Wild Animals in Captivity: An Analysis of Parasite Biodiversity and Transmission among Animals at Two Zoological Institutions with Different Typologies
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Location and Host Species
2.2. Sample Collection and Processing
2.3. Parasite Biodiversity, Housing Conditions, and Feeding Habits
3. Results
3.1. Overall Parasite Biodiversity and Prevalence
3.1.1. Avian Hosts
3.1.2. Mammalian Hosts
3.2. Biodiversity and Prevalence in Relation to Feeding Habits and Housing Conditions
4. Discussion
4.1. On the Parasite Epidemiology, Biodiversity, and Species Identification
4.1.1. Avian Hosts
4.1.2. Mammalian Hosts
4.2. Effect of Housing Conditions
4.3. Transmission Risks between Animals and Humans
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Zoo | Hosts | Diet Type | Animal Species Studied | Hosts Infected | Samples Analysed | Positive Samples |
---|---|---|---|---|---|---|
ZooAquarium | Mammals | Herbivores | 55 | 49 (89.1%) | 1891 | 956 (50.6%) |
Omnivores | 17 | 9 (53.0%) | 455 | 164 (36.0%) | ||
Carnivores | 11 | 2 (18.2%) | 254 | 27 (10.6%) | ||
Total | 83 | 60 (72.3%) | 2600 | 1147 (44.1%) | ||
Birds | Herbivores | 17 | 0 (0.0%) | 127 | 0 (0.0%) | |
Omnivores | 15 | 3 (20.0%) | 127 | 8 (6.3%) | ||
Carnivores | 32 | 4 (12.5%) | 285 | 26 (9.1%) | ||
Total | 64 | 7 (11.0%) | 539 | 34 (6.3%) | ||
Faunia | Mammals | Herbivores | 29 | 17 (58.6%) | 783 | 136 (17.4%) |
Omnivores | 23 | 7 (30.4%) | 671 | 46 (6.9%) | ||
Carnivores | 16 | 1 (6.3%) | 422 | 2 (0.5%) | ||
Total | 68 | 25 (36.8%) | 1876 | 184 (9.8%) | ||
Birds | Herbivores | 14 | 0 (0.0%) | 130 | 0 (0.0%) | |
Omnivores | 12 | 5 (41.7%) | 188 | 29 (15.4%) | ||
Carnivores | 14 | 0 (0.0%) | 94 | 0 (0.0%) | ||
Total | 40 | 5 (12.5%) | 412 | 29 (7.0%) | ||
Total results * | Mammals | Herbivores | 73 | 62 (84.9%) | 2674 | 1092 (40.8%) |
Omnivores | 34 | 16 (47.1%) | 1126 | 211 (18.7%) | ||
Carnivores | 25 | 4 (16.0%) | 676 | 30 (4.4%) | ||
Total | 132 | 82 (62.1%) | 4476 | 1333 (29.8%) | ||
Birds | Herbivores | 24 | 0 (0.0%) | 257 | 0 (0.0%) | |
Omnivores | 22 | 7 (31.8%) | 315 | 37 (11.8%) | ||
Carnivores | 40 | 4 (10.0%) | 379 | 26 (6.9%) | ||
Total | 86 | 11 (12.8%) | 951 | 63 (6.6%) |
ZooAquarium | Faunia | |||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Infected Host Species | Infected Host Species | |||||||||||||
Mammals | Birds | Mammals | Birds | |||||||||||
C (2) | O (9) | H (49) | C (4) | O (3) | H (0) | C (1) | O (7) | H (17) | C (0) | O (5) | H (0) | |||
Amoebae | ||||||||||||||
Entamoeba Casagrandi and Barbagallo 1897 | 1 | 6 | 34 | 3 | 3 | 9 | 1 | |||||||
Endolimax Kuenen and Swellengrebel 1913 | 2 | 6 | 2 | |||||||||||
Flagellates | ||||||||||||||
Giardia Künstler 1882 | 1 | 4 | 1 | 3 | ||||||||||
Chilomastix Aléxéieff 1910 | 3 | 8 | 2 | 2 | ||||||||||
Trichomonads | 1 | 1 | ||||||||||||
Coccidia | ||||||||||||||
Eimeria Schneider 1875 | 5 | 2 | ||||||||||||
Toxoplasma Nicolle and Manceaux 1909/Neospora Dubey et al. 1988 | 1 | |||||||||||||
Ciliates | ||||||||||||||
Balantioides Alexeieff 1931 | 5 | 8 | 1 | 2 | 1 | |||||||||
Buxtonella Jameson 1926 | 5 | |||||||||||||
Troglodytella (Brumpt and Joyeux 1912) | 1 | |||||||||||||
Endosymbiotic ciliates | 6 | 2 | ||||||||||||
Trematodes | ||||||||||||||
Unidentified eggs | 1 | |||||||||||||
Cestodes | ||||||||||||||
Unidentified eggs | 1 | 5 | 1 | |||||||||||
Nematodes | ||||||||||||||
Trichuris Roederer 1761 | 3 | 10 | 1 | 1 | 1 | 6 | ||||||||
Capillaria Zeder 1800/capillariids | 1 | 1 | 2 | 3 | 1 | 3 | ||||||||
Nematodirus Ransom 1907 | 2 | |||||||||||||
Trichostrongylids | 1 | |||||||||||||
Baylisascaris Sprent 1968 | 1 | 1 | ||||||||||||
Parascaris Yorke and Maplestone 1926 | 2 | |||||||||||||
Porrocaecum Railliet and Henry 1912 | 1 | |||||||||||||
Ascaridia Dujardin 1845/Heterakis Schrank 1790 | 2 | |||||||||||||
Ascarid (unidentified) | 1 |
Samples | ||||
---|---|---|---|---|
Order | Family | Species | (Total/Positives) | Parasites Found (% of Total Samples) |
Artiodactyla | Bovidae | Ammotragus lervia (Pallas 1777) | 21/14 | Entamoeba bovis-like (66.7%) |
Antilope cervicapra (Linnaeus 1758) | 18/9 | Entamoeba bovis-like (50.0%) | ||
Bison bison (Linnaeus 1758) | 37/15 | Entamoeba bovis-like (40.5%) | ||
Bison bonasus (Linnaeus 1758) | 27/19 | Entamoeba bovis-like (70.4%), Buxtonella sulcata Jameson 1926 (3.7%) | ||
Bos grunniens (Linnaeus 1766) | 17/12 | Entamoeba bovis-like (52.9%), Buxtonella sulcata (41.2%), unidentified cestode eggs (5.9%) | ||
Bos taurus (Linnaeus 1758) | 4/1 | Entamoeba bovis-like (25.0%) | ||
Boselaphus tragocamelus (Pallas 1766) | 13/12 | Entamoeba bovis-like (92.3%) | ||
Budorcas taxicolor Hodgson 1850 | 39/26 | Entamoeba bovis-like (66.7%) | ||
Capra hircus Linnaeus 1758 | 37/31 | Entamoeba bovis-like (81.1%), Eimeria spp. (5.4%), Trichuris spp. (5.4%) | ||
Capra pyrenaica Schinz 1838 | 30/20 | Entamoeba bovis-like (66.7%) | ||
Connochaetes gnou (Zimmermann 1780) | 23/14 | Entamoeba bovis-like (60.9%) | ||
Gazella dorcas osiris Blaine 1913 | 127/106 | Entamoeba bovis-like (70.1%), Eimeria spp. (1.6%), Trichuris spp. (16.5%), Nematodirus spp. (21.3%) | ||
Nanger dama mhorr (Bennett 1833) | 99/85 | Entamoeba bovis-like (74.7%), Entamoeba spp. (8-nucleated) (2.0%), Giardia spp. (2.0%), Chilomastix spp. (1.0%), Eimeria spp. (2.0%), Trichuris spp. (15.2%), Nematodirus spp. (8.1%), Trichostrongylids (10.1%) | ||
Ovis aries Linnaeus 1758 | 39/13 | Entamoeba bovis-like (25.6%), Chilomastix spp. (2.6%), Eimeria spp. (5.1%) | ||
Ovis gmelinii Blyth 1841 | 11/6 | Entamoeba bovis-like (54.6%) | ||
Syncerus caffer nanus Boddaert 1785 | 59/54 | Entamoeba bovis-like (89.8%), trichomonads (3.4%), Buxtonella sulcata (44.1%) | ||
Tragelaphus eurycerus (Ogilby 1837) | 17/15 | Entamoeba bovis-like (88.2%) | ||
Tragelaphus spekii gratus Sclater 1880 | 40/26 | Entamoeba bovis-like (60.0%), Chilomastix spp. (2.5%), Balantioides coli-like (15.0%) | ||
Camelidae | Camelus bactrianus Linnaeus 1758 | 40/19 | Entamoeba bovis-like (20.0%), Buxtonella cameli (Boschenko 1925) (25.0%), Trichuris spp. (5.0%) | |
Camelus dromedarius Linnaeus 1758 | 34/7 | Entamoeba bovis-like (5.9%), Buxtonella cameli (20.6%) | ||
Lama guanicoe (Müller 1776) | 19/8 | Entamoeba bovis-like (42.1%) | ||
Cervidae | Alces alces (Linnaeus 1758) | 16/11 | Balantioides coli-like (43.8%), Trichuris spp. (56.3%) | |
Capreolus capreolus (Linnaeus 1758) | 6/5 | Entamoeba bovis-like (83.3%) | ||
Cervus elaphus Linnaeus 1758 | 34/30 | Entamoeba bovis-like (85.3%), unidentified cestode eggs (2.9%) | ||
Dama dama (Linnaeus 1758) | 40/35 | Entamoeba bovis-like (87.5%), Capillaria spp. (5.0%) | ||
Elaphurus davidianus Milne-Edwards 1866 | 29/20 | Entamoeba bovis-like (69.0%) | ||
Muntiacus reevesi (Ogilby 1839) | 21/18 | Entamoeba bovis-like (85.7%), Chilomastix spp. (4.8%) | ||
Rangifer tarandus (Linnaeus 1758) | 23/4 | Entamoeba bovis-like (4.4%), Trichuris spp. (13.0%) | ||
Giraffidae | Giraffa camelopardalis (Linnaeus 1758) | 40/14 | Entamoeba bovis-like (35.0%), Trichuris spp. (2.5%) | |
Hippopotamidae | Hippopotamus amphibius Linnaeus 1758 | 11/1 | Unidentified cestode eggs (9.1%) | |
Suidae | Potamochoerus porcus (Linnaeus 1758) | 37/14 | Entamoeba polecki-like (29.7%), Giardia spp. (2.7%), Chilomastix spp. (8.1%), Balantioides coli (24.3%) | |
Sus scrofa Linnaeus 1758 | 59/43 | Entamoeba polecki-like (52.5%), Chilomastix spp. (8.5%), Balantioides coli (42.4%) | ||
Tayassuidae | Dicotyles tajacu (Linnaeus 1758) | 1/0 | ||
Carnivora | Ailuridae | Ailurus fulgens Cuvier 1825 | 33/2 | Capillaria spp. (6.1%) |
Canidae | Canis lupus occidentalis Linnaeus 1758 | 15/0 | ||
Speothos venaticus (Lund 1842) | 45/1 | Toxoplasma/Neospora (2.2%) | ||
Felidae | Lynx lynx (Linnaeus 1758) | 13/0 | ||
Lynx pardinus (Temminck 1827) | 20/0 | |||
Panthera leo (Linnaeus 1758) | 16/0 | |||
Panthera pardus saxicolor (Linnaeus 1758) | 22/0 | |||
Panthera tigris (Linnaeus 1758) | 16/0 | |||
Herpestidae | Suricata suricatta (Schreber 1776) | 10/0 | ||
Mustelidae | Mustela lutreola (Linnaeus 1761) | 30/0 | ||
Pteronura brasiliensis (Zimmermann 1780) | 20/0 | |||
Procyonidae | Nasua nasua (Linnaeus 1766) | 9/0 | ||
Procyon lotor (Linnaeus 1758) | 18/2 | Capillaria spp. (11.1%) | ||
Ursidae | Ailuropoda melanoleuca (David 1869) | 36/0 | ||
Helarctos malayanus (Raffles 1822) | 35/1 | Trematoda (2.9%) | ||
Tremarctos ornatus (Cuvier 1825) | 1/0 | |||
Ursus americanus Pallas 1780 | 16/0 | |||
Ursus arctos Linnaeus 1758 | 63/7 | Baylisascaris spp. (11.1%) | ||
Ursus thibetanus Cuvier 1823 | 37/0 | |||
Viverridae | Arctictis binturong (Raffles 1822) | 32/0 | ||
Diprotodontia | Macropodidae | Notamacropus rufogriseus (Desmarest 1817) | 6/0 | |
Petrogale xanthopus Gray 1855 | 20/5 | Entamoeba bovis-like (25.0%) | ||
Phascolarctidae | Phascolarctos cinereus (Goldfuss 1817) | 35/0 | ||
Lagomorpha | Leporidae | Oryctolagus cuniculus (Linnaeus 1758) | 65/4 | Eimeria spp. (6.2%) |
Perissodactyla | Equidae | Equus quaga Boddaert 1785 | 159/9 | Endosymbiotic ciliates (4.4%), Parascaris equorum (Goeze 1782) (1.3%) |
Equus asinus Linnaeus 1758 | 25/21 | Endosymbiotic ciliates (84.0%), Parascaris equorum (8.0%) | ||
Equus caballus Linnaeus 1758 | 44/28 | Endosymbiotic ciliates (63.6%) | ||
Rhinocerotidae | Ceratotherium simum (Burchell 1817) | 35/18 | Endosymbiotic ciliates (51.4%) | |
Rhinoceros unicornis Linnaeus 1758 | 32/27 | Endosymbiotic ciliates (84.4%) | ||
Tapiridae | Tapirus indicus (Desmarest 1819) | 31/1 | Chilomastix spp. (3.2%) | |
Tapirus terrestris (Linnaeus 1758) | 12/2 | Balantioides coli (8.3%), unidentified cestode eggs (8.3%) | ||
Pilosa | Myrmecophagidae | Myrmecophaga tridactyla Linnaeus 1758 | 47/26 | Entamoeba spp. (4-nucleated) (2.1%), Tetratrichomonas spp. Parisi 1910 (25.5%), Capillaria-like eggs (36.2%) |
Primates | Cebidae | Sapajus apella (Linnaeus 1758) | 26/0 | |
Cercopithecidae | Colobus guereza Rüppell 1835 | 45/40 | Entamoeba coli-like (24.4%), Entamoeba polecki-like (22.2%), Balantioides coli-like (2.2%), Trichuris spp. (84.4%) | |
Macaca spp. Lacepede 1799 | 1/0 | |||
Mandrillus sphinx (Linnaeus 1758) | 47/47 | Entamoeba polecki-like (76.6%), Entamoeba coli-like (10.6%), Chilomastix spp. (10.6%), Balantioides coli-like (66.0%), Trichuris spp. (2.1%), unidentified cestode eggs (2.1%) | ||
Papio spp. Erxleben 1777 | 17/17 | Entamoeba coli-like (94.1%), Endolimax spp. (5.9%), Trichuris spp. (82.4%) | ||
Hominidae | Pongo pygmaeus (Linnaeus 1760) | 103/79 | Balantioides coli-like (76.7%) | |
Gorilla gorilla (Savage 1847) | 29/17 | Entamoeba coli-like (3.5%), Balantioides coli-like (51.7%), Troglodytella abrassarti (Brumpt and Joyeux 1912) (10.3%) | ||
Pan troglodytes (Blumenbach 1775) | 28/21 | Entamoeba coli-like (39.3%), Entamoeba polecki-like (14.3%), Endolimax spp. (3.6%), Balantioides coli-like (39.3%) | ||
Hylobatidae | Hylobates lar (Linnaeus 1771) | 25/9 | Entamoeba coli-like (4.0%), Entamoeba polecki-like (4.0%), Balantioides coli-like (28.0%) | |
Hylobates muelleri (Martin 1841) | 28/12 | Entamoeba coli-like (28.6%), Balantioides coli-like (14.3%), Trichuris spp. (3.6%) | ||
Lemuridae | Eulemur fulvus (Geoffroy 1796) | 14/2 | Giardia spp. (7.1%), unidentified cestode eggs (7.1%) | |
Lemur catta Linnaeus 1758 | 16/2 | Entamoeba polecki-like (6.3%), Giardia spp. (6.3%), Trichuris spp. (6.3%) | ||
Varecia variegata (Kerr 1792) | 40/0 | |||
Proboscidea | Elephantidae | Elephas maximus Linnaeus 1758 | 55/30 | Chilomastix spp. (1.8%), endosymbiotic ciliates (54.5%) |
Rodentia | Caviidae | Cavia porcellus (Linnaeus 1758) | 17/0 | |
Dolichotis patagonum (Zimmermann 1780) | 27/8 | Entamoeba muris-like (3.7%), Giardia spp. (14.8%), Chilomastix spp. (7.4%), Trichuris spp. (3.7%) | ||
Hydrochoerus hydrochaeris (Linnaeus 1766) | 15/2 | Chilomastix spp. (6.7%), Balantioides coli-like (6.7%) | ||
Chinchillidae | Chinchilla spp. Bennett 1829 | 1/0 |
Samples | ||||
---|---|---|---|---|
Order | Family | Species | (Total/Positives) | Parasites Found (% of Total Samples) |
Accipitriformes | Accipitridae | Aegypius monachus (Linnaeus 1766) | 7/0 | |
Aquila adalberti Brehm 1861 | 13/0 | |||
Aquila verreauxii Lesson 1831 | 3/0 | |||
Buteo buteo (Linnaeus 1758) | 13/0 | |||
Geranoaetus melanoleucus (Vieillot 1819) | 3/0 | |||
Gypohierax angolensis (Gmelin 1788) | 2/0 | |||
Gyps fulvus (Hablizl 1783) | 23/0 | |||
Haliaeetus albicilla (Linnaeus 1758) | 3/0 | |||
Haliaeetus leucocephalus (Linnaeus 1766) | 3/0 | |||
Haliaeetus pelagicus (Pallas 1811) | 10/3 | Capillariids (34.3%) | ||
Ichtyophaga vocifer (Daudin 1800) | 3/0 | |||
Milvus migrans (Boddaert 1783) | 36/21 | Capillariids (38.9%), Porrocaecum spp. (33.3%) | ||
Neophron percnopterus (Linneaus 1758) | 3/0 | |||
Parabuteo unicinctus (Temminck 1824) | 28/1 | Trichuris spp. (3.6%) | ||
Anseriformes | Anatidae | Alopochen aegyptiaca (Linnaeus 1766) | 5/0 | |
Aythya nyroca (Güldenstädt 1770) | 1/0 | |||
Cairina moschata (Linnaeus 1758) | 8/0 | |||
Cygnus atratus (Latham 1790) | 1/0 | |||
Tadorna ferruginea (Pallas 1764) | 4/0 | |||
Tadorna tadorna (Linnaeus 1758) | 3/0 | |||
Bucerotiformes | Bucerotidae | Bycanistes brevis Friedmann 1929 | 5/0 | |
Bycanistes bucinator (Temminck 1824) | 8/0 | |||
Bucorvidae | Bucorvus leadbeateri (Vigors 1825) | 5/0 | ||
Cathartiformes | Cathartidae | Sarcoramphus papa (Linnaeus 1758) | 10/0 | |
Vultur gryphus Linnaeus 1758 | 5/0 | |||
Ciconiiformes | Ciconiidae | Ciconia ciconia (Linnaeus 1758) | 10/0 | |
Leptoptilos crumenifer (Lesson 1831) | 3/0 | |||
Columbiformes | Columbidae | Columba livia Gmelin 1789 | 11/0 | |
Coraciiformes | Alcedinidae | Dacelo novaeguineae Hermann 1783 | 2/0 | |
Falconiformes | Falconidae | Falco naumanni Fleischer 1818 | 13/0 | |
Caracara plancus (Miller 1777) | 1/0 | |||
Galliformes | Numididae | Numida meleagris (Linnaeus 1758) | 4/0 | |
Phasianidae | Gallus gallus (Linnaeus 1758) | 39/1 | Entamoeba gallinarum Tyzzer 1920 (2.6%) | |
Gruiformes | Gruidae | Balearica regulorum (Bennett 1834) | 4/0 | |
Musophagiformes | Musophagidae | Tauraco erythrolophus (Vieillot 1819) | 8/0 | |
Menelikornis leucotis (Rüppell 1835) | 5/0 | |||
Passeriformes | Corvidae | Corvus corax Linnaeus 1758 | 3/0 | |
Pelecaniformes | Pelecanidae | Pelecanus rufescens Gmelin 1789 | 8/0 | |
Threskiornithidae | Eudocimus ruber (Linnaeus 1758) | 11/0 | ||
Threskiornis aethiopicus (Latham 1790) | 23/0 | |||
Phoenicopteriformes | Phoenicopteridae | Phoenicopterus ruber Linnaeus 1758 | 7/0 | |
Piciformes | Ramphastidae | Ramphastos toco Müller 1776 | 5/0 | |
Psittaciformes | Cacatuidae | Cacatua alba (Müller 1776) | 6/0 | |
Cacatua galerita (Latham 1790) | 11/0 | |||
Cacatua goffiniana Roselaar and Michels 2004 | 5/0 | |||
Cacatua pastinator (Gould 1841) | 8/0 | |||
Cacatua sulphurea (Gmelin 1788) | 5/0 | |||
Psittacidae | Amazona aestiva (Linnaeus 1758) | 8/0 | ||
Ara ararauna (Linnaeus 1758) | 22/0 | |||
Ara chloropterus Gray 1859 | 8/0 | |||
Ara rubrogenys Lafresnaye 1847 | 1/0 | |||
Aratinga solstitialis (Linnaeus 1758) | 15/0 | |||
Myiopsitta monachus Boddaert 1783 | 1/0 | |||
Psittacus erithacus Linnaeus 1758 | 7/0 | |||
Trichoglossus haematodus (Linnaeus 1771) | 4/0 | |||
Psittaculidae | Eclectus roratus (Müller 1776) | 2/0 | ||
Strigiformes | Strigidae | Bubo bubo hispanus Rothschild and Hartert 1910 | 15/1 | Capillariids (6.7%) |
Bubo bubo sibiricus Gloger 1833 | 5/0 | |||
Bubo scandiacus (Linnaeus 1758) | 2/0 | |||
Strix nebulosa Forster 1772 | 1/0 | |||
Casuariformes | Casuariidae | Casuarius casuarius (Linnaeus 1758) | 12/0 | |
Struthioniformes | Dromaiidae | Dromaius novaehollandiae (Latham 1790) | 20/0 | |
Rheiformes | Rheidae | Rhea americana (Linnaeus 1758) | 7/2 | Entamoeba spp. (4-nucleated) (28.6%) |
Struthioniformes | Struthionidae | Struthio camelus Linnaeus 1758 | 12/5 | Entamoeba polecki-like (33.3%), Balantioides coli (8.3%) |
Samples | ||||
---|---|---|---|---|
Order | Family | Species | (Total/Positives) | Parasites Found (% of Total Samples) |
Afrosoricida | Tenrecidae | Echinops telfairi Martin 1838 | 2/0 | |
Artiodactyla | Bovidae | Capra hircus | 40/22 | Entamoeba bovis-like (55.0%), Eimeria spp. (2.5%) |
Madoqua kirkii (Günther 1880) | 43/15 | Entamoeba bovis-like (11.6%), Entamoeba spp. (8-nucleated) (27.9%), Trichuris spp. (2.3%) | ||
Ovis aries | 26/10 | Entamoeba bovis-like (34.6%), Eimeria spp. (3.9%) | ||
Cervidae | Subulo gouazoubira (Fischer 1814) | 12/11 | Entamoeba bovis-like (91.7%), Trichuris spp. (8.3%) | |
Muntiacus muntjack Zimmermann 1780 | 47/18 | Entamoeba bovis-like (36.2%), Entamoeba spp. (8-nucleated) (2.1%), Giardia spp. (2.1%), Trichuris spp. (4.3%) | ||
Suidae | Sus scrofa | 39/22 | Entamoeba polecki-like (46.2%), Chilomastix spp. (7.7%), Balantioides coli (28.2%) | |
Tayassuidae | Dicotyles tajacu | 16/1 | Balantioides coli (6.3%) | |
Carnivora | Ailuridae | Ailurus fulgens | 36/0 | |
Canidae | Vulpes zerda (Zimmermann 1780) | 52/2 | Trichuris spp. (1.9%), unidentified ascarid (1.9%) | |
Felidae | Leopardus pardalis (Linnaeus 1758) | 48/0 | ||
Herpestidae | Helogale parvula (Sundevall 1847) | 32/0 | ||
Suricata suricatta | 15/0 | |||
Mephitidae | Mephitis mephitis (Schreber 1776) | 50/3 | Baylisascaris spp. (6.0%) | |
Mustelidae | Mustela lutreola | 19/0 | ||
Mustela putorius furo Linnaeus 1758 | 5/0 | |||
Procyonidae | Nasua nasua | 45/0 | ||
Potos flavus (Schreber 1774) | 49/0 | |||
Procyon lotor | 30/0 | |||
Viverridae | Arctictis binturong | 25/0 | ||
Genetta genetta (Linnaeus 1758) | 45/0 | |||
Chiroptera | Phyllostomidae | Carollina perspicillata (Linnaeus 1758) | 13/0 | |
Pteropodidae | Rousettus aegyptiacus (Saint-Hilaire 1810) | 26/0 | ||
Cingulata | Chlamyphoridae | Euphractus sexcinctus (Linnaeus 1758) | 16/0 | |
Chaetophractus villosus (Desmarest 1804) | 16/0 | |||
Tolypeutes tricinctus (Linnaeus 1758) | 2/0 | |||
Dasyurimorpha | Dasyuridae | Dasyurus viverrinus (Shaw 1800) | 24/0 | |
Diprotodontia | Macropodidae | Notamacropus rufogriseus | 46/4 | Entamoeba spp. (one nucleated) (6.5%), Entamoeba spp. (8-nucleated) (2.2%) |
Osphranter rufus (Desmarest 1822) | 42/0 | |||
Eulipotyphla | Erinaceidae | Atelerix albiventris (Wagner 1841) | 35/0 | |
Lagomorpha | Leporidae | Oryctolagus cuniculus | 1/0 | |
Perissodactyla | Equidae | Equus africanus (Heuglin and Fitzinger 1866) | 27/9 | Endosymbiotic ciliates (33.3%) |
Equus caballus | 35/8 | Endosymbiotic ciliates (22.9%) | ||
Pilosa | Choloepodidae | Choloepus didactilus (Linnaeus 1758) | 46/13 | Entamoeba spp. (8-nucleated) (28.3%) |
Myrmecophagidae | Tamandua tetradactyla (Linnaeus 1758) | 36/0 | ||
Primates | Aotidae | Aotus nancymaae Hershkovitz 1983 | 7/1 | Entamoeba coli-like (14.3%) |
Aotus trivirgatus (Humboldt 1812) | 9/0 | |||
Callitrichidae | Callimico goeldii (Thomas 1904) | 47/0 | ||
Callithrix jacchus (Linnaeus 1758) | 38/0 | |||
Cebuella pygmaea (Spix 1823) | 11/0 | |||
Leontopithecus rosalia (Linnaeus 1766) | 31/0 | |||
Saguinus geoffroyi (Pucheran 1845) | 30/0 | |||
Saguinus imperator (Goeldi 1907) | 34/0 | |||
Saguinus oedipus (Linnaeus 1758) | 26/0 | |||
Cebidae | Sapajus apella | 30/0 | ||
Saimiri sciureus (Linnaeus 1758) | 53/0 | |||
Galagidae | Galago moholi Smith 1836 | 19/0 | ||
Lemuridae | Eulemur albifrons (Geoffroy 1796) | 17/0 | ||
Lemur catta | 26/0 | |||
Varecia variegata | 3/0 | |||
Varecia rubra (Geoffroy 1812) | 12/1 | Capillaria spp. (8.3%) | ||
Lorisidae | Xanthonycticebus pygmaeus (Bonhote 1907) | 5/0 | ||
Perodicticus potto (Müller 1766) | 26/0 | |||
Pitheciidae | Pithecia pithecia (Linnaeus 1766) | 33/2 | Entamoeba coli-like (6.1%) | |
Rodentia | Heterocephalidae | Heterocephalus glaber Rüppell 1842 | 29/0 | |
Caviidae | Cavia porcellus | 54/2 | Balantioides coli (3.7%) | |
Dolichotis patagonum | 24/7 | Giardia spp. (8.3%), Trichuris spp. (20.8%) | ||
Hydrochoerus hydrochaeris | 1/0 | |||
Dasyproctidae | Dasyprocta azarae Lichtenstein 1823 | 1/0 | ||
Dasyprocta fuliginosa Wagler 1832 | 23/3 | Trichuris spp. (13.0%) | ||
Dasyprocta punctata Gray 1842 | 8/0 | |||
Dipodidae | Jaculus orientalis Erxleben 1777 | 12/3 | Entamoeba muris (25.0%), Chilomastix spp. (16.7%) | |
Echimyidae | Capromys pilorides (Say 1822) | 94/15 | Trichuris spp. (16.0%) | |
Erethizontidae | Coendou prehensilis (Linnaeus 1758) | 43/5 | Chilomastix spp. (9.3%), Trichuris spp. (2.3%) | |
Hystricidae | Hystrix cristata Linnaeus 1758 | 47/5 | Entamoeba spp. (8-nucleated) (2.1%), Giardia spp. (8.5%) | |
Pedetidae | Pedetes capensis (Forster 1778) | 31/0 | ||
Sciuridae | Cynomys ludovicianus (Ord 1815) | 4/1 | Chilomastix spp. (25.0%) | |
Tubulidentata | Orycteropodidae | Orycteropus afer (Pallas 1766) | 7/1 | Giardia spp. (14.3%) |
Samples | ||||
---|---|---|---|---|
Order | Family | Species | (Total/Positives) | Parasites Found (% of Total Samples) |
Accipitriformes | Accipitridae | Necrosyrtes monachus | 8/0 | |
Aquila nipalensis Hodgson 1833 | 5/0 | |||
Buteo jamaicensis (Gmelin 1788) | 6/0 | |||
Buteo regalis (Gray 1844) | 5/0 | |||
Geranoaetus melanoleucus | 13/0 | |||
Gyps fulvus | 7/0 | |||
Parabuteo unicinctus | 14/0 | |||
Anseriformes | Anatidae | Cygnus atratus | 5/0 | |
Anhimidae | Chauna torquata (Oken 1816) | 11/0 | ||
Charadriiformes | Recurvirostridae | Recurvirostra avosetta Linnaeus 1758 | 1/0 | |
Falconiformes | Falconidae | Phalcoboenus australis (Gmelin 1788) | 2/0 | |
Galliformes | Numididae | Numida meleagris | 7/3 | Entamoeba gallinarum (14.3%), capillariids (14.3%), Ascaridia spp./Heterakis spp. (28.6%), Raillietina-like eggs (14.3%) |
Phasianidae | Gallus gallus | 14/1 | Ascaridia spp./Heterakis spp. (7.1%) | |
Meleagris gallopavo Linnaeus 1758 | 39/0 | |||
Gruiformes | Gruidae | Grus grus (Linnaeus 1758) | 6/1 | Capillariids (16.7%) |
Grus virgo (Linnaeus 1758) | 8/0 | |||
Musophagiformes | Musophagidae | Menelikornis leucotis | 11/0 | |
Passeriformes | Corvidae | Calocitta formosa (Swainson 1827) | 3/0 | |
Cotingidae | Rupicola peruvianus (Latham 1790) | 22/0 | ||
Sturnidae | Lamprotornis purpureus (Müller 1776) | 2/0 | ||
Pelecaniformes | Ardeidae | Bubulcus ibis (Linnaeus 1758) | 1/0 | |
Pelecanidae | Pelecanus onocrotalus Linnaeus 1758 | 2/0 | ||
Phoenicopteriformes | Phoenicopteridae | Phoenicopterus ruber | 5/0 | |
Piciformes | Ramphastidae | Ramphastos swainsonii Gould, 1833 | 21/17 | Capillaria spp. (81.0%) |
Ramphastos toco | 16/7 | Capillaria spp. (43.8%) | ||
Psittaciformes | Cacatuidae | Eolophus roseicapilla (Vieillot 1817) | 5/0 | |
Psittacidae | Amazona aestiva | 27/0 | ||
Ara ararauna | 17/0 | |||
Ara chloropterus | 6/0 | |||
Ara macao (Linnaeus 1758) | 3/0 | |||
Ara militaris (Linnaeus 1766) | 1/0 | |||
Ara rubrogenys | 2/0 | |||
Aratinga solstitialis | 9/0 | |||
Psittaculidae | Eclectus rotarus | 8/0 | ||
Trichoglossus haematodus (Linnaeus 1771) | 3/0 | |||
Strigiformes | Strigidae | Bubo bubo hispanus | 9/0 | |
Bubo bubo sibiricus | 6/0 | |||
Tytonidae | Tyto alba Scopoli 1769 | 11/0 | ||
Casuariiformes | Casuariidae | Dromaius novaehollandiae | 48/0 | |
Rheiformes | Rheidae | Rhea americana | 23/0 |
Zoological Park | |||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
ZooAquarium | Faunia | ||||||||||||||
Feeding Habits | Feeding Habits | ||||||||||||||
Host Class | Isolation | Soil | Carnivorous | Omnivorous | Herbivorous | Carnivorous | Omnivorous | Herbivorous | |||||||
Mammal | accessible | Natural | 2 | (10) | 8 | (13) | 48 | (53) | 0 | (1) | 2 | (3) | 12 | (19) | |
Artificial | 0 | (0) | 0 | (0) | 1 | (1) | 0 | (0) | 0 | (0) | 0 | (0) | |||
Mixed | 1 | (1) | 1 | (2) | 0 | (1) | 0 | (0) | 0 | (0) | 0 | (0) | |||
isolated | Natural | 0 | (0) | 0 | (0) | 0 | (0) | 0 | (0) | 0 | (0) | 0 | (0) | ||
Artificial | 0 | (0) | 1 | (2) | 0 | (0) | 1 | (14) | 5 | (20) | 5 | (10) | |||
Mixed | 0 | (0) | 0 | (0) | 0 | (0) | 0 | (1) | 0 | (0) | 0 | (0) | |||
Bird | accesible | Natural | 0 | (8) | 3 | (12) | 0 | (2) | 0 | (3) | 3 | (10) | 0 | (3) | |
Artificial | 0 | (0) | 0 | (0) | 0 | (0) | 0 | (0) | 0 | (0) | 0 | (1) | |||
Mixed | 4 | (24) | 0 | (3) | 0 | (15) | 0 | (11) | 2 | (2) | 0 | (10) | |||
isolated | Natural | 0 | (0) | 0 | (0) | 0 | (0) | 0 | (0) | 0 | (0) | 0 | (0) | ||
Artificial | 0 | (0) | 0 | (0) | 0 | (0) | 0 | (0) | 0 | (0) | 0 | (0) | |||
Mixed | 0 | (0) | 0 | (0) | 0 | (0) | 0 | (0) | 0 | (0) | 0 | (0) |
Function Coefficients | Wald’s X2 Test | ||||||
---|---|---|---|---|---|---|---|
Standard Error | Degrees of Freedom | ||||||
Parameter | B | Score | Significance | ||||
Feeding type | 14.733 | 2 | <0.001 | ||||
Omnivorous vs. carnivorous | 1.581 | 0.532 | 8.824 | 1 | 0.003 | ||
Herbivorous vs. carnivorous | 1.911 | 0.501 | 14.555 | 1 | <0.001 | ||
Soil type | 2.401 | 2 | 0.301 | ||||
artificial vs. natural | 0.063 | 1.710 | 0.001 | 1 | 0.971 | ||
mixed vs. natural | −0.878 | 0.572 | 2.352 | 1 | 0.125 | ||
Host Class (bird vs. mammal) | −2.103 | 0.480 | 19.150 | 1 | <0.001 | ||
Zoological institution (Faunia vs. ZooAquarium) | −0.649 | 0.405 | 2.567 | 1 | 0.109 | ||
Isolation type (isolated vs. accessible) | −1.326 | 1.777 | 0.577 | 1 | 0.456 | ||
Constant | −1.639 | 0.389 | 17.703 | 1 | <0.001 |
Function Coefficients | Wald’s X2 Test | ||||||
---|---|---|---|---|---|---|---|
Parameter | B | Standard Error | Score | Degrees of Freedom | Significance | ||
Feeding type | 21.061 | 2 | <0.001 | ||||
Omnivorous vs. carnivorous | 2.057 | 0.780 | 7.571 | 1 | 0.006 | ||
Herbivorous vs. carnivorous | 3.187 | 0.716 | 19.799 | 1 | <0.001 | ||
Soil type | 2.453 | 2 | 0.293 | ||||
artificial vs. natural | 18.336 | 25,170.708 | 0.000 | 1 | 0.999 | ||
mixed vs. natural | −2.016 | 1.287 | 2.453 | 1 | 0.117 | ||
Zoological institution (Faunia vs. ZooAquarium) | −1.245 | 0.531 | 5.496 | 1 | 0.019 | ||
Isolation type (isolated vs. accessible) | −18.995 | 25,170.708 | 0.000 | 1 | 0.999 | ||
Constant | −4.146 | 4195.118 | 0.000 | 1 | 0.999 |
Function Coefficients | Wald’s X2 Test | ||||||
---|---|---|---|---|---|---|---|
Parameter | B | Standard Error | Score | Degrees of Freedom | Significance | ||
Feeding type | 5.613 | 2 | 0.060 | ||||
Omnivorous vs. carnivorous | 2.107 | 0.889 | 5.613 | 1 | 0.018 | ||
Herbivorous vs. carnivorous | −18.913 | 7283.654 | 0.000 | 1 | 0.998 | ||
Soil type | 1.403 | 2 | 0.496 | ||||
artificial vs. natural | 0.833 | 40,847.685 | 0.000 | 1 | 1.000 | ||
mixed vs. natural | 1.030 | 0.870 | 1.403 | 1 | 0.236 | ||
Zoological institution (Faunia vs. ZooAquarium) | 0.121 | 0.684 | 0.031 | 1 | 0.860 | ||
Constant | −8.164 | 13,397.685 | 0.000 | 1 | 1.000 |
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Esteban-Sánchez, L.; García-Rodríguez, J.J.; García-García, J.; Martínez-Nevado, E.; de la Riva-Fraga, M.A.; Ponce-Gordo, F. Wild Animals in Captivity: An Analysis of Parasite Biodiversity and Transmission among Animals at Two Zoological Institutions with Different Typologies. Animals 2024, 14, 813. https://doi.org/10.3390/ani14050813
Esteban-Sánchez L, García-Rodríguez JJ, García-García J, Martínez-Nevado E, de la Riva-Fraga MA, Ponce-Gordo F. Wild Animals in Captivity: An Analysis of Parasite Biodiversity and Transmission among Animals at Two Zoological Institutions with Different Typologies. Animals. 2024; 14(5):813. https://doi.org/10.3390/ani14050813
Chicago/Turabian StyleEsteban-Sánchez, Lorena, Juan José García-Rodríguez, Juncal García-García, Eva Martínez-Nevado, Manuel Antonio de la Riva-Fraga, and Francisco Ponce-Gordo. 2024. "Wild Animals in Captivity: An Analysis of Parasite Biodiversity and Transmission among Animals at Two Zoological Institutions with Different Typologies" Animals 14, no. 5: 813. https://doi.org/10.3390/ani14050813
APA StyleEsteban-Sánchez, L., García-Rodríguez, J. J., García-García, J., Martínez-Nevado, E., de la Riva-Fraga, M. A., & Ponce-Gordo, F. (2024). Wild Animals in Captivity: An Analysis of Parasite Biodiversity and Transmission among Animals at Two Zoological Institutions with Different Typologies. Animals, 14(5), 813. https://doi.org/10.3390/ani14050813