GIANT FLUKE AND : JUST A FLUKE?

J. Trevor Vannatta1,3 and Ron Moen2

1University of Minnesota-Duluth, Duluth, Minnesota 55812, USA; 2Natural Resources Research Institute, University of Minnesota, Duluth, Minnesota 55811-1442, USA

ABSTRACT: The giant , magna, is a possible contributing factor to moose (Alces alces) declines in North America, but evidence linking F. magna infection directly to moose mortality is scarce. This review identifies knowledge gaps about the transmission and impact of F. magna infection on moose and proposes new directions for research and management of this para- site. We suggest that the importance of intermediate snail hosts has been largely neglected in current management discussions and warrants greater emphasis. The intermediate hosts responsible for F. magna transmission likely vary by region and recent genetic evidence suggests that F. magna was restricted to several isolated refugia during cervid extirpation events in North America. This distribu- tional history represents several coevolutionary and pathological implications for definitive hosts of F. magna. We suggest that F. magna infections are most ecologically significant as they relate to sublethal impacts and multiple parasitic infections. In assessing infection risk on landscapes, most models rely heavily on monitoring white-tailed (Odocoileus virginianus), but this approach only measures risk indirectly. The reliability and accuracy of models would probably improve if snail habitat in ephemeral wetlands was included as a predictor variable.

ALCES VOL. 52: 117–139 (2016)

Key Words: Alces alces, , host-parasite interactions, liver fluke, lymnaeid snails, moose, white-tailed deer

The giant liver fluke, Fascioloides magna, cervids is more controversial (Foreyt 1992, is a trematode parasite that infects the 1996, Pybus 2001, Lankester and Foreyt of white-tailed deer (Odocoileus virginianus), 2011). Whether damage from F. magna in- (Cervus canadensis), and caribou (Rangi- fection increases mortality in moose is of fer tarandus) across North America (Fig. 1; particular interest. In northwestern Minne- Pybus 2001). Moose (Alces alces) and other sota, Murray et al. (2006) concluded ~20% cervids often become infected with F. magna of moose mortality was probably related to where their range overlaps with these natural F. magna infection; however, cause of mor- fluke hosts (Karns 1972, Lankester 1974, tality was partly a classification by exclusion Pybus 2001). because if no other cause was evident, and Fascioloides magna is a parasite of the liver tissue contained an abundance of unknown significance for host mortality. fluke damage, individuals were classified as Although liver damage associated with in- probable fluke mortalities. Lankester (2010) fection appears to have little effect on white- notes that the prevalence of F. magna infec- tailed deer (Foreyt and Todd 1976, Presidente tion in northwestern Minnesota between et al. 1980, Pybus 2001), its impact on other 1972 (87%; Karns 1972) and the beginning

3Present Address: Department of Biological Sciences, Purdue University, West Lafayette, Indiana 47907, USA, [email protected]. 117 GIANT LIVER FLUKE – VANNATTA AND MOEN ALCES VOL. 52, 2016

Fig. 1. North American distribution of Fascioloides magna redrawn from Pybus (2001). North Dakota and Tennessee distributional information added from Maskey (2011) and Pursglove et al. (1977). of the Murray et al. (2006) study in 1995 THE LIFE CYCLE (89%) did not change when the moose popu- Fascioloides magna completes its life lation was increasing. Additionally, captive cycle using snail, plant, and cervid hosts moose infected experimentally with F. sequentially (Swales 1935, Pybus 2001). magna showed no outward clinical signs of Eggs released in deer pellets develop into infection (Lankester and Foreyt 2011), but miracidia (Fig. 2) that penetrate the foot of this study only used 3 individuals with ade- an aquatic lymnaeid snail, developing into quate food, minimal stress, and no predatory sporocysts that give rise to rediae by asexual interaction. Energy expenditure in free-ranging reproduction. Rediae then release free-swim- moose is likely higher when tissue repair and ming cercariae from the snail that encyst as metacercariae on aquatic vegetation, and if immune responses occur in concert with severe ingested by a cervid, will excyst and pene- malnutrition, predation pressure, and other trate the intestine as juvenile flukes. Juvenile pathogens (Pybus 2001, Lankester and Samuel flukes migrate to the liver and continue to the 2007). liver parenchyma until they find one or more In this review, we summarize the life other flukes (Foreyt et al. 1977). This migra- cycle of F. magna including the biology of tion is visible as black tracks, scarring, and lymnaeid snail intermediate hosts. We then hemorrhaging. Paired flukes settle in the draw on current concepts in parasitology in- liver and become encapsulated in a pseudo- cluding coevolution, sublethal effects, coin- cyst of host origin. The stimulus for capsule fections, landscape ecology, and ecological formation is unknown, but may be function- interactions to inform management strategies ally similar to the proline stimulus in the concerning the habitat and parasitic relation- related liver fluke, hepatica (Wolf- ships of F. magna and moose. Spengler and Isseroff 1983).

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Fig. 2. The life cycle of Fascioloides magna. Gray arrows indicate the normal life cycle progression. The hollow arrow indicates the dead-end host, moose, in which the parasite does not successfully shed eggs (drawings by J. Trevor Vannatta).

Lymnaeid snails our discussion on the ecology and geographic The , ecology, relative import- range of known F. magna host snails using ance, and North American geographic range the most current taxonomic information of specific lymnaeid snail hosts remains (Tables 1 and 2). poorly understood and a much debated topic The taxonomy of lymnaeid snails is still (Baker 1911, Hubendick 1951, Correa et al. debated and the varied growth patterns of 2010, Dillon et al. 2013). As such, we focus lymnaeid snails in different environments

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Table 1. Potential hosts of the giant liver fluke Fascioloides magna and their habitat associations. F. magna host snail General habitat description Source Fossaria Highly amphibious. Found on mud substrates in McCraw 1959, 1961, Clarke 1981, Laursen spp. ephemeral wetlands and ditches. et al. 1992, Laursen and Stromberg 1993, Dunkel et al. 1996 Lymnaea Found in floodplains, marshes, and other temporary Clarke 1981, Laursen et al. 1992, Laursen caperata waters. Can be tolerant of dry conditions. and Stromberg 1993, Dunkel et al. 1996 Lymnaea Found among vegetation in many water bodies, Clarke 1981, Laursen et al. 1992, Dunkel elodes primarily lakes, streams and ponds. et al. 1996 Lymnaea Found on vegetation (e.g., Typha) and rocks in large, Clarke 1981, Laursen et al. 1992, Dunkel stagnalis permanent lakes with diverse substrates. et al. 1996 Lymnaea In lakes or large, slow moving rivers on rocks or Clarke 1981, Laursen et al. 1992, Dunkel catascopium vegetation exposed to current. et al. 1996 Lymnaea Found in lakes and other slow moving waters on Clarke 1981 columella vegetation or submerged sticks. Lymnaea Found in ponds and marshes similar to the habitat of Hubendick 1951, Pointier and cubensis Fossaria spp. Augustin 1999 Lymnaea Occurs in many habitats from large to small lakes, Clarke 1981, Vannatta 2016 megasoma beaver ponds, and slow moving rivers on muddy and silty sediments Acella An exceptionally rare found in shallow Clarke 1981 haldemani water vegetation of ponds and lakes has led to taxonomic misclassifications in and L. elodes (Table 2; Swales 1935, Laursen the past (Hubendick 1951, Dillon et al. and Stromberg 1993). However, when the 2013). More recently, genetic analyses have geographic range of F. magna is overlaid revealed that almost all North American with the ranges of intermediate snail hosts, lymnaeid species are in a single clade, and no combination of known, natural inter‐ that they may be reclassified into the genera mediate hosts fully explains its distribution Catascopium and Hinkleyia to reflect (Fig. 3). Of primary interest are the F. magna shared ancestry in North America (Correa populations in Labrador, Canada and Florida, et al. 2010). Snails in the USA. It is most likely that natural infections (Lymnaea elodes and L. catascopium, Table in L. elodes explain the presence in Labrador, 2) may actually represent a single species despite this parasite population residing on of the new genus Catascopium. As a final the very northern range edge of L. elodes. taxonomic note, there is likely no group of In Florida, it is most likely that L. cubensis lymnaeids as taxonomically confused as the is an undocumented natural host as it is Fossaria genus (Stewart and Dillon 2004); also a host of the closely related liver fluke, hence, we refer to all Fossaria group snails , in Latin America (Cruz- as Fossaria spp., except for L. caperata and Reyes and Malek 1987). Not only is L. the circum-Caribbean snail, L. cubensis,which cubensis closely related to other Fossaria are long recognized as distinctive (Baker 1911, spp. snails (Correa et al. 2010), it also shares Hubendick 1951, Dillon et al. 2013). similar habitat characteristics (Table 1). The Three lymnaeid snail intermediate hosts natural hosts Fossaria spp. and L. caperata have been found naturally infected with are amphibious snails common to ephemeral F. magna: Fossaria spp., Lymnaea caperata, water habitats. Lymnaea caperata, L. elodes,

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Table 2. Known intermediate snail hosts for Fascioloides magna in North America, common synonymsa, and whether snails are known natural or experimental (e.g., infected with miracidia in the laboratory) hosts. F. magna host snail Common synonyms Natural or Experimental host (Source) Fossaria spp. Lymnaea humilis; L. bulimoides; L. Natural (Swales 1935, Laursen and modicella; L. parva; L. ferruginea; L. Stromberg 1993) obrussa; L. umbilicata; L. desidiosa; L. dalli Experimental (Sinitsin 1930, Krull 1933, Dutson et al. 1967, Griffiths 1973, Foreyt and Todd 1978) Lymnaea caperata Stagnicola caperata; S. caperatus Natural (Griffiths 1962, Laursen and Stromberg 1993) Experimental (Griffiths 1962, Foreyt and Todd 1978, Laursen 1993) Lymnaea elodes Stagnicola elodes; S. palustris; S. exilis; Natural (Swales 1935) Lymnaea palustris; L. reflexa; L. umbrosa; Experimental (Campbell and Todd 1955, S. reflexa 1956, Griffiths 1962, Dutson et al. 1967, Foreyt and Todd 1978, Laursen 1993) No relevant synonyms Experimental (Wu and Kingscote 1954, Griffiths 1973, Foreyt and Todd 1978) Lymnaea Stagnicola catescopium; Lymnaea Experimental (Laursen 1993) catascopium emarginata; L. woodruffi; L. walkeriana Lymnaea columella Experimental (Krull 1933, Dutson et al. 1967b, Laursen 1993, Flowers 1996) Lymnaea cubensis No relevant synonyms Host of closely related fluke, Fasciola hepatica, in Latin America (Cruz-reyes and Malek 1987) Lymnaea Bulimnea megasoma 12 specimens were found shedding megasoma gymnocephalus cercariae in Minnesota, presumably F. magna or F. hepatica. (Gilbertson et al. 1978) Acella haldemani Lymnaea gracilis Not evaluated a Synonyms derived from Baker 1911, Hubendick 1951, Clarke 1973, Dillon et al. 2013. b This account is far outside the known range of L. columella and in doubt. and L. catascopium are very closely related, hosts relative to their exposure to metacer- yet natural infections in L. catascopium cariae while foraging on aquatic plants. In have not been documented (Table 2). Fasciola hepatica, snail-plant associations The importance of snail intermediate hosts and other factors have been used to predict has been greatly overlooked to best understand where snails, and thus infection risk, are the ecology of F. magna in North America. more common (Rondelaud et al. 2011). The lymnaeid intermediate hosts of F. magna Similar methodology may be useful to pre- are potentially a critical bottleneck at which dict F. magna infection risk. The presence F. magna might be effectively managed. of Fossaria spp., L. caperata, and L. elodes Whereas white-tailed deer and elk disperse snails in ephemeral wetlands points to emer- widely and occupy a variety of habitats, the gent aquatic vegetation as the primary source snail hosts of F. magna are restricted to ephem- of giant liver fluke infection. eral wetlands or similar habitats (Table 1). However, regional adaptation of para- The habitat preferences of lymnaeid sites to their intermediate hosts is common snails are most pertinent for definitive cervid (Lively 1989, Vera 1991 as cited by Combes

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Fig. 3. Geographic range of lymnaeid snail intermediate hosts in North America. Different patterns represent the number of known, natural intermediate host snails in an area. Maps derived from Baker 1911, Hubendick 1951, Clarke 1973, 1981, Jokinen 1992, Laursen et al. 1992, Pybus 2001, Maskey 2011, and the 2016 IUCN Red List of Threatened Species.

2001). As such, management on a local scale content of aquatic vegetation and seasonal, must first identify which intermediate hosts nutritional requirements arguably influence are regionally important to identify habitats this months-long foraging behavior by moose to manage accordingly. For F. magna,it and other ungulates (Ceacero et al. 2014). is most likely that Fossaria spp. are the A comprehensive review of aquatic foraging most important hosts at lower latitudes and by moose suggests that this behavior varies L. elodes becomes progressively important regionally and is likely influenced by for- northward. aging efficiency and sodium acquisition (Morris 2014). For example, if moose in the Aquatic vegetation Great Lakes region feed on aquatic plants Aquatic feeding is common and seasonally more than moose in other regions, they might important for moose (de Vos 1958, Hennings be expected to have higher infection rates of 1977, Belovsky and Jordan 1981, Fraser et al. F. magna. 1982, 1984), but much less so for white-tailed Seasonality is also an important factor deer and other cervids (Skinner and Telfer in both aquatic foraging and parasite trans‐ 1974, Hennings 1977, Ceacero et al. 2014). mission (Lepitzki 1998, Morris 2014). Early Sodium requirements are hypothesized as and late season feeding by moose near the principal driver of aquatic feeding habits muddy lake and stream edges is more likely of moose in non-coastal areas (Belovsky to lead to infection because as temperature and Jordan 1981, Fraser et al. 1982, Ceacero increases in early spring, infected snails ap- et al. 2014); however, the high protein pear to generate a pulse of metacercariae

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(Lepitzki 1998) and moose may encounter represents the historical coevolution of F. more viable metacercariae and higher risk in- magna within its definitive hosts and explains fection; this general trend might also hold the patterns of variable pathology within true in the fall. Snails which became infected these hosts. Pybus (2001) proposed 2 ex‐ in spring would begin shedding cercariae planations for the patchy distribution: 1) ~50 days post-infection when wetlands pro- F. magna was never widely dispersed and vide green vegetation during early fall senes- only established in isolated pockets of cence. In fact, known peaks in metacercarial North America, or 2) a complex series of encystment match this seasonal variation events involving glaciation, deer speciation, in forage availability and feeding behavior extirpation, and restocking established F. (Lepitzki 1998). magna widely across the continent and it Although classic life cycle studies impli- was later reduced to a patchy distribution. cate aquatic vegetation as the only source The latter scenario involves human coloniza- of F. magna infection (Swales 1936, Pybus tion which extirpated the cervid hosts from 2001), some cercariae may encyst as free- many locations, followed by either re- floating metacercariae in surface water establishment from various refugia or cervid (Morley 2015). Little research has been restocking programs in current habitat pockets. done with free-floating metacercariae, but Recent genetic analyses indicate that the in human fascioliasis, certain patients have second, more complex hypothesis is more no other reported routes of infection other likely (Bazsalovicsová et al. 2015). than ingestion of free-floating metacercariae Fascioloides magna coevolved with an- (Mas-Coma 2004, Morley 2015). cestral Odocoileus spp. (Pybus 2001), and in It is also possible that moose become the Pliocene, the same glaciation events that infected with F. magna by drinking water generated speciation among Odocoileus or consuming wet soils at mineral licks (geo‐ spp. (Heffelfinger 2011) likely led to the gen- phagy), a common behavior in cervids (Weeks eration of the 2 distinct western (Pacific and Kirkpatrick 1976, Fraser et al. 1984, Northwest and Alberta) and eastern clades Abrahams 2013, Lavelle et al. 2014). The (southern USA, Great Lakes, Labrador; dissolved minerals in these soils could create Bazsalovicsová et al. 2015). Within the various a rich habitat for snails and represent a habitat patches analyzed by Bazsalovicsová shared resource between F. magna definitive et al. (2015), mitochondrial haplotypes appear and dead-end hosts, such as moose (Lavelle conserved, suggesting that F. magna remained et al. 2014). We found no information about within isolated refugia where white-tailed which, if any, snail species inhabit mineral deer were not extirpated during human colon- lick habitats. It is possible that the shallow ization of North America. If restocking ephemeral habitats of Fossaria spp., L. programs had distributed F. magna from caperata, and L. elodes are similar to that other infection foci, regionally conserved at mineral licks and high amounts of avail- haplotypes would likely be less common able calcium could facilitate high snail dens- (Bazsalovicsová et al. 2015). ity (Dillon 2000). We found little evidence supporting the hypothesis that the viability of miracidia DISTRIBUTION, COEVOLUTION, and metacercariae of F. magna has limited AND PATHOLOGY range expansions from refugia (Pybus 2001). The distribution of F. magna across It is a robust parasite which has been intro- North America has long been of interest duced to Europe at least twice and expanded (Pybus 2001). Its patchy distribution (Fig. 1) its European range considerably in the past

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100 years (Králová-Hromadová et al. 2011, the acquisition of a host spectrum: an en- Bazsalovicsová et al. 2015). It seems more counter filter and a compatibility filter. probable that natural processes and deer The encounter filter dictates that potential restocking programs near North American hosts must overlap spatially and temporally refugia have led to range expansion that with the parasite, as well as be exposed monitoring programs have not detected and to the parasite by some aspect of behavior. historical records cannot identify. Although The compatibility filter relates to whether F. magna readily expands its range as host the host is able to defend itself from the ranges expand (Pybus et al. 2015), it is likely parasite, immunologically or otherwise, and that abiotic factors such as precipitation, stipulates that the host must provide soil characteristics, and temperature have suitable resources to the parasite. For ex- limited expansion in parts of North America ample, foraging and/or drinking by white- (Pybus 2001, Maskey 2011). Further study tailed deer in aquatic habitats leads to is warranted, as with the related fluke F. encounters with F. magna , and the successful hepatica (Zukowski et al. 1991). establishment and reproduction of F. magna Coevolution between F. magna and re- within the liver with minimal hepatic dam- gional hosts would be expected assuming age verifies that the compatibility filter is that F. magna resided in isolated refugia. As open (Pybus 2001). Further, the damage a consequence, we cannot assume that one during the initial stages of infection does regional population will behave similarly as not appear to substantially reduce fitness in other parasite populations that coevolved with deer (Pursglove et al. 1977, Presidente et al. different hosts. In much of North America, 1980, Mulvey and Aho 1993, Mulvey et al. only white-tailed deer have a long co- 1994), indicating a finely tuned host-parasite evolutionary history with F. magna (Pybus coevolutionary history (Combes 2001). 2001); however, western populations of F. Elk present a slightly different scenario magna likely evolved with both deer and because although both filters are open, the elk (Bazsalovicsová et al. 2015). These evo- heightened severity of hepatic damage sug- lutionary histories may manifest as the pro- gests that the compatibility filter has only re- portion of susceptible individuals within a cently opened (Pybus 2001). Elk infected population (Pybus 2001). The prevalence with F. magna often survive, but infection in- of infection appears to plateau at ~70% of tensity can be high (Pybus 2001, Pybus et al. individuals in some white-tailed deer popula- 2015) and mortality occurs in certain tions, suggesting that ~30% develop re‐ (Foreyt 1996, Pybus et al. 2015). It is sistance to infection (Foreyt et al. 1977). believed that elk shed larger quantities of But, infection rate can be higher as elk in fluke eggs than white-tailed deer (Swales Kootenay National Park, Ontario plateau 1936, Pybus 2001). near 80% infection prevalence, and moose F. magna infections often lead to death at ~90% prevalence in northwestern Minne- in (Odocoileous hemionus), yet sota (Pybus 2001, Murray et al. 2006, Pybus mule deer successfully shed F. magna et al. 2015, Wünschmann et al. 2015). eggs (i.e., the compatibility filter is open; When examining the coevolutionary his- Foreyt 1992). The difference in mortality be- tory of F. magna and its definitive hosts, the tween white-tailed and mule deer is probably concept of host spectra ‘filters’ is useful to con‐ a function of habitat use where barriers have sider (Euzet and Combes 1980 in Combes prevented common exposure of F. magna to 2001), specifically, that 2 filters facilitate mule deer (i.e., the encounter filter is closed;

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Pybus 2001), suggesting that exposure his- Nudds 1994, Hudson and Greenman 1998). tory, not relatedness, is the principle explan- White-tailed deer habitat overlap with moose ation for the host spectrum. and elk is increasing with climatic and an- In the case of moose, the compatibility thropogenic habitat alterations (Waller and filter is closed. Moose are dead-end hosts Alverson 1997, Galatowitsch et al. 2009, that display a strong immune response, which Heffelfinger 2011, Minnesota Department some authors have suggested may contribute of Natural Resources 2015, Dawe and Boutin substantially to mortality (Murray et al. 2016). Heightened virulence of white-tailed 2006). It seems possible that if infections deer parasites could facilitate this range lead to death in some elk, they may also expansion through reduced competition lead to death in moose. The heightened im- with sympatric moose and elk, and benefit mune response in moose may contribute to both deer and their parasites (Schmitz and this mortality through thickening of fluke cap- Nudds 1994). Selection for virulence may sule walls, the inability of flukes to release also happen rapidly, as rapid evolution has eggs from capsules, and the eventual death of been identified in other parasites expanding the parasite (Lankester 1974). Remnant cap- along range edges (Kelehear et al. 2012). sules are often filled with dead flukes and INDIRECT MORTALITY AND other waste which may impair liver function SUBLETHAL EFFECTS (Pybus 2001). In the migratory phase of Viewing parasitic diseases only as direct their life cycle, immature F. magna appear to mortality factors presents a narrow perspec- migrate extensively in moose, sometimes dam- tive about wildlife disease. Many parasitic aging >50% of the liver tissue and possibly impacts, especially in mammalian hosts, causing secondary infection (Karns 1972, are subtle and may indirectly influence mor- Lankester 1974, Pybus 2001). The parasite tality (e.g., a weakened host exposed to population may be responding to an incompat- greater predation risk) or sublethal fitness ible host population by increasing virulence, impacts (e.g., reduced reproductive success; defined as damage to the host (Gandon and Yuill 1987). Identifying such relationships Michalakis 2000, Combes 2001). An increase in mammalian systems is often difficult be- in virulence associated with parasite migration cause they require substantial time, large and hepatic tissue damage may allow fluke sample sizes, and reliable metrics of host fit- eggs to make their way into pellets. ness. Given the complex interacting factors also do not shed fluke eggs, but in severe infec- evident in moose declines along their south- tions with substantial hepatic damage, some ern range (Rempel 2011, Murray et al. eggs escape in feces (Foreyt and Todd 1974). 2012), examining only direct mortality fac- If the identification of F. magna eggs in moose tors probably overlooks other indirect and pellets is accurate (Kingscote 1950, Wünsch- sublethal factors impacting the fitness of in- mann et al. 2015), successful reproduction of dividual moose. the parasite in this host could open the com- The most important question concerning patibility filter, possibly leading to selection F. magna in moose is if and how much direct for more virulent parasite strains (Gandon mortality is caused by infection. Some stud- and Michalakis 2000). ies suggest that white-tailed deer, a natural Virulent parasite strains may also become host which is thought to sustain little to no more common if natural hosts gain an in- harm from infection (Foreyt and Todd 1976, direct benefit through parasite-mediated Presidente et al. 1980, Pybus 2001), may competition (Price et al. 1988, Schmitz and suffer increased mortality when infected

125 GIANT LIVER FLUKE – VANNATTA AND MOEN ALCES VOL. 52, 2016 with F. magna (Cheatum 1951, 1952, Addison might further speculate that the lack of pre- et al. 1988). Cheatum (1951) found a two- dation stress in the northwestern population fold higher fluke infection prevalence in allowed it to increase despite fluke preva- winter-killed deer as compared to deer col- lence near 90%. lected by researchers. The mechanism by A direct study measuring the energetic which liver fluke infections in deer can cause cost of F. magna infection in moose should increased mortality are not fully understood, be a research priority. Immune responses but immune response, anemia, eosinophilia, and tissue repair costs are difficult to meas- and hepatic tissue damage associated with ure directly, but comparison of the resting fluke migration likely increase energetic metabolic rate of infected and uninfected costs in winter when deer are in an energy moose might provide an estimate of the asso- deficit (Cheatum 1951, Presidente et al. ciated energetic cost of infection (Yuill 1987, 1980, Marcogliese and Pietrock 2011). Robar et al. 2011). Further, neonatal survival Moderate to high liver damage from fluke and fitness (productivity) might be impacted infection was not correlated with body con- by reduced milk production as Ross (1970) dition in Minnesota moose found dead or euth‐ found a significant negative impact by the anized by wildlife officials (Wünschmann closely related fluke, Fasciola hepatica,on et al. 2015). However, 42% of malnourished the milk yield of cattle. moose had high liver damage (>50% of the Parasitic disease can also affect the in- tissue altered by flukes) compared to 13% vestment that host organisms partition to of animals in moderate condition; conversely, their offspring (Schwanz 2008). In a study 33% of individuals in good condition had with deer mice (Peromyscus maniculatus), high liver damage. Sample size of indivi- chronic trematode infection was related to duals in good condition was small (n = 8) an investment in fewer, larger offspring compared to moderate (24) and malnour- (Schwanz 2008). Lower twinning rates have ished individuals (28). been observed in white-tailed deer infected When infected cervids are attacked by with F. magna, but unfortunately, weight predators, flukes may indirectly contribute and health of fawns were not assessed to mortality through hepatic hemorrhage as (Mulvey 1994). Termed fecundity compen- fluke capsules are often near major blood sation (Minchella 1985), this strategy repre- vessels in the liver (Vannatta 2016). Although sents the host effort to maintain fitness while anecdotal, 9 black-tailed deer (Odocoileus under disease stress. Although examples of hemionus columbianus) died after being this phenomenon are rare in mammalian sys- chased by dogs (Cowan 1946) and subsequent tems (Schwanz 2008), testing this hypothesis necropsies suggested a combination of heavy in moose is theoretically possible. If parasitic fluke infestation and exertion caused the disease leads to fecundity compensation in hepatic portal system to hemorrhage. Hepatic moose, heavily diseased moose populations hemorrhage during chase events might par- should have a lower calf:cow ratio at birth, tially explain some differences between the albeit multiple factors influence productivity northwestern and northeastern Minnesota and single births, not twinning as in deer, are moose populations. Moose in northwestern the norm for moose. Minnesota experienced little direct predation Other fitness effects have been docu- mortality (~3%; Murray et al. 2006), whereas mented in F. magna-infected white-tailed predation accounted for ~34% of mortality deer in South Carolina (Mulvey and in northeastern Minnesota (Minnesota De- Aho 1993, Mulvey et al. 1994) where, after partment of Natural Resources 2016a). One controlling for habitat and year-to-year

126 ALCES VOL. 52, 2016 VANNATTA AND MOEN – GIANT LIVER FLUKE variation, males with heavy fluke infections and bacterial and viral microparasites. Vari- had fewer antler points and lower body ous helminths have been implicated in weight; however, these effects were less dra- immune suppression (Maizels et al. 1993, matic or absent in older males. Older males Behnke et al. 2009, Ezenwa et al. 2010), with heavy infections did lose more weight and it is likely that the complex proteome during the rut which could reduce their of F. magna contains some immune suppres- winter survival (Mulvey and Aho 1993). sing functions (Cantacessi et al. 2012). Fluke-infected female deer had higher body It is often difficult to identify the under- weights before the onset of breeding season lying causes of parasitic coinfections (Viney and, thus, conceived earlier and outside of and Graham 2013). In white-tailed deer in the optimal breeding window. Mulvey et al. Minnesota, a positive association was found (1994) suggested that the lower probability between F. magna and a tapeworm larvae of twinning in infected does allowed for (Taenia hydatigena) that inhabits the liver rapid weight gain, earlier breeding receptiv- (Vannatta 2016). This association was most ity, and earlier conception; however, these likely related to abiotic conditions necessary data and that of older males can also be inter- for parasite survival, immunological differ- preted as conflicting. In totality, these data ences in hosts, and/or behavioral differences are somewhat supportive of an impact on between host individuals. In order to tease fitness and may point to more effect on apart these variables, quality GIS or habitat younger-aged animals. data, immunological profiles of individuals, and metrics of space use are required. These COINFECTION AND MULTIPLE logistical difficulties likely underlie our lack PARASITIC INFECTIONS of knowledge about coinfection processes. Many wildlife disease studies are viewed A question of paramount importance to from a single-host, single-pathogen perspec- moose management is: how do the potentially tive. However, complicated within-host envi‐ pathogenic helminth parasites P. tenuis and ronments can have significant impacts on F. magna interact in moose? Using data disease dynamics and outcomes (Jolles et al. from opportunistically collected free-ranging 2008, Ezenwa et al. 2010, Hoverman et al. moose (Wünschmann et al. 2015), we found a 2013, Viney and Graham 2013, Garza- signifcant negative association between P. Cuartero et al. 2014). The within-host com- tenuis and F. magna (Fisher’sexacttestP = munity is comparable to symbioses in larger 0.022), with 12 mortalities positive for P. ecosystems with some infracommunity (within- tenuis and F. magna, 16 positive for P. tenuis host community) members remaining neutral only, 24 positive for F. magna only, and 9 towards one another (Telfer et al. 2010), negative for P. tenuis and F. magna. Since some appearing as antagonists (Canning the moose in this study were found dead, et al. 1983, Jolles et al. 2008, Telfer et al. accidentally killed, or euthanized, actual pro- 2010, Johnson and Buller 2011), and others portions of infected or coinfected individuals benefitting one another (Behnke et al. 2009, may be lower in the population than those in Karvonen et al. 2009, Ezenwa et al. 2010, the sample population. Telfer et al. 2010). Three primary variables may affect the The concept of infracommunities is par- rates of coinfection of F. magna and P. tenuis ticularly pertinent in declining moose popu- in moose: 1) differences in parasite habitat lations where F. magna may interact with outside the host, 2) space use differences be- other pathogens such as brainworm (Parela- tween individual moose hosts, or 3) the pres- phostronglyus tenuis), Echinococccus spp., ence of one parasite stimulating an immune

127 GIANT LIVER FLUKE – VANNATTA AND MOEN ALCES VOL. 52, 2016 defense in the host. It is unlikely that the linked infection risk to rooted and floating habitat of these parasites overlaps as aquatic marshes which contain many aquatic F. magna is most commonly associated plant species palatable to deer and moose with lowland and wetland habitat (Mulvey (Hop et al. 2001). Using similar techniques et al. 1994, Pybus 2001, Pybus et al. 2015, (VanderWaal et al. 2015) as employed in VanderWaal et al. 2015, Vannatta 2016), Voyageurs National Park, VanderWaal et al. whereas P. tenuis is mostly found in upland (unpublished data from winter 2014-2015) forest habitats frequented by terrestrial found that F. magna prevalence was highest gastropod hosts (Cyr et al. 2014). Beyond around Duluth, Minnesota and declined to non-overlapping habitat, a lack of coinfec- the northeast (Fig. 4A, B). These data match tions could represent the habitat of specific well with moose necropsy data from the re- individual moose and/or the relative density gion, purportedly due to higher deer dens- of white-tailed deer. Moose which are ities and, to a lesser extent, more wetland infected with P. tenuis may have home habitat (Peterson et al. 2013). Despite a lim- ranges with higher proportion of upland for- ited sample size, Vannatta (2016) found a est, moose with fluke infections could have strong correlation between F. magna bio- higher proportion of wetland habitat and mass and emergent herbaceous wetlands moose with coinfections may have high pro- using the National Land Cover Dataset. The portions of wetland and upland habitat infection risk on these landscapes was attrib- (Cyr et al. 2014). Lastly, it is possible that uted to the combination of palatable aquatic high intensity fluke infections trigger an im- forage for deer and suitable habitat for inter- mune response preventing other infections mediate host snails (VanderWaal et al. 2015, from establishing (Lankester 2010). Vannatta 2016). In considering coinfections, it is impor- The primary issue with all current land- tant to remember that managing one parasitic scape-level risk assessments is that infection infection will likely impact another (Telfer risk for moose is measured by the occurrence et al. 2010). Even exposure to other infections of F. magna within white-tailed deer or elk can increase the virulence of pre-existing diseases (Sandland et al. 2007). In the case (Peterson et al. 2013, Pybus et al. 2015, Van- of moose, further research is needed to deter- derWaal et al. 2015, Vannatta 2016). These mine how F. magna and P. tenuis infections models have some success because infected interact. deer or elk are necessary for F. magna per- sistence; however, this is only an indirect INFECTION ON LANDSCAPES measure of the risk landscape. The risk for Possible relationships between F. magna moose is a very narrow habitat which must infection risk and landscape characteristics include: 1) suitable intermediate hosts, 2) have been investigated in multiple studies palatable emergent vegetation, and 3) over- (e.g., Mulvey et al. 1994, Peterson et al. lapping use with infected definitive hosts. 2013, VanderWaal et al. 2015). Two studies Past emphasis has been placed on the distri- analyzed coarse metrics of upland/lowland bution of white-tailed deer, but other factors or soil moisture classes (Mulvey et al. 1994, necessary for transmission are important. Pybus et al. 2015), and two others found Although the landscape must contain infec- a direct relationship between certain cover ted deer, additional information about suit- types and increased infection risk or F. able snail habitat and emergent vegetation magna biomass (VanderWaal et al. 2015, will improve the accuracy of infection risk Vannatta 2016). VanderWaal et al. (2015) assessments for moose.

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Fig. 4. Deer permit areas (DPA) sampled for Fascioloides magna within pellet groups in 2015 in Minnesota’s arrowhead region (inset: Minnesota digital elevation model with arrowhead region DPAs highlighted). DPAs are labelled with their respective sample sizes and pie charts are labelled with the percentages represented by each slice. (A) Infection prevalence decreases from the southwest to the northeast (Black = proportion infected). (B) Mean infection intensity is less consistent across the region (Black = mean infection intensity in each DPA as a proportion of the greatest mean, 787 eggs per gram dry weight feces; VanderWaal et al. unpublished data).

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The riskiest habitats for moose are shal- breeding are not ecologically responsible, low, ephemeral water bodies which support nor cost effective. However, ad‐vances in natural infections in Fossaria spp. and other our understanding of ecological interactions ecologically similar snails (Tables 1 and 2). and their impacts on parasites may present Models in which all wetland habitat is con- novel management strategies in line with cur- sidered indiscriminately (Peterson et al. rent topics, such as One Health (American 2013, VanderWaal et al. 2015, Vannatta 2016) Veterinary Medical Association 2008). Eco- can be improved with measures of wetland logical interactions associated with bio- seasonality, water flow, and depth that influ- diversity have stark implications for ence the location of intermediate hosts and parasitic diseases (Thieltges et al. 2008, metacercarial encystment by the parasite Civitello et al. 2015) and several reviews (Laursen and Stromberg 1993, Pybus 2001). have recently emphasized the implications A discriminant model that buffers the inward of biodiversity for parasites (Thieltges et al. edges of wetlands to reflect appropriate 2008, Johnson and Thieltges 2010, Johnson water depths would provide a better mea‐ et al. 2010). sure of infection risk (Peterson et al. 2013, Free-living larval stages, such as the VanderWaal et al. 2015, Vannatta 2016). miracidia, cercariae, and metacercariae of The inclusion of all wetland habitats as an F. magna, are prey for many organisms. infection risk may have led Peterson et al. Oligochaetes may protect some snails (2013) to conclude that deer density, not wet- from trematode infections by ingesting mira- land habitat, was the primary driver of F. cidia or by limiting the parasites’ access magna infection in northeastern Minnesota. to the mantle cavity (Ibrahim 2007). In a Unfortunately, the wetlands inhabited by study of Ribeiroia ondatrae, cercariae were the intermediate host snails present a signifi- consumed by Hydra spp., copepods, and cant barrier to developing improved risk as- damselfly and dragonfly larvae, often at sessment models (Malone and Zukowski high rates (Schotthoefer et al. 2007). In 1992, DeRoeck et al. 2014). Fossaria spp. marine systems, some fish (Kaplan et al. 2009) and L. caperata inhabit ephemeral wetlands and filter-feeding barnacles (Prinz et al. that are more common in woodlands and 2009) predate parasite cercariae, and gastro- other water features not typically visible on pods may ingest metacercariae (Campbell aerial imagery (Laursen et al. 1989, 1992, and Todd 1956, Prinz et al. 2009). Van Meter et al. 2008). Identifying these habi- Competition for hosts and within hosts tats to accurately predict landscape risk is another example of how ecological inter- requires extensive GIS modeling and field con- actions may impact parasite success. The re- firmation of ephemeral wetland presence (Van cent discovery of soldier castes in some Meter et al. 2008), a collaborative effort for trematode species (Hechinger et al. 2011, researchers, managers, and wetland ecologists. Garcia-Vedrenne et al. 2015) indicates that competition for and within snail hosts is per- ECOLOGICAL INTERACTIONS AND vasive and likely explains why some trema- FASCIOLOIDES MAGNA CONTROL todes are stronger within host competitors The complex life cycle of F. magna cre- (Kuris and Lafferty 1994). However, some ates logistical issues when trying to manage snails may act as decoys for parasite mira- disease risk. Control measures such as vac- cidia, decreasing their transmission rates; cination, medicated baits, molluscicides, wet‐ for example, the mucus of the snail Helisoma land draining, removing aquatic vegetation, trivolvis is toxic to F. magna miracidia introducing competitor snails, or selective (Coyne et al. 2015). Parasites can also be

130 ALCES VOL. 52, 2016 VANNATTA AND MOEN – GIANT LIVER FLUKE sensitive to pathogens within the snail host. of the host-parasite relationship warrants care- The fungal group Microspora in the family ful consideration in areas where overlap of Unikaryonidae can act as a hyperparasite on elk, moose, and white-tailed deer will increase trematode larvae when ingested by a snail in the future. Impacts of F. magna infection host, and microsporidia can reduce Fasciola beyond direct mortality are also of increasing hepatica infections in snails (Canning relevance because infection may alter host fit- et al. 1983). ness, predation risk, and other stressors (e.g., Whereas most larval stages of F. magna climate change, competition, other pathogens) are best controlled by increasing non- in deer, elk, and moose. vertebrate biodiversity within aquatic habi- Viewing F. magna and moose as a tats, limiting the diversity of the definitive single-host, single-parasite system limits our vertebrate hosts may be a potential control understanding of the impact of this parasite. measure. Elk are suspected of shedding large Although these relationships are often cryptic, quantities of F. magna eggs when infected the interactions of multiple parasites within (Swales 1936, Pybus 2001), and the role of a host likely lead to a number of impacts elk in F. magna infection of sympatric moose on moose. For example, F. magna may act to needs to be evaluated as Minnesota plans facilitate other parasitic infections, or con- to expand its elk population (Minnesota versely, prevent infection by stimulating the Department of Natural Resources 2016b). In the northeastern part of Minnesota where host immune system. For moose, the relation- moose are declining, the Department of ship between F. magna and P. tenuis specific- Natural Resources is proposing changes in ally warrants further examination. harvest strategies of white-tailed deer to limit Past modeling efforts to predict F. exposure of moose to F. magna and other magna infection risk tended to ignore the im- pathogens carried by deer (Minnesota De- portance of intermediate snail hosts. Because partment of Natural Resources 2015). these hosts inhabit a very narrow range of habitats, they are an important aspect to in- CONCLUSIONS clude in F. magna management. Employing Fascioloides magna is a parasite with landscape-level GIS tools in concert with unknown significance in its definitive hosts One Health and biodiversity conservation/ (white-tailed deer, elk, and caribou) and the restoration concepts should improve both dead-end host, moose. Recent evidence sug- understanding and prediction of infection gests F. magna populations were divided into risk. Arguably, this strategy will help minim- eastern and western populations and subseq‐ ize infection risk to moose while avoiding uently limited to isolated refugia. This distri- negative environmental impacts. butional pattern impacted the coevolutionary history of the parasite with all of its definitive ACKNOWLEDGEMENTS hosts. White-tailed deer have a lengthy co- The authors would like to acknowledge evolutionary history with F. magna,which The University of Minnesota – Duluth, The may help explain the lessened severity of Environmental and Natural Resources Trust pathology in this species; however, different Fund, The Clean Water, Land, and Legacy coevolutionary histories with other hosts ap- Amendment, and the Minnesota Zoo for fi- pear to influence pathological severity. Moose nancial support. The presentation of this andelkoftencontainhighintensityfluke work was also facilitated by an Alces New- infections, which may represent a form of comer’s travel award. The authors are also parasite-mediated competition, and this aspect indebted to the reviewers and editors at

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