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Parasitic Diseases Session

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European Association of Zoo- and Wildlife Veterinarians (EAZWV) 4th scientific meeting,

joint with the

annual meeting of the European Wildlife Disease Association (EWDA)

May 8-12, 2002, Heidelberg, Germany.

This manuscript is reproduced in the IVIS website with the permission of EAZWV www.eazwv.org

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European Association of Zoo- and Wildlife Veterinarians (EAZWV) 4th scientific meeting, joint with the annual meeting of the European Wildlife Disease Association (EWDA) May 8-12, 2002, Heidelberg, Germany.

CAMEL COCCIDIOSIS IN THE UNITED ARAB EMIRATES

J. KINNE and U. WERNERY

Affiliation: Central Veterinary Research Laboratory, P.O. Box 597, Dubai, United Arab Emirates

Abstract

Between 1996 and 2001 a total 522 dromedaries from Dubai area (286 camel calves, 69 young camels, 112 racing camels and 55 breeding camels) were investigated at the CVRL in Dubai for the cause of mortality. 142 camels (60.2% of the 236 camels older than one year) were diagnosed as having Eimeria-stages in their gut, of which 108 revealed a coccidiosis, and 34 an Eimeria-infection. Ninety-four dromedaries older than 1 year (39.8%) and all 286 calves (younger than 1 year) were free of Eimeria-stages. In 55 camels suffering from coccidiosis enterotoxaemia caused either by Cl. perfringens or B. cereus was additionally diagnosed. Severe intestinal haemorrhages were found at necropsy and massive numbers of coccidian parasites of different stages belonging to Eimeria (E.) cameli and eosinophilic enteritis were detected in the jejunum and ileum by histopathology. Two young camels orally artificially infected with sporulated oocysts of E. cameli showed intermittent diarrhoea already after 1-week and excreted oocysts after 6 weeks (prepatency period). E. cameli caused coccidiosis was found in these camels euthanized after 8 weeks. These findings suggests that E. cameli is much more pathogenic than previously suspected and that E. cameli is the specific coccidian species for the dromedary camel. In winter 2001 eight camel calves (4 to 8 weeks old) were investigated, which suffered from a severe diphtheroid colitis. Histopathology revealed numerous small coccidian-stages in the colon mucosa and eosinophilic colitis. Oocysts containing 2 sporocysts with 4 sporozoites each were found in colon smears and faecal samples. These oocysts were very similar in size and shape to Isospora (I.) orlovi . Again the camel turned out as a unique species because of the unusual aspect of the association of an Isospora-parasite with colitis. There is no report of any Isospora spp. causing severe coccidiosis of the large intestine in any animal species.

Zusammenfassung

In den Jahren 1996 bis 2001 wurden 522 Dromedare aus dem Emirat Dubai (286 Kälber, 69 Jungkamele, 112 Rennkamele und 55 Zuchtkamele) am CVRL in Dubai auf ihre Todesursache hin untersucht. 142 Kamele (60.2% von 236 Kamelen älter als ein Jahr) hatten Eimeria-stadien im Dünndarm, bei 108 Tieren fand sich eine Kokzidiose, bei 34 eine Eimeria-Infektion. 94 der 236 Dromedare älter als ein Jahr (39.8%) and alle 286 Kälber (jünger als 1 Jahr) waren frei von Eimeria-stadien. Bei 55 an Kokzidiose erkrankten Tieren konnte zusaetzlich eine Enterotoxämie, verursacht durch Cl. perfringens oder B. Cereus, diagnostiziert werden. Bei der Sektion fanden sich hochgradige intestinale Hämorrhagien. Histologisch wurden massenhaft verschiedene Kokzidienstadien von Eimeria (E.) cameli und eine eosinophile Enteritis in der Lamina Propria von Jejunum und Ileum nachgewiesen. Zwei junge Kamele wurden experimentell oral mit sporulierten Oocysten von E. cameli infiziert. Beide Tiere zeigten bereits 1 Woche nach der Infektion intermittierende Diarrhoe und schieden den Parasiten nach 6 Wochen aus (Prepatenz-periode). Bei beiden, nach 8 Wochen euthanasierten Tieren, wurde histologisch eine durch E. cameli verursachte Kokzidiose nachgewiesen. Unsere Resultate unterstreichen, dass E. cameli erstens eine viel höhere Pathogenität besitzt als bisher angenommen, und dass zweitens E. cameli die spezifische Kokzidienart des Dromedars darstellt. Im Winter 2001 kamen 8 Kamelkälber (4 bis 8 Wochen alt) zur Untersuchung, die an einer schweren diphtheroiden Kolitis litten. Histologisch fanden sich zahlreiche kleine Kokzidienstadien in der Kolonmukosa sowie eine eosinophile Kolitis. Typische Oozysten mit 2 Sporocysten mit jeweils 4 Sporozoiten wurden in Kolonabstrichen und Stuhlproben gefunden. Diese Oozysten waren in Grösse und Form denen von I. orlovi sehr aehnlich. Eine Kolitis ausgelöst durch Isospora-Parasiten ist höchst ungewöhnlich. In der Literatur existiert für kein Bericht über Isospora-Parasiten, die eine Kolonkokzidiose beim Tier verursachen.



Résumé Entre 1996 et 2001, 522 dromadaires issus des alentours de Dubaï (286 juvéniles, 69 jeunes adultes, 112 dromadaires de course et 55 dromadaires reproducteurs) ont été autopsiés au CVRL de Dubaï afin de déterminer la cause de leur mort. Chez 142 dromadaires (60,2% des 236 dromadaires âgés de plus d'un an) des Eimeria ont été détectées dans le tube digestif. Parmi ces derniers, 108 étaient atteints de coccidiose et 34 présentaient une infection à Eimeria. 94 dromadaires âgés de plus de un an (39,8%) et 286 juvéniles (âgés de moins de un an) ne présentaient aucune forme d'Eimeria . En outre, chez 55 dromadaires souffrant de coccidiose, des entérotoxémies causées, soit par Clostridium perfringens, soit par Bacillus cereus ont été diagnostiquées. Des hémorragies intestinales sévères ont été retrouvées à l'autopsie, et des nombres importants de coccidies à différents stades appartenant au genre Eimeria (E. cameli) ont été constatés. De plus, des entérites éosinophiliques ont été détectées dans le jéjunum et l'iléon par histopathologie. Deux jeunes dromadaires ont été infestés artificiellement par voie orale avec des ookystes sporulés de E.cameli Ils ont présenté une diarrhée intermittente à partir d'une semaine et ont excrété des ookystes après 6 semaines (période prépatente). Après 8 semaines, ils ont été euthanasiés et E.cameli a été identifiée comme agent causal de la coccidiose à l'autopsie. Ces résultats suggèrent que E.cameli est bien plus pathogène qu'on ne le suspectait auparavant et que E.cameli est l'espèce de coccidie spécifiquement adaptée au dromadaire. En hiver 2001, 8 juvéniles (4 à 8 semaines d'âge) ont été autopsiés et ont révélé une colite dyptéroïde sévère. L'histopathologie a mis en évidence de nombreux stades coccidiens dans la muqueuse du colon et une colite éosinophilique. Des ookystes contenant deux sporocystes, contenant eux mêmes 4 sporozoïtes ont été retrouvés dans les frottis du colon et les échantillons fécaux. Ces ookystes étaient très similaires en taille et en forme à Isospora (I. orlovi). Une fois de plus, le dromadaire s'est démarqué des autres espèces, de par l'association originale d'une parasitose à Isospora avec une colite. Aucun cas d'infestation à Isospora responsable d'une coccidiose sévère du gros intestin n'a été rapporté chez d'autres espèces. Key words : Coccidiosis , Isospora, Eimeria cameli, Camelus dromedarius Introduction Six species of intestinal coccidian parasites have been described in Old World camelids (1, 2). These are five species of Eimeria (E.) and one species of Isospora (I. orlovi ). There are numerous reports on Eimeria findings in camelids in the literature. However, most of the reports are concerning the presence of coccidian oocysts in faecal samples of healthy camels (3 to 8). Severe coccidiosis causing enteritis and a mortality rate up to 10% in young camels have been reported in only few cases (1, 9 to 12). The coccidian species associated with disease (coccidiosis) are primarily E. cameli and E. dromedarii, but also E. rajasthani seems to be pathogenic (11). All these species belong to the Eimeria -genus but the validity of some of these coccidian species for camels is still in doubt. There is also some confusion in the literature regarding the species names, especially concerning E. cameli/noelleri and E. dromedarii (3, 13, 14). It seems to be difficult to distinguish between the four small Eimeria spp. (5) as they only vary slightly in size (4,5). There are only few reports of Isospora-infections in camels (16 to 18). The pathogenic role of I. orlovi is unknown (19). The aim of this study was to evaluate the incidence and importance of coccidiosis in necropsy material from the Central Veterinary Research Laboratory (CVRL) Dubai, UAE and to proof the pathogenicity of E. cameli in dromedary camels. Material and Methods Between 1996 and 2001 a total of 522 fresh camel carcasses (286 camel calves (up to 1 year of age), 69 young; 112 racing and 55 breeding camels) from Dubai area were submitted for necropsy examination including histological investigation. All necropsies were performed within 1 to 5 hours after death. Pieces of intestine, liver, spleen and lymph nodes were taken for microbiological investigations using routine methods. The intestinal samples were also tested for the growth of anaerobes using Zeissler agar containing antibiotic supplement (Oxoid, SR93). The plates were incubated under anaerobic conditions (Gas generating kit, Oxoid) at 37°C for 48 hours. All intestinal samples were also spread onto Bacillus (B.) cereus agar containing egg yolk emulsion and Polymixin B supplement (Oxoid, SR99). The specimens were enriched in tetrathionate broth followed by culture on brilliant green phenol red lactose agar and pril mannitol agar for the



detection of salmonella organisms. Faecal samples from each necropsied camel were collected for parasitological examination using the flotation method. For the histopathological investigation, small pieces of all parenchymatous organs, the gastrointestinal tract (compartments, abomasum, duodenum, jejunum, ileum, colon and caecum) as well as muscles and body lymph nodes were sampled. Samples from 10 locations of the small intestine (80-cm apart) were taken for histopathological investigations from 25 camels suspected for coccidiosis. All these samples were fixed in 10% buffered formalin solution for 24 hours and 5 µm thin sections were cut and stained with haematoxilin and eosin (H&E-stain). Coccidiosis was confirmed by histology when numerous coccidia stages in the intestinal mucosa (more than 1 per high-power field in several locations) in association with degeneration and desquamation of the intestinal epithelium and a eosinophilic enteritis was observed. In contrast, a coccidia-infection was characterized, when only a few coccidia stages and no inflammation of the mucosa were seen. To proof the pathogenicity of E. cameli, an infection trial was carried out. Colon contents of 25 dissected racing camels (out of the 236 camels) with coccidiosis were collected. Through repeated washing and sifting of the content the oocysts were concentrated. The oocysts were then sporulated within 6 to 8 weeks in 2.5% potassium dichromate solution at room temperature. Two, 18-month-old camels were orally infected with 100.000 sporulated E. cameli oocysts. Over a period of 6 weeks, faecal samples from both camels were collected every other day and investigated for coccidia oocysts. Both camels were euthanized after 8 weeks and a detailed post-mortem investigation was performed. Results

From 236 necropsied camels older than one year 142 (60.2%) were infected with Eimeria-spp . (Table 3). Coccidiosis was diagnosed in 108 camels (45.8%) and an Eimeria-infection in 34 cases (14.4%), only 94 animals (39.8%) were free of Eimeria (Table 1). The prevalence fluctuated between 58% and 76% in the first years and had a decreasing tendency in the last 3 years. Table 1. Eimeria-coccidiosis and Eimeria-infection in 236 necropsied dromedaries older than 1 year (diagnosed by histopathological investigation) between 1996 and 2001 Number of cases 1996 1997 1998 1999 2000 2001 Total

Dissected camels 36 50 50 25 35 40 236

With coccidiosis 18 31 32 8 8 12 108

With Eimeria-infection 3 6 6 7 5 7 34

Total positive for Eimeria 58.3% 72% 76% 60% 37.2% 47.5% 60.2%

Coccidiosis was highest in racing camels (50.9%) followed by breeding camels (41.8%) and young camels (40.5%), respectively (Table 2). The Eimeria-infection showed a similar pattern. Table 2. Distribution of Eimeria-coccidiosis and Eimeria-infection in 236 necropsied dromedaries of different age groups Group

Age in years Number dissected

Eimeria - Coccidiosis

Eimeria- infection

No coccidia found

1 Calves 286 - - 286 2 1 – 3 (young) 69 28 (40.5%) 4 (5.7%) 37 3 3 – 10 (racing) 112 57 (50.9%) 24 (21.2%) 31 4 > 10 (breeding) 55 23 (41.8%) 6 (10.9%) 26 Total 236 94 (45.8%) 34 (14.4%) 94

In all coccidiosis cases of groups 2 and 3, large amounts of barley were detected in the stomach compartments, which resulted in rumen acidosis of compartment 1. The main pathomorphological findings in these camels were severe haemorrhages with fresh blood in the intestinal lumen (Fig.



1), in combination with a swollen and reddened mucosa of the compartment 3, abomasum, jejunum and ileum. In several cases fresh ulcerations were present in the abomasum and the ascending colon was filled with tar-like blood. In the third group these lesions were not observed, but severe ascites was always found in conjunction with coccidiosis.

Figure 1: Gastrointestinal tract of a racing camel: severe haemorrhages in the small intestine Figure 2: Histology of Fig. 4: numerous coccidia stages (zygotes, oocysts, macroschizonts and meronts) located in the mucosa of the jejunum In all camels, which suffered from coccidiosis, numerous coccidia stages (zygotes, oocysts, macroschizonts and meronts) were located in the mucosa of the jejunum and ileum (Fig. 2), but rarely in the duodenum and none in the colon. In 25 camels, where intensive histology was carried out on the intestines (10 locations of the small intestine), the highest concentration of coccidia stages was found in the caudal part of the jejunum and in the ileum. The size and shape of these Eimeria stages are found in Table 3.

Table 3 . Description of Eimeria stages found in the intestinal mucosa of camels Stage Size (µm) Shape Wall Content Meront 240 to 330 Round to ovoid Thin Numerous merozoites Macroschizont

240 to 330 Round to ovoid Thin Numerous schizonts

Zygots/oocysts

Up to 100x80 Piliform Thick, brown Non sporulated

In locations with numerous coccidia stages (coccidiosis), a marked infiltration of the mucosa with eosinophilic granulocytes and a few macrophages were observed. Where few coccidia stages were found, the intestine showed a mild oedema of the mucosa, only (Eimeria - infection). Microscopic examination of lymph nodes and spleen demonstrated a severe sinus oedema and in combination with enterotoxaemia, depletion of the lymphatic tissues, central follicle necrosis and interstitial haemorrhages.

Figure 3: Faeces of a racing camel: large, brownish Eimeria-oocysts Figure 4: Colon of 8-week old camel calf: Severe diphtheroid to haemorrhagic colitis



No Eimeria-spp. were found in the 286 camel calves younger than 1 year. These calves died either from septicaemia, colon impaction or white muscle disease. However, between January and March 2001, eight camel calf were submitted for post-mortem examination. These calves (4- to 8-week-old) came from 2 farms and showed diarrhoea between 2 and 5 days with no response to any treatment. Gross pathological examination revealed severe diphtheroid colitis (Fig. 4). Massive numbers of small coccidian-stages were detected in the lamina propria of the colon by histopathological studies. Histological sections showed destruction and disorganisation of the mucosa together with haemorrhages and infiltration of eosinophilic granulocytes and macrophages. Numerous small coccidian stages (zygotes and oocysts) were located in the mucosa of the colon (Fig. 5), bu t not in the small intestine. These oocysts, containing 2 sporocysts with 4 sporozoites each (Fig. 6) were also found in colon smears and faecal samples. Most of the oocysts were sporulated at the time of investigation. The oocysts were ellipsoidal to ovoid, figure 8-shaped, 30-33 x 18-21 µm with a smooth, 2-layer wall about 1 µm thick; without a micropyle, polar granule, or residuum. The two sporocysts per oocyst were ellipsoidal with a size of 10-15 x 17–19 µm containing four elongated ellipsoidal sporozoites 4-6 x 11 - 13 µm in size. 51% (**) of the 108 coccidiosis-cases suffered simultaneously from a Cl. perfringens/B. cereus enterotoxaemia (Table 3). In 33(*) of the coccidiosis cases, no causative agent for enterotoxaemia was demonstrated. However, the same pathomorphological findings indicate a simultaneous enterotoxaemia as well. Most of the coccidiosis/enterotoxaemia camels showed a severe sickness with abdominal pain and inappetence for 3 to 7 days. Fifteen camels developed also bloody faeces, but no diarrhoea was observed. In combination with the enterotoxaemia, ecchymotic haemorrhages of varying severity were also seen subepicardial as well as subendocardial. All lymph nodes were enlarged, oedematous and hemorrhagic. The lungs were congested and showed severe alveolar oedema. In breeding camels severe ascites was always found in conjunction with coccidiosis, but no enterotoxaemia was observed.

Figure 5: Histology of Fig.1: destruction and disorganisation of the colon mucosa; infiltration with eosinophils and macrophages; numerous small coccidian stages (zygotes and oocysts) located in the mucosa Figure 6: Faeces of 8-week old camel calf: Isosporan-oocysts, containing 2 sporocysts with 4 sporozoites; one nonsporulated oocysts Table 4 . Relati on between Eimeria-infection/coccidiosis and main diseases in 236 necropsied dromedaries, older than 1 year

Coccidia-status Main diseases

Eimeria-Coccidiosis

Eimeria-Infection

No Coccidia

Enterotoxaemia 55 (23.3%)** - 18 (7.6%) Coccidiosis, only 33 (14%)* - - Ascites, CCN, Hepatosis 20 (8.5%) 34 (14.4%) 76 (32.2%) Total: 236 108 (45.7%) 34 (14.4%) 94 (39.8%)

Examination (flotation) of faecal samples from most of the 522 necropsied camels had negative results for Eimeria-oocysts, except of 31 samples (from camels with coccidiosis), which contained



large, brownish Eimeria-oocysts (Fig. 3). After repeated washing and sifting of the entire colon and rectum contents of 25 dissected camels suspicious of coccidiosis, the large brownish oocysts of E. cameli were concentrated and were detected microscopically in all cases. These concentrated oocysts then needed 6 to 8 weeks under room temperature to sporulate. Two young camels, which were artificially infected with sporulated oocysts of E. cameli by the oral route, excreted the parasite after 6 weeks (prepatency period). Both of the infected camels showed intermittent diarrhoea already after 1-week post infection and were euthanized after 8 weeks. Histopathology revealed severe coccidiosis with innumerable, different coccidia stages in the mucosa of jejunum and ileum in both dromedaries. Discussion Between 1996 and 2001 a total of 522 dromedaries were investigated at the Central Veterinary Research Laboratory (CVRL) in Dubai for the cause of their death and especially for the presence of coccidia. Of these, 286 were camel calves and 236 were dromedaries older than 1 year comprising of 3 different age groups (69 young camels, 112 racing camels and 55 breeding camels). In camels older than 1-year only Eimeria spp. and no Isospora spp. were found. 142 camels (60.2% of 236 camels older than one year) were diagnosed as having Eimeria-stages in their gut, of which 108 (45.7%) revealed a coccidiosis, and 34 (14.4%) an Eimeria- infection. Ninety-four dromedaries (39.8%) were free of coccidia. It is worth mentioning, that no Eimeria-spp. were detected in dromedary calves. In contrast to other camelids (20) and numerous domesticated and wild ruminants (21; 22), we found that camel coccidiosis in the UAE caused by E. cameli is not a disease of dromedary calves. This might be due to the fact that fresh alfalfa (the possible source of coccidia) is an important protein source for both young and racing camels in the UAE, but not for calves. Contamination of fresh alfalfa with coccidia oocysts may occur when alfalfa fields are fertilized with camel, cattle or goat manure. Another possibility of Eimeria infection is the habit of camels to ingest their own faeces and become reinfected. High levels of relative humidity contribute to the survival of oocysts outside the host (23). The spread of camel coccidiosis with many reported fatalities during the years 1996 to 1998 in the UAE was most probably associated with a very wet climate in these years, whereas in the years 1999 to 2001 only little rain fell in the Dubai area. Higher prevalence of Eimeria spp. in camel faecal samples were found in rainy season (31.2%) compared to dry season (20.6%) in India (8). Another factor might also be, that the alfalfa fields are regularly flooded. Future investigations should include the testing of fresh alfalfa for coccidian contamination. In 55 camels (15 young and 40 racing camels; Table 3) enterotoxaemia caused either by Cl. perfringens or B. cereus was additionally diagnosed. This disease is well known in the UAE as HD (haemorrhagic disease) or endotoxicosis (24). An outbreak of a similar disease with massive coccidiosis in 1200 camels occurred in India with a mortality rate of 40% (9). In 33 of our camels with coccidiosis (young and racing camels), no causative agent of enterotoxaemia was demonstrated. However, the same pathomorphological findings in these camels indicated a simultaneous enterotoxaemia as well. In the remaining cases showing either no Eimeria-stages or mild forms of coccidiosis, no other infectious disease was demonstrated (Table 3). Histological investigation of the coccidiosis cases revealed massive numbers of different coccidian stages in the intestinal mucosa. At least 5 different locations of the small intestine, especially the caudal ileum and jejunum must be examined to diagnose coccidiosis. Similar to the first scientific description of camel coccidiosis caused by E. (Globidium) cameli (25), the authors found numerous coccidia stages and a severe infiltration of the mucosa with eosinophilic granulocytes and few macrophages. Different stages of E. cameli (oocysts, zygotes, macroschizonts and meronts) were identified in the intestinal mucosa (Table 2). It was considered that these stages belong to E. cameli, because immature oocysts similar to E. cameli (2) were found within the intestinal epithelial mucosa. Our investigations showed that in young and racing camels more fatal cases were found in conjunction with enterotoxaemia and septicaemia. The increased fatalities may be explained with



the special feeding practices for racing purpose in the UAE (24). This is indicated by the detection of an increased amount of barley in the stomach compartments and the associated acidosis, which influence the natural intestinal flora. The altered intestinal environment can trigger the growth of Cl. perfringens and B. cereus bacteria causing enterotoxaemia. As described in chickens (26), a simultaneous infection with Eimeria spp. and Cl. perfringens increases clostridial population in the intestine and has synergic effects leading to an increased mortality. In contrast, breeding camels in the UAE do not receive a high energetic diet and therefore rarely develop enterotoxaemia (27). In this age group (group 4) a different disease pattern was observed with severe ascites and coccidiosis. Eimeria -infection without coccidiosis was found in 4 young, 24 racing and 6 breeding camels (Table 2). The main diseases in these cases were either cerebrocorticalnecrosis (CCN) in racing camels or hepatosis in breeding camels, but never enterotoxaemia. Most probably need E. cameli synergic effects from Cl. perfringens or B. cereus bacteria causing enterotoxaemia to develop a coccidiosis. It is worthwhile mentioning that only in 31 (2 1.8%) out of 142 Eimeria-cases E. cameli oocysts were found in faecal samples from the dissected camels. However, after using a concentration method oocysts were detected in the colon contents. This result indicates either a diagnostic problem in our routine parasitological investigation or a very low excretion of oocysts. The simple flotation method might not be adequate enough to isolate the large and heavy oocysts of E. cameli. This could also have been the reason, that E. dromedarii was found being the most, and E. cameli the least in 385 Saudi Arabian camels (11). Other authors (28) described the same diagnostic problem with oocysts of E. leuckartii in horses, which have similar size as E. cameli. Therefore a combined sedimentation and flotation method might be necessary for routine parasitology. To prove the pathogenicity of E. cameli, intestinal contents of 25 dissected camels suffering from coccidiosis were collected and the oocysts were concentrated and sporulated. The oocysts needed 6 to 8 weeks to sporulate. Two young camels artificially infected with sporulated oocysts of E. cameli by the oral route excreted the parasite after 6 weeks (prepatency period). Both of the infected camels showed intermittent diarrhoea already after 1-week post infection. Massive coccidiosis caused by innumerable different stages of E. cameli was found by histology in intestine of both camels euthanized after 8 weeks. Our findings support the thesis suggesting that E. (Clobidium) cameli is the specific coccidian species for the dromedary camel (29). It is interesting to note that the E. cameli-oocyst is nearly identical in size and shape to E. macusaniensis, found in South American camelids (30,31). All 286 camel calves (younger than 1 year) were free of Eimeria-spp. However, four species of Eimeria were found in faecal samples from 45 healthy Indian camel calves (14). A high prevalence (75.6%) of Eimeria-infection was found in camel calves below one year in India (8). However, between January and March 2001, a new camel calf disease occurred in Dubai. The calves on two farms showed diarrhoea between 2 and 5 days with no response to any treatment. Eight of these calves (4 to 8 weeks old) were submitted for post-mortem examination. Gross pathological examination of these eight calves revealed severe diphtheroid colitis. Massive numbers of small coccidian-stages were detected in the lamina propria of the colon by histopathological studies. Eimeria spp. are distinguished from Isospora spp. by the sporulated oocysts. Eimeria spp. contain 4 sporocysts with 2 sporozoites each, whereas Isospora spp. have 2 sporocysts with 4 sporozoites each (2). It was considered that the coccidian stages in these 8 calves cases belong to an Isospora spp., because typical oocysts (containing 2 sporocysts with 4 sporozoites each) were found in colon smears and faecal samples. The oocysts of I. orlovi are described as ellipsoidal, ovoid, piriform, to figure 8-shaped, 27-35 x 15-20 µm with a smooth, 2-layer wall about 1 µm thick without a micropyle, po lar granule, or residuum. The sporocysts are ellipsoidal to ovoid (13-15 µm in diameter) with a residuum and without Stieda body. The sporozoites are elongated ellipsoidal, 7-10 x 4-6 µm (2, 17). As the oocysts in our cases resembled I. orlovi, it is believed that the outbreak was caused by I. orlovi. It is worthwhile to note, that around 50 % of the oocysts were already sporulated in the faecal samples at time of investigation. In our laboratory it usually takes 6 to 24 hours to examine the slides after sa mpling. This might be long enough for oocysts to sporulate. The high number of sporulated oocysts in the faeces may be a reason, that I. orlovi is thought by (17) to be an avian



form, accidentally ingested. As they are multiplying in the colon mucosa causing severe colitis with no pathogenic bacteria detected, our Isospora spp. is thought to be an original camel pathogen. The source of infection remains unknown. The calves got only milk form their mothers (which were free of coccidia by parasitological investigation) and may have ingested also some hay. Since copper deficiency was diagnosed in dromedary calves and their dams in the UAE (32), the calves may have tried to compensate a copper deficiency by ingesting sand containing Isospora oocysts. Another case of Isospora-coccidiosis is described by (18) with a six-month-old camel calf showing diarrhoea and abdominal pain. Faecal examination revealed 2000 Isospora oocysts per gram faeces. Size and shape of the oocysts were similar to I. orlovi. However, the authors did not identify the parasite. Again the camel turns to be an unique species due to the unusual aspect of colitis caused by isospora. There is no report of any isosporan causing severe coccidiosis of the large intestine in any other animal species.

References 1. 2. Levine, N.D. and V. Ivens. 1970. III Biology Monograph Series No. 44, Urbana, University of Illinois Press. 3. Levine, N.D. 1985. Veterinary Protozoology, 1st ed. Iowa State University Press, Ames. 163-202. 4. Gill, H.S. (1976). Incidence of Eimeria and Infindibulorium in camel. Indian Vet. J., 53, 897-898. 5. Kasim, A.A., H.S. Hussein and Y.R. Al Shawa. 1985. Coccidia in camels (Camelus dromedarius) in Saudi Arabia. J.

of Protoz. 32: 202-203. 6. Yagoub, I.A. (1989). Coccidiosis in Sudanese camels (Camelus dromedarius ): 1. First record and description of

Eimeria spp. harbored by camels in the eastern region of Sudan. J. Protozoal, 36, 422-423. 7. Derwish, A.I. and V.G. Golemansky. 1993. Coccidia (Apicomplexa, Eucoccidiida) in camels (Camelus dromedarius

L.) from Syria. Acta Zoolog. Bulgarica. 46: 10-15. 8. Mahmoud, O.M., E.M. Haroum, M. Magzoub, O.H. Omer and A. Sulman. 1998. Coccidial infection in camels of

Gassim region, central Saudi Arabia. J. Camel Pract. and Res. 5: 257-260. 9. Partani, A.K., D. Kumar and G.S. Manohar. 1999. Prevalence of Eimeria infection in camels (Camelus dromedarius )

at Bikaner (Rajasthan). J. Camel Pract. and Res. 6(1): 69-71. 10. Hamanchandran, P.K., Ramachnadran, S. and Joshi, T.P. (1968). An outbreak of hemorrhagic gastro-enteritis in

camels. Ann. De Paras. 18, 5-14. 11. Chineme, C.N. (1980). A case report of coccidiosis caused by Eimeria cameli in a camel (Camelus dromedarius) in

Nigeria. J. Wildlife Dis. 16, 377-380. 12. Hussein, H.S., Kasim, A.A. and Shawa, Y.R. (1987). The prevalence and patholo gy of Eimeria infections in camels

in Saudi Arabia. J. Comp. Path., 107, 293-297. 13. Kinne, J. and Wernery, U. 1997. Severe outbreak of camel coccidiosis in the United Arab Emirates. J. Camel Pract.

and Res. 4, 261-265. 14. Enigk, K. (1934). Zur Kenntnis des Glob idium und der Eimeria cameli. Arch. Protistenkd. 83, 371-380. 15. Dubey, U.P. and Pande, B.P. (1964). On Eimerian oocysts recovered from Indian camel (Camelus dromedarius).

Indian J. Vet. Sci. 34, 28-34. 16. Tscherner, W. (1973). Kokzidien bei Wiederkauern im Tierpark Berlin. Verh. Ber. Erkrg. Zootiere, Kolmrden, 103-

110. 17. Zigankoff, A.A., 1950: Contribution to the knowledge of coccidian from the camel. Izv. Kazah. SSR. Ser. Par. 8, 174-

180. 18. Péllerdy, P. 1965. Coccidia and Coccidiosis. Akademiai Kiado, Publishing House of the Hungarian Academy of

Sciences, Budapest, 510-516. 19. Raisanghani, P.M., Manohar, G.S. and J.S. Yadav, 1987: Isospora infection in the Indian camel (Camelus

dromedarius). Indian J. of Parasitology. 11, 93-94. 20. Kaufmann, J. 1996. Parasitic infections of domestic animals - A diagnostic manual, Birkhäuser Verlag, Basel,

Boston, Berlin. 21. Haenichen, T., Wiesner, H. and Goebel, E. (1994). Zur Pathologie, Diagnostik und Therapie der Kokzidiose bei

Wiederkaeuern im Zoo. Erkr. Zootier, 36, 375-380. 22. Kiefer, I. (1993). Zum Kokzidienbefall bei Hochgebirgswiederkaeuern und Einfluss der Therapie mit Salinomycin.

Vet. Med. Dissertation, Munich, Germany. 23. Ziesche, T. (1994). Zum Kokzidenbefall beim domestizierten Wiederkaeuern unter Tierparkbedingungen und Einsatz

von Totrazuril als Prophylaktikum. Vet. Med. Dissertation, Munich, Germany. 24. Stepanova, N.J. (1982). Protozoal diseases of farm animals. Moscow, Kolos, 38. 25. Wernery, U. and J. Kinne (2001): Endotoxicosis in racing dromedaries: a review. Journal of Camel Research and

Practice, 8, 2001,65-72. 26. Henry, P.A. and Masson, G. (1932). La coccidiosis du dromedarie. Rec. de Med. Vet. Exotique. 57, 185-193. 27. Baba, E., Ikemoto, T., Fukata, T., Sasai, K., Arakawa, A., and McDouglad, L.R. (1997). Clostridial population and the

intestinal lesions in chickens infected with Clostridium prefringens and Eimeria necatrix. Vet. Microbiol. 54, 301-308. 28. Wernery, U., Ale, M., Wernery, R. and Seifert, H.S.H. (1992). Severe heart muscle degeneration caused by

Clostridium perfringens type A in camel calves (Camelus dromedarius). Rev. Elev. Med. Vet. Pays Trop. 45, (3-4), 255-259.



29. Bauer, C., Buerger, H.J. (1984). Zur Biologie von Eimeria leuckarti (Flesh, 1883 der Equiden). Berl. Muench. Tieraeztl. Wschr. 97, 367-372.

30. Richard, D. 1975. Study on the pathology of the dromedary in Borana Awraja (Ethiopia) Thesis, IEMTV, Paris. 31. Guerrero, C.A., H. Bazalar and J. AlvA. 1971. Eimeria macusaniensis n. sp. (Protozoa: Eimeriidae) of the alpaca

(Lama pacos ). J. Protozool. 18: 162-163. 32. Schrey, C.F., T.A. Abbott, V.A. Stewart and C.W. Marquardt. 1991. Coccidia of the llama, Lama glama, in Colorado

and Wyoming. Vet. Parasitol. 40: 21-28. 33. Wernery, U., M. Ali, J. Kinne, A. A. Abraham and R. Wernery, 2000: Copper deficiency: a predisposing factor to

septicaemia in dromedary calves. 2nd International Camelid Conference, Almaty, Kazakhstan. 8. -12.9.2000. Adress of the authors: Dr. med. vet. J. Kinne Dr. med. vet. habil. U. Wernery Central Veterinary Research Laboratory P.O. Box 597, Dubai, United Arab Emirates



European Association of Zoo- and Wildlife Veterinarians (EAZWV) 4th scientific meeting, joint with the annual meeting of the European Wildlife Disease Association (EWDA) May 8-12, 2002, Heidelberg, Germany.

SPONTANEOUS ECHINOCOCCOSIS IN A COLONY OF LION-TAILED MACAQUES (Macaca silenus)

A. BLANKENBURG1,2, K. MÄTZ -RENSING1, A. DINKEL 3, U. SAUERMANN2 and F.-J. KAUP 1

Affiliation: 1. Dept. Veterinary medicine & primate husbandry, 2. Working group primate genetics, German Primate Center Göttingen, 3. Universitä t Hohenheim Abstract Since 1997 several infections with the second larval stage of the fox tapeworm Echinococcus multilocularis were discovered in a colony of lion-tailed macaques. The animals were mostly kept in an open-air enclosure. In the surrounding of this enclosure, foxes have frequently been noticed. Up to now, three animals died in this colony. The alterations of echinococcosis were characterised using conventional pathomorphological methods. The animals showed typical symptoms like massive proliferative hepatitis and cyst formations. In a neighbouring husbandry, where another primate species (Papio hamadryas) was kept, no infections were diagnosed. For this reason we supposed that lion-tailed macaques have a special susceptibility for alveolar echinococcosis in comparison to the other species. Zusammenfassung Seit 1997 traten in einer Bartaffenkolonie mehrere Infektionen mit dem zweiten Larvenstadium des Fuchsbandwurmes Echinococcus multilocularis auf. Die Tiere wurden hauptsächlich in einem Außengehege gehalten. In der Umgebung dieser Gehege wurden Füchse häufig beobachtet. Bisher erlagen drei Tiere dieser Erkrankung. Zur Beschreibung der Veränderungen der Echinokokkose wurden konventionelle pathomorphologische Methoden angewandt. Die Tiere zeigten die für die Echinokokkose typischen Symptome, wie massive proliferative Hepatitis und Zysten. In einem benachbarten Freigehege einer anderen Primatenspezies (Papio hamadryas), wurden keine Infektionen festgestellt. Aus diesem Grund vermuten wir, dass Bartaffen, im Vergleich zu anderen Primatenspezies, eine besondere Empfänglichkeit für die alveoläre Echinokokkose besitzen. Résumé Depuis 1997 on a découvert plusieurs infections avec le deuxième stade du cestode de renard Echinococcus multilocularis dans une colonie de macaques. La plupart du temps les animaux vivaient dans un enclos de plein air. Aux environs de cet enclos on a souvent remarqué des renards. Jusqu’à présent trois animaux de cette colonie sont morts. On a characterisé les altérations causées par l’echinoccose par l’emploi de méthodes pathomorphologiques conventionnelles. Les animaux présentaient des symptômes typiques comme l’hépatite prolifère massive et la formation de kystes. Dans un enclos voisin où une autre espèce de primate (Papio hamadryas) vivait, on n’a pas diagnostiqué d’infections. Pour cette raison nous supposons que les macaques sont particulièrement susceptibles pour l’échinococcose alvéolaire comparés aux autres espèces. Key words: Macaca silenus, Echinococcus multilocularis, alveolar echinococcosis, MHC Introduction Echinococcus belongs to the phylum of Platyhelminthes, the class of Cestodea and subclass of Eucestodia. The genus of Echinococcus is subordinated to the order of Cyclophyllidea and the family of Taeniidae (11). Echinococcosis is a zoonotic disease, caused by adult or larval stages of cestodes, which belong to the genus Echinococcus. Up to now, four species of Echinococcus are



known – E. granulosus, E. multilocularis, E. oligarthrus and E. vogeli (3). The life of the parasites shows a cyclic structure. The alveolar echinococcosis is an infectious disease, which is caused by the second larval stage (metacestode) of the fox tapeworm. The adult parasite lives in the gastrointestinal tract of foxes of the genera Vulpes and Alopex, which are the definitive hosts. The eggs, including the first larval

Fig. 1: Histology of metacestoidic tissue of the liver. Alveolar echinococcosis, liver tissue with protoscollices (arrows). HE 376 x stage (oncosphere), get outside with the faeces and are ingested by intermediate hosts, which typically are rodents particularly of the family Arvicolidae . In the intermediate host, the oncosphere penetrates the intestinal wall and enters the blood system by this way. Via the bloodstream, the oncosphere reaches different organs, but usually the liver. Once the oncosphere has reached the liver it starts to develop into the metacestode stage (3). In contrast to E. granulosus with the development of an unilocular cyst, the typical cyst of E. multilocularis shows an multilocular structure (8). The cyst with broodcapsules and protoscolices may disturb the functions of the liver, depending on its size and location. The development of protoscolices can take several months. There may be several thousand protoscolices within a cyst (3), (Fig. 1). If protoscolices are ingested by a definitive host, they develop to the sexually mature adult tapeworm, approximately four to six weeks after infection. Thus the cycle is closed (3, 1). All mammals (including man and nonhuman primates) in which metacestodes develop may be an "intermediate host", but it is important to distinguish between a real intermediate host, which plays a role in the perpetuation of the cycle, and an "accidental intermediate host" which is a dead end for the parasite. The latter is not involved in the transmission of the disease, because the metacestode stages do not become fertile or these hosts do not interact in the transmission cycle (3). Here we describe cases of echinococcosis in a colony of lion-tailed macaques.



Case report Since 1997 three cases of echinococcosis occured in the lion-tailed macaque colony (with totally 12 animals) of the German Primate Center. The animals (animal 1: female, 11 years old; animal 2: female, 11 years old; animal 3: male, 6 years old) showed no remarkable disturbances of the general condition. The only symptom was an enlargement of the abdomen in all three cases. Techniques like x-ray, ultrasound, laparatomy and PCR were used for diagnosis. All animals were euthanised and necropsied. Pathology The main pathological findings in all three cases were severe hepatomegaly with fibrous transformation of the liver tissue. Multiple cysts of different size were distributed throughout the fibrous hepatic tissues. The cysts had a diameter up to 20 cm and a weight up to 4000 g. They were filled with gelatinous to liquid material and contained hydatid sand. A generalised subacute peritonitis was a concomitant finding in all three animals investigated. All mesenteric lymph nodes appeared enlarged. In one animal comparable cysts were found within the lung tissue. Histology Histology revealed that large, infiltrating growing cysts of different size, surrounded by thick fibrous hyaline membranes destroyed the liver tissue. Most cysts appeared empty. Some fertile cysts containing protoscolices were demonstrable (Fig. 1). The cysts were surrounded by chronic inflammatory cell infiltration with foreign body - type giant cells. Some areas contained calcified materia l. But only the liver showed fertile cysts, which means that they contained protoscolices. In all other infected organs (lungs, colon, lymph nodes) the cysts were sterile, without protoscolices and broodcapsules. This is typical for accidental intermediate hosts, which normally represent a dead end for the parasite.

Fig. 2: Results of E. multilocularis –specific nested PCR. Lane 1: Macaca silenus animal 1; lane 2: Macaca silenus animal 2; lane 3: Macaca silenus animal 3; lane nK: negative control; lane pK: positive control (E. multilocularis).



Diagnosis According to the characteristic pathomorphological and histological findings with the typical cyst formation, infiltrating growth pattern and the hooklet shape, E. multilocularis was diagnosed in all three cases. This could be confirmed by PCR (Fig. 2). Discussion This report represents the first description of alveolar echinococcosis (AE) in lion-tailed macaques. AE has been described in Macaca mulatta (2), Macaca sylvana (5), Gorilla gorilla (7), Lemur catta (7), Macaca fascicularis (9), however it is a rare but severe disease in primates. Foxes and other carnivores like dogs and cats are the definitive hosts of E. multilocularis. Primates including man can be dead-end hosts, because normally they are not involved in the transmission of the disease. Reasons for this could be 1. the cysts do not become fertile in primates, or/and 2. primates do not interact in the transmission cycle. Foxes in Lower Saxony have a prevalence of E. multilocularis of up to 50 % (4, 10). The most important way of infection is a contamination of the environment with faeces from foxes, especially in this case a contamination of branches and grass, which will be picked up by the animals during food intake. Some primate species seem to be more susceptible for E. multilocularis than man (9) and other primate species. This apparently applies to lion-tailed macaques. Due to this phenomenon we started a genetical characterisation of the Major Histocompatibility Complex (MHC) in lion-tailed macaques, as basis for further studies in the field of immunology and infectious diseases in this primate species. References 1. Ammann RW and Eckert J. Cestodes: Echinococcus. In: Weinstock JV (Ed) Parasitic Diseases of the Liver and

Intestines. Gastroenterology Clinics of North America. W.B. Saunders Company. Philadelphia 1996; 655-89. 2. Brack M, Tackmann K, Conraths FJ and Rensing S. Alveolar hydatidosis (Echinococcus multilocularis) in a captive

rhesus monkey (Macaca mulatta) in Germany. Trop Med Int H 1997; 2 : 754-59. 3. Eckert J, Gemmell MA, Meslin F-X and Pawlowski ZS (Eds).WHO/OIE Manual on Echinococcosis in Humans and

Animals: a Public Health Problem of Global Concern. World Organisation for Animal Health and World Health Organisation 2001.

4. Eckert J. Epidemiology of Echinococcus multilocularis and E. granulosus in Central Europe. Parasitologia 1997; 39: 337-44.

5. Haddane B. Hydatid disease in macaques. Erkrankungen der Zootiere 1993; 35: 213-15. 6. Janeway CA and Travers P. Immunologie. 2. Auflage Spektrum Verlag Heidelberg Berlin Oxford 1997. 7. Kondo H, Wada Y, Bando G, Kosuge M, Yagi K and Oku Y. Alveolar Hydatidosis in a Gorilla and a Ring-Tailed

Lemur in Japan. J Vet Med Sci 1996; 58: 447-49. 8. Mehlhorn H, Piekarski G. Grundriß der Parasitenkunde.5. Auflage Gustav Fischer Verlag Stuttgart Jena Lübeck Ulm

1998. 9. Rietschel W, Kimmig P. Alveoläre Echinokokkose bei einem Javaneraffen. Tierärztl Prax 1994; 22: 85-8. 10. Romig T, Bilger B, Mackenstedt U. Zur aktuellen Verbreitung und Epidemiologie von Echinococcus multilocularis.

Dtsch tierärztl Wschr 1999; 106: 352-57. 11. Rommel M, Eckert J, Kutzer E, Körting W and Schnieder T. Veterinärmedizinische Parasitologie. 5. Auflage,

Blackwell Wissenschafts-Verlag, Berlin Wien 2000. Address Anja Blankenburg German Primate Center Department of Veterinary Medicine and Primate Husbandry Kellnerweg 4 D-37077 Göttingen, FRG Phone: +49-551 -3851 -270 Fax: +49-551-3851 -277 e-mail:[email protected]



European Association of Zoo- and Wildlife Veterinarians (EAZWV) 4 th scientific meeting, joint with the annual meeting of the European Wildlife Disease Association (EWDA) May 8-12, 2002, Heidelberg, Germany.

BIOHELMINTHS: LIFE CYCLES ESTABLISHED IN THE TIERPARK BERLIN-FRIEDRICHSFELDE

W. TSCHERNER

Affiliation: Tierpark Berlin-Friedrichsfelde, Am Tierpark 125, D-10307 Berlin, Germany Abstract Self-sustaining life cycles of heteroxenous helminths may get established in zoological gardens. Examples are given from the Tierpark Berlin-Friedrichsfelde comprising trematode, cestode, acanthocephalid and nematode life cycles. Zusammenfassung Der Entwicklungskreislauf heteroxener Parasiten kann sich in Tiergärten etablieren. Beispiele von Trematoden, Cestoden, Acanthocephalen und Nematoden aus dem Tierpark Berlin-Friedrichsfelde werden genannt. Résumé Des cycles autonomes d'helminthes hétéroxènes peuvent s'établir dans les parcs zoologiques. Des exemple décrivant des cycles de trématodes, cestodes, acanthocéphales et nématodes sont exposés ici à partir de données du zoo de Berlin-Friedrichsfelde Key words: Biohelminths, life cycles, and zoo animals. Introduction In contrast to geohelminths which develop directly biohelminths have indirect life cycles requiring at least one intermediate host (= larval host). Trematodes and acanthocephalids are entirely biohelminths as are with very few exceptions the tapeworms and pentastomids. 75 % of the nematodes are nonparasitic, the remaining are parasites developing directly or indirectly. In zoological gardens geohelminths find best conditions for development. The zoo animal as the only host is always present, usually living in groups at more or less limited areas. Those helminths therefore are a stock item in zoo animal collections. Species of Trichuris, Capillaria, Toxocara, Toxascaris, Baylisascaris, Ascaridia, Heterakis, Strongylus, and Strongyloides are examples. In the ontogenetic cycle of biohelminths zoo animals may be final hosts or intermediate hosts. In many cases the ontogenesis of such parasites ends after having invaded the zoo animal. This is always the case when zoo animals harbour larval stages, e.g. hydadits of Echinococcus, and sometimes also when harbouring adult parasites which are lacking suitable intermediate hosts in the zoo. Zoo animals share their habitats with wild animals, vertebrates as well as invertebrates. Adult parasites of such vertebrates, e.g. stray cats, foxes, mallards, pigeons, and many other bird species may shed and distribute eggs or larvae. Invertebrates, e.g. earth worms, insects or crustaceans, are potential intermediate hosts. Parasites can be introduced into the biotope zoo by



- newly acquired animals - plant or meat food - free living animals. In the new environment they may find suitable intermediate and final hosts eventually leading to the establishment of a self sustaining life cycle. Now I give some examples from the Tierpark Berlin. All the parasites mentioned were gained from animals hatched or born in our zoo. Therefore the infestation must have taken place under zoo conditions.

Fig. 1: Life cycle of Echinuria uncinata Trematodes Trematode cycles are rarely seen in zoos. Most trematodes need two intermediate hosts the first one always being a snail. We found the relatively big-sized species Echinostoma revolutum in the large intestine of various anseriform birds. First and second intermediate hosts are water snails. A 3-weeks-old common pochard (Aythya nyroca) and a young black swan (Cygnus atratus ) harboured the notocotylid trematode Catatropis verrucosa. Again snails are the first and second intermediate hosts. Cestodes Numerous tapeworm species are registered in our animal collection, mainly in waterfowl (3). Most of the species found belong to the family Hymenolepididae, genera Aploparaxis, Dicranotaenia, Diploposthe, Microsomacanthus, Retinometra, Sobolevi-canthus. Intermediate hosts are crustaceans, „waterfleas“, crowding in vast numbers the water moats of the zoo. The most



frequent species of the genera Diploposthe and Sobolevicanthus we also find in wild mallards. Obviously such mallards are the main sources of the infestation of zoo birds. Species of the genus Raillietina occur mainly in terrestric birds. We have found them in various parrot species but there were single cases in a muscovy duck (Cairina moschata) and a swan goose (Anser cygnoides). Intermediate hosts are snails and insects (ants, beetles, and flies). Moniezia are extremely large cestodes of ruminants. We diagnosed M. expansa in musk oxen (Ovibos moschatus ) and muflon (Ovis ammon musimon) and M. benedeni in Pere David’s deer (Elaphurus davidianus ). Intermediate hosts are many species of oribatid mites.

Fig. 2: Life cycle of Geopetitia aspiculata (after French et al., 1994) Acanthocephalids Thorny-headed worms of waterfowl find suitable intermediate hosts among the crustaceans in moats and lakes of the Tierpark. Polymorphus minutus occurred in an 8-weeks-old yellow billed duck (Anas undulata) and Filicollis anatis we found in juv. moorhens (Gallinula chloropus ) and a Philippine duck (Anas luzonica). Intermediate hosts of Filicollis anatis are fresh water isopods. Their hook-armed proboscis anchors deeply to the intestinal wall. There are cases of penetration into the visceral cavity (2). Not yet determinated acanthocephalids we detected in juv. red-winged laughing thrushes (Garrulax formosus) and eye-browed thrushes (Turdus obscurus ) thus representing terrestric cycles of such parasites. As intermediate hosts insects and terrestric isopods play a role. Nematodes As mentioned before homoxenous nematodes are important parasites of zoo animals. But heteroxenous life cycles are also occurring under zoo conditions, mainly represented by spirurid, ascarid and capillarid nematodes.



Fig. 3: Life cycle of Porrocaecum ensicaudatum (after R.C. Anderson 1992) Spirurids Echinuria uncinata is a specific parasite of anatid birds. In our zoo we have recognised these worms in 42 species (4). Its larvae we found in two crustacean species, Daphnia pulex and D. magna (fig. 1). The adult worms are located in the proventriculus of their hosts. They are very pathogenous parasites especially in ducklings and young swans. The main reservoirs of the parasite are mallards living and breeding in great numbers in our zoo. Swans from the Berlin environment were also frequently found infested. Immature spirurid nematodes of the acuariid family were found in the small intestine of two juvenile Kessler’s thrushes (Turdus kessleri) bred in an outdoor aviary. The nestlings were fed all the invertebrates the adult birds pecked up from the humus layer offered by the keepers. The nestlings



died when they were 9 and 11 days old. Additionally to the spirurids they harboured gapeworms, ascarids, tapeworms and coccidia of the Isospora type. The stomach worm Geopetitia aspiculata is a parasite of terrestric birds. Principal final hosts are passeriform birds but they are also found in other bird orders, e.g. woodpeckers or pigeons (5). Intermediate hosts are insects, in zoos mainly cockroaches and crickets (fig. 2). Being free from that parasite during a 40-years period it was introduced into our zoo with newly acquired green wood hoopoes (Phoeniculus purpureus). In the meantime the parasite disseminated through our tropical house and could be identified in the following bird species: scaly-breasted bulbul (Pycnonotus squamatus ), short-billed minivet (Pericrotus brevirostris), chestnut-flanked white-eye (Zosterops erythropleura), superb starling (Spreo superbus ), glossy starling (Aplonis panayensis), hill mynah (Gracula religiosa), pale-legged ovenbird (Furnarius leucopus ), thick-billed ground pigeon (Trugon terrestris). Geopetitia aspiculata is a highly pathogenic parasite. Located in the proventriculus-gizzard border area they penetrate into the tissue, sometimes breaking through the wall. Death may be a consequence especially in smaller birds. The spirurid genera Tetrameres and Microtetrameres are closely related to Geopetitia. They are also parasitic in the proventriculus of birds. The female worms are deeply embedded in the fundic glands and are recognisable as small, red spots. The tiny colourless male worms harbour the mucosal layer and are often overlooked. Intermediate hosts of Tetrameres in waterbirds are small crustaceans and intermediate hosts of Microtetrameres which are mainly found in terrestric birds are various insects. In our zoo we recognised Tetrameres fissispina in 9 species of waterfowl. Microtetrameres spp. occurred in a white-rumped shama (Copsychus malabaricus) and a laughing gull (Larus atricilla). Ascariids Many common and frequently found ascarid worms of zoo animals have a direct life cycle. But some members of the ascarid group develop indirectly as do the bird ascarids of the genus Porrocaecum. Intermediate hosts are earthworms (1). In our zoo at least two such life cycles are established. P. ensicaudatum commonly occurs in starlings and thrushes (fig. 3). Blackbirds (Turdus merula) probably are the source of the infestation. These birds are frequently infested with P. ensicaudatum and sometimes we observed great numbers of worms per bird. Anatid birds are the principal hosts of P. crassum and we have observed the species exclusively in birds of that order. Capillariids Hairworms or capillariids may have direct or indirect life cycles. In our zoo birds at least two heteroxenic life cycles take place. Earthworms are necessary intermediate hosts. Capillaria anatis is a parasite of anseriform birds. We could find it in 13 species. Mallards seem to supply the worms continuously. C. caudinflata is mainly a parasite of terrestric birds. With the exception of a spotbill duck (Anas poecilorhyncha) these worms occured only in gallinacious birds. The cited examples may focus our attention on the possibilities of the development of heteroxenous as well as homoxenous parasitic life cycles in the biocenotic system of a zoo. References 1. Anderson RC. Nematode parasites of vertebrates. C.A.B. International. Cambridge UK 1992. 2. Hofmann U, Gräfner G und Tscherner W. Epizootiologie, klinischer Verlauf und Diagnostik der Akanthozephalose

(Filikollose) bei Hausenten. Mh VetMed 1989; 44; 576-8. 3. Priemer, J und Tscherner W. Bandwurmfunde bei Vogeluntersuchungen im Tierpark Berlin-Friedrichsfelde.

VerhBer Erkrg Zootiere 1992; 34; 371-6. 4. Tscherner, W. Der Magenparasit Echinuria uncinata (Rudolphi, 1819) Soloviev,1912 bei Wasservögeln im

Tierpark Berlin-Friedrichsfelde.ZoolGarten NF 2001; 71; 354-64. 5. Tscherner W, Wittstatt U und Göltenboth R. Geopetitia aspiculata Webs ter, 1971 - ein pathogener Nematode

tropischer Vögel in Zoologischen Gärten. Zool. Garten NF 1997; 67; 108-20.


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