Impact on waterborne protozoan parasites

Both, floodings and droughts can lead to epidemics caused by waterborne protozoan parasites: cysts of Giardia intestinalis, oocysts of Cryptosporidium parvum and Toxoplasma gondii, due to their small size and specific weight close to that of water, may get flushed from soil surfaces, transported by run-off water to various types of water reservoirs and thus contaminate such water sources destinated for the provision of drinking water. On the other hand, drought conditions may force animals and humans to resort to unsafe water resources, infecting themselves with waterborne pathogenic agents (Cann et al., Reference Cann, Thomas, Salmon, Wyn-Jones and Kay2013). Whereas the latter situation may occur more frequently in countries with poor sanitary infrastructures, flood borne epidemics caused by protozoal agents, mainly Cryptosporidium, have been observed to a major extend in the northern hemisphere and reported from Europe and the United States (Karanis et al., Reference Karanis, Kourenti and Smith2007). A large outbreak caused by Cryptosporidium occurred in the city of Milwaukee in 1993 causing diarrhoeal disease in 403 000 inhabitants (MacKenzie et al., Reference MacKenzie, Hoxie, Proctor, Gradus, Blair, Peterson, Kazmierczak, Addiss, Fox, Rose and Davis1994). Inefficiency of drinking water treatment plants was found to be the likely cause. In fact, after strong thunderstorms the plants were challenged with highly turbid water overriding their capacity of maintaining adequate removal of pathogens by the coagulation and filtration process (Leland et al., Reference Leland, McAnulty, Keene and Stevens1993; Corso et al., Reference Corso, Kramer, Blair, Addiss, Davis and Haddix2003).

In the nineties, several Cryptosporidium outbreaks were reported in the UK. More than 500 cases of diarrhoeal disease were notified in Sheffield and in Swindon & Oxfordshire, respectively (Karanis et al., Reference Karanis, Kourenti and Smith2007) and about 1840 individuals were affected by the outbreak of Warrington. Interestingly in all the three events Cryptosporidium infections were of zoonotic origin. Flooding of pastures grazed by oocysts eliminating cattle, had led to the contamination of the drinking water. In the case of Warrington, an area geologically characterized by sandstone, the heavy rainfalls most likely have caused oocysts bypass of natural sandstone filtration. This example illustrates the importance of including geological assessments in any endeavours to estimate the risk of flood related epidemics.

Extreme heavy rains may also lead to the inundation of pastures with manure, industrial waste waters or raw sewage water. Thus, pig and beef farms not only constitute a potential source of human infections but extensively raised beef themselves risk of getting infected/contaminated when feeding on pastures polluted with microbial or chemical agents, protozoan parasite cysts or even with Taenia saginata eggs in case of inundation with sewage water of human origin (Crist et al. (Reference Crist, Mori and Lee Smith2020).

Two succeeding large toxoplasmosis outbreaks stroke the city of Victoria (British Columbia, Canada) in October 1994 and April 1995, involving 2894 and 7718 inhabitants respectively. Also in this case, oocyst contamination of municipal drinking water was responsible for the epidemics. The events occurred following periods of excess rainfall that led to fecal contamination of the water reservoir by domestic and feral cats and cougars, found Toxoplasma positive in subsequent investigations (Karanis et al., Reference Karanis, Kourenti and Smith2007).

Not only terrestrial but also aquatic environments are at risk of increased pathogen contamination because of climate change. Investigating watersheds of coastal regions in California, USA, vanWormer et al. (Reference VanWormer, Carpenter, Purnendu, Shapiro, Wallender, Conrad, Largier, Maneta and Mazet2016) found highest T. gondii oocyst levels in regions of increased T. gondii infection monitored in sentinel marine mammals. Heavy precipitation phenomena raised oocyst delivery to the ocean by 79%. Thus, extreme climatic events combined with anthropogenic changes in landscapes can accelerate runoff of diverse pathogens from terrestrial to aquatic environments, increasing the risk of transmission to people, domestic animals and wildlife in coastal areas (vanWormer et al., Reference VanWormer, Carpenter, Purnendu, Shapiro, Wallender, Conrad, Largier, Maneta and Mazet2016).

Impact on soil-borne parasites and fluke diseases

In Haiti, deforestation, heavy rains and subsequent silting of a river, led to periodic flooding of the area of Leogane town with the deposition of a sandy loam topsoil increasing soil moisture (Lilley et al., Reference Lilley, Lammie, Dickerson and Eberhard1997). A longitudinal coprological study, that followed up small children for about 6 years (1990–96), allowed to detect an impact of the environmental change on the local hookworm cycle. Following years of regular flooding events, the prevalence of hookworm infected children was found increased from zero in 1990 to about 15% in 1996, while other helminthic infections remained constant. Increased soil moisture, given by the sandy loam depositions after river floodings, might have provided an ideal environment for the larval development of hookworms and thus facilitated the infection of children with this parasite (Lilley et al., Reference Lilley, Lammie, Dickerson and Eberhard1997).

Worth mentioning are 2 recent cases of human fasciolosis (HF) in Belgium, probably caused by eating metacercariae contaminated vegetables from a garden that was inundated by runoff from pasture after heavy rains. Because native HF is rare and the transmission route was unusual, HF was not diagnosed until 6 months after symptom onset in both cases (Milas et al., Reference Milas, Rossi, Philippart, Dorny and Bottieau2020).

Regarding fasciolosis disease in sheep farms in endemic areas of Italy, outbreaks were found to be associated to a significant increase (P < 0.001) of temperature and of the number of rainy days in those areas compared to previous years’ data (Bosco et al., Reference Bosco, Rinaldi, Musella, Amadesi and Cringoli2015). Taking into consideration all the Mediterranean area, the potential effects of these phenomena on the epidemiology of F. hepatica and the implications for sheep farming have been illustrated in a recent overview by Alba et al. (Reference Alba, Vazquez and Hurtrez-Boussès2021).

When man-made disasters such as wars superimpose effects of extreme events caused by climate change, parasites may take profit of newly created habitats and facilitated transmission conditions. Once again war has brought about deleterious effects on human, animal and environmental health (Mantovani et al., Reference Mantovani, Lasagna, Senigalliesi, Comin and Duque2006) during the events that devastated the Balkans from 1991 to 2001. Croatian Public Health Services revealed a dramatic increase in human trichinellosis cases in a country already considered to be at high risk of this infection (Marinculic, personal com.). If this was foreseeable due to the collapse of the public health service, the same cannot be said for what has been recorded in wildlife regarding a trematode parasite: Fascioloides magna in Europe is an imported liver fluke of game animals, such as red deer, not previously reported in Croatia. In non-specific hosts such as domestic ruminants, pigs, horses and rodents parasite infection is frequently fatal. In 1999 the parasite was found in deer of the Baranja region (Marinculic et al., Reference Marinculic, Dzakula, Zdravko, Zlatko, Snjezana and Zivienjak2002). Among the possible causes of its occurrence, Croatian parasitologists recall floods that may have transferred infective eggs and intermediate hosts from endemic areas of Hungary, but also mentioned, that the migration of deer, disturbed by war operations, to Hungary and their subsequent return to Croatia after the war, might explain the F. magna introduction in this country (Marinculic et al., Reference Marinculic, Dzakula, Zdravko, Zlatko, Snjezana and Zivienjak2002).

Impact on fluke disease and risk of metacestadosis in Sardinia

Recently, in Ottana, (Nuoro province), after very heavy rains at the end of September 2020, acute fasciolosis cases in sheep farms were found to be increased, aggravated by a compromised nutritional status of the animals due to the loss of the entire fodder supply destinated for the winter period (Sedda, Reference Sedda2020).

In the early nineties, a fasciolosis outbreak has been observed on the basaltic Giara plateau in wild horses grazing in promiscuity with domestic ruminants, reservoir of F. hepatica. Following a particularly rainy season, a significant number of temporary water pools locally called ‘paulis’, and extended areas of shallow marshes were created, forming excellent proliferation conditions for Limnea (Galba) spp. In this situation, it was possible to detect fasciolosis also in these horses, an animal species in which fasciolosis does not represent a common parasitoses. This case illustrates how changed environmental conditions can increase metacercariae colonization of semi-disseminated pastures such as ‘paulis’, favouring the metacercaria ingestion by horses which are used to graze within these ‘paulis’ (Scala and Cancedda, Reference Scala and Cancedda1993).

Furthermore, the death of numerous husbandry animals reared in territories affected by such environmental catastrophes may also cause the geographical spread of metacestodosis, including those of zoonotic interest, such as cystic echinococcosis (CE). In fact, in Sardinia, during the floods of 2013, the death of a considerable number of sheep was documented, of which about 70% were estimated to be affected by CE (Scala et al., Reference Scala, Garippa, Varcasia, Tranquillo and Genchi2006). Their carcasses, abandoned on the pastures or carried away by flooding even over considerable distances (Figs 1 and 2) (in many cases up to the sea which then beached very far) were likely to get predated by feral and/or stray dogs and ingesting viscera possibly infected themselves with cestode species such as Echinococcus granulosus, Taenia multiceps and T. hydatigena.

Figure 1. Sheep washed by the flood on a tree, north-eastern part of Sardinia Island (Italy), November 2013.

Figure 2. Sheep washed by the flood up to the sea, north-eastern part of Sardinia Island (Italy), November 2013.

Other disastrous events possibly exacerbating flooding impacts on parasitosis

In the subchapters above it is illustrated how floods may lead to an increase in human and animal infections with parasitic agents. However, the fact that floodings, whether caused by heavy rains or by fluvial inundations involve also industrialized areas and thus may lead to environmental contamination with toxic chemicals or to the diffusion of contaminants already present in the soil, must be kept in mind. Such contaminations may affect large areas impacting directly on human and animal health but may also act on a wide range of organisms including free-living parasite stages.

Grigorieva and Livenets (Reference Grigorieva and Livenets2022) illustrate how floods in Russia can affect ecosystems and can lead to the release and diffusion of toxic chemicals and microbes already present in the soil. The authors estimated that there could be significant toxic and microbial health effects on people living near industrial or agricultural areas due to flooding.

In this regard, worth mentioning is the dioxin accident that occurred in Seveso (Milan province, Italy) in the 70ties. It was caused by the massive loss of the highly cancerogenic substance from the Icmesa plant, leading to the contamination of a large, densely populated area. This disaster frightened not only experts but the entire population of the affected areas and beyond. The CBS Broadcasting Inc., an American commercial broadcast television and radio network, has listed the disaster among the 12 worst environmental human catastrophes ever. Collecting earthworms in the contaminated area, it was possible to demonstrate that these worms contributed to moving dioxin from the surface into the soil. Of course, earthworms are not parasites, but excellent intermediated and/or paratenic hosts for many parasites (Martinucci et al., Reference Martinucci, Crespi, Omodeo, Osella, Traldi and Satchelli1983). Unfortunately, to our knowledge, studies targeted to assess dioxin effects on parasites either free-living stages or present in contaminated hosts haven't been conducted.

In this context another chemical disaster that cannot be forgotten is related to pesticide production and happened in 1984, in India where a cloud of methyl isothiocyanate gas leaking from the Union Carbide pesticide plant killed about 10 000 people in Bhopal during the first three days. The disaster was blamed as the ‘genocide of the poor’. The tragic event prompted an animated debate among Italian parasitologists within the SoIPa, with colleagues sustaining the likelihood that this chemical soil pollution may impact on a wide range of organisms including parasitic forms present in pastures. Since the compound methyl isothiocyanate is a pesticide active on insect as well as nematode pests, its presence in the soil may modify the epidemiology of parasitic Diptera causing myasis and of gastro-intestinal nematodes species. Also in this case it would have been important to conduct studies on contamination effects not only in proximity of the plant but also in adjacent areas likely to be at secondary contamination risk because of specific hydro-geological characteristics.

Natural disaster fires vs deliberately set fires for parasite control

Considering the impact on ecosystems, fires consume not only the vegetation but also affect the upper soil layer where many parasites spend part of their life cycle, thus reducing habitat availability, with consequent potential benefits for the hosts (Álvarez-Ruiz et al., Reference Álvarez-Ruiz, Belliure, Santos and Pausas2021). As reviewed by Scasta (Reference Scasta2015), North American studies have illustrated how fires altered the micro-habitat of ticks and reduced the density of larvae, nymphs and adults (Scifres et al., Reference Scifres, Oldham, Teel and Drawe1988; Mather et al., Reference Mather, Duffy and Campbell1993; Stafford et al., Reference Stafford, Ward and Magnarelli1998; Cully, Reference Cully1999).

In Tanzania and South Africa, similar reductions in ticks have been attributed to the drastic impact of fires on the micro-habitat. In this case fires were set deliberately due to concerns about tick-borne diseases such as babesiosis (Trollope, Reference Trollope2011). Although fire return intervals vary widely (from 3 years in tallgrass grasslands to 230 years in Douglas-fir forests) in African settings, fires are crucial in regulating ecosystems, ecological processes and pest dynamics (Agee, Reference Agee1993; Anderson, Reference Anderson2006).

In Australia, (not to forget the massacre of koalas and marsupials in the 2021 bushfires) already in earlier fire events free-living stages of gastrointestinal parasites of sheep were found to be reduced (Hepworth and Hutchens, Reference Hepworth and Hutchens2011) and going back to the 70ies, controlled burning of pastures has been recommended as a control measure to reduce gastrointestinal nematodes (GIN) (Barger, Reference Barger, Donald, Southcott and Dineen1978). To light fires on pastures is also traditionally operated by Sardinian and Sicilian farmers at the end of the summer, with the intent to favour the revival of forage crops and to ‘sterilize’ the pastures from infesting parasitic forms.

Sheep examined in British Columbia, Canada, that had access to recently burnt areas had up to 10 times minor lungworm burdens (Protostrongylus spp.) than sheep kept on unburnt areas (Seip and Bunnell, Reference Seip and Bunnell1985). In an area of the south-eastern United States bushfires were deliberately applied to destroy the micro-habitat of the gastropod hosts of Parelaphostrongylus tenuis, the brain meningeal worm. This intervention allowed to control the parasites’ diffusion, proven to have devastating effects on native ungulates such as elk and deer (Weir, Reference Weir2009).

Impact on sheep breeding and risks of parasite diffusion in Sardinia

In Sardinia, concerns were raised that the death of numerous animals killed by fires may increase the diffusion of cestode species, as in the case of floods. However, this most probably did not occur in the areas affected by the 2021 fires, since the carcasses of the sheep and other animals caught by the fires in the pastures or in their shelters were charred (Fig. 3). Furthermore, on-the-spot inspections carried out in the affected areas for more than 30 days after the event did not reveal the presence of feral and/or stray dogs.

Figure 3. Carbonized sheep in the area of Montiferru (central-western area of Sardinia), after the fire in summer 2021.

The epidemiology of some parasitoses most likely was also influenced by the transfer of sheep from original burnt grazing areas to other pastures with different pedoclimatic characteristics in which ‘new’ or ‘different’ parasite forms or agents of the herd pathocenosis may have been present. Such newly encountered parasites such as Dicrocoelium dendriticum, F. hepatica or different species of bronchopulmonary and/or gastro-intestinal nematodes, may have established themselves in the transferred animals, which could then, in the absence of adequate control measures, have been imported into the original grazing areas with the return of the animals on their home pastures. Obviously, such areas, at least in the first season of reintroduction of grazing animals, would be ‘sterile’ regarding L3 contamination of GIN, possible cestode eggs and the presence of intermediate hosts.

Unfortunately, these fire disasters have caught many public services in Sardinia unprepared to tackle adequately the numerous husbandry/sanitary problems that have arisen. On many occasions, not even the actual number of animals involved was available. From the Sardinian experiences emerge the need for solid, area specific data on the ‘normal’ epidemiology of endoparasitoses in grazing animals but also for assessments of parasitological risks according to type of disaster. Such knowledge may help guiding prevention and mitigation programs at farm and community level by local services.

Regarding the increase in frequency and extension of fire disasters in Sardinia, this may be related also to the depopulation of rural areas and their consequent re-naturalization. Abandonment of agricultural activities brought the proportion of forest over the total area to grow from 13% in the early 50ties (Camarda and Vacca, Reference Camarda and Vacca2021) to the current 54%. Over the last decade, population loss has become an alarming phenomenon all over Italy mainly affecting small municipalities in half of the 20 regions, from North to South, with a negative population trend observed in over 50% of the area in the affected regions (Amodio, Reference Amodio2022).

Therefore, to contain fires and mitigate their effects, it is most important to adopt at farm level preventive measures such as: improve the structure of fences including escape routes for animals; secure sheds (primarily barns); create water points; provide viability in every direction and part of the farm; provide food supply for animals (Camarda and Vacca, Reference Camarda and Vacca2021). In addition, the promotion of silvopastoralism as a wildfire prevention strategy should be considered (Nuss-Girona et al., Reference Nuss-Girona, Soy, Canaleta, Alay, Domènech and Prat-Guitart2022). According to the local forest characteristics and type of breeding practiced in the area, various ruminant species might be employed (Nuss-Girona et al., Reference Nuss-Girona, Soy, Canaleta, Alay, Domènech and Prat-Guitart2022). In this context, also the grazing of horses has been found effective in controlling easily combustible underwood vegetation in an area of Spain (Rigueiro et al., Reference Rigueiro, Mosquera, Lopez, Pastor, Gonzales Hernandez, Romero and Villarino Urtiaga2002). Other Iberian experiences demonstrate how the breeding of donkeys, goats and sheep, the latter together in large flocks, are able to reduce the risk of fires compared to areas where abandonment has induced natural reforestation. (Bartolomè et al., Reference Bartolomé, Miró, Panadès, Broncano, Plaixats, Rigau, Milán and Baraza2020). Botanical studies have allowed to identify the plant species involved in the phenomenon (Lasanta-Martínez et al., Reference Lasanta-Martínez, Vicente-Serrano and Cuadrat-Prats2005; Mancilla-Leytón et al., Reference Mancilla-Leytón, Pino, Mejías and Martín Vicente2013). In Italy, however, experiences in this sector are lacking and mainly directed to the organoleptic characteristics of animal products from extensive husbandry (Pugliese et al., Reference Pugliese, Franci, Acciaioli, Bozzi, Campodini, Sirtori and Gandini2006).

Impact on GIN transmission and evasive grazing control strategies

Regarding GIN, the dynamics of larval development in response to climatic variables such as temperature and humidity has been studied extensively, both in the laboratory and the field, and various models have been developed to predict infection risks of ruminant hosts (Vineer et al., Reference Vineer, Verschave, Claerebout, Vercruysse, Shaw, Charlier and Morgan2020). With the help of such models the design of GIN control programs is facilitated, allowing to reduce pharmacological treatments to a minimum and intervene with alternative measures such as evasive grazing. However, the predictive capacity of such models might be challenged by exceptional events. Indeed, extraordinary heavy rains, extremely high temperatures or prolonged drought periods may create conditions that possibly exceed value ranges of the climatic parameters considered in the models.

A drought period that struck the Netherland in summer 2003, allowed Eysker et al. (Reference Eysker, Bakker, Kooyman, van der Linden, Schrama and Ploeger2005) to observe the capacity of Haemonchus contortus to adapt to environmental stress: whereas the development of free-living stages was poor as expected, L3 larvae that have matured before the drought period reached to survive in comparable numbers as in previous years. Moreover, in the absence of re-infection, adult nematodes were found to survive in the hosts for up to 3 months (Eysker et al., Reference Eysker, Bakker, Kooyman, van der Linden, Schrama and Ploeger2005). This example illustrates the complexity of parasite–host–environment relationships, but also suggests that programmed parasite control will be more and more difficult to realize in the era of increasing extreme events. Evasive grazing programs for GIN control will have to cope not only with altered parasite transmission patterns, but also with changed pasture availability. In an area affected by drought, grazable plots will be reduced in numbers and the quality of the forage altered, possibly affecting the nutritional status and resilience of ruminant hosts. Until now, evasive grazing as a GIN control strategy has been considered indispensable, since it allows to reduce numbers of anthelmintic treatments and thus contributes to delay resistance development of GIN species to available drugs. Drug and multiple drug resistance has already become a serious threat in many contexts, but the expected increase in frequency and intensity of droughts may even enhance the problem, given that drought conditions decrease the amount of free-living GIN stages, i.e. reduce the proportion of the nematode populations in refugia (Knapp-Lawitzke et al., Reference Knapp-Lawitzke, von Samson-Himmelstjerna and Demeler2016).

Experiments were performed to assess the effects of drought stress and different temperature/humidity ranges over time on the survival and fitness of Cooperia oncophora L3 and their distribution in grass and soil under controlled conditions using a climate chamber (Knapp-Lawitzke et al., Reference Knapp-Lawitzke, von Samson-Himmelstjerna and Demeler2016). Weed containers inoculated with L3 were analysed after 1–6 weeks using descriptive statistics and linear modelling. A large proportion of L3 was recovered from the ground where fitness was even better preserved than on grass. The obtained results highlight the relative importance of these factors and will help to design better models for L3 population dynamics on pasture in the future. Furthermore, the results of these investigations may offer explanations concerning the interdependencies of the development of anthelmintic resistance and the presence of hot/dry climatic conditions (Knapp-Lawitzke et al., Reference Knapp-Lawitzke, von Samson-Himmelstjerna and Demeler2016)

In contrast to floodings or fires, droughts are not causing situations of immediate emergency. Farmers and breeders are given the time to frame the problem and intervene to mitigate effects on husbandry production parameters and to prevent levels of parasite infections that may lead to disease (Morgan and Wall, Reference Morgan and Wall2009). However, to tackle these new challenges, breeders should be assisted more closely by veterinary practitioners and breeders’ associations. As an example, during 2021, the Marche Region (Central Italy) experienced an exceptionally dry summer that forced sheep breeders in the Apennine Mountains to modify grazing practices and integrate feeds with hay. Thanks to regular monitoring of gastro-intestinal parasites conducted in local sheep farms by staff of the University of Camerino (Marche Region), a substantial increase of GIN egg counts in autumn was detected in some of the monitored farms. Prompt anthelmintic treatment of the sheep groups involved, allowed to preserve the good health status of the animals. This example suggests that intensified parasitological monitoring should become the first line response to climate change. Presumably, more frequent parasitological examinations increase production costs, however regular monitoring might still prevent more substantial expenses linked to parasite born disease outbreaks.

Impact on the geographical distribution of parasite species

Another example of extreme climatic events’ impact on parasites, comes from the recent dramatic drought episodes in Sicily in 2017: in that occasion emerged how such events may affect the geographical distribution patterns of parasites, in this case of ectoparasites that seemed to belong to the distant past, namely leeches; once used for therapeutic purposes (hypertension, bloodletting, swelling) due to their ravenous hematophagy or employed for cosmetic purposes for colouring black hair, beard and moustache (Hoeppli, Reference Hoeppli1959). During the heavy drought episode, leeches of the species Limnatis nilotica were found to have established in high densities in remnant water puddles, provoking significant lesions in the oral cavity of the animals that took water from those puddles. In the absence of Hirudo medicinalis this represented the first observation of the species L. nilotica in an Italian region (Arfuso et al., Reference Arfuso, Gaglio, Ferrara, Abbate, Giannetto and Brianti2019).