Abstract
Cryptosporidium has adapted to a broad range of hosts in all major vertebrate classes, and the species associated with humans and livestock represent a small fraction of the diversity in the genus. This review focuses on Cryptosporidium and cryptosporidiosis in terrestrial vertebrates other than humans and livestock. As the known host range of Cryptosporidium continues to expand, major orders of amphibians (Anura), reptiles (Squamata and Testudines), avians (17 out of 26 orders), and mammals (18 out of 29 orders) are now represented. The greatest Cryptosporidium diversity appears to be in mammals, which may be an Artifact of undersampling in other classes, but more likely reflects a different mechanism of Cryptosporidium diversification in mammals relative to other classes.
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1 Introduction
The emergence of Cryptosporidium as a serious human pathogen in the 1980s spurred research efforts to understand the biology and ecology of this enigmatic parasite. While early studies were hindered by a lack of tools to type isolates, the widespread use of genotyping during the last 15 years has begun to uncover the enormous diversity that exists in the genus Cryptosporidium.
The major focus of Cryptosporidium research over the past 30 years has been the control of cryptosporidiosis in humans and livestock, and the primary motivation to study other vertebrates has been to understand the ecology of human cryptosporidiosis. Wildlife-associated cryptosporidia account for a relatively small but significant proportion of human cryptosporidiosis cases (Feltus et al. 2006; Robinson et al. 2008; Elwin et al. 2011), the recent emergence of C. cuniculus as a human pathogen illustrates the connection between wildlife and public health. Rabbit-adapted C. cuniculus was not on the public health radar until the misadventures of a rabbit at a UK water treatment facility in 2008 resulted in a waterborne outbreak of cryptosporidiosis (Chalmers et al. 2009). Genetically, C. cuniculus is remarkably similar to the major human pathogen C. hominis, and the two cannot be differentiated by some routine molecular diagnostics (Robinson et al. 2010). However, prompted by the waterborne outbreak, samples from 3,030 sporadic cryptosporidiosis cases in the UK were reexamined using enhanced diagnostics, and C. cuniculus was detected in 1.2 % of samples (Elwin et al. 2012a). Apart from the obvious benefit of knowing the species, and hence the likely source of the Cryptosporidium causing human disease, these studies raise interesting and fundamental questions about the biology of Cryptosporidium; such as, how does Cryptosporidium diversify and how does diversification affect host specificity and disease potential? These questions can be addressed by examining Cryptosporidium diversity across the range of vertebrate hosts, not just humans and livestock.
This chapter addresses the occurrence of Cryptosporidium in vertebrate hosts other than fish (Chap. 1), humans (Chaps. 2 and 3), and livestock (Chap. 4). Information is organized by vertebrate class (Amphibia, Reptilia, Aves, and Mammalia), and by order within each class. Background information is provided on each order, including orders that do not currently contain identified Cryptosporidium hosts. It is hoped that this approach will facilitate the identification of knowledge gaps and will stimulate ideas for future research.
2 Cryptosporidium and Cryptosporidiosis of Amphibians
To date, Cryptosporidium has been detected in only one of the three orders of amphibians: the Anura. It has not been detected in the Caudata, an order that contains more than 550 species in ten families and approximately 30 genera of salamanders, or the Gymnophonia, which are snake-like amphibians with about 180 species in ten families and 35 genera. The Caudata require freshwater for reproduction and they consume invertebrates. Gymnophonia are tropical in distribution, have larvae that may only be partially aquatic, and typically inhabit loose soil layers.
2.1 Anura
Anura is the largest order of Amphibians, with over 6,000 species of frogs and toads in 33 families and over 65 genera. Frogs and toads require at least some water for reproduction, but they occupy a wide variety of terrestrial and freshwater habitats. There are no marine species, and only a few inhabit brackish waters. All Anurans consume invertebrate prey, lacking teeth or grinding organs in their digestive tract.
Cryptosporidium fragile, the only amphibian-adapted species described to date, was isolated from the doubtful toad (Duttaphrynus melanostictus) originating in Malaysia (Jirků et al. 2008). Oocysts of C. fragile measure 6.2 μm (5.5–7.0 μm) × 5.5 μm (5.0–6.5 μm) and are readily lysed in hypertonic solutions. Cryptosporidium fragile infects the gastric epithelium and clusters with gastric cryptosporidia in molecular phylogenies (Table 5.1 and Fig. 5.1). Other reports of Cryptosporidium and cryptosporidiosis in reptiles have been rare. Cryptosporidiosis was diagnosed in a captive South African clawed frog (Xenopus laevis) that was euthanized after becoming grossly emaciated from illness (Green et al. 2003). Endogenous Cryptosporidium stages were identified in the gastric mucosa, and oocysts were isolated from water in the infected frog’s enclosure. Cryptosporidium oocysts also have been reported in a captive Bell’s horned frog (Ceratophrys ornata) (Crawshaw and Mehren 1987).
3 Cryptosporidium and Cryptosporidiosis of Reptiles
Cryptosporidium has been detected in two of the four orders of reptiles: Squamata and Testudines. It has not yet been reported in Crocodylia, a small order of 25 species in three families and eight genera, or the Rhynchocephalia, which is represented by two living species: the Brother’s Island tuatara (Sphenodon guntheri) and the northern tuatara (Sphenodon punctatus). Crocodylians, which include crocodiles and alligators, have a two-chambered stomach that is unique among reptiles. The first chamber contains stones and functions much like the avian gizzard, and the second chamber is extremely acidic to facilitate almost complete digestion of prey. Tuataras, which are found only in New Zealand, are similar to the Squamates, but have different dentition and skull characteristics. They feed primarily on invertebrates, but occasionally eat small vertebrates or eggs.
3.1 Squamata
The order Squamata – snakes and lizards – is the largest and most diverse reptilian order, with more than 9,000 species in 50 families. They occupy diverse habitats, though most species inhabit drier terrestrial areas. All are predators that consume a wide variety of prey. Many produce venom or toxins to assist in immobilization of prey, which are swallowed without mastication.
Two Cryptosporidium species have been described in the Squamata: Cryptosporidium serpentis, which infects the gastric epithelium, and C. varanii (syn. C. saurophilum), which is an intestinal species (Table 5.1 and Fig. 5.1).
Cryptosporidium serpentis, which was described by Brownstein et al. (1977) and later named by Levine (1980), can cause chronic, insidious, and often fatal hypertrophic gastritis in both immature and mature ophidian hosts (Brownstein et al. 1977; Cranfield and Graczyk 1994; Kimbell et al. 1999). Clinical signs include mid-abdominal swelling and postprandial regurgitation, but not all cases are symptomatic (Brownstein et al. 1977; Cranfield and Graczyk 1994).
Although it is primarily a parasite of snakes (Table 5.2), C. serpentis also causes asymptomatic infections in a number of lizard species (Table 5.3). Unsuccessful attempts to experimentally infect Balb/c mice (Fayer et al. 1995), Pekin ducklings (Anas platyrhynchos) (Graczyk et al. 1998b), African clawed frogs (Xenopus laevis), and wood frogs (Rana sylvatica) (Graczyk et al. 1998c) suggest that C. serpentis is restricted to reptiles. However, strict reptile-specificity is brought into question by a recent report that C. serpentis was isolated from cattle in China, and was infectious for immunosuppressed and non-immunosuppressed Balb/c mice under experimental conditions (Chen and Qiu 2012).
Snakes are not susceptible to experimental infection with cryptosporidia from homothermic animals, including C. andersoni (calves), C. baileyi (chickens), C. meleagridis (turkeys), C. muris (mice), C. muris-like (Bactrian camels), and C. wrairi (guinea pigs), but they are susceptible to other reptilian cryptosporidia (Graczyk and Cranfield 1998). Reports of C. tyzzeri (previously mouse genotype I) in a black rat snake (Elaphe obsoleta obsoleta), boa constrictor (Boa constrictor ortoni), California king snake (Lampropeltis getulus californiae), corn snake (Pantherophis guttatus guttatus), emerald tree boa (Corallus caninus), fox snake (Elaphe vulpina gloydi), milk snake (Lampropeltis triangulum), mangrove monitor (Varanus indicus), and prairie king snake (Lamproletis calligaster); C. muris in a corn snake (Pantherophis guttatus guttatus); and rat genotype I in a boa constrictor probably represent passive transmission as a consequence of feeding on infected rodents (Xiao et al. 2004).
Koudela and Modrý (1998) identified and named the species C. saurophilum from five lizard species: the desert monitor (Varanus griseus), emerald monitor (Varanus prasinus), leopard gecko (Eublepharis macularius), Schneider’s skink (Eumeces schneideri), and skink (Mabuya perrotetii). Pavlásek and Ryan (2008) subsequently showed that C. saurophilum was indistinguishable from C. varanii, a species described 4 years earlier in an emerald monitor (Pavlásek et al. 1995), and proposed that C. varanii should take precedence as the species name. Cryptosporidium varanii (syn. saurophilum) infects the intestine and cloaca of a number of lizard species (Table 5.3), causing weight loss and abdominal swelling (Koudela and Modrý 1998). In contrast to C. serpentis in snakes, the disease is observed in juveniles but not adults (Koudela and Modrý 1998). Oocysts are smaller than C. serpentis at 5.0 μm (4.4–5.6 μm) × 4.7 μm (4.2–5.2 μm) with a shape index of 1.09 (1.04–1.12) (Koudela and Modrý 1998). Under experimental conditions, C. varanii was not infectious for snakes, birds, or mice (Koudela and Modrý 1998); however, natural C. varanii infections have been detected in at least nine snake species from three families (Table 5.2).
Other Cryptosporidium taxa identified in Squamata include a genotype sharing 99 % identity with C. serpentis from a leopard gecko (Richter et al. 2011), avian genotype V from a green iguana (Iguana iguana) (Kik et al. 2011), C. ducismarci and the tortoise genotype from a ball python (Pedraza-Diaz et al. 2009), C. ducismarci from a veiled chameleon (Pedraza-Diaz et al. 2009), and a genotype from a New Guinea boa (Candoia aspera) and Japanese grass snake (Rhabdophis tigrinus) sharing 98 % similarity with C. ducismarci and avian genotype II (Xiao et al. 2002; Kuroki et al. 2008).
3.2 Testudines
The order Testudines is comprised of 250 species of turtles in 14 families and more than 20 genera. All species possess a bony and cartilaginous carapace. Turtles are found in a great variety of habitats, including dry upland regions as well as marine and fresh waters. Diet is similarly varied, with mostly omnivorous species, but also some herbivorous and carnivorous species.
Cryptosporidium ducismarci (previously known as Cryptosporidium sp. ex Testudo marginata CrIT-20) has been proposed as a new Cryptosporidium species (Traversa et al. 2008; Traversa 2010). This species, which infects the intestinal epithelium of Testudo marginata, also has been detected in an asymptomatic veiled chameleon and ball phyton in Spain (Pedraza-Diaz et al. 2009) and in the pancake tortoise (Malacochersus tornieri) and Russian tortoise (Testudo horsfieldi) in the US (Griffin et al. 2010). Biological data, including descriptions of pathology, and oocyst morphometry data are lacking for this species description.
The Cryptosporidium tortoise genotype has been identified in an asymptomatic Indian star tortoise (Geochelone elegans) at the Lisbon Zoo (Alves et al. 2005). The SSU rRNA sequence of the isolate identified by Alves et al. (2005) is identical to a sequence previously reported by Xiao et al. (2002) in an Indian star tortoise at the St. Louis Zoo (GenBank accession no. AY120914), and a sequence from an environmental isolate in Maryland, USA (Yang et al. 2008). In a study of pet reptiles, Pedraza-Diaz et al. (2009) detected Cryptosporidium sp. in 17.6 % of tortoise samples and identified the Cryptosporidium tortoise genotype in a Hermann’s tortoise (Testudo hermanni) and a ball python (Python regius).
4 Cryptosporidium and Cryptosporidiosis of Birds
GenBank accession numbers and phylogenetic relationships among representative Cryptosporidium small subunit rRNA sequences from birds are presented in Table 5.4 and Fig. 5.2. Three avian-associated Cryptosporidium species are recognized: Cryptosporidium meleagridis, Cryptosporidium baileyi, and Cryptosporidium galli. These species infect a broad range of birds; however, they differ in host range and site of infection. Cryptosporidium meleagridis also causes disease in humans (McLauchlin et al. 2000; Alves et al. 2003; Cama et al. 2003).
Cryptosporidium meleagridis is primarily a parasite of intestinal epithelial cells of birds, particularly turkeys (Slavin 1955; Sreter and Varga 2000). Cryptosporidium baileyi inhabits the respiratory tract, bursa of Fabricius, and cloaca of the domestic chicken and a broad range of other birds (Current et al. 1986; Sreter and Varga 2000). Endogenous stages of C. galli are localized on glandular epithelial cells of the proventriculus (Ryan et al. 2003b).
The three avian species can be distinguished based on oocyst morphology. Oocysts of C. meleagridis are the smallest of the three, measuring 4.5–6.0 μm × 4.2–5.3 μm with a shape index (length/width) of 1.0–1.3. Cryptosporidium baileyi oocysts measure 6.0–7.5 μm × 4.8–5.7 μm with a shape index of 1.1–1.8 (Lindsay et al. 1989), and oocysts of C. galli measure 8.2 × 6.3 μm with a shape index of 1.3 (Ryan et al. 2003b). Relatively little is known about the biology of other cryptosporidia infecting birds.
Cryptosporidium has been reported in 17 out of 26 avian orders. Members of the following orders have not yet been identified as hosts:
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Tinamiformes: This is a very old avian lineage comprising one family, nine genera, and 47 species. Members are ominvorous, feeding on a variety of seeds and invertebrates. Many species occur in forests or open grasslands, but they generally prefer dryland habitats.
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Gaviiformes: This order comprises one family, one genus, and five species of aquatic birds that primarily inhabit North America and Eurasia. They feed on fish, amphibians, or aquatic invertebrates and inhabit both freshwater and marine environments during their annual cycle.
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Podicipediformes: This order comprises 22 species in one family and six genera of aquatic birds. Molecular phylogenies indicate that they are closely related to loons and flamingoes. They feed on fish, amphibians, and aquatic invertebrates.
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Procellariiformes: This order comprises four families, 26 genera, and about 112 species of seabirds. All inhabit offshore marine environments and most return to land only for nesting. Although, most feed exclusively on marine invertebrates or fish, a couple of species scavenge carrion on islands.
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Opisthocomiformes: This order comprises one species, genus, and family of tropical birds that inhabit swamps and mangroves of South America. They feed on vegetable matter (seeds, nuts, leaves, and fruits), and have well-developed ceca that facilitates fermentation in the digestive tract.
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Cuculiformes: This is a medium sized order comprising six families, 30 genera, and 143 species. Members inhabit Africa, Asia, Australasia, Eurasia, and the Americas (South, Central, and North).
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Apodiformes: This order comprises two families containing approximatley 24 genera and 100 species of small birds. They mostly inhabit the northern hemisphere and can be found in a variety of habitats. They feed aerially on insects.
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Trochiliformes: These small, nectar-feeding birds include hermits and hummingbirds. There are approximately 330 species in one family with about 100 genera. The majority of species occur in tropical and subtropical Central and South America.
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Trogoniformes: Trogons comprise approximately 39 species in one family with six to eight genera. They inhabit tropical forests, where they feed mainly on insects or fruit.
4.1 Struthioniformes
The order Struithioniformes (including cassowaries, emus, kiwis, ostriches, and rheas) is comprised of some of the oldest avian species. There are about 12 species in five families and six genera. All are flightless, forage on insects or vegetation, and lay large eggs with thick shells. Ceca are often well developed in these species.
Cryptosporidium infections in ostriches can be subclinical (Gajadhar 1993), or characterized by a prolapsed phallus/cloaca (Bezuidenhout et al. 1993; Santos et al. 2005), and edema/necrosis of the pancreas (Jardine and Verwoerd 1997). In Brazil, ostriches with a prolapsed cloaca shed oocysts of Cryptosporidium avian genotype II measuring 6.0 μm (5.0–6.5 μm) × 4.8 μm (4.2–5.3 μm) with a shape index of 1.31 (Santos et al. 2005; Meireles et al. 2006). Cryptosporidium avian genotype II is not infectious for 1-day-old chicks under experimental conditions (Meireles et al. 2006), although it has been detected in a naturaly infected chicken (GenBank accession no. JX548291; unpublished). Cryptosporidium avian genotype II was detected in 23 % of farmed ostriches (Struthio camelus) in Vietnam (Nguyen et al. 2013). The highest prevalence and oocyst shedding intensity was observed in birds aged 61–90 days; younger and older birds had a lower prevalence and shed fewer oocysts (Nguyen et al. 2013). Oocysts from subclinical Cryptosporidium infections in ostriches being imported into Canada measured 4.6 μm (3.9–6.1 μm) × 4.0 μm (3.3–5.0 μm) with a shape index of 1.15 (range 1.0–1.4) (Gajadhar 1993), which is similar to oocysts of C. meleagridis. Oocysts were not infectious for suckling mice, chickens, turkeys, or quail (Gajadhar 1993, 1994). Cryptosporidium baileyi oocysts were identified in an ostrich from the Czech Republic (Ryan et al. 2003a). Cryptosporidium sp. was detected in 60 % of farmed ostriches and rheas originating from Belgium, France, Netherlands Portugal, and Spain (Gordo et al. 2002).
4.2 Anseriformes
Waterfowl, including ducks, geese and swans, form the order Anseriformes, with about 162 species in three families and 52 genera. These birds are omnivorous, feeding on combinations of vegetation and invertebrates, with a few groups feeding on small aquatic vertebrates.
Three species and five named genotypes of Cryptosporidium have been identified in ducks, geese, mergansers, and swans (Table 5.5). In addition, five unnamed genotypes have been reported in Canada geese (Branta canadensis) (Jellison et al. 2004), however, sequences have not been deposited in GenBank, and it is not clear if they differ from subsequently named genotypes. Canada geese have also been shown to host the human pathogens C. hominis and C. parvum, and the rodent-specific muskrat genotype I (Graczyk et al. 1998d; Zhou et al. 2004b; Jellison et al. 2009). It is hypothesized that birds serve as mechanical vectors for mammalian cryptosporidia, and this is supported by data showing that C. parvum does not infect Canada geese or Pekin ducks (Anas platyrhynchos) under experimental conditions but oocysts remain viable following passage (Graczyk et al. 1996b, 1997).
Cryptosporidium has been reported to cause varying degrees of respiratory distress in ducks and geese (O’Donoghue et al. 1987). Cryptosporidium baileyi has been identified in the bursa of Fabricius and cloaca of ducks with mild symptoms (Lindsay et al. 1989), and the bursa of Fabricius and conjunctiva of domestic geese with no clinical symptoms (Chvala et al. 2006).
4.3 Galliformes
There are approximately 290 species in five families and 80 genera of gallinaceous birds. These terrestrial species feed mostly on seeds and small insects. This group has been extensively domesticated for agricultural purposes, and many species have been introduced to areas well outside of their historic range.
A number of gallinaceous birds including the domestic chicken (Gallus gallus domesticus), grouse (Tetrastes bonasia rupestris), and capercaillie (Tetrao urogallus), are natural hosts of C. galli (Ryan et al. 2003b; Ng et al. 2006).
Non-genotyped cryptosporidia have been detected in the common quail (Coturnix coturnix), common peafowl (Pavo cristatus), great argus (Argusianus argus), great currasow (Crax rubra), red-legged partridge (Alectoris rufa), and ring-necked pheasant (Phasianus colchicus) (O’Donoghue et al. 1987; Rohela et al. 2005; Lim et al. 2007). Infections in the common quail and ring-necked pheasant have been associated with clinical signs of respiratory disease, and oocysts recovered from these hosts were infectious for chickens (O’Donoghue et al. 1987). Cryptosporidium meleagridis caused an outbreak of respiratory and diarrheal cryptosporidiosis with greater than 50 % mortality in red-legged partridges (Alectoris rufa) on a game farm in Spain (Pages-Mante et al. 2007).
4.4 Phoenicopteriformes
Phoenicopteriformes is a small order of five species in one family and three genera of flamingoes. These long-legged wading birds use a specialized bill to filter-feed invertebrates or algae from shallow waters. The intestine is relatively long compared to other avian species.
In the only report from this order, C. galli was identified in a Cuban flamingo (Phoenicopterus ruber) from the Czech Republic (Ng et al. 2006).
4.5 Sphenisciformes
Sphenisciformes is comprised of 17 penguin species in one family and six genera. Penguins are flightless birds of the southern oceans, feeding on fish and krill in offshore areas. Very little is known about cryptosporidiosis in this group of birds.
Cryptosporidium oocysts have been detected in 6.6 % (11/167) of stools from the Adelie penguin (Pygoscelis adeliae) from the Antarctic territory (Fredes et al. 2007), and in 32.8 % (21/64) of gentoo penguins (Pygoscelis papua) from Ardley Island, King George Island, South Shetland Islands, and the Antarctic Specially Protected Area no. 150 (Fredes et al. 2008).
4.6 Pelecaniformes
Pelecaniformes includes waterbirds comprising approximately 65 species in eight families and ten genera. These birds feed mostly on aquatic vertebrates. A gular pouch is usually present, and prey is often swallowed whole. Almost all inhabit marine waters for part of their annual cycle.
There have been just two reports of Cryptosporidium from the order Pelecaniformes. Cryptosporidium baileyi and a non-genotyped Cryptosporidium sp. were reported in a cormorant and great cormorant (Phalacrocorax carbo), respectively (Jellison et al. 2004; Plutzer and Tomor 2009).
4.7 Ciconiiformes
There are approximately 116 ciconiiform species in three families and 39 genera. All are long-legged wading birds, feeding in aquatic environments on a variety of invertebrates and vertebrates.
Cryptosporidium has been reported in a marabou stork (Leptoptilos crumeniferus) from a zoo in Malaysia (Rohela et al. 2005) and 12.5 % (3/24) of white storks (Ciconia ciconia) from Poland (Majewska et al. 2009). The species infecting white storks was identified as C. parvum using fluorescence in situ hybridization.
4.8 Falconiformes
There are approximately 304 species in three to five families and 83 genera of falconiform birds. These birds feed on vertebrate prey or carrion. Most nest in trees or cliffs and are terrestrial in their habits.
Cryptosporidium baileyi and C. parvum have been identified in Falconiforms, and both are associated with disease. Cryptosporidium parvum caused anorexia, mild respiratory difficulties, and mild bilateral ocular discharge in a 3-month old gyrfalcon (Falco rusticolus), and C. baileyi caused mild bilateral conjunctivities and sinusitis in a 13-year-old gyrfalcon × Saker falcon hybrid (Falco rusticolus × Falco cherrug) (Barbon and Forbes 2007). Both raptors recovered following treatment with paromomycin. Cryptosporidium baileyi similarly caused an upper respiratory tract infection in three mixed-bred falcons (Falco rusticolus × Falco cherrug) (van Zeeland et al. 2008). One of the birds had epiglottal swelling and laryngeal stridor, and two had nasal discharge and sneezing. Oocyst shedding was not detected in any of the birds. Cryptosporidium baileyi also was identified in a Saker falcon (Falco cherrug) with inflammation of the middle ears, conjunctivae, third eyelids, choanae, larynx, trachea, salivary glands of the tongue, syrinx, and turbinates (Bougiouklis et al. 2012), and in a captive black vulture (Coragyps atratus) (Nakamura et al. 2009).
4.9 Charadriiformes
Charadriiformes is a diverse order of shorebirds, with about 367 species distributed among 17 families and 88 genera. Most species feed on invertebrate prey, and utilize marine habitats during part of their annual cycle.
Cryptosporidium sp. has been reported in black-headed gulls (Chroicocephalus ridibundus) (Pavlásek 1993; Smith et al. 1993; Ryan et al. 2003a), herring gulls (Larus argentatus) (Smith et al. 1993; Bogomolni et al. 2008), and kelp gulls (Larus dominicanus) (GenBank accession no. GQ355891; unpublished). Smith et al. (1993) detected Cryptosporidium oocysts measuring 4.7 μm (4.4–5.2 μm) × 5.2 μm (4.7–5.8 μm) in feces from gulls trapped at two refuse sites and other locations in Scotland, and found no difference in Cryptosporidium prevalence between the black-headed gull and the herring gull. Cryptosporidium baileyi was identified as a cause of significant morbidity and mortality in 28–100 % of black-headed gulls in the Czech Republic (Pavlásek 1993). Cryptosporidium baileyi from black-headed gulls infected 4-day-old chickens (Gallus gallus f. domestica), causing 40 % mortality (Pavlásek 1993). The intestinal locations of developmental stages are similar to those in the black-headed gull (Pavlásek 1993). Cryptosporidium baileyi was reported in a black-headed gull, and a novel Cryptosporidium genotype (GenBank accession no. AY273769) was identified in a wild-caught Eurasian woodcock (Scolopax rusticola) from the Czech Republic (Ryan et al. 2003a).
4.10 Gruiformes
Gruiformes contains 212 species distributed among 11 families and 61 genera. Most species inhabit marshland areas, and feed on invertebrates, seeds, or other vegetation. Ceca and hindgut fermentation are common in this group.
Cryptosporidium baileyi has been identified in a crane from the Czech Republic (Ng et al. 2006). In Korea, a 4-month old white naped crane (Grus vipio) that died from a disseminated Eimeria infection also had an incidental Cryptosporidium infection of the cloaca (Kim et al. 2005). In Hungary, Plutzer and Tomor (2009) identified C. parvum in a wild Eurasian coot (Fulica atra) (GenBank accession no. FJ984565).
4.11 Columbiformes
Pigeons and doves make up the order Columbiformes. Although there are 308 species worldwide, only one or two families containing 42 genera are recognized. These birds occupy a diverse range of terrestrial habitats, feeding almost exclusively on seeds and grains.
There have been relatively few reports of Cryptosporidium in pigeons (Ozkul and Aydin 1994; Rodriguez et al. 1997; Abreu-Acosta et al. 2009; Qi et al. 2011; Radfar et al. 2012). Cryptosporidium hominis has been reported in rock pigeons (Columba livia) on Tenerife, one of the Canary Islands, suggesting that pigeons can play a role in the transmission of human-pathogenic cryptosporidia (Abreu-Acosta et al. 2009). In a study of Cryptosporidium in birds at pet stores in China, Qi et al. (2011) detected C. meleagridis in a fan-tailed pigeon and a rufous turtle dove (Streptopelia orientalis).
4.12 Psittaciformes
Birds in the order Psittaciformes order, which contains 364 species from 85 genera in the family Psittacidae, inhabit trees in dense, tropical or subtropical forests, and feed almost exclusively on fruits and seeds. Although there have been few studies of psittaciforms in their natural environment, captive psittaciforms host a number of Cryptosporidium species and genotypes (Table 5.6). The greatest diversity of taxa has been detected in the cockatiel (Nymphicus hollandicus), which hosts four species (C. baileyi, C. galli, C. meleagridis, and C. parvum) and three genotypes (avian genotypes II, III, and V) (Abe and Iseki 2004; Ng et al. 2006; Antunes et al. 2008; Nakamura et al. 2009; Abe and Makino 2010; Qi et al. 2011; Gomes et al. 2012). The galah (Eolophus roseicapilla), which is in the same subfamily as the cockatiel, also hosts avian genotype II (Ng et al. 2006).
Although most cases of Cryptosporidium infection in psittaciform birds have been asymptomatic, there have been reports of clinical disease. Latimer et al. (1992) diagnosed cryptosporidiosis in four cockatoos with psittacine beak-and-feather disease. Cryptosporidium infection was confined to the bursa of Fabricius in three of the birds, and was more widespread in the intestine of the fourth. All birds had intermittent diarrhea. Makino et al. (2010) detected avian genotype II in 35 % (13/37) of infected peach-faced lovebirds (Agapomis roseicollis). All birds had symptoms of infection including weight loss and chronic vomiting.
4.13 Strigiformes
The owls make up a small order of about 180 species in two families and 29 genera. All species are predators of small vertebrates, principally rodents. Most species are nocturnal and inhabit forested areas, though a few nest underground in burrows.
In a study of 12 adult owls held in captivity in south Brazil, da Silva et al. (2009) isolated Cryptosporidium oocysts measuring 5–6 μm × 4–5 μm from a barn owl (Tyto alba), great horned owl (Bubo virginianus), and striped owl (Phinoptynx clamator). Owls showed no clincal signs of disease.
Molina-Lopez et al. (2010) diagnosed ocular and respiratory cryptosporidiosis in 16 wild fledgling scops owls (Otus scops) up to 2 months after they were admitted to a wildlife rehabilitation center in Catalonia, northern Spain; the owls were born in the wild and were healthy when they arrived at the center. Blepharoedema, conjunctival hyperaemia, and mucopurulent ocular discharge were diagnosed unilaterally in 75 % (12/16) of the birds and bilaterally in 25 % (4/16). Five owls (31 %) developed diffuse epithelial corneal edema, one exhibited mild anterior exudative uveitis, and another developed rhinitis. Cryptosporidium baileyi, measuring 6.5–7.0 μm × 5.0–5.5 μm, was identified in samples from two birds that were euthanized due to the severity of their disease. The remaining owls recovered following a 15-day treatment with azithromycin.
4.14 Caprimulgiformes
This small order of insectivorous birds has about 118 species in five families and 22 genera. Most feed nocturnally, on the wing. These species generally occur near upland forests, and almost all species nest on the ground.
Cryptosporidium muris has been detected in the tawny frogmouth (Podargus strigoides); although, the bird may have been a mechanical vector (Ryan et al. 2003a; Ng et al. 2006).
4.15 Piciformes
The piciform birds include woodpeckers and toucans, with approximately 398 species in five to nine families and eight genera. Most species occur in forests of the Americas, and almost all nest in cavities. The woodpeckers feed mostly on insects, but toucans are fruigivorous and the honeyguides have the unique ability to eat beeswax.
Cryptosporidium infection has been reported in a channel-billed toucan (Rhamphastus vitellinus), chestnut-eared aracari (Pteroglossus castanotis), and Toco toucan (Ramphastos toco) (Ryan et al. 2003a; Nakamura et al. 2009). The channel-billed toucan was infected with C. baileyi (Ryan et al. 2003a).
4.16 Coraciiformes
Hornbills, kingfishers, and rollers make up the order Coraciiformes, which has about 209 species in 11 families and 51 genera that are found mostly in Eurasia. These birds are generally omnivorous, feeding on a variety of invertebrates, small vertebrates, or fruits and seeds. The coraciiform birds typically inhabit forests, but ground dwelling species occur in sub-Saharan Africa. Most nest in cavities or burrows.
To date, only a few species from the order Coraciiforme have been identified as hosts for Cryptosporidium. Cryptosporidium galli was identified in a captive rhinocerous hornbill (Buceros rhinoceros) in the Czech Republic (Ng et al. 2006). In Malaysia, Cryptosporidium sp. was detected in a wrinkled hornbill (Aceros corrugatus) and a wreathed hornbill (Aceros undulates) at the Kuala Lumpur National Zoo and Zoo Negara, respectively (Rohela et al. 2005; Lim et al. 2007).
4.17 Passeriformes
Passeriformes is the largest avian order, with over 5,700 species in approximately 96 families and more than 1,200 genera. All species have feet for perching, and they occupy a wide range of habitats from dense forests to open grasslands. Fruits, seeds and invertebrates are the dominant foods in their diet.
Passerines are relatively frequent hosts of Cryptosporidium sp., some of which are human pathogens (Table 5.7). Yet, despite having more than 50 % of the avian diversity, passerines host only four species (C. baileyi, C. galli, C. meleagridis, and C. parvum) and three genotypes (avian genotypes I, III, and IV) of Cryptosporidium (Table 5.6).
Australian passerines infected with avian genotypes I, III, and IV showed no clinical signs; whereas, birds from the Czech Republic, which were primarily infected with C. baileyi and C. galli, had diarrhea and anorexia (Ng et al. 2006).
5 Cryptosporidium and Cryptosporidiosis of Mammals
Oocyst size and gastrointestinal localization of Cryptosporidium species reported in wild mammals are shown in Table 5.8. In contrast to cryptosporidia of domestic animals, oocyst morphometry, infection site, and course of infection are unknown for many Cryptosporidium genotypes infecting wild mammals, including bear, beaver, brushtail possum II, chipmunk II and III, C. bovis-like, C. hominis-monkey, C. muris-like, C. ryanae-variant, C. suis-like, deer, deer mouse I–IV, elephant seal, fox, giant panda, guinea pig, hamster, hedgehog, horse, kangaroo I, mink, mouse II, muskrat I and II, opposuum II, raccon, rat I–IV, Sbey/Sbld A, Sbey B, Sbey/Sbld/Sltl C, Sbld D, seal I and II, shrew, skunk, vole, W12, W18, and many other unnamed genotypes (Fig. 5.3).
Table 5.9 shows GenBank accession numbers for representative SSU rRNA gene sequences from mammal-associated cryptosporidia. Cryptosporidium has been identified in the three major groups of mammals: the egg-laying mammals (Protheria), marsupials (Metatheria), and placental mammals (Eutheria).
6 Egg-Laying Mammals
Monotremata, which is the only order of egg-laying mammals, contains two families, three genera, and five species. All lack teeth as adults, forage on insects or other invertebrates, and are native to Australia and New Guinea.
The only report of Cryptosporidium from this order has been in a short-beaked echidna (Tachyglossus aculeatus), a species that inhabits Australia and New Guinea (O’Donoghue 1995).
7 Marsupials
Marsupials comprise seven orders of about 334 species primarily inhabiting Australia and surrounding islands, and South America. Cryptosporidium has thus far been detected in species from the orders Dasyuromorphia, Peramelemorphia, and Diprotodontia in Australia, and Didelphimorphia in South America. Members of the Notoryctemporphia, which contains two species of marsupial moles (Notoryctes typhlops and Notoryctes caurinus) that are native to Australia; the Microbiotheria, which contains a single species (Dromiciops gliroides) that is native to the southwestern part of South America; and the Paucituberculata, which contains six species of shrew opossum (Rhyncholestes raphanurus, Lestoros inca, Caenolestes caniventer, Caenolestes condorensis, Caenolestes convelatus, and Caenolestes fuliginosus) that are native to South America, have yet to be identified as hosts for Cryptosporidium.
7.1 Dasyuromorphia
This order of carnivorous species includes the Tasmanian Devil (Sarcophilus harrisii), numbat (Myrmecobius fasciatus), and the shrew-like antechinus species.
To date, only the brown antechinus (Antechinus staurtii) has been identified as a host for Cryptosporidium (Barker et al. 1978).
7.2 Peramelemorphia
This order of omnivorous marsupials, which includes bandicoots and bilbies, is found in Australia and New Guinea.
Cryptosporidium sp. and C. fayeri have been reported in a southern brown bandicoot (Isoodon obesulus) and western-barred bandicoot (Peremeles bougainville), respectively (O’Donoghue 1995; Power 2010). Cryptosporidium muris was detected in greater bilbies (Macrotis lagotis) at a captive breeding colony in Australia. Although some animals cleared the infection within 2 months, others remained infected for 6 months (Warren et al. 2003). Mice trapped in the pens of infected bilbies were positive for C. muris and were considered to be the likely source of the infection.
7.3 Diprotodontia
Diprotodontia, a large and diverse order of herbivorous marsupials that are native to Australia and surrounding islands, hosts a number of Cryptosporidium species and genotypes. Cryptosporidium fayeri, which was first isolated from a koala (Phascolarctos cincereus) (Morgan et al. 1997), has been reported in the red kangaroo (Macropus rufus), eastern grey kangaroo (Macropus giganteus), and yellow-footed rock wallaby (Petrogale xanthopus) (Ryan et al. 2008). Cryptosporidium macropodum (previously marsupial genotype II) has been reported in the red kangaroo, eastern grey kangaroo, western grey kangaroo, and swamp wallaby (Wallabia bicolor). Neither C. fayeri nor C. macropodum are known to cause clinical disease in diprodonts or any other marsupial. The Cryptosporidium kangaroo genotype I, which was identified in the western grey kangaroo (Yang et al. 2011), clusters with the opossum genotype in a neighbour-joining phylogeny of SSU rRNA sequences (Fig. 5.3b). Brushtail possum genotypes I and II have been identified in the brushtail possum (Trichasuris vulpecula) (Power et al. 2003; Hill et al. 2008). Non-genotyped Cryptosporidium sp. have been reported in the red-necked wallaby (Macropus rufogriseus), pademelon (Thylogale billardierii), and koala (Jakob 1992; O’Donoghue 1995).
7.4 Didelphimorphia
The didelphimorphs (opossums) are native to the American continent.
The C. fayeri-opossum genotype (previously opossum genotype I; this genotype is 99 % similar to C. fayeri at the SSU rRNA locus), C. fayeri (identified by RFLP analysis), and opossum genotype II have been reported in Virginia opossums (Didelphis virginiana) from California and New York, USA (Xiao et al. 2002; Ziegler et al. 2007b). Cryptosporidium also has been detected in the white-eared opossum (Didelphis albiventris) (Zanette et al. 2008).
8 Placental Mammals
Of the 21 orders of placental mammals, 13 contain species that have been identified as hosts for Cryptosporidium. The following eight orders have yet to be identified as hosts:
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Cingulata and Pilosa: These two orders – totalling 19 species in five families and 18 genera – constitute the superorder Xenarthra. Representatives of these orders include armadillos (Cingulata), anteaters (Cingulata), and sloths (Pilosa). Many species are now extinct. The habitats and diets within the group are quite varied. Most are omnivores, but many are insectivores or herbivores.
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Macroscelididae, Afrosordida, and Tublidentata: These are three of the six orders in the superorder Afrotheria. They include tenrecs (Afrosoricida), elephant shrews (Macroscelidia), and aardvarks (Tubulidentata).
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Pholidota: This order compromises about eight species in one family and one genus. They are insectivores, inhabiting Africa and southern areas of Asia.
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Dermoptera: These comprise a small family of two genera and two arboreal species of gliding mammals, colugos, in Southeast Asia.
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Scandentia: These are native of Indonesia and comprise two families, five genera, and 20 species. These small omnivores, commonly referred to as treeshrews, are found in densely forested habitats.
8.1 Hyracoidea
Hyracoidea (hyraxes) are in the superorder Afrotheria. They have a digestive system that is similar in function to that of ruminants.
A single species, C. muris, has been identified in the rock hyrax (Procavia capensis) (Graczyk et al. 1996a; Xiao et al. 1999a).
8.2 Sirenia
The order Sirenia, which contains aquatic herbivores such as the dugong and manatee, is most closely related to elephants in the order Proboscidea.
Reports of Cryptosporidium in the sirenians have been rare. Hill et al. (1997) described a case of intestinal cryptosporidiosis in a dugnong (Dugong dugon) from Queensland, Australia. Three dugongs died as a consequence of the disease and a fourth, the subject of the study, was humanely euthanized (Hill et al. 1997). Sequence analysis of SSU rRNA and acetyl CoA synthethase genes amplified from preserved tissue specimens revealed that the dugong was infected with C. hominis (Morgan et al. 2000a).
8.3 Proboscidea
There have been few studies of Cryptosporidium in the herbivorous elephants that comprise the order Proboscidea.
Cryptosporidium sp. has been detected in African elephants (Loxodonta africana) at Kruger National Park, South Africa (6/144 positive) (Abu Samra et al. 2011) and the Barcelona Zoo (Gracenea et al. 2002).
8.4 Erinaceomorpha
Hedgehogs (Erinceomorpha) contain 24 species in one family (Erinceidae) and ten genera. Some recent phylogenies include this group in the order Soricomorpha (moles and shrews); hedgehogs are similar to shrews in many ways, including an omnivorous diet that may include carrion.
Cryptosporidium can cause clinical and sometimes fatal infections in hedgehogs. Graczyk et al. (1998a) reported fatal cryptosporidiosis in juvenile African hedgehogs (Ateletrix albiventris) housed at the Baltinore Zoo. Cryptosporidium developmental stages were detected in the ileum, jejunum, and colon, and moderate to severe villous atrophy was detected in the ileum and jejunum. Meredith and Milne (2009) reported on a case of cryptosporidiosis in an adult European hedgehog (Erinaceus europaenus) with hemorrhagic diarrhoea. Similar to the juvenile African hedgehogs, moderate to severe villous atrophy was detected in the ileum and jejunum. Sturdee et al. (1999) detected Cryptosporidium oocysts in feces of a free-living European hedgehog from the UK with an estimated infection intensity of 3,000 oocysts per gram. Cryptosporidium spp. was detected in 30.0 % (56/188) of European hedgehogs in Germany (Dyachenko et al. 2010). Cryptosporidium parvum from gp60 subtype families IIa and IIc, and Cryptosporidium hedgehog genotype from gp60 subtype family XIIa (previously VIIa) were identified in positive samples. Although Cryptosporidium positive hedgehogs had diarrhea, any association between a Cryptosporidium sp. and clinical signs was not determined.
8.5 Soricomorpha
The Soricomorpha (moles and shrews) represent about 420 species in four families and 44 genera. These are small omnivorous mammals, though invertebrates (especially insects) form a large component of the diet. Many are nocturnal or fossorial. Shrews and moles occupy a variety of habitats, and often live in close association with water.
Cryptosporidium has been reported in the greater white-toothed shrew (Crocidura russula), common shrew (Sorex araneus), masked shrew (Sorex cinereus), northern short-tailed shrew (Blarina brevicauda), pygmy shrew (Sorex minutus), and Brewer’s mole (Parascalops brewer) (Siński 1993; Sturdee et al. 1999; Torres et al. 2000; Ziegler et al. 2007a). The shrew genotype (also known as W5) has been identified in 2/5 northern short-tailed shrews in New York (Feng et al. 2007). It is not known to what extent Cryptosporidium infection of shrews is associated with clinical disease.
8.6 Cetacea
Cetaceans include approximately 90 species in 11 families and 40 genera of dolphins and whales. There are two main groups. The Mysticeti (baleen whales) have baleen rather than teeth for filtering invertebrates from water or bottom sediments. The Odontoceti (toothed whales) have teeth and generally are piscivorous. Most species inhabit marine waters, but a few occur in coastal rivers. Cetaceans are most closely related to the hippopotamus.
Cryptosporidium has been detected in fecal samples from 5.1 % (2/39) of bowhead whales (Balaena mysticetus) and 24.5 % (12/49) of North Atlantic right whales (Eubalaena glacialis) (Hughes-Hanks et al. 2005). Isolates were not genotyped.
8.7 Artiodactyla
The Artiodactyl mammals include about 240 species in 10 families and 89 genera. These even-toed ungulates include three main groups that differ in their digestive system: Suiformes (pigs) have non-ruminating stomachs, Tylopoda (camels) have three-chambered ruminating stomachs, and Ruminantia (deer, antelope, cows, and hippos) have four-chambered ruminating stomachs. They occupy a wide variety of habitats, but many utilize grasslands or savannahs.
8.7.1 Pigs
Most research has focused on the domestic pig, and there is relatively limited data regarding Cryptosporidium and cryptosporidiosis in wild pigs (described variously as wild boars and feral pigs). Although domestic pigs can host several Cryptosporidium taxa, including C. felis, C. hominis, C. meleagridis, C. muris, C. parvum, C. scrofarum, C. suis, C. tyzzeri, Cryptosporidium sp. Eire w65.5, Cryptosporidium rat genotype, and C. suis-like (Morgan et al. 1999a; Ebeid et al. 2003; Chen and Huang 2007; Kváč et al. 2009a, c), only C. parvum, C. suis, and C. scrofarum have been detected in wild pigs (Table 5.10) (Atwill et al. 1997; Němejc et al. 2012; Garcia-Presedo et al. 2013). The occurrence of non-adapted cryptosporidia in domestic pigs, and their absence from wild pigs, may be a consequence of farming operations that place pigs in close proximity to humans and cattle (e.g. C. parvum), cats (C. felis), and rodents (C. tyzzeri, C. muris, and rat genotype).
Similar to domestic pigs, it appears that shedding of Cryptosporidium oocysts by wild pigs is associated with age and population density. Atwill et al. (1997) reported a 4.2-fold greater likelihood of oocyst shedding in animals younger than 8 months compared to older animals. Also, wild pigs from sites with ≥2.0 wild pigs/km2 had approximately a tenfold greater likelihood of shedding Cryptosporidium oocysts compared to animals from sites with ≤1.9 feral pigs/km2.
There is no association between diarrhea in wild pigs and the presence of cryptosporidia, and infection intensity is generally less than 2,000 oocyts per gram of feces (Castro-Hermida et al. 2011a; Němejc et al. 2012).
8.7.2 Camels and Llamas
Camels are susceptible to infection with two closely related gastric cryptosporidia, C. muris and C. andersoni, which prior to 2001 were considered a single species, C. muris (Lindsay et al. 2000). A key difference between these species is that only C. muris is infectious for neonatal mice under experimental conditions (Lindsay et al. 2000). Therefore, when Anderson (1991) isolated C. muris-like oocysts from a camel and demonstrated their infectivity for 2–20-day-old mice, it is probable that the isolate was C. muris, and not C. andersoni. Molecular studies have subsequently shown that C. muris from a Bactrian camel clusters with C. muris from mice, a hamster, and a rock hyrax in phylogenies constructed from SSU rRNA, Internal transcribed spacer region 1, and HSP-70 sequences (Xiao et al. 1999a; Morgan et al. 2000c).
A C. andersoni isolate with oocysts measuring 7.0–7.2 μm × 5.1–5.2 μm (shape index: 1.37–1.39) from a 3-year-old Bactrian camel did not infect immunosuppressed or immunocompetent calves, immunosuppressed or immunocompetent Kun-ming mice, or severe combined immunodeficiency mice (Wang et al. 2007).
Kváč et al. (2008b) infected two out of three lambs and three out of three goat kids with C. muris isolate CB03, which originated from a naturally infected Bactrian camel. Cryptosporidium muris CB03 was also infectious for Balb/c mice and southern multimammate mice (Mastomys coucha). Developmental stages were detected in the plicae spirales curvature major in the abomasum of infected lambs and kids. Gastric glands were slightly dilated, and covered with cuboidal and metaplased cells. Infiltration or congestion in the lamina propria was not detected, and there was no diarrhea.
Oocysts isolated from rectal samples of camels at a slaughterhouse in Iran had a diameter of 4.56 ± 0.65 μm (range: 4.20–5.70 μm), which is consistent with the morphology of intestinal cryptosporidia (Razawi et al. 2009). However, the isolates were not genotyped so this could not be confirmed. Ryan et al. (2003a) identified C. parvum in an alpaca (Lama pacos), and Gómez et al. (2000) detected Cryptosporidium sp. in a guanaco (Lama guanicoe).
A study of dromedary camels (Camelus dromedaries) in Iran showed a high Cryptosporidium prevalence in animals younger than 1 year (20 %) relative to adult camels (6.5 %) (Yakhchali and Moradi 2012). Another study in Iran showed a relatively high prevalence of Cryptosporidium sp. (20.3 %; 61/300) in asymptomatic camels (Sazmand et al. 2012).
8.7.3 Giraffe and Okapi
Cryptosporidium muris and Cryptosporidium sp. have been detected in giraffes (Giraffa camelopardalis) from zoos in the Czech Republic and Spain, respectively (Gómez et al. 1996; Kodádková et al. 2010). The C. muris isolate was identical to isolates from the rock hyrax and Bactrian camel at the SSU rRNA locus, and was not infectious for Balb/c mice under experimental conditions (Kodádková et al. 2010).
8.7.4 Deer and Moose
Cryptosporidium parvum, C. ubiquitum, and the Cryptosporidium deer genotype have been detected at varying rates in deer and moose worldwide. Cryptosporidium parvum and C. ubiquitum have been reported in 12.5 % (4/32) of swamp deer (Cervus duvauceli) from Nepal (Feng et al. 2012), in a roe deer from England (Robinson et al. 2011), in a red deer (Cervus elaphus) from the Czech Republic (Hajdušek et al. 2004), and in a sika deer (Cervus nippon) from China (Wang et al. 2008a). The Cryptosporidium deer genotype, which is closely related to C. ryanae, has been reported in white-tailed deer (Odoileus virginianus) from the US (Xiao et al. 2002). Cryptosporidium sp. has been detected in 1.3 % (2/149) and 6 % (3/49) of caribou (Rangifer tarandus) from Canada and Alaska, respectively; 8.3 % (2/24), 8.8 % (4/35), and 5.0 % (72/360) of white-tailed deer from the US; 7.9 % (3/38) of black-tailed deer (Odocoileus hemionus columbianus) from the US; 25 % (10/40) of tule elk (Cervus canadensis ssp. nannodes) from the US; 1.3 % (3/224), 9.1 % (2/22), and 6.2 % (18/291) of roe deer (Capreolus capreolus) from Spain, Poland, and Norway, respectively; 14.4 % (17/118), 0.3 % (1/289), 41.5 % (135/325), and 100 % (2/2) of red deer from Poland, Norway, Ireland, and the US, respectively; and 3.3 % (15/455) of moose (Alces alces) from Norway (Simpson 1992; Fayer et al. 1996; Deng and Cliver 1999; Rickard et al. 1999; Skerrett and Holland 2001; Siefker et al. 2002; Hamnes et al. 2006; Ziegler et al. 2007b; Johnson et al. 2010; Castro-Hermida et al. 2011b). Other deer that have been identified as hosts of Cryptosporidium sp., include the fallow deer (Dama dama), axis deer (Axis axis), barasingha deer (Cervus duvauceli), Eld’s deer, muntjac deer, sambar (Rusa unicolor), Thorold’s deer (Cervus albirostris), and Père David’s deer (Elaphurus davidianus) (Heuschele et al. 1986; Sturdee et al. 1999).
8.7.5 Bovids
Cryptosporidium has thus far been identified in wild bovid species representing eight of the ten bovid subfamilies (Table 5.11). It has not yet been identified in the Tibetan antelope (Pantholops hodgsonii) or grey rhebok (Pelea capreolus), which are the sole representatives of the Pantholopinae and Peleinae subfamilies, respectively. Most studies of wild bovid species have been limited to captive animals outside their native habitat.
In a study of cryptosporidiosis in wild bovids, Cryptosporidium developmental stages were identified in the small intestine, cecum, spiral colon, and colon (Van Winkle 1985). Four mountain gazelles (Gazella cuvieri) at the Munich Zoo with cryptosporidiosis had anorexia and weight loss but no diarrhea (Pospischil et al. 1987). Cryptosporidium developmental stages were detected in the abomasum only. The mucosa was hyperplastic and diffusely infiltrated with small lymphocytes, and the mucosal glands were elongated and hypercellular.
8.7.5.1 Hippopotamus
Cryptosporidium sp. has been detected in a pygmy hippopotamus (Choeropsis liberiensis) at the Barcelona Zoo (Gómez et al. 2000).
9 Chiroptera
Bats represent a diverse order of flying mammals with over 1,100 species in 18 families and 202 genera. The group is split into the Megachiropterans, which are large, fruit or nectar-eating bats that lack certain ear structures, and the Microchiropterans, which are small, omnivorous or insectivorous species that utilize echolocation and possess associated ear structures. Most (but not all) bats hibernate, and are generally associated with forest habitats.
Despite representing about 20 % of the mammalian fauna, few bat species have been identified as hosts for Cryptosporidium. Cryptosporidiosis was diagnosed in a big brown bat (Eptesicus fuscus) from Oregon, USA (Dubey et al. 1998). In New York, Cryptosporidium sp. and C. parvum were identified in a small brown bat (Myotis lucifugus) and big brown bat, respectively (Ziegler et al. 2007b). Cryptosporidium tyzzeri was detected in a large-footed bat (Myotus adversus) from New South Wales, Australia (Morgan et al. 1999b).
10 Perissodactyla
The Perissodactyl mammals include about 16 species in three families and six genera. These are odd-toed ungulates that include horses, tapirs and rhinoceroses. The digestive system is much simpler than that of the ruminants, with cellulose broken down by fermentation in the latter portion of the gut. They occupy mainly grassland or savannah habitat.
10.1 Equids
Equids include the zebra, ass, kiang, and wild horse. Cryptosporidium was detected in 28 % (7/25) of zebras (Equus zebra) at Mikumi National Park in Tanzania (Mtambo et al. 1997). Cryptosporidium horse genotype was identified in a Przewalski’s wild horse foal at the Prague Zoo (Ryan et al. 2003a). Although, no other cryptosporidia have been reported in wild Equids, domestic horses have been identified as hosts for C. parvum, Cryptosporidium horse genotype, and Cryptosporidium hedgehog genotype (Laatamna et al. 2013).
10.2 Rhinoceros and Tapirs
Cryptosporidium sp. has been reported in a southern white rhinoceros (Ceratotherium simum simum), rhinoceros (Rhinoceros unicornis), and a South American tapir (Tapirus terrestris) at the Barcelona Zoo (Wang and Liew 1990; Gómez et al. 1996, 2000).
11 Carnivora
11.1 Fin-Footed Mammals (Pinnipedia)
Cryptosporidium muris, which was isolated from a ringed seal (Phoca hispida) in Northern Quebec, Canada (Santín et al. 2005), remains the only species identified in Pinnipeds to date. Cryptosporidium sp. has been reported in the ringed seal (Phoca hispida), harbor seal (Phoca vitulina), harp seal (Pagophilus groenlandicus), Weddell seal (Leptonychotes weddellii), California sea lion (Zalophus californianus), grey seal (Halichoerus grypus), and southern elephant seal (Mirounga leonina) (Deng et al. 2000; Hughes-Hanks et al. 2005; Santín et al. 2005; Bogomolni et al. 2008; Rengifo-Herrera et al. 2011, 2013; Bass et al. 2012). In a neighbor-joining phylogeny, SSU rRNA gene sequences from the ringed seal (seal genotype I, GenBank accession no. AY731234 and seal genotype II, GenBank accession no. AY731235), harbor seal (GenBank accession nos. JN858906–JN858908), harp seal (GenBank accession no. JN858909), and hooded seal (GenBank accession no. JN858905) form a separate clade that is most closely related to a group containing sequences from the shrew (Soricidae), wildebeest (Connochaetes gnou), and eastern chipmunk (Tamias striatus) (Fig. 5.3c). Isolates from southern elephant seals (Mirounga leonina) on the west coast of the Antarctic Peninsula shared 99 % identity with a skunk genotype and C. tyzzeri at the SSU locus and are named southern elephant seal genotype (Rengifo-Herrera et al. 2011, 2013). Isolates from the Weddell seal are most closely related to the ferret genotype and C. parvum (99 % identity at the SSU locus). Cryptosporidium sp. detected in California sea lions (Zalophus californianus) from the northern California coastal area share 98 % identity with C. parvum at the COWP locus (Deng et al. 2000).
11.2 Domestic Dogs
There have been few molecular studies of Cryptosporidium in dogs (Table 5.12). Cryptosporidium canis is the most frequently identified species in dogs (Abe et al. 2002) and it appears to be relatively host adapted. Other species found in dogs include C. parvum (Hajdušek et al. 2004), C. muris (Ellis et al. 2010), and C. meleagridis (Hajdušek et al. 2004). Cryptosporidium muris caused chronic gastritis in an 18-month male, mixed-breed dog (Ellis et al. 2010). It appeared that the dog had a concurrent infection with Helicobacter.
In a study of parasites infecting sled dogs in Poland, Bajer et al. (2011) found a higher prevalence of Cryptosporidium in dogs infected concurrently with Giardia (35.5 %) than in dogs without Giardia (2.7 %). In contrast, Cryptosporidium prevalence was three times lower in dogs infected with nematodes. Other studies have shown a higher prevalence of Cryptosporidium in dogs with diarrhea (Mirzaei 2012; Tupler et al. 2012), and dogs less than 1-year-old (Mirzaei 2012). It is not known if the association with diarrhea is dependent on the Cryptosporidium species/genotype causing the infection.
Cryptosporidium canis does occasionally cause human disease (Leoni et al. 2006; Hijjawi et al. 2010), and a UK study found that dogs are the most likely companion animals to shed Cryptosporidium (46/139) (Smith et al. 2009).
11.3 Raccoon Dogs
Cryptosporidium parvum has been identified in a raccoon dog (Nyctereutes procyonoides viverrinus) at a zoo in Osaka, Japan (Matsubayashi et al. 2005).
11.4 Foxes
Cryptosporidium has been reported in the two genera of true foxes: Vulpes and Urocyon. Current (1989) identified Cryptosporidium sp. in the gray fox (Urocyon cinereoargenteus), which is native to southern parts of North America and northern parts of South America. Cryptosporidium canis fox genotype (n = 4), C. canis (n = 1), and muskrat genotype I (n = 1) were identified in 6/76 Cryptosporidium positive samples from unidentified fox species in Maryland, USA (Zhou et al. 2004a). Cryptosporidium was detected in 38.7 % (24/62) and 8.1 % (10/124) of red foxes (Vulpes vulpes) from the Slovak Republic and Ireland, respectively (Nagano et al. 2007; Ravaszová et al. 2012). Two of the isolates from the study in Ireland were identified as C. parvum by sequence analysis of the SSU rRNA and gp60 loci. In contrast to the relatively high prevalence reported in the Slovak Republic, Cryptosporidium sp. was detected in only 2.2 % (6/269) and 8.7 % (2/23) of red foxes from Norway and England, respectively (Sturdee et al. 1999; Hamnes et al. 2007).
11.5 Wolves
Two large Canadian studies were consistent in showing a relatively low prevalence of Cryptosporidium in gray wolves. The prevalence was 1.7 % in a study of 1,558 fecal samples from wolves in British Columbia (Bryan et al. 2012), and 1.2 % in a study of 601 fecal samples from wolves in Manitoba (Stronen et al. 2011). In contrast, 54.9 % of fecal samples (28/51) from wolves in northeast Poland were positive for Cryptosporidium (Kloch et al. 2005). A subsequent study in the same region of Poland reported a prevalence of 35.7 %, and C. parvum was identified by sequence analysis of the COWP gene (GenBank accession number: AF266273) (Paziewska et al. 2007).
11.6 Coyotes
Cryptosporidium has been detected in 27 % (6/22) and 26.3 % (5/19) of fecal samples from coyotes (Canis latrans) in northeastern Pennsylvania (Trout et al. 2006) and New York (Ziegler et al. 2007a), respectively. One isolate from the Pennsylvania study shared 99.7 % sequence identity with C. muris at the SSU rRNA locus, and the remaining five isolates were identical to the C. canis coyote genotype (Trout et al. 2006). In a study of coyotes in southern Alberta and Saskatchewan, Canada, Cryptosporidium was not found during winter, and the prevalence was 17.4 % during summer. SSU rRNA sequences from two of the isolates were identified as the C. canis coyote genotype (Thompson et al. 2009).
11.7 Bears
Cryptosporidium has been detected in three of the five genera in the family Ursidae (Ailuropoda, Helarctus, and Ursus). There have been no reports in the sloth bear (Melursus ursinus) or spectacled bear (Tremarctos ornatus), which are the only extant representatives of their genera.
Cryptosporidium has been reported in two captive Malayan sun bears (Helarctos malayanus) at a zoological park in Taiwan (Wang and Liew 1990).
Cryptosporidium has been detected in black bears (Ursus americanus), brown bears (Ursus arctos), and polar bears (Ursus maritimus) in the genus Ursus (Siam et al. 1994; Duncan et al. 1999; Xiao et al. 2000; Ravaszová et al. 2012). Xiao et al. (2000) identified the Cryptosporidium bear genotype in a black bear and showed that it is most closely related to C. canis at the SSU rRNA and HSP-70 loci.
Karanis et al. (2007) detected C. tyzzeri (previously mouse genotype I) in a lesser panda (Ailurus fulgens). An isolate from a giant panda (Ailuropoda melanoleuca) was named the Cryptosporidium giant panda genotype based on sequences of the SSU rRNA, actin, COWP, and HSP-70 genes. Although the study has not been published, the sequences are available in GenBank under the accession numbers JF970610, JN969985, JN588570, and JN588571.
11.8 Raccoons
A number of studies have identified Cryptosporidium in raccoons (Procyon lotor) (Snyder 1988; Perz and Le Blancq 2001; Zhou et al. 2004a; Ziegler et al. 2007a; Chavez et al. 2012). Zhou et al. (2004a) identified the skunk genotype in 3.9 % (2/51) of raccoon samples collected in the Chesapeake Bay area of Maryland, USA. Cryptosporidium was detected in 11 out of 44 fecal samples from raccoons in Colorado, USA. Five out of six of the isolates that were genotyped were identified as the skunk genotype, and one was identified as C. parvum (Chavez et al. 2012).
Cryptosporidium also causes clinical disease in raccoons. A juvenile raccoon, estimated to be between 6 and 12-months-old was found in a moribund condition in Fort Collins, Colorado. The animal was emaciated and dehydrated, and had diarrhea and a mucoid oculonasal discharge. Cryptosporidium sp. was identified on intestinal villi (Martin and Zeidner 1992).
11.9 Ferrets
Rehg et al. (1988) reported cases of subclinical cryptosporidiosis in 40 % of ferrets at an animal research facility in Tennessee. Subsequent studies identified the Cryptosporidium ferret genotype in the black-footed ferret (Mustela nigripes) and domestic ferret (Mustela putorius furo) in the USA and Japan (Xiao et al. 1999b; Sulaiman et al. 2000; Abe and Iseki 2003). The ferret genotype is genetically closely related to C. parvum, sharing 99 %, 98 %, 98 %, and 97 % identity at the SSU rRNA, actin, COWP, and HSP-70 genes, respectively. Ferret genotype isolates from the USA (Sulaiman et al. 2000) and Japan (Abe and Iseki 2003) have identical sequences, suggesting that this genotype is geographically conserved.
Cryptosporidium also causes clinical disease in ferrets. Gómez-Villamandos et al. (1995) reported an outbreak of fatal cryptosporidiosis in captive 11–12 month-old non-pregnant female ferrets (Mustela putorius furo) kept on a goat farm. Animals died 48–72 h after the onset of signs, which included anorexia, depression, and diarrhea. Cryptosporidium developmental stages were identified in feces and tissue, but the species/genotype causing the infection was not identified.
11.10 Otters
Cryptosporidium has been detected in the European or wild otter (Lutra lutra), river otter (Lontra canadensis), and sea otter (Enhydra lutris nereis) (Feng et al. 2007; Gaydos et al. 2007; Méndez-Hermida et al. 2007; Oates et al. 2012). In Spain, Cryptosporidium oocysts were detected in 17 out of 437 fecal samples from wild otters (Méndez-Hermida et al. 2007). In the USA, nine river otters from the Puget Sound Georgia Basin were positive for the Cryptosporidium mink genotype (Gaydos et al. 2007), and a river otter in New York was positive for the Cryptosporidium skunk genotype (Feng et al. 2007). Cryptosporidium sp. was detected in a single sea otter in California (Oates et al. 2012).
11.11 Mink and Martens
Rademacher et al. (1999) isolated Cryptosporidium oocysts measuring 3–5 μm from captive beech martens (Martes foina) with episodes of diarrhea. Cryptosporidium oocysts (4.5–5.5 μm) were also detected in 24.2 % (8/33) of fecal samples from captive American minks (Mustela vison) in Spain. The animals did not show clinical signs associated with cryptosporidiosis. Three isolates had COWP sequences that differed from the ferret genotype by a single nucleotide polymorphism (Gómez-Couso et al. 2007). In China, eight Cryptosporidium isolates were obtained from 469 fecal samples of American minks (Mustela vison) originated from a farm in Hebei Province in China. Six of the eight Cryptosporidium-positive samples contained a novel genotype, the Cryptosporidium mink genotype, that was most closely related to the Cryptosporidium ferret genotype (Wang et al. 2008b). In New York, one of four mink (Mustela vison) in a watershed study was positive for Cryptoporidium mink genotype, and an ermine (Mustela erminea) had a mixed infection with Cryptosporidium shrew genotype (also known as W5 genotype) and W18 genotype (Feng et al. 2007). Also in New York, Ziegler et al. (2007a) detected Cryptosporidium sp. in one of three ermine (Mustela erminea) and in one of 58 American mink (Musela vison).
11.12 Skunk
Cryptosporidium has been detected in the striped skunk (Mephitis mephitis) in New York, USA (Perz and Le Blancq 2001; Ziegler et al. 2007a), and the Cryptosporidium skunk genotype has been described from this host (Xiao et al. 2002; Feng et al. 2011). Cryptosporidium prevalence in the striped skunk in New York was 14 % (12/86) (Ziegler et al. 2007a).
11.13 Badger
Cryptosporidium has been reported in 15.4 % (4/26) of European badgers (Meles meles) in England (Sturdee et al. 1999). The Cryptosporidium species/genotype infecting badgers is not yet known.
11.14 Banded Mongoose
The banded mongoose (Mungos mungo) has been identified as a host of a Cryptosporidium genotype that is most closely related to the bear genotype at the SSU rRNA and HSP-70 loci (Abe et al. 2004).
11.15 Domestic Cat
Two Cryptosporidium species, C. felis and C. muris, have been reported in domestic cats (Felis catus). Cryptosporidium felis was first identified in cats in Japan (Iseki 1979) and has since been reported in cats worldwide. Cryptosporidium muris has been reported in cats less frequently (Santín et al. 2006; Pavlásek and Ryan 2007; FitzGerald et al. 2011). FitzGerald et al. (2011) reported a C. felis/C. muris coinfection in a cat with chronic diarrhea. Cryptosporidium muris was identified within the glands of the gastric mucosa. Interestingly, the cat appeared to be persistently infected with C. muris, but not C. felis. Cryptosporidium felis has been identified as an infrequent cause of human cryptosporidiosis (Pedraza-Diaz et al. 2001; Caccio et al. 2002; Caccio 2005; Leoni et al. 2006). The prevalence of Cryptosporidium sp. in cats from different countries is shown in Table 5.13.
11.16 Wild Cats
Cryptosporidium tyzzeri has been identified in black leopards (Pantera pardus) (Karanis et al. 2007). Cryptosporidium sp. also has been reported in bobcats (Lynx rufus) in California (Carver et al. 2012) and New York, USA (Ziegler et al. 2007a).
12 Lagomorpha
Lagomorpha (rabbits, hares and pikas) includes about 87 species in two families and 12 genera. The phylogeny of the lagomorphs is not well understood. They have four upper incisors, and all are herbivorous. All produce both a hard fecal pellet and a soft, grease-like pellet derived from the cecum. The soft pellet is reingested, and contains a much higher concentration of vitamins and minerals than the uningested hard pellet. Lagomorphs occupy both forested and grassland areas.
Rabbits are the major host of C. cuniculus (previously Cryptosporidium rabbit genotype). Cryptosporidium cuniculus is closely related to C. hominis, sharing 99.5, 100, 99.9, and 99.5 % nucleotide sequence identity at the SSU rRNA, COWP, actin, and HSP-70 loci, respectively (Robinson et al. 2010). It emerged as a human pathogen in 2009 when it was identified as the cause of a waterborne cryptosporidiosis outbreak in Northhamptonshire, England (Robinson et al. 2010). A subsequent study identified C. cuniculus in 1.2 % of 3,030 samples from human cryptosporidiosis cases in the UK during the period 2007–2008 (Chalmers et al. 2011). In a comprehensive review of the literature on Cryptosporidium in rabbits, which will not be duplicated here, Robinson and Chalmers (2010) noted that in studies employing genotyping tools, C. cuniculus was the only species/genotype detected. More recently, C. cuniculus was the only species detected in rabbits in Australia (Nolan et al. 2010, 2013) and China (Shi et al. 2010; Zhang et al. 2012), and prevalence was highest in younger (1–3-month-old) rabbits (Shi et al. 2010).
13 Rodentia
Rodents comprise about 40 % of the mammalian diversity, with over 2,200 species in 31 families and 481 genera. Five suborders are typically recognized: Myomorpha (mice, rats, gerbils, and relatives), Sciuromorpha (tree squirrles and relatives), Castorimorpha (beavers, gophers, and relatives), Anumaluromorpha (scaly-tailed squirrels, and springhares), and Hystricomorpha (gundis, capybaras, and relatives). With such diversity, rodents occupy a wide range of habitats, and generalizations regarding their natural history are difficult. All rodents have two upper and two lower incisors that grow continuously (and are self-sharpening) but lack canines. Most species are herbivorous or omnivorous.
13.1 Muridae
Old world mice and rats comprise the subfamily Murinae in the largest mammal family, the Muridae. Gerbils, which also are members of the family Muridae, have yet to be identified as a natural host for Cryptosporidium, although they are susceptible to experimental infections (Baishanbo et al. 2005; Kváč et al. 2009d).
Four Cryptosporidium species (C. tyzzeri, C. muris, C. parvum, and C. scrofarum) and six genotypes (C. suis-like genotype, rat genotypes I–IV and mouse genotype II) have been reported as natural infections in several species of Mus, Apodemus, and Rattus in Australia, China, the Czech Republic, Germany, Kenya, New Zealand, the Philippines, Poland, Portugal, Spain, the UK, and the US (Table 5.13). The C. suis-like genotype and C. scrofarum were reported in rats in the Philippines; C. suis-like genotype was found exclusively in Asian house rats, and C. scrofarum was additionally identified in brown rats (Ng-Hublin et al. 2013). The C. suis-like genotype, which is 99.7 % similar to C. suis at the SSU rRNA locus, has additionally been reported in cattle and humans (Ong et al. 2002; Langkjær et al. 2007; Robinson et al. 2011). Cryptosporidium scrofarum is a pig-adapted species that also has been reported in cattle and humans (Kváč et al. 2009b; Ng et al. 2011). Cryptosporidium muris, a rodent adapted species, has been detected the domestic mouse (Mus musculus domesticus) in the UK (Chalmers et al. 1997), the Algerian mouse (Mus spretus) in Spain (Torres et al. 2000), and the East African mole rat (Tachyoryctes splendens) in Kenya (Kváč et al. 2008b). Cryptosporidium mouse genotype II has been identified in 11 domestic mice in Australia (Foo et al. 2007). Rat genotypes I–IV have been reported in various rat species in Australia, China, and the Philippines (Table 5.14). Although C. tyzzeri (previously mouse genotype I) has been reported in the yellow-necked mouse, voles, snakes, and rats (Morgan et al. 1998, 1999b; Bajer et al. 2003; Xiao and Ryan 2004; Karanis et al. 2007), the house mouse is considered the major host for this species (Ren et al. 2012).
The fate of the house mouse (Mus musculus) has been intimately connected to humans since the establishment of a commensal relationship at the dawn of civilization. Two house mouse subspecies, Mus musculus musculus and Mus musculus domesticus, diverged approximately 0.5 million years ago in the Middle East (Geraldes et al. 2008; Duvaux et al. 2011; Auffray and Britton-Davidian 2012; Bonhomme and Searle 2012). Mus m. musculus spread to northern Eurasia and migrated westward through Europe. Mus m. domesticus expanded westward through Asia Minor to southern and western Europe, northern Africa, and the New World (Boursot et al. 1993; Guénet and Bonhomme 2003; Rajabi-Maham et al. 2008; Duvaux et al. 2011; Auffray and Britton-Davidian 2012; Bonhomme and Searle 2012; Cucchi et al. 2012). About 6,000 years ago, westward migrating M. m. musculus and eastward-migrating M. m. domesticus reestablished contact in central Europe, and formed a stable, narrow (approximately 20 km wide) hybrid zone that stretches 2,500 km from Norway to the Black Sea (Macholán et al. 2003; Jones et al. 2011; Ďureje et al. 2012). This hybrid zone affords a rare opportunity to study speciation through the interactions between two subspecies that have been separated for about 500,000 years.
The hybrid zone was recently used to test the hypothesis that the house mouse-adapted species C. tyzzeri is coevolving with subspecies of M. musculus. Cryptosporidium tyzzeri isolates from naturally infected M. m. musculus and M. m. domesticus in the hybrid zone differed genetically, morphometrically, and biologically (Kváč et al. 2013b), which supports the coevolution hypothesis.
13.2 Cricetidae
Cricetidae, which includes muskrats, deer mice, voles, cotton rats, and hamsters, are the second largest family of mammals with greater than 681 species in 130 genera. To date, members of this family have been reported as hosts for four Cryptosporidium species (C. muris, C. parvum, C. andersoni, and C. ubiquitum) and ten genotypes (vole genotype, muskrat genotypes I and II, W12, hamster genotype, chipmunk genotype I, and deer mouse genotypes I–IV) (Table 5.15).
Within the Cricetidae, C. muris and C. andersoni have been detected only in hamsters (Ryan et al. 2003a; Lv et al. 2009). Cryptosporidium andersoni, a ruminant adapted species, was detected in 5.9 % (8/136) of pet hamsters from three different species in China (Lv et al. 2009), suggesting that hamsters may be a significant host for C. andersoni, at least in that country. Cryptosporidium muris and C. parvum are the only Cryptosporidium species or genotypes known to infect members of both the Muridae and Cricetidae family. These species also are found in the family Sciuridae (see below).
13.3 Sciuridae
Five species (C. andersoni, C. baileyi, C. muris, C. parvum, and C. ubiquitum) and ten genotypes have been detected in the family Sciuridae, which includes squirrels and chipmunks (Table 5.16). In addition to C. parvum and C. muris, which are found in Muridae, Cricetidae, and Sciuridae, two species (C. andersoni and C. ubiquitum) and two genotypes (chipmunk genotype I and deer mouse genotype III) are common to the Cricetidae and Sciuridae (Fig. 5.4).
13.4 Hystricomorpha
Hystricomorphs include the guinea pig, capybara, and chinchilla, which were the first rodents to colonize South America about 40 million years ago, probably from Africa, and they remained the only rodents in South America until the arrival of murids about five million years ago (Antoine et al. 2012).
Table 5.17 shows the Cryptosporidium sp. that have been reported in Hystricomorphs. Cryptosporidium wrairi is found only in guinea pigs (Vetterling et al. 1971; Lv et al. 2009), and the prevalence of infection can be as high as 85 % in pet guinea pigs (Lv et al. 2009). Guinea pigs also host a guinea pig genotype (GenBank Accession nos. DQ885337 and DQ885338) that is only 93 % similar to C. wrairi at the SSU rRNA locus. Cryptosporidium parvum has been identified in capybara (Hydrochoerus hydrochaeris) in Brazil (Meireles et al. 2007); however, it is likely that the infections resulted from exposure of capybara to water polluted by anthroponotic activities.
13.5 Beaver and Gophers
Cryptosporidium has been detected in the American and European beavers and the plains pocket gopher (Table 5.18). Combining the data from three studies in the eastern US (Fayer et al. 2006; Feng et al. 2007; Ziegler et al. 2007b), the prevalence of Cryptosporidium in American beavers (Castor Canadensis) was 4.0 % (7/176). In Europe, Cryptosporidium was detected in 19.2 % (10/52) of European beavers (Castor fiber) in northeastern Poland (Paziewska et al. 2007). Cryptosporidium ubiquitum and a novel beaver genotype were identified in beavers in New York. The beaver genotype clusters with mink and ferret genotypes in a neighbor-joining phylogeny of SSU rRNA sequences, (Fig. 5.3b) and is most similar to a ferret-like genotype, sharing 99.6 % identity at the SSU rRNA locus.
14 Non-Human Primates
There are about 375 species of non-human primates in 15 families and 68 genera. All are omnivorous, and occupy both forest and open grassland habitats. There is potential for Cryptosporidium transmission between humans and endangered non-human primates in areas where the two live in close proximity (Nizeyi et al. 1999, 2002; Graczyk et al. 2001). Yet, knowledge of Cryptosporidium and cryptosporidiosis in our closest relatives remains relatively poor, and few studies have genotyped isolates (Table 5.19). Among those that have, the potential for zoonotic transmission is clearly evident in the species detected.
Cryptosporidium parvum has been identified in the mountain gorilla (Gorilla gorilla beringei) from Uganda; toque macaque (Macaca sinica sinica), gray lagur (Semnopithecus entellus thersites), and purple-faced lagur (Trachypithecus vetulus philbricki) from Sri Lanka; and rhesus macaque (Macaca mulatta) from China (Graczyk et al. 2001; Ekanayake et al. 2007; Ye et al. 2012). Cryptosporidium hominis has been reported in rhesus macaques from the US and China and olive baboons (Papio anubis) from Kenya (Feng et al. 2011; Li et al. 2011; Ye et al. 2012). Isolates from the red-tailed guenon, red colobus, and black-and-white colobus were indistinguishable from C. hominis, C. parvum and C. cuniculus at the COWP locus (Salyer et al. 2012). Other Cryptosporidium taxa detected in primates include C. felis in rhesus macaques at a park in China (Ye et al. 2012) and a Cryptosporidium sp. closely related to C. suis in a Coquerel’s sifaka (Propithecus coquereli) in the US (da Silva et al. 2003).
The clinical signs of cryptosporidiosis in infant non-human primates resemble those seen in human infants. Cryptosporidiosis was diagnosed in 81/157 infant primates, predominantly pigtailed macaques (Macaca nemestrina), housed in a nursery unit at the Washington Regional Primate Research Center. The mean age at onset of oocyst shedding was 38 ± 25 days, and animals shed oocysts for 7–78 days. All but one of the animals had clinical symptoms of enteric infection, which included severe diarrhea and dehydration. The outbreak was confined to the nursery and no cases were detected among juvenile or adult animals (Miller et al. 1990a). A follow-up study (Miller et al. 1990b) characterized the course of experimental infections in pigtailed macaques infected with 10 or 2 × 105 oocysts from naturally infected macaques (the species/genotype of the isolate was not reported). Infected animals suffered clinical enteritis, watery stools, lethargy, and loss of appetite. Animals infected with 10 and 2 × 105 oocysts began shedding oocysts on day 8 and day 7, respectively, and there was no difference in the duration of intense oocyst shedding or clinical symptoms between the treatments.
Cryptosporidiosis in immunocompromised non-human primates resembles cryptosporidiosis in immunocompromised humans with respect to extraintestinal involvement. Kaup et al. (1994) diagnosed biliary and pancreatic cryptosporidiosis in several rhesus monkeys following an experimental simian immunodeficiency virus (SIV) infection. Yanai et al. (2000) reported moderate to severe bronchopneumonia with cryptosporidiosis in macaques experimentally infected with SIV. Endogenous stages were detected in the trachea, lungs, bile ducts, pancreas, and intestine. Conjunctival infections were detected in six SIV-infected, immunodeficient rhesus monkeys (Baskin 1996). Although conjunctival cryptosporidiosis has been reported in birds, there have been no reported cases in humans. Singh et al. (2011) examined the time during an SIV infection when a self-limiting Cryptosporidium parvum infection becomes persistent due to mucosal immune defects. One group of SIV-infected macaques was challenged with C. parvum during acute SIV infection and the second group was challenged during the chronic infection phase. Interestingly, persistent cryptosporidiosis developed during acute SIV infection.
15 Diversity of Cryptosporidium in Different Vertebrate Classes
The diversity of mammalian cryptosporidia appears to reflect mammal diversity. We compared Cryptosporidium diversity in the order Rodentia – the most diverse order of mammals – to diversity in other mammalian orders. Figure 5.5 presents 68 mammalian Cryptosporidium taxa (species and genotypes) in a Venn diagram with two sets: ‘Rodentia’ and ‘other mammals’ Among the taxa that are members of both sets (the intersection), C. andersoni, C. scrofarum, and the ferret genotype primarily infect non-rodent hosts and are therefore included with ‘other mammals’. Similarly, C. tyzzeri and C. muris are primarily parasites of rodents and are included with the Rodentia set. Cryptosporidium baileyi was excluded from the analysis because it primarily infects avian hosts. Forty percent (27/67) of mammalian Cryptosporidium taxa are associated with the order Rodentia, which reflects the diversity of Rodentia within mammals (Rodentia contains 40 % of mammalian species). Three percent (2/67) of Cryptosporidium taxa (C. parvum and C. ubiquitum) can be considered generalists, and 57 % (38/67) of taxa are associated with non-rodent mammals. These data suggest that cryptosporidia diverged in close association with mammal species.
In contrast to mammals, it appears that the diversity of avian cryptosporidia does not reflect avian diversity. The order Passeriformes comprises about 50 % of avian species; species diversity in the Passeriforme order is comparable to that of the entire mammal class. Figure 5.6 presents 17 Cryptosporidium taxa from avians in a Venn diagram with two sets: ‘Passeriformes’ and ‘other avians’. Muskrat genotype I, C. hominis, C. hominis-like, C. muris, and C. parvum were excluded from the analsysis because they are not considered avian-associated taxa. Seventeen percent (2/12) of avian Cryptosporidium taxa are exclusively found in passerines (avian genotypes I and IV), 50 % (6/12) are found only in non-passerine orders, and 33 % (4/12; C. baileyi, C. meleagridis, C. galli, and avian genotype III) infect multiple avian orders and can be considered generalists. From these data, it can be hypothesized that the mechanisms of Cryptosporidium diversification in avians and mammals are fundamentally different.
The diversity of Cryptosporidium in reptiles and amphibians appears to be low. Despite a comparable faunal diversity with birds, and considerably greater faunal diversity than mammals, relatively few Cryptosporidium taxa have been reported in reptiles or amphibians.
16 Gaps in Knowledge and Suggestions for Future Work
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Cryptosporidium remains poorly characterized in many vertebrate orders. For example, Chiroptera (bats), an order that comprises 20 % of mammal species, has not been well studied. If Cryptosporidium diversity reflects bat diversity, then we should expect to find many bat-adapted Cryptosporidium taxa.
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Cryptosporidium viatorum is a recently described species that has thus far been identified only in cases of human cryptosporidiosis in the UK (n = 10) and Sweden (n = 2); all cases were associated with travel to countries in the Indian subcontinent, Africa, and South America (Elwin et al. 2012b; Insulander et al. 2013). Studies are needed to determine if there is a major animal host for this species. Greater sampling in general, particularly of animals in their natural habitat, will help to help to identify emerging sources of human disease.
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Relatively little is known about the general biology of many of the Cryptosporidium genotypes identified. Experimental evidence of infection characteristics and host specificity will enhance understanding of the biological diversity and will clarify taxonomy.
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Kváč, M., McEvoy, J., Stenger, B., Clark, M. (2014). Cryptosporidiosis in Other Vertebrates. In: Cacciò, S., Widmer, G. (eds) Cryptosporidium: parasite and disease. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1562-6_5
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