International Journal For Parasitology: Parasites and Wildlife

International Journal for Parasitology: Parasites and Wildlife 5 (2016) 88e109
Contents lists available at ScienceDirect
International Journal for Parasitology:

Parasites and Wildlife
journal homepage: www.elsevier.com/locate/ijppaw
Invited review
Public health significance of zoonotic Cryptosporidium species in

wildlife: Critical insights into better drinking water management
Alireza Zahedi a, Andrea Paparini a, Fuchun Jian b, Ian Robertson a, Una Ryan a, *
a
School of Veterinary and Life Sciences, Murdoch University, Perth, Australia
b
Henan Agricultural University, Henan, China
a r t i c l e i n f o a b s t r a c t
Article history: Cryptosporidium is an enteric parasite that is transmitted via the faecaleoral route, water and food.
Received 29 September 2015 Humans, wildlife and domestic livestock all potentially contribute Cryptosporidium to surface waters.
Received in revised form Human encroachment into natural ecosystems has led to an increase in interactions between humans,
1 December 2015
domestic animals and wildlife populations. Increasing numbers of zoonotic diseases and spill over/back
Accepted 2 December 2015
of zoonotic pathogens is a consequence of this anthropogenic disturbance. Drinking water catchments
and water reservoir areas have been at the front line of this conflict as they can be easily contaminated by
Keywords:
zoonotic waterborne pathogens. Therefore, the epidemiology of zoonotic species of Cryptosporidium in
Cryptosporidium
Zoonotic
free-ranging and captive wildlife is of increasing importance. This review focuses on zoonotic Crypto-
Wildlife sporidium species reported in global wildlife populations to date, and highlights their significance for
Epidemiology public health and the water industry.
© 2015 The Authors. Published by Elsevier Ltd on behalf of Australian Society for Parasitology. This is an
open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Contents
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89
2. Taxonomy and zoonotic potential of Cryptosporidium species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89
3. Wildlife associated outbreaks and water contamination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90
3.1. Cryptosporidium in mammals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95
3.1.1. Cryptosporidium hominis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95
3.1.2. C. parvum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95
3.1.3. Cryptosporidium cuniculus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 96
3.1.4. Cryptosporidium ubiquitum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 96
3.1.5. Cryptosporidium muris . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 96
3.1.6. Cryptosporidium andersoni . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97
3.1.7. Cryptosporidium canis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97
3.1.8. Cryptosporidium erinacei . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97
3.1.9. Cryptosporidium fayeri and Cryptosporidium macropodum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97
3.1.10. Cryptosporidium meleagridis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97
3.1.11. Other Cryptosporidium species and genotypes reported in wild mammals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97
3.2. Cryptosporidium in birds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99
3.2.1. C. meleagridis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99
3.2.2. Cryptosporidium baileyi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99
3.2.3. Cryptosporidium galli . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99
3.2.4. Other Cryptosporidium species and genotypes reported in birds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99
3.3. Cryptosporidium in fish and marine mammals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99
3.4. Cryptosporidium in amphibians and reptiles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 100
4. The role of urbanisation in the transmission of zoonotic Cryptosporidium species from wildlife . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 100
* Corresponding author.
E-mail address: [email protected] (U. Ryan).
http://dx.doi.org/10.1016/j.ijppaw.2015.12.001
2213-2244/© 2015 The Authors. Published by Elsevier Ltd on behalf of Australian Society for Parasitology. This is an open access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/).
A. Zahedi et al. / International Journal for Parasitology: Parasites and Wildlife 5 (2016) 88e109 89
5. Perspectives for the water industry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102

Conflict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103
1. Introduction at high risk need additional treatment (in the form of properly
controlled coagulation/flocculation filtration systems or membrane
More than 15% of the world's population has no access to safe or UV treatment systems). The UK regulations also require com-
drinking water (Cauchie et al., 2014). Waterborne parasitic proto- panies to design and continuously operate adequate treatment and
zoan diseases with worldwide distribution, result in four billion disinfection. A proven failure to comply with this is now an offence
cases of diarrhoea, 1.6 million deaths annually (www.who.int) and (DWI, 2010).
62.5 million Disability Adjusted Life Years (DALYs) worldwide Cryptosporidium species are able to infect a broad range of hosts
(Wright and Gundry, 2009; WHO, 2009). Yet, despite the latest including humans, domestic and wild animals (mammals, birds,
advances made in water treatment measures, protecting drinking fish, marsupials, reptiles and amphibians) worldwide (Table 1),
water supplies against waterborne pathogens remains by far, as one causing asymptomatic or mild to severe gastrointestinal disease in
of the most challenging concerns for the entire drinking water their host species (Monis and Thompson, 2003; Hunter et al., 2007;
supply chain worldwide (Cotruva et al., 2004; Betancourt and Rose, Ryan and Power, 2012; Xiao, 2010; Kv a
c et al., 2014a; Ryan et al.,
2004; Thompson and Smith, 2011; Plutzer, 2013; Burnet et al., 2014). Current treatment options for cryptosporidiosis are limited
2014). In response to this, in 2009, the World Health Organization and only one drug, nitazoxanide (NTZ), has been approved by the
has developed guidelines for water suppliers on how to implement United States (US) Food and Drug Administration (FDA). This drug,
“Water Safety Plans” (WSPs), in the hope of halving the number of however, exhibits only moderate clinical efficacy in children and
people without safe access to drinking water by the end of 2015 immunocompetent people, and none in people with HIV (Abubakar
(WHO, 2009). et al., 2007; Amadi et al., 2009; Pankiewicz et al., 2015; Gargala,
In less developed countries, lack of basic infrastructure for 2008; Rossignol, 2010).
providing safe drinking water is considered a major cause of poor Oocyst transport to surface water can occur by deposition of
water quality which contributes to the spread of endemic/epidemic manure directly in the water or surface runoff. Hence, humans,
waterborne diseases. However, even in industrialized nations, wildlife and domestic livestock all potentially contribute Crypto-
highly advanced infrastructures are not yet a protective factor sporidium contamination to water systems (Ryan et al., 2014).
against outbreaks (Cummins et al., 2010; Smith and Nichols, 2010; Identification of the sources/carriers of human pathogenic strains is
Castro-Hermida et al., 2010; Burnet et al., 2014; Smolders et al., therefore essential for accurate risk assessment and optimal
2015). This appears to be largely due to a lack of knowledge about catchment management. However, most studies to date have
the epidemiology and transmission dynamics of waterborne focused on humans and the potential role of livestock in the
pathogens (e.g. from animals ranging within the catchments) epidemiology of zoonotic cryptosporidiosis, while wildlife as a
which leads to poor management practices for drinking water potential risk factor to source water, has only been studied oppor-
catchments (Gormley et al., 2011; Castro-Hermida et al., 2010). tunistically. Thus, the aim of this review is to summarize available
Waterborne parasitic protozoans are responsible for the ma- information about molecular characterisation of Cryptosporidium
jority of waterborne outbreaks worldwide, with socio-economic species in wildlife with emphasis on the public health significance
impacts even in developed countries (Cotruva et al., 2004; Pond, of zoonotic species.
2005; Baldursson and Karanis, 2011; Cauchie et al., 2014). Of
these, Cryptosporidium was the etiological agent in 60.3% (120) of
2. Taxonomy and zoonotic potential of Cryptosporidium
the waterborne protozoan parasitic outbreaks that have been re-
species
ported worldwide between 2004 and 2010 (Baldursson and
Karanis, 2011). For the global water industry, therefore, Crypto-
The application of advanced molecular techniques has led to an
sporidium represents the major public health concern, as its oocyst
improved taxonomy and systematics, and better understanding of
(the environmentally stable stage) is able to survive and penetrate
Cryptosporidium phylogeny (Ryan et al., 2014). Given the morpho-
routine wastewater treatment and is resistant to inactivation by
logical similarity of oocysts by microscopy, these advances are
commonly used drinking water disinfectants (Fayer et al., 2001;
crucial for confident identification, description of host/parasite
Baldursson and Karanis, 2011; Burnet et al., 2014). As a result of
intractions and ultimately accurate risk assessment. Currently, 29
these waterborne outbreaks of cryptosporidiosis, Cryptosporidium
Cryptosporidium species have been recognised as valid (Table 1),
testing in source or finished water is now mandatory in most
including the recently described C. rubeyi in ground-dwelling
industrialised nations. For example, the U.S. EPA, working with the
squirrels (Spermophilus sp.) (Li et al., 2015a). More than 17 species
U.S. public water supply industry, developed and implemented the
have been identified in humans (Table 1). Of these, C. parvum and
Long-term Stage 2 Enhanced Surface Water Treatment Rule
C. hominis are by far the most common species reported in humans
(LT2ESWTR), known as LT2 to control Cryptosporidium in public
worldwide (Xiao, 2010; Ryan and Xiao, 2014) and have been
water supplies (US EPA, 2006). LT2 requires all public water sup-
responsible for the majority of waterborne outbreaks typed to date
pliers using surface water sources and serving populations >10,000
with the exception of a waterborne outbreak in the UK caused by C.
to monitor their sources for Cryptosporidium by analysing at least
cuniculus from rabbits (Oryctolagus cuniculus) (Chalmers et al.,
24 consecutive monthly samples. In the UK, the Drinking Water
2009; Xiao, 2010; Ryan et al., 2014).
Inspectorate (DWI) requires that water companies carry out risk
The most widely molecular markers used for typing of Crypto-
assessments on all their water supply sites to ascertain the level of
sporidium isolates are the 18S ribosomal RNA (18S rRNA) gene and
risk Cryptosporidium poses to the final treated water quality. Those
the 60-kDa glycoprotein (gp60) gene. The latter locus encodes a
90 A. Zahedi et al. / International Journal for Parasitology: Parasites and Wildlife 5 (2016) 88e109
Table 1
Valid Cryptosporidium species confirmed by molecular analysis.
Species name Author(s) Type host(s) Major Reports in humans

host(s)
C. rubeyi Li et al., 2015a Spermophilus beecheyi (California ground Squirrels None reported
squirrel)
C. scophthalmi Alvarez-Pellitero Scophthalmus maximus (Turbot) Turbot None reported
et al., 2004; Costa
et al., 2015
C. huwi Ryan et al., 2015 Poecilia reticulata (Guppy), Paracheirodon Fish None reported
innesi (Neon tetra) and Puntius tetrazona
(Tiger barb)
C. erinacei
Kva c et al., 2014b Erinaceus europaeus (European Hedgehogs,
Kva c et al., 2014a
hedgehog) horses
C. scrofarum Kva
c et al., 2013 Sus scrofa (Pig) Pigs
Kva c et al., 2009a, 2009b
C. viatorum Elwin et al., 2012 Homo sapiens (Human) Humans Elwin et al., 2012; Insulander et al., 2013
C. tyzzeri Tyzzer, 1912; Ren Mus musculus (Mouse) Rodents Raskov a et al., 2013
et al., 2012
C. cuniculus Robinson et al., 2010 Oryctolagus cuniculus (European rabbit) Rabbits Chalmers et al., 2009; Anon, 2010; Molloy et al., 2010; Chalmers et al., 2011;
Anson et al., 2014; Koehler et al., 2014; Chalmers, 2012
C. ubiquitum Fayer et al., 2010 Bos taurus (Cattle) Ruminants, Commonly reported (cf. Fayer et al., 2010; Elwin et al., 2012)
rodents,
primates
C. xiaoi Fayer et al., 2010 Ovis aries (Sheep) Sheep and Adamu et al., 2014
goats
C. ryanae Fayer et al., 2008 Bos taurus (Cattle) Cattle None reported
C. macropodum Power and Ryan, Macropus giganteus (Kangaroo) Marsupials None reported
2008
C. fragile Jirk
u et al., 2008 Duttaphrynus melanostictus (Toad) Toads None reported
C. fayeri Ryan et al., 2008 Macropus rufus (Kangaroo) Marsupials Waldron et al., 2010
C. bovis Fayer et al., 2005 Bos taurus (Cattle) Cattle Khan et al., 2010; Ng et al., 2012; Helmy et al., 2013
C. suis Ryan et al., 2004 Sus scrofa (Pig) Pigs Xiao et al., 2002a; Leoni et al., 2006; Cama et al., 2007; Wang et al., 2013a
C. galli Pavalasek, 1999; Spermestidae, Frangillidae, Gallus gallus, Birds None reported
Ryan et al., 2003 Tetrao urogallus, Pinicola enucleator
(Birds)
C. hominis Morgan Ryan et al., Homo sapiens (Human) Humans Most common species in humans
2002
C. molnari Alvarez-Pellitero Sparus aurata (Gilt-head sea bream) and Fish None reported
-Bobadilla, Dicentrarchus labrax (European seabass)
and Sitja
2002
C. canis Fayer et al., 2001 Canis familiaris (Dog) Dogs Many reports (cf. Lucio-Forster et al., 2010)
C. andersoni Lindsay et al., 2000 Bos taurus (Cattle) Cattle Leoni et al., 2006; Morse et al., 2007; Waldron et al., 2011; Agholi et al.,
2013; Jiang et al., 2014; Liu et al., 2014
C. varanii sek et al., 1995
Pavla Varanus prasinus (Emerald Monitor) Lizards None reported
C. baileyi Current et al., 1986 Gallus gallus (Chicken) Birds None reported
C. parvum Tyzzer, 1912 Bos taurus (Cattle) Ruminants Commonly reported in humans
C. meleagridis Slavin, 1955 Meleagris gallopavo (Turkey) Birds and Commonly reported in humans
humans
C. serpentis Levine, 1980 Elaphe guttata, E. subocularis, Sanzinia Snakes and None reported
madagascarensus (Snakes) lizards
C. felis Iseki, 1979 Felis catis (Cat) Cats Many reports (cf. Lucio-Forster et al., 2010)
C. wrairi Vetterling et al., Cavia porcellus (Guinea pig) Guinea pigs None reported
1971
C. muris Tyzzer, 1907; and Mus musculus (House mouse) Rodents Many reports e Guyot et al., 2001; Gatei et al., 2002; Tiangtip and
1910 Jongwutiwes, 2002; Gatei et al., 2003; Palmer et al., 2003; Gatei et al., 2006;
Leoni et al., 2006; Muthusamy et al., 2006; Azami et al., 2007; Al-Brikan
et al., 2014; Petrincov
et al., 2008; Neira et al., 2012; Hasajova a et al., 2015;
Spanakos et al., 2015
precursor protein, that is cleaved to produce mature cell surface non-zoonotic Cryptosporidium species and subtypes in wildlife
glycoproteins (gp45/gp40 and gp15) implicated in zoite attachment populations (Appelbee et al., 2005; Ziegler et al., 2007; Ryan et al.,
to, and invasion of enterocytes (Xiao, 2010; Ryan et al., 2014). Most 2014). Conclusive molecular evidence, linking contamination of
of the genetic heterogeneity in the gp60 gene is the variation in the water supplies by wild animals in catchments with outbreaks of
number of a tri-nucleotide repeat (TCA, TCG or TCT) in the 50 end cryptosporidiosis in human populations is scant. However, a recent
(gp40) of the coding region, although extensive sequence poly- waterborne outbreak in the UK caused by C. cuniculus from rabbits
morphism is also present in the rest of the gene. The repeats are has highlighted the importance of wildlife in the dissemination of
used to define the subtype families within a species, whereas the Cryptosporidium to drinking water sources and the associated hu-
remaining polymorphic sites are used to identify subtypes within a man health risk (Chalmers et al., 2009; Elvin et al., 2012).
subtype family (Ryan et al., 2014). A wide range of Cryptosporidium species and genotypes have
been identified in drinking source water, storm water runoff,
3. Wildlife associated outbreaks and water contamination stream sediment, wastewater and seawater in various geographic
locations including C. hominis, C. parvum, C. andersoni, C. muris,
Relatively little is known about the distribution of zoonotic and C. cuniculus, C. meleagridis and C. canis as well as various wildlife
Table 2
Cryptosporidium species and genotypes identified by molecular tools in wild terrestrial mammals and their zoonotic importance.
Cryptosporidium Wildlife hosts Zoonotic importance gp60 subtypes reported in wildlife References
species/
genotypes
C. hominis Fallow deer (Dama dama), Dugong Main Cryptosporidium species IbA12G3, IbA10G2R2, IiA17, IfA12G2, Morgan et al., 2002; Salyer et al., 2012;
(Dugong dugon), Chinchillas (Chinchilla infecting humans IaA13R7, IaA13R8, IaA14R7, IdA20, Ye et al., 2012; Ng et al., 2011; Dowle
lanigera), Baboons (Pabio anubis), IeA11G3T3, IfA16G2, IkA7G4 (novel et al., 2013; Nolan et al., 2013; Karim
Chimpanzees (Pan troglodytes subtype) et al., 2014; Ryan et al., 2014; Liu et al.,
schweinfurthii), Red colobus 2015b; Parsons et al., 2015; Zahedi
(Procolobus rufomitratus), Black-and- et al., 2015
white colobus (Colobus guereza),
Rhesus macaque (Macaca mulatta),
Cynomolgus monkey (Macaca
fascicularis), Francois' leaf monkey
(Trachypithecus francoisi), Lemurs
(Lemur sp.), Bandicoots (Isoodon
obesulus), Bushtail possums
(Trichosurus vulpecula), Estern grey
kangaroos (Macropus giganteus),
Brush-tailed rock-wallabies (Petrogale
penicillata), Wild dingo (Canis lupus
dingo), Squirrel monkey (Saimiri
sciureus)
C. parvum Alpaca (Lama pacos), Swamp deer Major IIdA15G1, IIdA18G1, IIdA19G1, Morgan et al., 1999a; Atwill et al.,
(Cervus duvauceli), Red deer (Cervus IIaA15G2R1, IIaA19G2R1, IIaA19G3R1, 2001; Perez and Le Blancq, 2001;
elaphus), Roe deer (Capreolus IIaA19G4R1, IIaA20G3R1, IIaA20G3R2, Matsui et al., 2000; Matsubayashi
capreolus), Fallow deer (Dama dama), IIaA20G4R1, IIaA21G3R1, IIaA16G2R1, et al., 2004; Ryan et al., 2003, 2004;
Addaxes (Addax nasomaculatus), IIaA14G1R1, IIaA14G2R1, IIaA16G3R1, Ekanayake et al., 2007; Feng et al.,
Arabian oryx (Oryx leucoryx), IIcA5G3, IIcA5G3a, IIoA13G1, IIpA9 2007; Meireles et al., 2007; Paziewska
Gemsboks (Oryx gazella), Sable (novel subtype) et al., 2007; Starkey et al., 2007; Ziegler
antelopes (sable antelopes), White- et al., 2007; Cinque et al., 2008; Lv
tailed deer (Odocoileus Virginianus), et al., 2009; Feng, 2010; Go mez-Couso
Game grey wolves (Canis lupus), et al., 2012; Ravaszova et al., 2012; Ye
Racoon dog (Nyctereutes procyonoides et al., 2012; Dowle et al., 2013; Nolan
viverrinus), Rabbit (Oryctolagus et al., 2013; Liu et al., 2014; Lv et al.,
cuniculus), Nutria (Myocastor coypus), 2009; Reboredo-Ferna ndez et al.,
Prezewalski's wild horse (Equus 2014; Bodager et al., 2015; Liu et al.,
przewalskii), Alpaca (Lama quanico 2015a; Montecino-Latorre et al., 2015;
pacos), Eastern grey squirrel (Sciurus Qi et al., 2015; Wang et al., 2015; Wells
carolinensis), Ground Squirrels et al., 2015; Zahedi et al., 2015; Zhao
(Spermophilus beecheyi), Siberian et al., 2015a, 2015b
chipmunk (Tamias sibiricus), Hamsters
(Cricetinae), Wood mice (Apodemus
sylvaticus), White-footed mouse
(Peromyscus leucopus), Yellow-bellied
marmot (Marmota flaviventris),
Bamboo rats (Rhizomys sinensis), Small
brown bat (Myotis lucifugus), Campbell
hamster (Phodopus campbelli), Golden
hamster (Mesocricetus auratus),
Capybara (Hydrochoerus hydrochaeris),
Racoon dog (Nictereutes procyonoides
viverrinus), Red fox (Vulpes vulpes),
Rhesus macaques (Macaca mulatta),
Toque macaques (Macaca sinica
sinica), Grey langurs (Semnopithecus
priam thersites), Purple-faced langurs
(Trachypithecus vetulus philbricki),
Common dolphins (Delphinus delphis),
Golden takins (Budorcas taxicolor
bedfordi), Eastern grey kangaroos
(Macropus giganteus), Asian house rat
(Rattus tanezumi), Brown rat (Rattus
norvegicus), Bamboo rats (Rhizomys
sinensis)
C. cuniculus European rabbit (Oryctolagus Responsible for several VaA18,VbA18, VbA19, VbA21, VaA22, Xiao et al., 2002a; Ryan et al.,
cuniculus), Eastern grey kangaroo waterborne outbreaks and VbA24, VbA26, VbA29, VbA32, 2003;Chalmers, 2012; Nolan et al.,
(Macropus giganteus) (single report) sporadic cases of VbA22R4, VbA23R3, VbA24R3, 2010; Robinson et al., 2010; Elwin
cryptosporidiosis in the UK and VbA25R4,VbA26R4 et al., 2012; Zhang et al., 2012; Nolan
has been identified in a human et al., 2013; Kapuke et al., 2014;
in Australia Koehler et al., 2014; Liu et al., 2014;
Puleston et al., 2014
C. ubiquitum Swamp deer (Cervus duvauceli), Deer Emerging human pathogen XIIa, XIIb, XIIc, XIId, XIIe, XIIf Perez and Le Blancq, 2001; da Silva
mouse (Peromyscus), Eastern grey et al., 2003; Ryan et al., 2003; Feng
squirrels (Sciurus carolinensis), Red et al., 2007; Karanis et al., 2007; Ziegler
(continued on next page)
Table 2 (continued )
species/
genotypes
squirrel (Sciurus vulgaris), Eastern et al., 2007; Wang et al., 2008; Fayer
chipmunk (Tamias striatus), Lemur et al., 2010; Cinque et al., 2008; Feng,
(Lemuroidea), North American beaver 2010; Robinson et al., 2010, 2011;
(Castor canadensis), Woodchuck Feng et al., 2012; Abu Samraa et al.,
(Marmota monax), Raccoon (Procyon 2013; Nolan et al., 2013; Murakoshi
lotor), White-tailed deer (Odocoileus et al., 2013; Li et al., 2014; Ma et al.,
virginianus), Sika deer (Cervus Nippon), 2014; Perec-Matysiak et al., 2015; Qi
Roe deer (Capreolus capreolus), et al., 2015a, 2015b; Stenger et al.,
Blesbok (Damaliscus pygargus 2015b
phillipsi), Ibex (Capara sibirica), Nyala
(Niyala anagasii), Coquerel's sifaca
(Propithecus coquereli), Large Japanese
field mouse (Apodemus speciosus),
Foxes
C. muris Wild rats (Rattus sp.), Mice (Mus sp.), Numerous reports in humans Chalmers et al., 1997; Hurkova et al., Dubey et al., 2002; Morgan et al.,
Greater bilblies (Macroties lagotis), 2003 1999a; Xiao et al., 2002a, 2004b;
Girrafes house mice (Mus musculus), Warren et al., 2003; Nakai et al., 2004;
Eastern grey squirrel (Sciurus Hikosaka and Nakai, 2005; Santín
carolinensis), Golden hamster et al., 2005; Azami et al., 2007; Brikan
(Mesocricetus auratus), Rock hyrax et al., 2008; Kvac et al., 2008; Lupo
(Procavia capensis), Large footed et al., 2008; Lv et al., 2009; Kodadkova
mouse-eared bat (Myotis adversus), et al., 2010; Feng, 2010; Murakoshi
Japanese field mouse (Apodemus et al., 2013; Yang et al., 2011, 2013;
argenteus), Bilbies (Macrotis lagotis), Ng-Hublin et al., 2013; Karim et al.,
Bank voles (Clethrionomys glareolus), 2014, Qi et al., 2014; Sak et al., 2014;
Campbell hamster (Phodopus Du et al., 2015; Laatamna et al., 2015;
campbelli), Siberian hamster (Phodopus Petrincova et al., 2015, Zhao et al.,
sungorus), Golden hamster 2015b
(Mesocricetus auratus), Mountain goats
(Oreamnos americanus), Cynomolgus
monkeys (Macaca fascicularis), East
African mole rat (Tachyoryctes
splendens), Ringed seal (Pusa hispida),
Donkey (Giraffa camelopardalis),
Ringed seal (Phoca hispida), Large
Japanese field mouse (Apodemus
speciosus), Cynomolgus monkey
(Macaca fascicularis), Slow loris
(Nycticebus coucang), Ostriches
(Struthio camelus), Mountain gorillas
(Gorilla beringei beringei), Asian house
rat (Rattus tanezumi), Brown rat
(Rattus norvegicus), House mouse (Mus
musculus)
C. andersoni Bacterian camel (Camelus bactrianus), Minor e Matsubayashi et al., 2005; Wang et al.,
European wisent (Bison bonasus), 2008; Lv et al., 2009; Stuart et al.,
Marmots Campbell hamster (Phodopus 2013; Du et al., 2015; Wang et al.,
campbelli), Golden hamster 2015; Zhao et al., 2015a
(Mesocricetus auratus), Golden takins
(Budorcas taxicolor bedfordi), Giant
panda (Ailuropoda melanoleuca),
Macaca mulatta (Rhesus macaque),
American mink (Mustela vison)
C. felis Rhesus macaques (Macaca mulatta); Numerous reports in humans e Lucio-Forster et al., 2010; Ye et al.,
Pallas's cat (Felis Manul) 2012; Beser et al., 2015; Ebner et al.,
2015; Li et al., 2015c
C. canis dog Unidentified fox, Coyote (Canis latrans) Numerous reports in humans e Xiao et al., 2002a; Ryan et al., 2004;
genotype Zhou et al., 2004; Trout et al., 2006;
Ziegler et al., 2007; Elwin et al., 2012;
Koompapong et al., 2014
C. canis fox Fox No reports in humans to date e Zhou et al., 2004; Swaffer et al., 2014
genotype
C. canis coyote Coyotes No reports in humans to date e Xiao et al., 2002a; Zhou et al., 2004
genotype
C. erinacei European hedgehog (Erinaceus One report in humans XIIIaA21R11, XIIIaA22R9, XIIIaA21R10, Dyachenko et al., 2010; Laatamna
europaeus), Horses XIIIa20R10, XIIIaA19R12, XIIIaA22R11 et al., 2013; Nolan et al., 2013; Kv
ac
et al., 2014a, 2014b; Meredith and
Milne, 2009
C. fayeri Southern brown bandicoot (Isodon Minor IVaA9G4T1R1, IVaA10, IVaA7, Power et al., 2005; Ryan et al., 2008;
obesulus), Western-barred bandicoot IVbA9G1T1, IVcA8G1T1, IVdA7G1T1, Yang et al., 2008, 2011; Power, 2010;
(Permeles bougainville), Koala IVfA12G1T1 Waldron et al., 2010; Feng et al.,
(Phascolarctos cincerus), Red kangaroo 2011b; Nolan et al., 2013; Swaffer
(Macropus rufus), Eastern grey et al., 2014; Vermeulen et al., 2015
species/
genotypes
kangaroo (Macropus giganteus), Yellow

footed rock wallaby (Petrogale
xanthopus), Western grey kangaroo
(Macropus fuliginosus), Koalas
(Phascolarctos cinereus)
Opossum Opossum (Didelphimorphia) No reports in humans to date XIaA4G1T1 Feng et al., 2011b
genotype I
(C. fayeri)
Opossum Virginia opossum (Didelphis virginiae) No reports in humans to date e Xiao et al., 2002b; Oates et al., 2012
genotype II
C. meleagridis Mountain gorillas (Gorilla beringei Major IIIbA, IIIgA (closest match to Morgan et al., 2000; Cama et al., 2003;
beringei), Brush-tailed rock wallabies IIIeA19G2R1) Gatei et al., 2006; Leoni et al., 2006;
(Petrogale penicillata), deermouse Muthusamy et al., 2006; Feng et al.,
(Peromyscus sp.) 2007; Elwin et al., 2012; Silverlås et al.,
2012; Kurniawan et al., 2013; Adamu
et al., 2014; Ryan and Xiao, 2014;
Ghaffari and Kalantari, 2014; Sak et al.,
2014; Rahmouni et al., 2014; Wang
et al., 2014; Stensvold et al., 2015;
Vermeulen et al., 2015
C. tyzerri Mice (Mus musculus), Brown rats Occasionally reported in IXaA5R2, IXaA6R1, IXaA6R2, IXaA6R3, Morgan et al., 1999a, Xiao et al., 2002a;
(Rattus norvegicus), Large-footed bat humans IXbA6, IXbA6R2 Bajer et al., 2003; Alves et al., 2005;
(Myotus adversus), Yellow-necked Foo et al., 2007; Karanis et al., 2007;
mouse (Apodemus flavicollis), Bank Ziegler et al., 2007; Lv et al., 2009; Feng
vole (Myodes glareolus), Common vole et al., 2011b; Carver et al., 2012; Kv a
c
(Microtus arvalis), Red panda (Ailurus et al., 2012; Ren et al., 2012; Raskova
fulgens), Leopard (Panthera pardus), et al., 2013; Silva et al., 2013; Swaffer
Takin (Budorcas taxicolor), Prairie et al., 2014
bison (Bison bison), Lesser panda
(Ailurus fulgens), Black leopards
(Pantera pardus), Bobcats (Lynx rufus)
C. macropodum Red kangaroo (Macropus rufus), No reports in humans to date e Power et al., 2004, 2005; Power and
Eastern grey kangaroo (Macropus Ryan, 2008; Power, 2010; Yang et al.,
giganteus), Swamp wallaby (Wallabia 2011; Nolan et al., 2013
bicolor), Western grey kangaroos
(Macropus fuliginosus)
C. bovis Yaks, foxes, Gorillas (single report), Occasionally reported in e Robinson et al., 2011; Helmy et al.,
Roe deer (Capreolus capreolus) humans 2013; García-Presedo et al., 2013b; Sak
et al., 2013; Qi et al., 2015b; Qin et al.,
2014
C. ryanae Roe deer (Capreolus capreolus), Water No reports in humans to date e Feng et al., 2012; García-Presedo et al.,
buffaloes (Bubalus bubalis) 2013b
C. wrairi Guinea pig (Cavia porcellus), California No reports in humans to date VIIaA13T1, VIIaA17T1, VIIaA16T1 Atwill et al., 2004; Feng et al., 2007,
ground squirrels (Spermophilus 2011b, Lv et al., 2009
beecheyi)
C. scrofarum Asian house rat (Rattus tanezumi), Occasionally reported in e García-Presedo et al., 2013a; Ng-
Brown rat (Rattus norvegicus), Eurasian humans Hublin et al., 2013, Nemeic et al., 2013;
wild boars (Sus scrofa) Bodager et al., 2015; Parsons et al.,
2015
C. suis Chimpanzees (Pan troglodytes Occasionally reported in e Nemeic et al., 2012, 2013; Bodager
schweinfurthii), Eurasian wild boars humans et al., 2015; Parsons et al., 2015
(Sus scrofa), Rodents
C. suis-like Asian house rat (Rattus tanezumi) No reports in humans to date e Ng-Hublin et al., 2013
C. rubeyi California ground squirrel (S. beecheyi), No reports in humans to date e Pereira et al., 2010; Li et al., 2015a
Belding's ground squirrel (S. beldingi),
Golden
Mantled ground squirrel (S. lateralis)
Bear genotype Black bear (Ursus americanus) No reports in humans to date e Xiao et al., 2000
Bat genotype I Chinese rufous horseshoe bat No reports in humans to date e Wang et al., 2013b
(Rhinolophus sinicus), Stoliczka's
trident bat (Aselliscus stoliczkanus)
Bat genotype II Chinese rufous horseshoe bat No reports in humans to date e Wang et al., 2013b
(Rhinolophus sinicus), Fulvus roundleaf
bat (Hipposideros fulvus), Leschenault's
rousette (Rousettus leschenaultii)
Bat genotype III Big brow bat (Eptesicus fuscus) No reports in humans to date e
Kva c et al., 2015
Bat genotype IV Western barbastelle (Barbastella No reports in humans to date
Kva c et al., 2015
barbastellus)
Beaver genotype North American beaver (Castor No reports in humans to date e Feng et al., 2007
canadensis)
Brushtail Brushtail possum (Trichasuris No reports in humans to date e Hill et al., 2008
possum I vulpecula)
(continued on next page)
species/
genotypes
Chipmunk Chipmunk sp. (Tamias sp.), Eastern Emerging human pathogen XIVaA18G2T1, XIVaA18G2T2 Jiang et al., 2005; Feltus et al., 2006;
genotype I grey squirrel (Sciurus carolinensis), Feng et al., 2007; ANOFEL, 2010;
Deer mice (Peromyscus maniculatus) Insulander et al., 2013; Lebbad et al.,
2013; Guo et al., 2015
Chipmunk Eastern chipmunk (Ramias striatus) No reports in humans to date e Feng et al., 2007; Stenger et al., 2015a
genotype II
Chipmunk Siberian chipmunk (Tamias sibiricus) No reports in humans to date e Lv et al., 2009
genotype III
Deer mouse Deer mouse (Peromyscus) No reports in humans to date e Xiao et al., 2002b; Feng et al., 2007,
genotype I 2011b
Deer mouse Deer mouse (Peromyscus) No reports in humans to date e Xiao et al., 2002b; Feng et al., 2007
genotype II
Deer mouse Deer mouse (Peromyscus) No reports in humans to date e Feng et al., 2007; Stenger et al., 2015b
genotype III
Deer mouse Deer mouse (Peromyscus) No reports in humans to date e Feng et al., 2007
genotype IV
Ferret genotype Ferret (Mustelidae), Siberian chipmunk No reports in humans to date VIIIaA5G2 Xiao et al., 2002a; Abe and Iseki, 2003;
(Tamias sibiricus), River otters (Lontra Gaydos et al., 2007; Kvac et al., 2008;
canadensis), Black-footed ferret Lv et al., 2009; Feng et al., 2011b
(Mustela nigripes), Red squirrel (Sciurus
vulgaris)
Giant panda Giant panda (Ailuropoda melanoleuca) No reports in humans to date e Liu et al., 2013
genotype
Squirrel Golden-mantled ground squirrels No reports in humans to date e Atwill et al., 2004; Pereira et al., 2010;
genotypes I (Callospermophilus lateralis), Belding's Stenger et al., 2015b
eIII ground squirrels (Urocitellus beldingi),
California ground squirrels
(Otospermophilus beecheyi), Black-
tailed prairie dog (Cynomys
ludovicianus)
Hamster Siberian hamster (Phodopus sungorus) No reports in humans to date e Lv et al., 2009
genotype
Horse genotype Przewalski's wild horse (Equus Identified in humans in the UK VIaA11G3, VIbA13 Ryan et al., 2003; Robinson et al., 2008;
przewalski), Four-toed hedgehog Abe and Matsubara, 2015
(Atelerix albiventris)
Mink genotype River otter (Lontra canadensis), Several reports in humans XaA5G1 Feng et al., 2007, Wang et al., 2008;
American minks (Mustela vison), Feng et al., 2011b; Ng-Hublin et al.,
Ermine (Mustela ermine) 2013; Stuart et al., 2013; Ebner et al.,
2015
Mouse genotype House mouse (Mus musculus) No reports in humans to date e Foo et al., 2007; Silva et al., 2013
II House mouse (Mus musculus) No reports in humans to date e Silva et al., 2013
Mouse genotype
III
Muskrat Muskrat (Ondatra zibethicus), Boreal No reports in humans to date e Xiao et al., 2002a; Zhou et al., 2004;
genotype I red-backed vole (Myodes rutilus) Feng et al., 2007
Muskrat Muskrat (Ondatra zibethicus), Red fox No reports in humans to date e Ziegler et al., 2007; Robinson et al.,
genotype II (Vulpus vulpus), Deer mouse 2011
(Peromyscus maniculatus), Meadow
vole (Microtus pennsylvanicus)
Naruko Large Japanese field mouse (Apodemus No reports in humans to date e Murakoshi et al., 2013
genotype speciosus)
Rat genotype I Brown rat (Rattus norvegicus) No reports in humans to date e Ng-Hublin et al., 2013
Rat genotype II Brown rat (Rattus tanezum), Wild black No reports in humans to date e Lv et al., 2009; Paparini et al., 2012;
rat (Rattus rattus), Brown rat (Rattus Ng-Hublin et al., 2013; Silva et al.,
norvegicus). 2013
Rat genotype III Asian house rat (Rattus tanezumi), No reports in humans to date e Lv et al., 2009; Paparini et al., 2012;
Wild black rat (Rattus rattus). Ng-Hublin et al., 2013; Silva et al.,
2013
Rat genotype IV Tanezumi rat (Rattus tanezumi), Asian No reports in humans to date e Ng-Hublin et al., 2013
house rat (Rattus tanezumi), Brown rat
(Rattus norvegicus)
Seal genotypes I Ringed seals (Phoca hispida), Harbour No reports in humans to date e Santín et al., 2005; Bass et al., 2012
and II seals (Phoca vituline), Hooded seal
(Cystophora cristata)
Seal genotype III Harp seal (Pagophilus groenlandicus) No reports in humans to date e Bass et al., 2012
Seal genotype IV Southern elephant seal (Mirounga No reports in humans to date e Rengifo-Herrera et al., 2011, 2013
(similar to leonina)
skunk
genotype)
Seal genotype V Weddel seal (Leptonychotes weddellii) No reports in humans to date e Rengifo-Herrera et al., 2013
(Weddell seal
genotype)
Shrew genotype No reports in humans to date e
species/
genotypes
Northern short-tailed shrew (Blarina Torres et al., 2000; Alves et al., 2005;
brevicauda), Wildebeest Feng et al., 2007; Ziegler et al., 2007
(Connochaetes), White-toothed shrew
(Crocidura russula), Common shrew
(Sorex araneus), Masked shrew (Sorex
scinereus), Pygmy shrew (Sorex
minutus), Brewer's mole (Parascalops
brewer), Ermine (Mustela ermine)
Skunk/skunk- Striped skunk (Mephitis mephitis), Has been reported in humans e Xiao et al., 2002b; Zhou et al., 2004;
like genotype Raccoon (Procyon lotor), Eastern grey Feng et al., 2007; Ziegler et al., 2007;
squirrel (Sciurus carolinensis), River Robinson et al., 2008; Chalmers et al.,
otter (Lontra canadensis), Raccoon 2009; Feng et al., 2011b; Rengifo-
(Procyon lotor), Southern elephant seal Herrera et al., 2011; Elwin et al., 2012;
(Mirounga leonina), Raccoon (Procyon Stenger et al., 2015b
lotor), Shunk (Mephitis mephitis),
American red (Tamiasciurus
hudsonicus), Fox squirrel (Sciurus
niger)
Vole genotype Meadow vole (Microtus No reports in humans to date e Feng et al., 2007
pennynsylvanicus)
Wildbeast Black wildbeast (Connochaetos) No reports in humans to date e Alves et al., 2005
genotype
adapted genotypes and unidentified “environmental sequences” like isolates at the 18S locus in marsupials including bandicoots,
which probably represent as yet unidentified wildlife genotypes brushtail possums, eastern grey kangaroos and brush-tailed rock-
and which also highlight the potential for contamination of water wallabies (Hill et al., 2008; Ng et al., 2011; Dowle et al., 2013;
supplies by wildlife (Zhou et al., 2004; Jiang et al., 2005; Yang et al., Vermeulen et al., 2015). However, despite efforts, the identifica-
2008; Jellison et al., 2004; Nichols et al., 2010; Koompapong and tion of C. hominis/C. parvum could not be confirmed at other loci.
Sukthana, 2012; Van Dyke et al., 2012; Xiao et al., 2012; Galv an This might be due to low numbers of oocysts and the multi copy
et al., 2014; Li et al., 2014; Mahmoudi et al., 2015). For example, nature of the 18S rRNA gene. Another study reported a C. hominis-
studies on Cryptosporidium contamination from wildlife from New like sequence at the 18S locus in a wild dingo, but was also unable
York watersheds have shown that wildlife are the major source of to confirm this at other loci (Ng et al., 2011).
Cryptosporidium in protected drinking source water, including Subtyping of C. hominis at the gp60 locus has identified nine
some emerging human pathogens such as C. ubiquitum and chip- subtype families (Ia to Ij) (Ryan et al., 2014). To date, few C. hominis
munk genotype I (Jiang et al., 2005; Feng et al., 2007). subtypes have been reported in wild mammals but include subtype
IbA12G3 in Rhesus macaques, subtype IiA17 in Cynomolgus mon-
3.1. Cryptosporidium in mammals keys and Rhesus monkeys and subtype IfA12G2 in baboons and
Mitumba chimpanzees (Feng et al., 2011b; Karim et al., 2014;
Due to the morphological similarity of Cryptosporidium oocysts Bodager et al., 2015; Parsons et al., 2015).
from different host species, initial findings of Cryptosporidium in- Recently, C. hominis has been identified and enumerated from
fections in wild animals were assumed to be due to C. parvum eastern grey kangaroos and cattle faecal samples from Sydney
leading to an overestimation of the potential role of wildlife as catchments and characterised at multiple loci (Zahedi et al., 2015).
reservoirs of human disease (Appelbeea et al., 2005). However, In that study, C. hominis isolates were typed at three loci (18S, a
with the assistance of advanced molecular techniques, many of novel mucin-like glycoprotein that contains a C-type lectin domain
these species were identified as host-adapted genotypes (Table 2). and the gp60 gene) (Zahedi et al., 2015). The C. hominis IbA10G2
Both wild terrestrial and marine mammals have been studied as subtype was identified in the marsupials and cattle (Zahedi et al.,
potential reservoirs for human-infectious Cryptosporidium species 2015), which is the main subtype associated with outbreaks of
and genotypes using molecular tools (Table 2). The prevalence of cryptosporidiosis by C. hominis (Xiao, 2010).
Cryptosporidium in wild placental mammal hosts has been reported
in detail in a recent review (Feng, 2010) and varies widely between 3.1.2. C. parvum
mammalian hosts. C. parvum was first described in mice (Tyzzer, 1912) and is pri-
marily a parasite of artiodactyls and humans (Xiao, 2010). C. parvum
3.1.1. Cryptosporidium hominis has however been frequently reported in wildlife, infecting a broad
Although humans are the major host species for C. hominis, it range of wild species including various rodents, bovids, camelids,
has been reported in a number of wildlife hosts including a dugong equids, canids, non-human primates and marine mammals
and non-human primates (Table 2) (Xiao et al., 1999; Ye et al., 2012; (Table 2) (Morgan et al., 1999a; Atwill et al., 2001; Perez and Le
Karim et al., 2014; Bodager et al., 2015; Parsons et al., 2015). C. Blancq, 2001; Matsubayashi et al., 2004; Ryan et al., 2004;
hominis/Cryptosporidium parvum-like sequences were identified in Appelbee et al., 2005; Feng et al., 2007; Meireles et al., 2007;
red and black-and-white colobus monkeys in Uganda (Salyer et al., Paziewska et al., 2007; Starkey et al., 2007; Ziegler et al., 2007;
2012). However, typing was obtained using a short fragment of the Go mez-Couso et al., 2012; Ye et al., 2012; Abu Samraa et al., 2013;
Cryptosporidium oocyst wall protein (COWP) gene, which is not Liu et al., 2013; García-Presedo et al., 2013b; Reboredo-Ferna ndez
reliable for differentiating Cryptosporidium species. In Australia, a et al., 2014; Montecino-Latorre et al., 2015; Wells et al., 2015;
number of recent studies have also identified C. hominis/C. parvum- Matsui et al., 2000).
Few studies have identified C. parvum in captive wild mammals lower New York State and referred to it as genotype 3. Since then it
but red deer, fallow deer, addaxes, Arabian oryx, gemsboks, and has been described in a wide variety of hosts worldwide including
sable antelopes are among mammals to be infected with C. parvum humans and was formally described as a species in 2010 (Fayer
in captivity (Perez and Le Blancq, 2001; Ryan et al., 2003; Hajdusek et al., 2010). C. ubiquitum is of public health concern because of
et al., 2004; Abe et al., 2006; Feng et al., 2007; Meireles et al., 2007; its wide geographic distribution and broad host range (Li et al.,
Matsubayashi et al., 2004; Bodager et al., 2015; Wang et al., 2015; 2014). In addition to domestic animals (in particular sheep) and
Zhao et al., 2015a). wildlife, C. ubiquitum has been frequently reported from drinking
Subtyping of C. parvum at the gp60 locus has identified fourteen source water, storm water runoff, stream sediment and wastewater
subtype families (IIa to IIo (Ryan et al., 2014)). Few studies which in various geographic locations, suggesting potential contamina-
identified C. parvum in wild mammals have conducted typing at the tion of water sources with oocysts of C. ubiquitum shed by animals
gp60 locus but a variety of C. parvum subtypes including IIdA15G1, inhabiting water catchments (Nolan et al., 2013; Li et al., 2014). C.
IIdA18G1, IIdA19G1 have been reported from golden takins, lemurs, ubiquitum is considered an emerging zoonotic pathogen (Li et al.,
chipmunks and hamsters, and IIaA15G2R1, IIaA19G2R1, 2014), as it has been identified in many human cases of crypto-
IIaA19G3R1, IIaA19G4R1, IIaA20G3R1, IIaA20G4R1, IIaA20G3R2 and sporidiosis in the United Kingdom, Slovenia, the United States,
IIaA21G3R1 have been reported from deer and Eastern grey kan- Canada, Spain, New Zealand, Venezuela and Nigeria (Charlmers
garoos (Lv et al., 2009; Bodager et al., 2015; Montecino-Latorre et al., 2011; Wong and Ong, 2006; Fayer et al., 2010; Cieloszyk
et al., 2015; Zhao et al., 2015a; Zahedi et al., 2015). These are all et al., 2012; Elwin et al., 2012; Blanco et al., 2015; Qi et al., 2015a).
C. parvum subtypes that have been reported in humans (Xiao, In wildlife, C. ubiquitum has been reported sporadically in ro-
2010). dents, wild ruminants, carnivores, marsupials and primates
(Table 2) (Perez and Le Blancq, 2001; da Silva et al., 2003; Ryan
3.1.3. Cryptosporidium cuniculus et al., 2003; Feng et al., 2007; Feng, 2010; Karanis et al., 2007;
C. cuniculus (previously known as rabbit genotype) was first Ziegler et al., 2007; Wang et al., 2008; Fayer et al., 2010; Cinque
described in rabbits by Inman and Takeuchi (1979), who described et al., 2008; Robinson et al., 2011; Feng et al., 2011b; Abu Samraa
the microscopic detection and ultra-structure of endogenous et al., 2013; Mi et al., 2013; Murakoshi et al., 2013; Li et al., 2014;
Cryptosporidium parasites in the ileum of an asymptomatic female Ma et al., 2014; Perec-Matysiak et al., 2015; Qi et al., 2015a,
rabbit. Molecular characterisation of C. cuniculus was first con- 2015b; Stenger et al., 2015b; Vermeulen et al., 2015).
ducted on rabbit faecal samples from the Czech Republic (Ryan Because C. ubiquitum is genetically distant from C. hominis and
et al., 2003) and C. cuniculus was formally re-described as a spe- C. parvum, until recently, gp60 homologs had not been sequenced.
cies in 2010 (Robinson et al., 2010). Since then, it has been described However, the gp60 gene of C. ubiquitum was identified by whole-
from rabbits across a wide geographic area including Australia, genome sequencing and six subtype families (XIIaeXIIf) within
China, the UK, the Czech Republic, Poland, France and Nigeria (Ryan C. ubiquitum were identified (Li et al., 2014). Application of this new
et al., 2003; Nolan et al., 2010; Shi et al., 2010; Chalmers et al., 2011; tool to human, animal, and environmental (water) isolates has
Zhang et al., 2012; Nolan et al., 2013; Liu et al., 2014; Koehler et al., suggested that sheep and rodents are a key source of C. ubiquitum
2014; Puleston et al., 2014; Zahedi et al., 2015). C. cuniculus has a transmission to humans, through either direct human contact with
close genetic relationship with C. hominis and its zoonotic potential infected animals or by contamination of drinking source water (Li
became clear in 2008, when it was responsible for a drinking-water et al., 2014). For example, in the US, all C. ubiquitum specimens
associated outbreak of cryptosporidiosis in the UK (Chalmers et al., from humans characterized belonged to the same subtype families
2009; Robinson et al., 2011; Puleston et al., 2014) and has also been found in wild rodents in the US (XIIb, XIIc and XIId) (Li et al., 2014).
identified in many sporadic human cases of cryptosporidiosis However, as persons in the United States usually have little direct
(Robinson and Chalmers, 2011; Chalmers et al., 2011; Elwin et al., contact with wild rodents, the authots concluded that transmission
2012; Koehler et al., 2014). It is also the third most commonly of C. ubiquitum to humans from rodents was likely to come from
identified Cryptosporidium species in patients with diarrhoea in the drinking untreated water contaminated by wildlife (Li et al., 2014).
UK (Chalmers et al., 2011). Subtyping at the gp60 locus has iden-
tified two distinct subtype families, designated Va and Vb 3.1.5. Cryptosporidium muris
(Chalmers et al., 2009). Most cases described in humans relate to C. muris is a gastric parasite and was first identified in the gastric
clade Va and the first waterborne outbreak was typed as VaA22 glands of mice in 1907 by Tyzzer (1907). Since then, molecular tools
(Robinson et al., 2008; Chalmers et al., 2009). C. cuniculus has been have shown that it has a wide host range, including various
reported in rabbits and humans (subtypes VaA9eVaA22 and mammals (rodents, canids, felids, suids, giraffida, equids, non-
VbA20eVbA37 e see Wang et al., 2012) but has recently been human primates and marsupials) and birds (Tables 1 and 2). C.
identified in marsupials (subtype VbA26) (and a human e subtype muris is considered a zoonotic species as there have been numerous
VbA25) in Australia (Nolan et al., 2013; Koehler et al., 2014). The reports of C. muris in humans and one report in human sewage
widespread occurrence of C. cuniculus genotypes in rabbits and the (Guyot et al., 2001; Gatei et al., 2002; Tiangtip and Jongwutiwes,
fact that it has been now been identified in marsupials in Australia 2002; Gatei et al., 2003; Palmer et al., 2003; Gatei et al., 2006;
suggests that C. cuniculus might be a species more ubiquitous than Leoni et al., 2006; Muthusamy et al., 2006; Azami et al., 2007; Al-
previously thought, and might be able to spread to other mammals Brikan et al., 2008; Neira et al., 2012; Hasajov a et al., 2014; Pet-
as well as humans. Therefore, there is a need to diligently monitor rincova et al., 2015; Spanakos et al., 2015; Hurkova et al., 2003).
for C. cuniculus in the vicinity of drinking water catchments and in In a recent human infectivity study, C. muris was examined in six
drinking water. healthy adults (Chappell et al., 2015). Volunteers were challenged
with 105 C. muris oocysts and monitored for 6 weeks for infection
3.1.4. Cryptosporidium ubiquitum and/or illness. All six patients became infected. Two patients
C. ubiquitum (previously cervine genotype, cervid, W4 or ge- experienced a self-limited diarrhoeal illness. C. muris oocysts shed
notype 3) was first identified by Xiao et al. (2000) in storm water during the study ranged from 6.7 106 to 4.1 108, and C. muris-
samples in lower New York State (storm water isolate W4, GenBank infected subjects shed oocysts longer than occurred with other
accession no. AF262328). Subsequently, Perez and Le Blancq (2001) species studied in healthy volunteers. Three volunteers shed oo-
identified this genotype in white-tailed deer-derived isolates from cysts for 7 months (Chappell et al., 2015). The authors concluded
that healthy adults are susceptible to C. muris, which can cause mild and II) (Table 2) (Morgan et al., 1997; Power et al., 2004, 2005;
diarrhoea and result in persistent, asymptomatic infection Power and Ryan, 2008; Ryan et al., 2008; Nolan et al., 2010;
(Chappell et al., 2015), which confirms the zoonotic status of Power, 2010; Ng et al., 2011a; Yang et al., 2011; Ryan and Power,
C. muris and highlights the public health risks of finding C. muris in 2012; Nolan et al., 2013; Vermeulen et al., 2015; Zahedi et al.,
wildlife in drinking water catchments. 2015). Neither of these species is associated with diarrhoea in
their marsupial hosts (Ryan and Power, 2012). C. macropodum has
3.1.6. Cryptosporidium andersoni not been reported in humans but cryptosporidiosis caused by
Like C. muris, C. andersoni is also a gastric parasite and primarily C. fayeri has been reported in a 29-year-old female patient in
infects the abomasum of cattle and to a lesser extent, sheep and Australia (Waldron et al., 2010). The woman was immuno-
goats (Ryan et al., 2014; Wang et al., 2012). C. andersoni produces competent but suffered prolonged gastrointestinal illness. The pa-
oocysts that are morphologically similar to, but slightly smaller tient resided in a national forest on the east coast of New South
than those of C. muris (7.4e8.8 5.8e6.6 mm vs Wales, Australia, an area where marsupials are abundant. She had
8.2e9.4 6.0e6.8 mm, respectively) and was originally mistakenly frequent contact with partially domesticated marsupials (Waldron
identified in cattle as C. muris based on its oocyst size. In 2000, it et al., 2010). Identification of C. fayeri in a human patient is a
was described as a new species based on the location of endoge- concern for water catchment authorities in the Sydney region. The
nous stages in the abomasum, its host range, and genetic distinct- main water supply for Sydney, Warragamba Dam, covers 9050 km2
ness at multiple loci (Lindsay et al., 2000). It has only occasionally and is surrounded by national forest inhabited by diverse and
being detected in wild animals (Table 2) (Ryan et al., 2004; Wang abundant marsupials. At the gp60 locus, the subtype family IV has
et al., 2008, 2015; Lv et al., 2009; Feng et al., 2010; Zhao et al., been identified with 6 subtypes (IVaeIVf) (Power et al., 2009).
2015a). Several studies have reported that C. andersoni is the Subtyping of the human-derived isolate of C. fayeri identified
dominant species in source and tap water (Feng et al., 2011; Nichols IVaA9G4T1R1, which has also been identified in eastern grey kan-
et al., 2010), suggesting that cattle may be the primary source of garoos in Warragamba Dam, suggesting possible zoonotic trans-
contamination. Interestingly, in a recent study, it was found at a mission (Power, 2010; Waldron et al., 2010).
prevalence of 15.6% (19/122) and 0.5% (1/200) in captive and wild In addition to C. fayeri and C. macropodum, there have been
giant pandas, respectively in China (Wang et al., 2015). It is occa- several other host-adapted genotypes identified in Australian
sionally detected in humans (Leoni et al., 2006; Morse et al., 2007; marsupials. Possum genotype I has been described in brushtail
Waldron et al., 2011; Agholi et al., 2013; Jiang et al., 2014; Liu et al., possums, a host species found in a range of habitats throughout
2014). Two studies in China by the same research group have re- Australia (Hill et al., 2008) and the novel kangaroo genotype I in
ported that C. andersoni was the most prevalent Cryptosporidium western grey kangaroos (Yang et al., 2011). Possum genotype I and
species detected in humans (Jiang et al., 2014; Liu et al., 2014). kangaroo genotype I have not been reported in humans or other
However, further research is required to better understand the animals and their zoonotic potential is unknown.
zoonotic importance of C. andersoni.
3.1.10. Cryptosporidium meleagridis
3.1.7. Cryptosporidium canis Although primarily a bird parasite (see section 3.2.1 and
C. canis (previously dog genotype 1) was first identified as the Table 3), C. meleagridis has been identified in deermice, mountain
dog genotype by Xiao et al. (1999) and described as a species in gorillas and marsupials (Feng et al., 2007; Sak et al., 2014;
2001 (Fayer et al., 2001), on the basis that C. canis oocysts were Vermeulen et al., 2015). It is also the third most prevalent species
infectious for calves but not mice and were genetically distinct from infecting humans (Morgan et al., 2000; Cama et al., 2003; Gatei
all other species. C. canis and its sub-genotypes (C. canis fox geno- et al., 2006; Muthusamy et al., 2006; Leoni et al., 2006; Berrilli
type and C. canis coyote genotype) have been reported in dogs, et al., 2012; Elwin et al., 2012; Neira et al., 2012; Silverlås et al.,
foxes and coyotes (Table 2) (Xiao et al., 2002a; Zhou et al., 2004; 2012; Kurniawan et al., 2013; Sharma et al., 2013; Wang et al.,
Fayer, 2010; Feng, 2010). C. canis has also been reported world- 2014; Adamu et al., 2014; Ghaffari and Kalantari, 2014; Ryan and
wide in humans (Lucio-Forster et al., 2010; Fayer, 2010; Elwin et al., Xiao, 2014; Ghaffari and Kalantari, 2014; Rahmouni et al., 2014;
2012; Mahmoudi et al., 2015; Parsons et al., 2015). Wang et al., 2014; Stensvold et al., 2014, 2015). In some studies,
C. meleagridis prevalence is similar to that of C. parvum (Gatei et al.,
3.1.8. Cryptosporidium erinacei 2002; Cama et al., 2007). The ability of C. meleagridis to infect
Little is known about epidemiology and pathogenicity of zoo- humans and other mammals, and its close relationship to C. parvum
notic C. erinacei in wildlife. C. erinacei (previously known as and C. hominis at multiple loci, has led to the suggestion that
hedgehog genotype) was first identified morphologically in a mammals actually were the original hosts, and that the species has
captive four-toed hedgehog (Ateletrix albiventris) in 1998 (Graczyk later adapted to birds (Xiao et al., 2002a,). Subtyping at the gp60
et al., 1998). An isolate from a European hedgehog originating locus has identified seven subtype families (IIIa to IIIg) (Stensvold
from Denmark was typed in 2002 (Enemark et al., 2002) and shown et al., 2015). More details on transmission dynamics will be dis-
to be distinct. Subsequent studies have identified C. erinacei in cussed in section 3.2.1.
hedgehogs, horses and humans (Dyachenko et al., 2010; Laatamna
et al., 2013; Kv
ac et al., 2014a, 2014b; Meredith and Milne, 2009). At 3.1.11. Other Cryptosporidium species and genotypes reported in
the gp60 locus, C. erinacei isolates are identified as subtype family wild mammals
XIII (Dyachenko et al., 2010; Laatamna et al., 2013; Lv et al., 2009; A number of other Cryptosporidium species and genotypes have
Kvac et al., 2014b). Previously reported C. erinacei subtypes been identified in wildlife (Table 2). Most are host-adapted geno-
include XIIIaA20R10 (KF055453), XIIIaA21R10 (GQ214085), types that are not of public health significance, however several
XIIIaA22R9 (KC305644), XIIIaA19R12 (GQ214081), and XIIIaA22R11 have been identified in humans (Table 2). Of these, the chipmunk
(GQ259140) Kva c et al., 2014b). genotype I is considered an emerging human pathogen (Jiang et al.,
2005; Feltus et al., 2006; Feng et al., 2007; ANOFEL, 2010;
3.1.9. Cryptosporidium fayeri and Cryptosporidium macropodum Insulander et al., 2013; Lebbad et al., 2013; Guo et al., 2015). At
The two main species identified in a wide range of marsupials the gp60 locus, 15 different subtypes have been identified but
are C. fayeri and C. macropodum (previously marsupial genotype I subtypes differ only in the number of tandem repeats (TCA/TCG/
Table 3
Cryptosporidium species and genotypes in avian hosts confirmed by molecular analysis (Modified from Ryan and Xiao, 2014).
Species name Major host(s) Site of References

infection
C. meleagridis Turkey (Meleagris gallopavo), Indian ring-necked parrot (Psittacula Intestine Morgan et al., 2000; Glaberman et al., 2001; Abe and Iseki, 2004; Abe
kameri), Red-legged partridge (Alectoris rufa), Cocktails (Nymphicus and Makino 2010; Wang et al., 2010; Qi et al., 2011; Berrilli et al.,
hollandicus), Bohemian waxwing (Bombycilla garrulous), Rufousturle 2012; Wang et al., 2012; Baroudi et al., 2013; Wang et al., 2014;
dove (Streptopelia orientalis), Fan-tailed pigeon (Columba livia), Koompapong et al., 2014; Maca and Pavlasek, 2015; Reboredo-
Chicken (Gallus gallus), Quails (Coturnixcoturnix japonica), Pekin Fernandez et al., 2015
ducks (Anas platyrhynchos), Domestic Pigeons (Columba livia
domestica), European turtle dove (Streptopelia turtur), Red-legged
partridge (Alectoris rufa)
C. baileyi Turkey (Meleagris gallopavo), Chicken (Gallus gallus), Brown squail Cloaca, bursa, Morgan et al., 2001; Abe and Iseki, 2004; Ng et al., 2006; Huber et al.,
(Synoicus australis), Cocktails (Nymphicus hollandicus), Whooping trachea 2007; Kimura et al., 2004; Nakamura et al., 2009; Abe and Makino,
crane (Grus vipio), Grey-bellied bulbul (Pycnonotus spp.), Black 2010; Wang et al., 2010; Qi et al., 2011; Wang et al., 2012; Baroudi
vulture (Coragyps atratus), Saffron finch (Sicalis flaveola), Mixed-bred et al., 2013; Baines et al., 2014; Hamidinejat et al., 2014; Wang et al.,
falcons (Falcorusticolus x Falco cherrug), Reddy Shelduck 2014; Li et al., 2015c; Maca and Pavalasek, 2015
(Tadornaferruginea), Red-billed leiothrixes (Leiothrix lutea), Pekin
ducks (Anas platyrhynchos), Buffy-fronted seedeater (Sporophila
frontalis), Javva sparrows (Padda oryzivora), Mynas (Acridotheres
tristis), Zebra finches (Taeniopygia guttata), Crested Lark (Galerida
cristana), Gouldian finch (Chloebia gouldiae), Black-billed magpie (Pica
pica), Ostriches (Struthio camelus), Quails (Coturnixcoturnix japonica),
Red grouse (Lagopus lagopus scotica), Red-crowned crane (Grus
japonenis)
C. galli Chicken (Gallus gallus), Finches (Spermestidae and Fringillidae), Preventriculus Ryan et al., 2003; Ng et al., 2006; Antunes et al., 2008; Nakamura
Capercaille (Tetrao urogallu), Pine grosbeak (Pinicola enuncleator), et al., 2009; da Silva et al., 2010; Qi et al., 2011; Nakamura et al., 2014
Turqoise parrots (Neophema pulchella), Cuban flamingo
(Phoenicopterus ruber ruber), Rhinoceros hornbill (Buceros rhinoceros),
Red-cowled cardinal (Paroaria dominicana), Zebra finches
(Taeniopygia guttata), Chocolate parson finches (Peophila cincta),
Chesnut finches (Lonchura castaneothorax), Painted firetali finches
(Ebmlema picta), Canaries (Serinus sp.), Glosters (Serinus canaria),
Green-winged saltatros (Saltator similis), Slate-collard seedeater
(Sporophila schistaceca), Great-billed seed-fench (Oryzoborus
maximiliani), Ultermarine grosbeak (Cyanocompsa brissonii),
Bohemian waxwing (Bombycilla garrulous), Silver-eared Mesia
(Leiothrix argentauris), Cockatiel (Nymphicus hollandicus), Chopi
blackbird (Gnorimopsar chopi), Green-winged saltator (Saltator
similis), Rufous-collared sparrow (Zonotrichia capensis)
Avian Red factor canary (Serinus canaria), Canary (S. canaria), Indian e Ng et al., 2006; Nakamura et al., 2009
genotype I peafowl (Pavo cristatus)
Avian Eclectus (Eclectus roratus), Galah (Eolophus roseicapilla), Cockatiel e Meireles et al., 2006; Ng et al., 2006; Nakamura et al., 2009; Seva
genotype (Nymphicus hollandicus), Major Mitchel Cockatoo (Cavcatua lead et al., 2011; Nguyen et al., 2013
II beater), Ostriches (Struthio camelus), White-eyed parakeet (Aratinga
leucophthalma)
Avian Galah (Eolophus roseicapilla), Cockatiel (Nymphicus hollandicus), Java e Ng et al., 2006; Nakamura et al., 2009; Makino et al., 2010;
genotype sparrow (Padda oryzivora), Son conure (Aratinga solstitialis), Peach Koompapong et al., 2014; Nakamura et al., 2014; Ravich et al., 2014;
III faced lovebirds (Agapornis roseicollis), Seagull (Laridae sp), Blue- Li et al., 2015c; Gomes et al., 2012
fronted amazon (Amazona aestival), Cockatiel (Nymphicus
hollandicus), Rufous-collared sparrow (Zonotrichia capensis), Lovebird
(Agapornis species), Cockatiel (Nymphicus hollandicus)
Avian Japanese white-eye (Zosterops japonica) e Abe and Makino, 2010; Qi et al., 2011
genotype
IV
Avian Cockatiel (Nymphicus hollandicus), Budgerigar (Melopsittacus e Abe and Makino, 2010; Qi et al., 2011; Zhang et al., 2015
genotype undulates)
V
Duck Black dock (Anus rubripes), Canada geese (Branta canadensis) e Jellsison et al., 2004; Zhou et al., 2004
genotype
Eurasian Eurasian woodcock (Scolopax rusticola) e Ryan et al., 2003; Ng et al., 2006
woodcock
genotype
Goose Canada geese (Branta canadensis) e Xiao et al., 2002b; Jellison et al., 2004; Zhou et al., 2004
genotype I
Goose Canada geese (Branta canadensis) e Jellison et al., 2004; Zhou et al., 2004
genotype
II
Goose Canada geese (Branta canadensis) e Jellison et al., 2004
genotype
III
genotype
IV
genotype
V
TCT) and comprise a single subtype family (XIVa). Analysis in- 3.2.3. Cryptosporidium galli
dicates that subtypes from humans and wildlife are genetically Unlike other avian species, C. galli is a gastric species with
similar and zoonotic transmission might play a potential role in endogenous developmental stages occurring in the glandular
human infections (Guo et al., 2015). The skunk and mink genotypes epithelial cells of the proventriculus (Pavl
asek, 1999, 2001; Ryan
have also been reported in a few human cases of cryptosporidiosis et al., 2003; Ng et al., 2006; Ryan and Xiao, 2014). It predomi-
(Robinson et al., 2008; Chalmers et al., 2009; Rengifo-Herrera et al., nantly infects birds of the family Spermestidae, Fringilidiae and
2011; Elwin et al., 2012; Ng-Hublin et al., 2013; Ebner et al., 2015). domestic chickens (Gallus gallus), and seems to be more prevalent
among songbirds (Table 3). Successful experimental cross-
transmission of C. galli to other chickens have been reported,
3.2. Cryptosporidium in birds however the full extent of its host range is still unknown (Ryan,
2010). It has not been reported in humans.
The mobility of migratory birds, together with their distribution
and ability to form large colonies, makes them potentially suitable 3.2.4. Other Cryptosporidium species and genotypes reported in
to spread pathogens. Due to their easy access to drinking water birds
catchments and other water sources, wild birds are believed to be a In addition to C. meleagridis, other zoonotic species of Crypto-
potential risk to drinking water safety. The epidemiology of avian sporidium reported in birds include C. hominis, C. parvum, C muris
cryptosporidiosis, in particular zoonotic Cryptosporidium species and C. andersoni (Zylan et al., 2008; Jellison et al., 2009; Ryan, 2010;
infecting birds is therefore of public health importance. Currently Reboredo-Fernandez et al., 2015; Gomes et al., 2012). In addition,
only three avian Cryptosporidium spp. are recognised; twelve genotypes; avian genotypes IeV, the black duck genotype,
C. meleagridis, C. baileyi and C. galli (Table 3) (Ryan and Xiao, 2014). the Eurasian woodcock genotype and goose genotypes IeV have
been reported (Table 3). To date, there is no evidence of human
3.2.1. C. meleagridis cryptosporidiosis caused by these genotypes.
C. meleagridis infects the intestinal (small and large intestine and
bursa) epithelial cells of a wide range of birds (Table 3) (Ryan and 3.3. Cryptosporidium in fish and marine mammals
Xiao, 2014). It was first detected in a wild turkey (Meleagris gallo-
pavo) by Tyzzer in 1929, but named as a valid Cryptosporidium Cryptosporidium has been described in both fresh and marine
species in 1955 (Slavin, 1955). C. meleagridis oocysts have been water piscine species with parasitic stages located either on the
experimentally infected into broiler chickens, ducks, turkeys, stomach or intestinal surface, or deep within the epithelium
calves, pigs, rabbits, rats and mice (Darabus and Olariu, 2003; Ryan (Table 4). The first account of Cryptosporidium in a piscine host was
and Xiao, 2014). It has also been reported as one of the most Cryptosporidium nasorum, identified in a Naso tang, a tropical fish
commonly detected human-infectious Cryptosporidium species in species (Hoover et al., 1981). However, currently only three species
wastewater (Feng et al., 2007, 2011a; Li et al., 2012). are recognized; C. molnari, C. scophthalmi and C. huwi (previously
Molecular analysis has revealed that C. meleagridis has relatively known as piscine genotype I) (Alvarez-Pellitero and Sitja-Bobadilla,
low host specificity, and many C. meleagridis subtypes at other loci 2002; Alvarez-Pellitero et al., 2004; Palenzuela et al., 2010; Costa
have been found in both birds and humans and both anthroponotic et al., 2015; Ryan et al., 2015), none of which have been reported in
and zoonotic transmission routes have been suggested (Cama et al., humans. In fish hosts, Cryptosporidium fish species and genotypes
2003; Elwin et al., 2012; Silverlås et al., 2012). Subtyping at the are typically located either in the stomach or intestine and the
gp60 locus has identified seven subtype families (IIIaeIIIg) and the parasite can cause clinical manifestations, such as emaciation,
likely occurrence of cross-species transmission of C. meleagridis decrease in growth rate, anorexia, whitish faeces, abdominal
between birds and humans (Wang et al., 2014). Human volunteer swelling, and ascites (Alvarez-Pellitero et al., 2004; Ryan et al.,
studies have shown that healthy adults can be infected and become 2015). Most studies on Cryptosporidium in fish have been re-
ill from ingestion of C. meleagridis oocysts (Chappell et al., 2011). In ported in farmed or aquarium fish (Table 4) and little data are
the study by Chappell et al., five volunteers were challenged with currently available regarding the molecular identification of Cryp-
105 C. meleagridis oocysts and monitored for six weeks for faecal tosporidium species and genotypes in wild fish populations and, in
oocysts and clinical manifestations. Four volunteers had diarrhoea; particular, in edible fish (Palenzuela et al., 2010; Reid et al., 2010;
three had detectable faecal oocysts; and one infected volunteer Barugahare et al., 2011; Gibson-Keuh et al., 2011; Koinari et al.,
remained asymptomatic. All infections were self-limited and oo- 2013; Certard et al., 2015).
cysts were cleared within 12 days of challenge (Chappell et al., In addition to the three recognized species of Cryptosporidium in
2011). piscine hosts, numerous Cryptosporidium species and genotypes
have been reported in fish including; piscine genotypes 2 to 8, un-
named novel genotypes (n ¼ 5), rat genotype III, C. parvum,
3.2.2. Cryptosporidium baileyi C. hominis, C. xiaoi and C. scrofarum (Table 4). Of these, only
C. baileyi is generally associated with the respiratory form of C. parvum, C. hominis and C. scrofarum are of public health interest.
cryptosporidiosis in birds and has been predominantly reported in Cryptosporidium scrofarum was identified in a whiting (Reid et al.,
broiler chickens. Compared to C. meleagridis, C. baileyi is capable of 2010); C. parvum was found in School whiting, Nile tilapias, a Sil-
infecting a larger spectrum of avian hosts (Table 3), targeting ver barb, Arctic char and European whitefish and C. hominis was
various sites of infection mostly associated with digestive and reported in Mackerel scad (Reid et al., 2010; Gibson-Kueh et al.,
respiratory tracts (Ryan and Xiao, 2014). Experimental cross- 2011; Koinari et al., 2013; Certad et al., 2015). In one of the most
transmission of C. baileyi to other birds has been successfull, recent studies, C. parvum was identified in freshwater fish from
however there has been no reports of cross-transmission between Lake Geneva (Lac Le man) by both histology and molecular analysis
birds and other vertebrates (Lindsay and Blagburn, 1990; Cardozo (Certad et al., 2015). In that study, the overall prevalence of Cryp-
et al., 2005), except for a single unsubstantiated report of human tosporidium was 36.6% (15/41); the prevalence of C. parvum and
infection with C. baileyi which did not include any molecular C. molnari was 86.7% (13/15) and 6.7% (1/15), respectively, while
analysis (Ditrich et al., 1991). Therefore, C. baileyi is not considered 6.7% (1/15) were mixed C. parvum and C. molnari infections (Certad
to be of public health significance. et al., 2015). Histological analysis identified C. parvum
Table 4
Cryptosporidium sp. reported in fish using molecular tools (modified from Ryan et al., 2014).
Species Host Site of Reference

infection
C. molnari Gilthead sea bream (Sparus aurata), European sea bass (Dicentrarchus labrax), Murray Stomach Palenzuela et al., 2010; Barugahare
cod (Maccullochella peelii peelii) (and et al., 2011; Certad et al., 2015
intestine)
C. scophthalmi Turbot (Scophthalmus maximus) Intestine Costa et al., 2015
C. huwi (previously piscine Guppy (Poecilia reticulata) Stomach Ryan et al., 2004; Ryan et al., 2015
genotype 1)
Piscine genotype 2 Angelfish (Pterophyllum scalare) Stomach Murphy et al., 2009
Piscine genotype 3 Mullet (Mugil cephalus) Intestine Reid et al., 2010
Piscine genotype 4 Golden algae eater (Crossocheilus aymonieri), Kupang damsel (Chrysiptera Intestine Reid et al., 2010; Morine et al., 2012
hemicyanes), Oscar fish (Astronatus ocellatis), Neon tetra (Paracheirodon innesi)
Piscine genotype 5 Angelfish (Pterophyllum scalare), Butter bream (Monodactylidae), Golden algae eater e Zanguee et al., 2010
(Crossocheilus aymonieri)
Piscine genotype 6/genotype Guppy (Poecilia reticulata), Gourami (Trichogaster trichopterus) e Zanguee et al., 2010; Morine et al.,
6-like 2012
Piscine genotype 7 Red eye tetra (Moenkhausia sanctaefilomenae) e Morine et al., 2012
Piscine genotype 8 Oblong silver biddy (Gerres oblongus) e Koinari et al., 2013
Rat genotype III, C. hominis, C. Whiting (Sillago vittata), Barramundi (Lates calcarifer), Arctic char (Salvelinus alpinus), e Reid et al., 2010; Gibson-Kueh et al.,
parvum, C. xiaoi and Nile tilapias (Oreochromis niloticus), Silver barb (Puntius gonionotus), Mackerel scad 2011; Koinari et al., 2013; Certad et al.,
C. scrofarum (Decapterus macarellus), European whitefish (Coregonus lavaretus), School whiting 2015
(Sillago vittata)
Novel un-named genotypes Orange clownfish (Amphiprion percula), Azure damsel (Chrysiptera hemicyanea), Blue e Yang et al., 2015
(n ¼ 5) tang (Paracanthurus hepatus), Platyfish (Xiphophorus maculatus), Oscar (Astronotus
ocellatus), Goldfish (Carassius auratus)
developmental stages in the stomach and intestine suggesting that identified in cattle (Azami et al., 2007; Chen and Qiu, 2012). A new
C. parvum was infecting the fish, rather than being passively carried intestinal species, Cryptosporidium ducismarci (tortoise genotype II)
which has important public health implications. has been reported in several species of tortoises, snakes and lizards
Subtyping of Cryptosporidium isolates in fish has identified (Traversa, 2010). Because only molecular data are presented, this
C. parvum subtype IIaA18G3R1 in School whiting from Australia species is regarded as a nomen nudum, pending the support of
(Reid et al., 2010), three C. parvum subtypes (IIaA14G2R1, morphological and biological data.
IIaA15G2R1 and IIaA19G4R1) in Nile tilapia, silver barb and mack- C. parvum, C. muris and Cryptosporidium tyzzeri are also
erel scad and a C. hominis subtype (IdA15G1) in mackerel scad in commonly reported in reptiles, particularly snakes but this is
Papua New Guinea (Koinari et al., 2013), and C. parvum subtypes thought to be due to mechanical transmission due to predation of
IIaA15G2R1, IIaA16G2R1 and IIaA17G2R1 in Arctic char and Euro- infected rodents and is not thought to present a substantial zoo-
pean whitefish from France (Certad et al., 2015). All of these notic risk (Morgan et al., 1999; Xiao et al., 2004b; Pedraza-Diaz
C. parvum subtypes are zoonotic and commonly found in cattle and et al., 2009; Díaz et al., 2013; da Silva et al., 2014). In addition,
humans (Xiao, 2010). The identification of the C. hominis subtype various host-adapted genotypes have been identified including
probably reflects human sewage contamination of the water. tortoise genotype I and snake genotypes I and II (cf. Ryan and Xiao,
Clearly further studies in this area are required to better understand 2014), which have not been reported in humans (Table 5) (Xiao
the transmission dynamics of Cryptosporidium in fish. et al., 2004b; Pedraza-Diaz et al., 2009; Traversa, 2010; Seva Ada
et al., 2011; Richter et al., 2011; Rinaldi et al., 2012; da Silva et al.,
3.4. Cryptosporidium in amphibians and reptiles 2014; Abe and Matsubara, 2015). There is also a single report of
avian genotype V from green iguanas (Iguana inguana) (Kik et al.,
Little is known about Cryptosporidium species infecting am- 2011).
phibians. Of the three orders of amphibians; Anura, Caudata and
Gymnophonia, Cryptosporidium has been only reported in Anura 4. The role of urbanisation in the transmission of zoonotic
which includes frogs and toads and only one species, C. fragile is Cryptosporidium species from wildlife
recognised (Table 5) (Jirku et al., 2008). In transmission experi-
ments, C. fragile was not infective in one fish species (Poecilia The risk of waterborne outbreaks of cryptosporidiosis depends
reticulate), four amphibian species (Bufo bufo, Rana temporaria, on a complex interplay of factors, associated with both the envi-
Litoria caerulea and Xenopus laevis), one species of reptile (Pan- ronment and the biology and ecology of host and parasite. Cryp-
therophis guttatus) and SCID mice (Jirk u et al., 2008). This species tosporidium detection in an animal faecal sample does not
has not been reported in humans. necessarily mean active infection in the host, nor does this guar-
Cryptosporidium infections are ubiquitous in reptiles and have antee that the parasite prevalence and the host-population dy-
been reported in more than 57 reptilian species (O'Donoghue, 1995; namics are conducive to an outbreak. For these reasons the
Ryan and Xiao, 2014). Unlike in other animals in which Crypto- epidemiological potential of detection of Cryptosporidium in wild-
sporidium infection is usually self-limiting in immunocompetent life cannot be easily and fully extrapolated. An increased epidemi-
individuals, cryptosporidiosis in reptiles is frequently chronic and ological risk, however, can be identified when there is an overlap
sometimes lethal in some snakes. Both intestinal and gastric between humans and the distribution and dispersal of animal
cryptosporidiosis has been described in snakes and lizards. To date, hosts. This is largely due to human encroachment into wildlife-
two species are recognised; C. serpentis (gastric) and C. varanii populated areas, which, by extension, also includes conversion of
(C. saurophilum) (intestinal) (Levine, 1980; Pavlasek et al., 1995; natural environments to drinking water catchments. Similarly, ur-
Koudela and Modry, 1998; Pavla sek and Ryan, 2008); neither of ban environments may also represent attractive new habitats for
which have been reported in humans, but C. serpentis has been animals harbouring zoonotic Cryptosporidium spp. Thus, it is clear
Table 5
Amphibian and reptile Cryptosporidium species and genotypes and their hosts confirmed by molecular analyses (modified from Ryan et al., 2014).
Species/genotype Amphibian/Reptile host species Site of infection Reference
C. fragile Black-spined toads (Duttaphrynus melanostictus) Stomach Jirk

u et al., 2008
C. serpentis Amazon tree boa (Corallus hortulanus), Black rat Stomach Kimbell et al., 1999; Morgan et al., 1999b; Hajdusek
snake (Elaphe obsoleta obsolete), Bornmueller's et al., 2004; Xiao et al., 2004b; Pedraza-Díaz et al.,
viper (Vipera bornmuelleri), Bull snake (Pituophis 2009; Richter et al., 2011; Seva -Ada et al., 2011;
melanoleucus melanoleucus), California kingsnake Rinaldi et al., 2012; Díaz et al., 2013; da Silva et al.,
(Lampropeltis getulus californiae), Cornsnake (Elaphe 2014; Abe and Matsubara, 2015
guttata guttata), Common death adder (Acanthophis
antarticus), Desert monitor (Varanus griseus),
Eastern/Mainland Tiger snake (Notechis scutatus),
Frilled lizard (Chlamydosaurus kingui), Giant
madagascar or Oustalet's chameleon (Chamaeleo
oustaleti), Leopard gecko (Eublepharis macularius),
Mexican black kingsnake (Lampropeltis getulus
nigritus), Milk snake (Lampropeltis triangulum),
Mountain viper (Vipera wagneri), Python (Python
molurus), Savannah monitor (Varanus
exanthematicus), Skink (Mabuya perrotetii), Taipan
(Oxyuranus scutellatus), Red-tailed boa (Boa
constrictor constrictor), Rainbow boa (Epicrates
cenchria cenchria)
C. varanii African fat-tailed gecko (Hemitheconyx Intestine and Cloaca Koudela and Modry, 1998; Morgan et al., 1999b;
caudicinctus), Leopard gecko (Eublepharis Hajdusek et al., 2004; Xiao et al., 2004b; Plutzer and
macularius), Boa constrictor (Boa constrictor), Karanis, 2007; Pedraza-Díaz et al., 2009; Richter
Cornsnake (Elaphe guttata guttata), Leopard gecko et al., 2011; da Silva et al., 2014; Abe and Matsubara,
(Eublepharis macularius), Desert monitor (Varanus 2015
griseus), Gecko (Gekkoninae sp.), Green iguana
(Iguana iguana), Lampropeltis sp; Louisiana pine
snake (Pituophis ruthveni), Plated lizard
(Gerrhosaurus sp.), Schneider's Skink (Eumeces
schneideri), Taipan (Oxyuranus scutellatus), Baron's
green racer (Philodryas baroni), Yellow anaconda
(Eunectes notaeus), Cornsnake (Elaphe guttata
guttata), Mato Grosso lancehead (Bothrops
matogrossensis)
Lizard genotype/C. serpentis-like Leopard gecko (Eublepharis macularius), Cornsnake e Xiao et al., 2004b; Richter et al., 2011, Abe and
(Pantherophis guttatus), Chinese wonder gecko Matsubara, 2015
(Teratoscincus scincus)
Tortoise genotype I Indian star tortoises (Geochelone elegans), Herman's Stomach Xiao et al., 2002b, 2004b, Alves et al., 2005; Pedraza-
tortoise (Testudo hermanii), Ball python (Python Díaz et al., 2009; Griffin et al., 2010; Richter et al.,
regius), Russian tortoise (Agrionemys [Testudo] 2012
horsfieldii)
Tortoise genotype II (C. duismarci) Marginated tortoise (Testudo marginata), Ball Intestine Traversa et al., 2008; Pedraza-Díaz et al., 2009;
python (Python regius), Veiled chameleon Griffin et al., 2010; Traversa, 2010; Richter et al.,
(Chamaeleo calyptratus), Pancake tortoise 2012
(Malacochersus tornieri), Russian tortoise
(Agrionemys [Testudo] horsfieldii)
Snake genotype I New Guinea Viper boa (Candoia asper), Japanese e Xiao et al., 2002b; Kuroki et al., 2008
grass snakes (Rhabdophis tigris) e
Snake genotype II Boa constrictor (Boa constrictor ortoni) Xiao et al., 2004b
that wildlife-associated Cryptosporidium is an increasing concern (Feng et al., 2007; Kv ac et al., 2008; Ziegler et al., 2007; Stenger
for cryptosporidiosis in humans. et al., 2015b), and because they frequently share habitats with
During the last 100 years in many countries of the world, there humans they may be a significant reservoir of human infection.
have been dramatic changes in natural/rural landscapes due to Squirrels can reach relatively high densities in suitable habitats,
urbanization (Mackenstedt et al., 2015). Although urbanization is resulting in high rates of environmental loading of Cryptosporidium
one of the leading causes of species extinction (McKinney, 2006), oocysts (Atwill et al., 2001). For example, California ground squir-
for adaptable species, urban and periurban areas can be very rels can reach densities as high as 92 adults hectare1 (Owings
attractive due to increased food and water resources (waste food, et al., 1977; Boellstorff and Owings, 1995), which when combined
pet food, garden produce, water tanks etc) (Mackenstedt et al., with shedding of up to 2 105 oocysts animal1 day1 results in
2015). In these environments, wildlife species may reach far rates of environmental loading equivalent to
higher population densities than in more natural or rural land- 1 107 oocysts hectare1 day1 (Atwill et al., 2004). Further
scapes (Bradley and Altizer, 2007), potentially increasing the fae- analysis of squirrel populations however has suggested that most
caleoral transmission of oocysts between wildlife and humans and tree squirrels host zoonotic species and genotypes while ground
contamination of drinking water catchments. squirrels host species and genotypes that are tribe-specific and
Shifting boundaries between wildlife and humans have been unlikely to cause human disease, despite overlapping ranges
responsible for the emergence of species like C. ubiquitum and (Stenger et al., 2015b). This highlights the importance of extensive
chipmunk genotype I in human populations. For example, squirrels molecular epidemiological studies of wildlife to better understand
host C. ubiquitum, chipmunk genotype I, the skunk genotype and the public health risks.
other Cryptosporidium genotypes associated with human disease While urban-environment-induced increases in wildlife
population densities are conducive to elevated rates of Cryptospo- unusual species and genotypes are not significant (Chalmers et al.,
ridium transmission, the host specificity of some wildlife species 2009; Robinson et al., 2011).
and genotypes may limit the potential for spillover of wildlife ge- Accurate, quantitative identification of Cryptosporidium in
notypes to sympatric populations of humans. For example, in wildlife excreta is an essential starting point for estimating catch-
Australia, the common brushtail possum is one of the most abun- ment loads (Davies et al., 2003). Quantitative PCR (qPCR) (real-time
dant native marsupials in urban environments, having successfully PCR) therefore represents an invaluable tool that enables rapid,
adapted to utilise anthropogenic resources (Hill et al., 2008). A high-throughput and cost-effective detection and quantitation of
higher Cryptosporidium prevalence in urban compared to woodland Cryptosporidium oocysts and is increasingly being used to monitor
possum populations (11.3 versus 5.6%) has been reported, but the oocyst shedding by animals in catchments (Yang et al., 2014a). Due
majority of possums sampled shed low numbers of host adapted to the intrinsic constraints of qPCR however, standards of known
(possum genotype) oocysts (1 to 102) (Hill et al., 2008). However, concentration are required to generate calibration curves used to
the finding a C. fayeri clinical infection in a human, which had estimate the concentration of pathogens in a sample (Hindson
previously been thought to be a host-adapted species (Waldron et al., 2013; Racki et al., 2014). Therefore the quantification of the
et al., 2010), highlights our lack of knowledge about the human target molecules in the unknown sample is only as good as that of
infectious potential of many species and genotypes of Cryptospo- the standards used. Droplet digital PCR (ddPCR) (Hindson et al.,
ridium infecting wildlife. 2013) is the third-generation implementation of conventional
PCR that facilitates the quantitation of nucleic acid targets without
5. Perspectives for the water industry the need for calibration curves (Vogelstein and Kinzler, 1999). A
recent study compared ddPCR with qPCR for the quantitative
Management of Cryptosporidium public health risks for the detection of Cryptosporidium DNA in animal and human faecal
drinking water industry requires the implementation of a holistic samples (Yang et al., 2014b) and revealed that ddPCR appeared to
approach including research, monitoring Cryptosporidium oocysts be less sensitive to inhibitors than qPCR and that inaccurate cali-
in animals and source water and catchment management (e.g., bration of qPCR standards resulted in qPCR overestimating the
access protection, vegetation cover, etc). As watersheds are numbers of oocysts present (Yang et al., 2014b). This has important
vulnerable to contamination with both zoonotic and non-zoonotic implications for catchment risk management. However, qPCR is
species from wildlife, sensitive detection of Cryptosporidium oo- cheaper and provides better throughput and therefore using ddPCR
cysts in water and correct identification of oocysts to the species/ to precisely quantify qPCR standards would be one way to combine
genotype level are essential for source water management and risk the advantages of the two technologies and provide more accurate
assessment (Li et al., 2015b). The routine practice of assessing assessment of Cryptosporidium catchments loads from wildlife
Cryptosporidium contamination of catchments and drinking water faecal samples.
supplies using total oocyst counts based on the U.S. Environmental Besides quantitative considerations, measuring the infectivity is
Protection Agency (EPA) Method 1622/1623, cannot differentiate also important for adjusting the risk profile of oocysts from wildlife
Cryptosporidium species and cannot reliably access viability in source waters (Swaffer et al., 2014). For example, a recent study
(infectivity). This microscopy-based method, therefore over- has shown that the infectivity fraction of oocysts within source
estimates the human health risk, as wildlife in catchments water samples in South Australian catchments was low (~3.1%),
frequently carry non-zoonotic genotypes and species and not all which provided a much more accurate water quality risk assess-
oocysts are viable. ment (Swaffer et al., 2014). This low infectivity fraction is consistent
The introduction of molecular identification techniques has with source water infectivity reported by Di Giovanni et al. (1999)
therefore been an important advance for water management and of 4.9% and Lalancette et al. (2012) of 0%. The ability to routinely
quantification of the risk to drinking water supplies from Crypto- measure oocyst infectivity has been hampered by a number of is-
sporidium-infected wildlife (Nolan et al., 2013; Zahedi et al., 2015). sues including the distribution and low numbers of oocysts, costs
Identification of Cryptosporidium to the species/genotype level is and reproducibility (Di Giovanni and LeChevallier, 2005; Swaffer
especially challenging for environmental (faecal and water) sam- et al., 2014). However, recent improvements in cell culture immu-
ples because of the usual presence of very low numbers of oocysts nofluorescence assays have led to the development of a single
and high concentrations of PCR inhibitors and non-target organ- format assay that provides information on method performance
isms (Li et al., 2015b). It is essential however, for the assessment of (recovery rate), oocyst number, oocyst infectivity and genotype of
the public health importance of Cryptosporidium oocysts from infectious oocysts, overcoming these obstacles (King et al., 2015).
wildlife. Recently, the use of fluorescence resonance energy trans- This assay should therefore enable a more comprehensive under-
fer (FRET) probes combined with melt curve analysis has been used standing of Cryptosporidium risk for different water sources,
for rapid and sensitive differentiation of zoonotic from non- assisting in the selection of appropriate risk mitigation measures
zoonotic species in water samples (Li et al., 2015b). Another study (King et al., 2015). It is however important to remember that the
of a drinking water supply in Australia, found no C. hominis in any detection of non-viable oocysts in the 10e20 L of the water column
water sample tested, but Cryptosporidium genotypes associated that is usually sampled, does not mean that other oocysts in the
with native and non-native wildlife made up 70% of all isolates water body are also non-viable.
typed (Swaffer et al., 2014). Similarly, Ruecker et al. (2012) reported Factors that affect the viability of Cryptosporidium oocyst load in
that non-zoonotic wildlife species and genotypes of Cryptospo- faecal samples from wildlife in the catchment and water (runoffs,
ridium accounted for 64.3% of Cryptosporidium identified in envi- water column and sediments), include solar inactivation, desicca-
ronmental water samples in Canada and that only 7.2% of human- tion, temperature and residence time in catchments and these
infectious species were detected. A low prevalence of C. hominis dynamics should be factored into risk assessments (Hijen et al.,
and C. parvum was also reported by Nolan et al. (2013) in Mel- 2006; King and Monis, 2007; Monis et al., 2014). Transport,
bourne catchments, who detected C. hominis and C. parvum in only including hydrodynamically-driven accumulation, settlemement,
0.6% of samples, despite screening >2000 animal faecal samples. dispersion, dilution etc. can also affect oocyst concentrations in the
However, the human-infectious potential of many wildlife-adapted water, either positively or negatively. Peak flow periods (when the
Cryptosporidium is currently unknown and the UK outbreak caused maximum area of catchment is contributing to stream flow), are a
by C. cuniculus should act as a caution against assuming these major driver behind the transport of oocysts to surface water.
Therefore monitoring the distribution of Cryptosporidium during 645e658.

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Bajer, A., Caccio , S., Bednarska, M., Behnke, J.M., Pieniazek, N.J., Sinski, E., 2003.
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ridium research from the Australian Research Council Linkage Grant Barugahare, R., Dennis, M.M., Becker, J.A., Slapeta, J., 2011. Detection of Cryptospo-
number LP130100035. ridium molnari oocysts from fish by fluorescent antibody staining assays for
Cryptosporidium spp. affecting humans. Appl. Environ. Microbiol. 77,
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International Journal for Parasitology: Parasites and Wildlife 5 (2016) 88e109

Contents lists available at ScienceDirect

International Journal for Parasitology:

Public health signiﬁcance of zoonotic Cryptosporidium species in

5. Perspectives for the water industry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102

Species name Author(s) Type host(s) Major Reports in humans

kangaroo (Macropus giganteus), Yellow

Species name Major host(s) Site of References

Species Host Site of Reference

Species/genotype Amphibian/Reptile host species Site of infection Reference

C. fragile Black-spined toads (Duttaphrynus melanostictus) Stomach Jirk

Therefore monitoring the distribution of Cryptosporidium during 645e658.

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