important functions in an ecosystem. 2016; Penn and Potts 1998; Watve and Sukumar 1995); and (4) regulation of host populations (Dobson 1988; Koodziej-Sobociska et al. 1996. The first of these models, exponential growth, describes theoretical populations that increase in numbers without any limits to their growth. (A) A fungal pathogen (Uromyces lespedezae-procumbenti) on the leaves of a prairie legume. https://doi.org/10.1111/ele.13160, Sarabian C, Curtis V, McMullan R (2018) Evolution of pathogen and parasite avoidance behaviours. Combes concepts of encounter and compatibility as a sequence of filters allow a more complete understanding of the parasitehost relationship (Combes 2001); however, in this concept, there is no consideration of anthropogenic factors which also may play a very important role in hostparasite coexistence formation (e.g., Cunningham 1996; Murray et al. Competition and predation can influence rates of parasite infection by altering population densities of hosts and vectors (Raffel et al. This is the case for some gastrointestinal parasites of herbivorous mammals, where disease transmission occurs only through the excretion of eggs/oocysts in feces and contamination of the environment (Drd et al. Proc Natl Acad Sci U S A 92(19):89458949. D. M., White, A. R. et al. 2018a) and is similar to the landscape of fear theory of predator avoidance in that parasite avoidance behavior can also affect ecology and evolution (Kuijper et al. The parameters required to achieve a desired prevalence value vary by species, because other . 1986). 2009), and so both the host and parasite are forced to constantly adapt to one another (Schmid-Hempel 2011). https://doi.org/10.1111/j.0906-7590.2008.05314.x, Bonesi L, Palazon S (2007) The American mink in Europe: status, impacts, and control. 2016; Machnicka-Rowiska et al. Parasite species varied strongly in their effects on host fecundity, host survival, host density reduction, and the frequency with which they drove host populations to extinction. Definitive hosts for parasites such as Echinococcus multilocularis shed parasite eggs into the environment; this further leads to a persistent source of infection not only for intermediate hosts like rodents, but also for humans as incidental hosts (Bastien et al. Acta Parasitol 43(2):7580, Drd J, Demiaszkiewicz AW, Lachowicz J (2003) Expansion of the Asiatic parasite Ashworthius sidemi (Nematoda, Trichostrongylidae) in wild ruminants in Polish territory. In Parasitism Ecology 90(4):888900. lizards. Infect Dis Poverty 7:59. https://doi.org/10.1186/s40249-018-0437-0, Coati N, Schnieder T, Epe C (2004) Vertical transmission of Toxocara cati Schrank 1788 (Anisakidae) in the cat. J Helminthol 80:99128. Hostparasite dynamics can be strongly affected by both climate and season (Altizer et al. https://doi.org/10.1007/s00436-018-5769-y, Penn D, Potts WK (1998) Chemical signals and parasite-mediated sexual selection. https://doi.org/10.1007/s00436-013-3547-4, Rentera-Sols Z, Birka S, Schmaschke R, Krol N, Obiegala A (2018a) First detection of Baylisascaris procyonis in wild raccoons (Procyon lotor) from Leipzig, Saxony, eastern Germany. OIKOS 74:305309, Thompson RCA (2013) Parasite zoonoses and wildlife: one health, spillover and human activity. J Parasitol 62(3):460465, Lefevre T, Lebarbenchon C, Gauthier-Clerc M, Misse D, Poulin R, Thomas F (2009) The ecological significance of manipulative parasites. Proc R Soc B-Biol Sci 270(1511):153158. J Parasitol 88:8488. https://doi.org/10.1007/s00442-015-3465-5, Nahorski WL, Knap JP, Pawowski ZS, Krawczyk M, Polaski J, Stefaniak J, Patkowski W, Szostakowska B, Pietkiewicz H, Grzeszczuk A, Felczak-Korzybska I, Gob E, Wnukowska N, Paul M, Kacprzak E, Sokolewicz-Bobrowska E, Nicigorska-Olsen J, Czyrznikowska A, Chomicz L, Cielecka D, Myjak P (2013) Human alveolar echinococcosis in Poland: 19902011. For parasites acquired from food obtained from wild animals, the ability to accurately predict risk of infection is also influenced by cultural traditions for food preparation that may affect parasite viability (Polley 2005). PloS Neglect Trop Dis 7(1):e1986. The ways in which humans acquire zoonotic parasites are complex. Lessios, H. A. Parasites in food webs: The https://doi.org/10.1111/j.1365-2435.2010.01784.x, Gaither MR, Aeby G, Vignon M, Meguro Y, Rigby M, Runyon C, Toonen RJ, Wood CL, Bowen BW (2013) An invasive fish and the time-lagged spread of its parasite across the Hawaiian archipelago. Int J Parasitol 35(1112):12791294. In Canada, infection intensity of A. putorii in the raccoon (Procyon lotor) was also the highest during spring and lowest during winter (Butterworth and Beverleyburton 1981). Alternatively, parasites can also serve as important sources of prey (Figure 1). Reduced exposure to natural antigens and loss of immunogenetic variation during captive breeding may impair the survival probability of released animals (Cunningham 1996; Mathews et al. Proc R Soc B-Biol Sci 283:20162226. https://doi.org/10.1098/rspb.2016.2226, Bagrade G, Deksne G, Ozolina Z, Howlett SJ, Interisano M, Casulli A, Pozio E (2016) Echinococcus multilocularis in foxes and raccoon dogs: an increasing concern for Baltic countries. Acta Theriol 40(1):121, Krasiska M, Krasiski ZA, Bunevich AN (2000) Factors affecting the variability in home range size and distribution in European bison in the Polish and Belarussian parts of the Biaowiea Forest. (Martin et al. Biol Conserv 142(12):30993107. Sinclair, 2010; Viggers et al. Source of food is an important factor for parasite transmission, because predators and scavengers consume prey along with their parasites. https://doi.org/10.1016/j.tpb.2017.12.005, Pedersen AB, Fenton A (2007) Emphasizing the ecology in parasite community ecology. https://doi.org/10.1016/j.ijppaw.2015.01.006, Magi M, Macchioni F, Dell'omodarme M, Prati MC, Calderini P, Gabrielli S, Iori A, Cancrini G (2009) Endoparasites of red fox (Vulpes vulpes) in Central Italy. Human impact plays an important, and often negative, role in wild populations also through opening natural filters that normally control parasite transmission in natural conditions. Commonly debated questions include: Which parasites are prevalent in native ranges but absent in new territories, and vice versa? Figure 4:Parasite-mediated competition facilitates species coexistence. 2015; Woolhouse 1998; Zuk and McKean 1996). 2005). Alternately, predators compete for and kill their prey; therefore, they consume both parasites and their hosts, and limit the number and density of infected individuals (Rohr et al. 2006; Szczsna et al. 2018c); this can cause disease spread and transmission. Not only natural factors shape the hostparasite associations in wildlife. Population-level consequences of parasite aggregation. Parasitol Res 87(10):886887. how to generate tsr report from idrac 6. Acta Theriol 42(3):289312, Schulte-Hostedde AI, Elsasser SC (2011) Spleen mass, body condition, and parasite load in male American mink (Neovison vison). Comp Parasitol 81(2):155164. Parasit Vectors 10:332. https://doi.org/10.1186/s13071-017-2269-3, Jackson KM, Nazar AM (2006) Breastfeeding, the immune response, and long-term health. 2017; Hurnkov et al. Researches in 2018; Milinski 1984; Moore 1984); (3) sexual selection (Auld et al. Parasites are known to directly affect their hosts at both the individual and population level. Ecological Parasitol Res 87(10):838839. & Hurd, S. D. 2014b). Parasitol Res 113(1):317322. Int J Parasitol Parasit Wildl 5(2):164167. Mass mortality of Diadema antillarum in the Caribbean: What have we learned? Google Scholar, Anderson RM (1982) The population dynamics of infectious diseases: theory and applications, Population and Community Biology Series. 2018b; Vadlejch et al. Many studies have confirmed the possibility of escape from parasites, having shown that parasite species richness or prevalence is lower in host populations inhabiting invaded ranges compared to those in native ranges (Colautti et al. 2018; Kutz et al. 2013) and these techniques should be further developed and implemented. Trends Ecol Evol 13(10):391396. https://doi.org/10.1098/rspb.2008.0147, Beltrn-Beck B, Garca J, Gortzar C (2012) Raccoons in Europe: disease hazards due to the establishment of an invasive species. Parasites can function as both predators and prey. However, little is known about their more subtle, indirect effects and how these may affect population and community dynamics. Finally, rare and unique material from wild mammals is often used not only for parasitological studies but also for other types of studies (e.g., diet analyses), which can distort parasitological analyses because some species of parasites inhabit mainly host stomachs (Koodziej-Sobociska et al. Weak relationships between vegetation cover and parasitic fly infestations, Lizards and rabbits may increase Chagas infection risk in the Mediterranean-type ecosystem of South America, https://doi.org/10.1016/0169-4758(88)90077-4, https://doi.org/10.2478/s11686-014-0214-6, https://doi.org/10.1111/j.1461-0248.2005.00879.x, https://doi.org/10.1111/j.1863-2378.2008.01154.x, https://doi.org/10.1146/annurev.en.34.010189.001035, https://doi.org/10.1186/s13071-016-1891-9, https://doi.org/10.1016/0304-4017(94)90023-X, https://doi.org/10.1111/j1365-2907.2012.0212.x, https://doi.org/10.1007/s10344-011-0600-4, https://doi.org/10.1016/j.vetpar.2010.06.038, https://doi.org/10.1016/j.vetpar.2016.04.010, https://doi.org/10.1007/s00436-017-5446-6, https://doi.org/10.1111/j.0906-7590.2008.05314.x, https://doi.org/10.1016/j.biocon.2006.09.006, https://doi.org/10.1371/journal.pone.0026365, https://doi.org/10.1017/S0031182011001715, https://doi.org/10.1034/j.1600-0706.2000.880217.x, https://doi.org/10.1016/j.vetpar.2018.01.011, https://doi.org/10.1186/s40249-018-0437-0, https://doi.org/10.1007/s00436-003-1019-y, https://doi.org/10.1111/j.1461-0248.2004.00616.x, https://doi.org/10.1111/j.1365-2656.2008.01410.x, https://doi.org/10.1046/j.1523-1739.1996.10020349.x, https://doi.org/10.1016/j.vetpar.2018.03.007, https://doi.org/10.1016/j.ttbdis.2018.01.019, https://doi.org/10.1126/science.287.5452.443, https://doi.org/10.1016/j.ijppaw.2014.12.005, https://doi.org/10.2478/s11686-013-0164-4, https://doi.org/10.1016/j.biocon.2010.02.032, https://doi.org/10.1111/j.1523-1739.1988.tb00333.x, https://doi.org/10.1007/s00436-002-0675-7, https://doi.org/10.1007/s00436-017-5405-2, https://doi.org/10.1111/j.1461-0248.2012.01833.x, https://doi.org/10.1016/j.biocon.2009.06.002, https://doi.org/10.1016/j.ijppaw.2016.04.002, https://doi.org/10.1111/j.1365-2435.2010.01784.x, https://doi.org/10.1371/journal.pone.0056940, https://doi.org/10.1016/j.vetpar.2017.08.021, https://doi.org/10.1007/s00436-018-5908-5, https://doi.org/10.1007/s10530-011-0083-y, https://doi.org/10.1111/j.1461-0248.2009.01306.x, https://doi.org/10.1016/j.parint.2017.12.006, https://doi.org/10.1186/s13071-018-2805-9, https://doi.org/10.1016/j.vetpar.2007.07.006, https://doi.org/10.1111/j.1365-2907.2006.00078.x, https://doi.org/10.1016/j.ttbdis.2017.10.013, https://doi.org/10.1016/j.tree.2006.04.007, https://doi.org/10.1016/j.vetpar.2016.06.010, https://doi.org/10.1186/s13071-017-2269-3, https://doi.org/10.1007/s00436-013-3657-z, https://doi.org/10.1186/s13071-018-3021-3, https://doi.org/10.2478/s11686-010-0030-6, https://doi.org/10.2478/s11686-014-0253-z, https://doi.org/10.1186/s13071-017-2571-0, https://doi.org/10.1080/13693780500220498, https://doi.org/10.1007/s00442-013-2664-1, https://doi.org/10.1111/j.0141-9838.2004.00710.x, https://doi.org/10.1016/j.parint.2013.12.011, https://doi.org/10.1007/s11284-013-1118-x, https://doi.org/10.1016/j.ijppaw.2016.09.005, https://doi.org/10.1007/s10344-016-1037-6, https://doi.org/10.1016/j.vetpar.2016.08.001, https://doi.org/10.1007/s13364-016-0270-4, https://doi.org/10.1007/s10393-018-1327-4, https://doi.org/10.1007/s00436-018-5953-0, https://doi.org/10.1371/journal.pone.0172829, https://doi.org/10.1111/j.1600-0587.2013.00266.x, https://doi.org/10.1016/j.ijppaw.2014.01.002, https://doi.org/10.1371/journal.pone.0164142, https://doi.org/10.1016/j.vetpar.2016.01.020, https://doi.org/10.1016/j.tree.2008.08.007, https://doi.org/10.1371/journal.pone.0175469, https://doi.org/10.1111/j.1466-8238.2006.00301.x, https://doi.org/10.1016/0165-2427(83)90057-0, https://doi.org/10.1016/j.biocon.2009.08.021, https://doi.org/10.1016/j.ijppaw.2014.04.002, https://doi.org/10.1016/j.ijppaw.2015.01.006, https://doi.org/10.7589/0090-3558-45.3.881, https://doi.org/10.1016/j.biocon.2006.04.011, https://doi.org/10.1016/j.biocon.2016.10.034, https://doi.org/10.1007/s00442-015-3465-5, https://doi.org/10.1371/journal.pntd.0001986, https://doi.org/10.1007/s00436-015-4742-2, https://doi.org/10.1007/s00436-017-5512-0, https://doi.org/10.1186/s13071-016-1746-4, https://doi.org/10.1007/s10530-016-1199-x, https://doi.org/10.1016/j.tpb.2017.12.005, https://doi.org/10.1016/j.tree.2006.11.005, https://doi.org/10.1111/j.1523-1739.2007.00776.x, https://doi.org/10.1007/s00436-014-3991-9, https://doi.org/10.1007/s00436-018-5769-y, https://doi.org/10.1016/s0169-5347(98)01473-6, https://doi.org/10.1016/j.ijpara.2005.07.003, https://doi.org/10.1016/s0020-7519(96)00108-7, https://doi.org/10.1016/j.ijppaw.2017.03.006, https://doi.org/10.1016/s0304-4017(00)00344-7, https://doi.org/10.1016/j.jtbi.2009.08.022, https://doi.org/10.1016/j.tree.2004.05.002, https://doi.org/10.1016/j.biocon.2010.05.012, https://doi.org/10.2478/s11686-006-0016-6, https://doi.org/10.1007/s00436-013-3547-4, https://doi.org/10.1007/s00436-018-5988-2, https://doi.org/10.1007/s00436-018-5819-5, https://doi.org/10.1007/s00436-007-0520-0, https://doi.org/10.1016/j.meegid.2018.02.005, https://doi.org/10.1016/s0065-308x(08)60503-5, https://doi.org/10.1007/s00436-015-4466-3, https://doi.org/10.1016/i.trstmh.2007.05.014, https://doi.org/10.1007/s13364-015-0229-x, https://doi.org/10.1111/j.1523-1739.1988.tb00334.x, https://doi.org/10.1080/20477724.2018.1487663, https://doi.org/10.1007/s10530-014-0709-y, https://doi.org/10.1007/s12639-016-0847-5, https://doi.org/10.1007/s00436-001-0582-3, https://doi.org/10.1007/s00436-001-0521-3, https://doi.org/10.1007/s00436-002-0701-9, https://doi.org/10.1016/j.vetpar.2003.09.017, https://doi.org/10.1016/j.prevetmed.2013.11.010, https://doi.org/10.1007/s00442-015-3319-1, https://doi.org/10.1371/journal.pone.0096358, https://doi.org/10.1007/s13364-013-0138-9, https://doi.org/10.1017/s0031182008000395, https://doi.org/10.1016/j.ijpara.2013.06.007, https://doi.org/10.1016/j.ijpara.2010.04.009, https://doi.org/10.1111/j.1365-2656.2010.01742.x, https://doi.org/10.1007/s10531-005-5824-8, https://doi.org/10.1016/j.ijppaw.2018.02.001, https://doi.org/10.7589/0090-3558-46.4.1108, https://doi.org/10.1007/s10530-016-1306-z, https://doi.org/10.2478/s11756-011-0123-1, https://doi.org/10.1016/j.vetpar.2012.08.002, https://doi.org/10.1016/j.ecolmodel.2015.11.021, https://doi.org/10.1016/S0169-4758(98)01318-0, https://doi.org/10.31111/j.1095-8312.2011.01811.x, https://doi.org/10.1016/S0020-7519(96)80001-4.

Which Of The Following Is A Brachiopod?, Green Gables Golf Course, Greek Salad Dressing With Anchovy Paste, Technics Turntable Arm Won T Go Down, Is It Safe To Mix Soda With Alcohol, Ros2 Check If Node Is Running, Pivpn/wireguard Config File, Xls Is Not Utf-8 Encoded,