International Journal for Parasitology 49 (2019) 625–634 Contents lists available at ScienceDirect International Journal for Parasitology journal homepage: www.elsevier.com/locate/ijpara Major determinants of the occurrence of a globally invasive parasite in riverine fish over large-scale environmental gradients ⇑ Alberto Maceda-Veiga a,b, , Ralph Mac Nally c,d, Andy J. Green e, Robert Poulin f, Adolfo de Sostoa a a Department of Evolutionary Biology, Ecology, and Environmental Sciences-Institute of Research in Biodiversity (IRBio), University of Barcelona, 08028 Barcelona, Spain b Department of Integrative Ecology, Estación Biológica de Doñana (EBD-CSIC), 41092 Sevilla, Spain c Institute for Applied Ecology, University of Canberra, Bruce 2617, ACT, Australia d Sunrise Ecological Research Institute (SERI), Ocean Grove 3226 Australia e Department of Wetland Ecology, Estación Biológica de Doñana (EBD-CSIC), 41092 Sevilla, Spain f Department of Zoology, University of Otago, P.O. Box 56, Dunedin, New Zealand article info abstract Article history: The increased rate of outbreaks of infectious diseases in ecosystems is a dramatic consequence of global Received 9 December 2018 change, particularly when outbreaks affect important resources such as freshwater fish. However, the Received in revised form 4 March 2019 links between disease-inducing epizootics and widespread human impacts, including nutrient pollution Accepted 6 March 2019 and high water conductivity, in freshwater organisms are largely unexplored. We used data from exten- Available online 21 May 2019 sive surveys in northeastern Spain (99,700 km2, 15 river catchments, n = 530 sites) to explore the envi- ronmental factors that singly, or in combination, are likely to influence the occurrence of the invasive Keywords: parasite, Lernaea cyprinacea, after accounting for host fish characteristics. Smaller fish, lower altitudes, Alien species higher water conductivity and nutrient pollution were associated with higher probabilities of infection Eutrophication Water pollution in 19 endemic and widely distributed fish species. We found no evidence that interactive effects among Copepoda riverine stressors related to water and physical habitat quality better explained the probability of occur- Host size rence of L. cyprinacea in fish than did additive-stressor combinations. Nutrient pollution and high water Multiple stressors conductivity were two of the major factors contributing to the increased occurrence of L. cyprinacea. Fish parasite Therefore, the improvement of wastewater treatment processes and agricultural practices probably would help to reduce the occurrence of this parasite among native fish. Ó 2019 Published by Elsevier Ltd on behalf of Australian Society for Parasitology. 1. Introduction Wiedmann, 2014), understanding how human impacts affect infec- tion dynamics is a priority for disease ecology under global change. Infectious diseases are emerging at unprecedented rates and Global change factors consist of a variety of biotic and abiotic scales, raising concerns among conservationists, ecologists, and alterations induced by human actions (hereafter referred to as public health agencies (Jones et al., 2008; Smith et al., 2014). stressors), which may interact in complex ways (see Piggott Although the causes of the emergence of many diseases are uncer- et al., 2015; Côté et al., 2016). Native hosts are often more vulner- tain, human actions probably contribute substantially to many epi- able to alien parasites than to native parasites (Dunn and Hatcher, demics (Rogalski et al., 2017). Human activities such as intensive 2015). Other global change processes such as aquatic nutrient pol- agriculture (Ponisio et al., 2016), fishing (Kaiser et al., 2015), and lution (Sinha et al., 2017) can further increase host vulnerability if dam construction (Poff et al., 2007) are homogenising aquatic such processes increase the virulence of a disease (Budria, 2017). ecosystems around the world, and disease outbreaks often arise However, the impacts of pollution on host-parasite relationships when ecosystems are simplified (Elton, 1958). Ecosystems are are difficult to predict due to context (Marcogliese and Pietrock, altered further by the accumulation of alien species, which contin- 2011). While high concentrations of pollutants, including nutri- ues unabated (Seebens et al., 2017). Given that the global human ents, can kill both parasites and hosts (Vidal-Martínez et al., footprint is expected to increase even further (Hoekstra and 2010; Smallbone et al., 2016), nutrients sometimes may improve host body condition and allow hosts to better cope with the effects of pollutants and parasites (Marcogliese and Pietrock, 2011; ⇑ Corresponding author at: Department of Evolutionary Biology, Ecology, and Environmental Sciences-Institute of Research in Biodiversity (IRBio), University of Budria, 2017). Nutrient pollution also is expected to promote the Barcelona, 08028 Barcelona, Spain. spread of horizontally transmitted parasites (e.g. ectoparasites) E-mail address: [email protected] (A. Maceda-Veiga). because nutrients increase host population density (McKenzie https://doi.org/10.1016/j.ijpara.2019.03.002 0020-7519/Ó 2019 Published by Elsevier Ltd on behalf of Australian Society for Parasitology. 626 A. Maceda-Veiga et al. / International Journal for Parasitology 49 (2019) 625–634 and Townsend, 2007). External parasites often are more sensitive might affect a host–parasite system along upstream–downstream to environmental fluctuations in aquatic systems than are internal gradients. Fish species included endemic taxa (e.g. Barbus haasi parasites (Overstreet, 1993). Riverine ecosystems are among the Mertens 1925, Parachondrostoma miegii Steindachner, 1866) and most dynamic and human-affected ecosystems in the world widely distributed European native (e.g. Anguilla anguilla Linnaeus, (Williamson et al., 2008), yet the ways in which multiple natural 1758, Salmo trutta Linnaeus, 1758) and alien fish species (e.g. Cypri- and anthropogenic factors affect interactions and epidemiology nus carpio Linnaeus, 1758, Gambusia holbrooki Girard, 1859) (Fro- in host–parasite systems remain little studied (Blasco-Costa ese, R., Pauly, D., 2017. FishBase. World Wide Web electronic et al., 2013; Hofmann et al., 2016; but see individual stressors publication. www.fishbase.org. (Last accessed 03/02/2019)). Alien reviewed in Sures et al., 2017). fish often replace native fish in degraded rivers (Maceda-Veiga The Asiatic anchor worm Lernaea cyprinacea Linnaeus 1758 is a et al., 2017), but the anchor worm has low host specificity parasitic copepod introduced, incidentally, widely into temperate (Hoffman, 1999; Noga, 2011) and can exploit most host fish. and tropical regions with fish stocking (Hoffman, 1999; Hassan Anchor worm infections were expected to occur mostly in low- et al., 2008; Welicky et al., 2017). The anchor worm is capable of land rivers because the copepod prefers warmer waters, and infec- infecting fish and amphibians (Hoffman, 1999), and high mortali- tions may be more limited by the riverine environment than by ties have been reported for fish suffering from anchor worm infec- host availability given the parasite’s lack of host specificity. We tions (Noga, 2011; Raissy et al., 2013). The anchor worm is expected the probability of parasite presence to be the highest in expected to spread further with global warming (Bulow et al., degraded rivers because pollution often induces immunosuppres- 1979; Marcogliese, 1991; Sánchez-Hernández, 2017) and when sion in fish and promotes disease (Yada and Tort, 2016; Bly et al., fish are forced into high concentrations during drought 1997; but see Biagianti-Risbourg et al., 2013; Smallbone et al., (Medeiros and Maltchik, 1999; but see Welicky et al., 2017). Infec- 2016). We explored the occurrence of interactions among some tions by parasitic copepods including L. cyprinacea are influenced of the major natural and anthropogenic stressors that may govern by fish size (Poulin et al., 1991), water quality stressors such as parasite dynamics. Given that such stressor combinations are com- nutrient pollution, and other contaminants which can kill the par- mon around the world, the identification of these interactions will asites (Noga, 2011; Palm, 2011). However, rivers are subject to help to project the distribution of the parasite well beyond our other stressors such as alterations in river morphology and riparian study system. areas than can reduce body condition in host fish (Maceda-Veiga et al., 2014), potentially increasing fishes’ susceptibility to disease. 2. Materials and methods However, interactions among stressors may be advantageous to the fish if sewage effluents contain chlorides, which are strongly 2.1. Study area correlated with river-water conductivity (Fernandez-Turiel et al., 2003) and reduce the toxicity of some nutrients such as nitrite We gathered data on river environmental conditions and fish (Noga, 2011). from surveys performed in northeastern Spain from 2002 to 2009 Determining the spatial location of disease outbreaks, the indi- (e.g. Maceda-Veiga et al., 2013, 2017). This data set consisted of viduals that are most vulnerable, and the environmental condi- 530 sampled sites that involved all Catalonian catchments from tions that promote infection, are central thinking in disease the Muga to Riudecanyes basins, and the whole River Ebro and part ecology (Stephens et al., 2016). The limited spatial extent of data- of the Garonne basin (Fig. 1). We surveyed