| Livestock Research for Rural Development 29 (10) 2017 | Guide for preparation of papers | LRRD Newsletter | Citation of this paper |
This study was conducted to determine the prevalence of gastrointestinal parasites in the agouti, the species of endoparasites present in the gastrointestinal tract and the body condition of the affected animals. Endoparsites in rabbits were also investigated to determine if there were common parasites of the rabbit and the agouti. This study was done in two phases. Phase 1 entailed the collection and analyses of faecal samples, using the faecal floatation technique from the agoutis which were intensively reared in cages and on a cement floor at four locations in Trinidad. The average live body weight of the agoutis ranged from 2.69 kg to 2.56 kg. Helminth eggs found in the agoutis in Phase 1 (n=65) of the study included Strongyloides spp. 36.9%, Trichuris spp. 4.62% and Paraspidodera uncinata 15.4%. In Phase 2 of the study eight agoutis and eight rabbits were slaughtered and contents of different anatomical regions of the gastrointestinal tract were examined using faecal floatation techniques for parasites of both mammals. The cage reared agoutis were captive reared at the University of the West Indies University Field Station (UFS). The rabbits were commercially cage reared at the Sugarcane Feed Centre (SFC). Coccidia oocysts were observed in the contents of the stomach, caecum, colon and rectum of the rabbit. In the agoutiStrongyloides spp. eggs and were found in the caecal contents. Trichuris spp. eggs were found in the caecum and rectum and Paraspidodera uncinata eggs were found in the rectum only. The agoutis sampled had an average body condition score of three.
Key words: caecotroph, endoparasitism, helminth, neo-tropical rodent, rabbit
The agouti (Dasyprocta leporina) is a shy, sequestered, hystricomorphic rodent of the Dasyproctidae family. The literature indicated that they are indigenous to Central and South America including the Guianas and Brazil. The agouti was also found in the islands of the Lesser Antilles including Trinidad and Tobago (Emmons and Feer 1997; Ramdial and Ramdial 1978). Agoutis have been reported to be diurnal being most active early in the morning and late in the afternoon in their natural environment. The average adult weight ranges from of 3-5.9 kg and has been reported to be solitary animals unless they have young (Eisenberg and Redford 1999). In countries where the agoutis are found they have been hunted for their meat (Garcia 1999, 2000). Recently, there has been an increase in the number of agoutis being hunted in Trinidad and Tobago because of the great demand for its meat. This is evident by the increase in the number of hunting permits issued by the Forestry Division of Trinidad and Tobago. Permits issued in the 1990/1991 hunting season amounted to 3037 compared to 6794 in 2012/2013 (Rackal unpublished). This has led to initiatives to rear the agouti intensively and production systems to this effect have been suggested and outlined (Brown-Uddenberg et al 2004).
In cultivated areas, agoutis can eat sweet cassava root (Manihot esculenta), breadfruit (Artocarpus spp.), corn (Zea mays), banana (Musa cvs.) and sugar cane (Saccharium spp.) making this animal into a pest to farmers (Miller and Miller 1986). The agouti’s diet in the wild may also consist of nuts, fruits and seeds. These rodents may bury nuts in the ground and return for them when food is limited (Eisenberg and Redford 1999; Emmons and Feer 1997). The agouti, like the rabbit, is a monogastric hindgut fermenter with a fully functional caecum. In the agouti, the caecum is approximately two thirds the weight of the digestive tract. The length of the small intestines of the agouti when compared to that of a rabbit’s is much longer, thus making the agouti’s digestive tract more efficient in the absorption of nutrients than the rabbit (Garcia et al 2000).
Caecotrophy is practiced by hindgut fermenters as a source of vitamins (especially B12) and amino acids. Small hindgut fermenters like the agouti require more energy for metabolic functions and have a large caecum when compared to their body size (Sakaguishi 2003). Significant work has been done on the male agouti’s reproductive system (Mollineau et al 2006,2008(a),2008(b),2009,2010,2011(a),2011(b),2012, 2013). The gross and microscopic anatomy of the female agouti reproductive system has also been studied (Guimaraes et al 2009,2011; Singh et at 2014). The digestive system has also been studied in captive reared agoutis but there is a paucity of published data on the diseases and parasites of captive reared agoutis (Garcia et al 2000). Some work has been done on diseases which affect the agouti but little has been done on the effects of infections by gastrointestinal parasites (Brown-Uddenberg et al 2004).
Phase 1 consisted of faecal samples being taken from February to May 2016. These samples were taken from captive reared agoutis under two management systems-: cage reared and ground reared (on concrete floors). The four locations where samples were taken from the UWI University Field Station (UFS) at Mt. Hope, The Sugarcane Feed Centre (SFC) at Longdenville, The University of Trinidad and Tobago (UTT) Corinth Campus, San Fernando and Miguel Reece’s Farm (Santa Cruz) (Fig. 1).
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| Figure 1. A map of Trinidad, Republic of Trinidad and Tobago, showing collection sites of samples |
The agoutis, which were intensively reared, were never dewormed at all locations prior to collection of the samples. All of the agoutis at the UWI UFS were captive born, grown in cages and were fed a wide variety of feedstuff that consisted of a mix of local fruits and root-vegetables. Some concentrate feed was also offered to the animals. At the SFC the agoutis were reared on the floor (ten animals per enclosure) and in cages. Their diet consisted solely of locally grown feedstuff e.g. pumpkin fruit ( Cucurita pepo) and sweet cassava root (M. esculenta). At the UTT (San Fernando) agoutis were reared in cages and on floors and their diet consisted of locally grown feedstuff (e.g. M. esculenta and C. pepo) and a National Feed Mill® Rabbit Ration. At Miguel’s Farm one agouti was reared in a cage and the others on the floor and their diets consisted of locally grown fruits and vegetables (e.g M. esculenta and C.pepo) with concentrate feed supplementation.
Faecal samples were taken from sixty-five agoutis intensively reared, with fifty-seven were cage reared and eight floor reared. Approximately one gram of expelled faeces were taken and added to fifteen milli-litres of a 26% saturated solution of sodium chloride (Na Cl) at 1.21 specific gravity. The suspension was poured into the faecalyzer®kit until a positive meniscus was attained. A cover slip was then placed at the top of the tube and allowed to stand for fifteen minutes at room temperature. The coverslip was then removed with forceps and placed on a slide and observed under a light microscope (x 40 and 100 magnification). The eggs and oocyst were identified based on size and morphological characteristics (de Mendoca et al 2006).
This was conducted in March 2016, at the SFC where eight cage-reared male agoutis (average weight, 2.69 kg) and eight male rabbits (average weight, 2.56 kg) were sacrificed. The agoutis were cage reared as described above. The rabbits at the SFC were housed in individual cages. They were provided with feed and water ad libitium. The rabbits were held in conditions in accordance with The World Rabbit Association (Maertens and Coudert 2006). The gastrointestinal tracts contents of both agoutis and rabbits of animals were collected by anatomical regions: stomach, caecum, colon and rectum. Respective samples were taken for faecal floatation treatment (Polozowski et al 2006). The faecal floatation method used was as the standard protocol used by licensed veterinarians in Trinidad and Tobago (Hendrix and Robinson 2017). The agoutis were sacrificed by dislocation of the spine and death occurred by jugular puncture.
The rabbits that were obtained from the SFC were treated with a coccidiostat (Anchoban®) every three months but the agoutis from the UFS were never treated with any form of coccidiostats. The diet of the rabbits consisted of National Flour Mills® Rabbit ration and Trichantera gigantera whilst the agouti diet consisted of uncooked pumpkin fruit (C.pepo), pawpaw fruit (Asimina triloba) and sweet cassava root (M. esculenta) which was grown in the Longdenville area.
The body condition for each agouti sampled was assessed using the method developed for mice (Ullman-Cullere and Foltz 1999). An animal with a body condition score one is emaciated. Skeletal structures are prominent and there is little or no flesh cover. A score of two is given to under-conditioned animals. Segmentation of vertebral column is evident and dorsal pelvic bones are readily palpable. A score of three is given to an animal that is well conditioned. Vertebral and dorsal pelvic bones are not prominent and palpable under slight pressure. A score of four is given to over-conditioned animals. Spine is continuous column. Vertebral palpable with firm pressure. A score of five is given to an obese animal. The animal is smooth and bulky with disappearance of bone structure under flesh and subcutaneous tissue (Ullman-Cullere and Foltz 1999)
In Phase 1 samples were collected from captive reared agoutis at the four locations. Three genera of gastrointestinal parasites were found, they wereParaspidodera uncinata, Strongyloides spp. and Trichuris spp. (Fig. 2- 4) (Table 2). Based on location, the prevalence of gastrointestinal parasites within the agouti was 42.3% at the UFS (n=52), 100% at the SFC (n=7), 0.00% at the UTT (n= 4) and 0.00% at Miguel’s Farm (n=2) (Table 1).
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Table 1. Showing the prevalence of endoparasites found in the Agouti at different locations |
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Location |
Prevalence (%) |
Samples (n) |
|
UFS |
42.3 |
52 |
|
SFC |
100 |
7 |
|
UTT |
0.00 |
4 |
|
Miguel’s Farm |
0.00 |
2 |
 |
 |
 |
| Figure 2. Paraspidodera uncinaria egg found in D. leporina in Trinidad, x40 magnification. |
Figure 3. Strongyloides spp. found in D. leporina in Trinidad, x 100 magnification. |
Figure 4. Trichuris spp. egg found in D. leporina in Trinidad, x 40 magnification |
The overall prevalence of gastrointestinal helminths present within the intensively reared agoutis in Trinidad was 44.6 % (n=65). This indicated that nearly half of the agoutis sample population was positive for parasites in their gastrointestinal tract. Strongyloides spp. was seen in 36.9% of samples, Trichuris spp. were seen in 4.62% of the samples and Paraspidodera uncinata was seen in 15.4% in the agouti intensively reared in Trinidad (Table 2). This suggests thatStongyloides spp. was the most prevalent endoparasite followed by Paraspidodera uncinata and finally Trichuris spp. In the faecal samples collected from the agouti no coccidia were observed.
In Phase 2 of the study the stomach contents of eight agoutis were examined and no helminth eggs were observed. However, Strongyloides spp. eggs were found in the caecum of five animals. Strongyloides spp eggs were found in the colon of two animals and Strongyloides spp. eggs were found in the rectum of one animal. Trichuris spp. eggs were found in the caecum of one animal. Paraspidodera uncinata eggs were found in the rectum of one sample. The agoutis which were euthanized were in good health, having a body condition score of three and had no history of gastrointestinal illness prior to slaughter (Fig. 5-8).
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Table 2. Showing the prevalence of different endoparasites found in the Agouti |
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Endoparasite |
Prevalence (%) |
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Strongyloides spp. |
36.9 |
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Paraspidodera uncinate |
15.4 |
|
Trichuris spp. |
4.62 |
 |
| Figure 5. A male agouti which has a body condition score of 3 out of 5 before slaughter |
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 |
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| Figure 6. Showing the slaughtering process and the subcutaneous fat present on the agouti carcass. | ||
The gastrointestinal tracts of the rabbits collected and examined showed the presence of coccidian oocysts. Coccidia oocysts were found in all sections of the eight samples analyzed (stomach, rectum, caecum and colon). It can also be seen that there were no gastrointestinal parasites which were common to the two caecotrophs (agouti and rabbit). These rabbits were given a coccidiostat (Anchoban®) every three months as part of the normal rearing protocol at the SFC.
In Trinidad, gastrointestinal parasites of wild agoutis have been reported to include Stichochis gianteus, Raillietella trinitatae,Strongyloides agouti, Trichostongyles,Trichuris trinitatae, Helminthoxy cameroni and Aspidodera binansate agouti (Cameron and Reesal 1951; Reesal 1950). A later study in Trinidad reported Strongyloides spp., Ascarid spp., Trichuris spp., a trematode and a hookworm (Suepaul et al 2016). In Brazil, wild agoutis were sampled and Trichuris gracilis and Helminthoxy urichi were found in the caecum, and Physaloptera torresi, and Physocephalus mediospiralis in the stomach using histopathology (Goncalcaves et al 2006). Giardia and Eimeria was found in agoutis using faecal sedimentation in Rio Grande do Sul in Brazil (da Silva et al 2008). Also in Brazil nematodes in the agouti were identified using faecal floatation and these includedTrichuris gracilis, Strongyloides agouti and Paraspidodera uncinata (Macedo2008). A similar study was done on the gastrointestinal parasites of captive D. leporiana foundStrongyloides spp., coccidian oocyst and Trichuris gracilis (de Mendonca et al 2006). Brown-Uddenberg et al (2004) recorded Trichuris gracilis, Strongyloides agouti,Paraspidodera uncinata, Helminthoxy urichi, Physaloptera torresi,Physocephalus mediospiralis, Aspidodera binansate agouti, Ecchinocoocus spp. and Trichostrongyles spp.
Helminth eggs found within the agouti of this study includedTrichuris spp., Paraspidodera uncinata and Strongyloides spp. which were the same parasites reported in Brazil (Macedo 2008; de Mendonca et al 2006). The endoparasites seen in the agouti if they were seen in other domesticated animals such as sheep and goat, would be expected to induce weight loss, diarrhoea, decreased body condition, rough hair coat and inappetance (Cicek et al 2007; Krecek and Waller 2006). However, these signs were not seen in the agouti; in fact the animals had a body condition score of three and there were no clinical signs of gastrointestinal illness(eg. diarrhoea, vomiting, melena). In this study it was evident that the sample population had good body condition scores and adequate subcutaneous fat (Fig. 6).
The results in this paper were similar to those seen in small mammal species in Brazil where there was no correlation between endoparasitic burden and body condition (Puttker et al 2008). The agouti seemed to have some inherent ability to withstand or endure these endoparasites. Similar findings were reported in the Capybara (Hydrochoreis hydrocharias )where they were heavily parasitized with gastrointestinal parasites but were in good body condition (Cueto 2013). In an earlier study done in Trinidad Srongyloides spp. and Trichuris spp. were found which was similar to what was found in this study (Suepaul et al 2016). However, in that paper there was a relatively small sample size (n=13) as compared to this paper in which has a larger sample saize (n=65)and the correlation between the body condition of the animals and endoparastism were not taken into account.
The farm containing agoutis with the highest prevalence of endoparasites was the SFC. This may have been due to two factors. Firstly, these animals were the only samples from the study which were fed solely on local feed resources (no concentrates). Secondly, the diet of these animals may have promoted caecotrophy causing an increase in the rate of faeco-oral transmission. No gastrointestinal parasitic eggs were detected in agoutis from the UTT and Miguel’s Farm (Santa Cruz). At the UFS Strongyloides spp. and Paraspidodera uncinata were the two helminth ova found in the samples. The faecal samples obtained from that location showed a 42.3% prevalence of gastrointestinal parasitism. Animals which were fed concentrate and the local feed had a lower prevalence of endoparasitism as compared to those which were fed on local feed sources only.
If the act of caecotrophy can be controlled by manipulation of the diet the faeco-oral route of transmission of endoparasites can be avoided. Like the rabbit the agouti is a caecotrophs but in captivity this behaviour may be altered due to the components of the diet (Brown-Uddenberg et al 2004). In this study it was seen that whether cage reared or floor reared there was no statistical significance in the prevalence of endoparasitism. This may bedue to the caecotrophic nature of the agouti.
Gastrointestinal samples that were taken directly from sections of the agoutis’ gastrointestinal tract suggest that adult Trichuris spp. and Strongyloides spp. may have had a predilection for the caecum and colon due to the presence of their helminth ova found in these segments. This was similar to literature from Brazil where adult Trichuris vulpis were recovered in the caecum of the agouti (Macedo2008). The results obtained herein were preliminary in determining the predilection site for each endoparasites, but Paraspidodera uncinata eggs were found in the rectum only leading to speculation that the adults may reside there. Results from this study showed that the agouti has an inherent ability to withstand the effect of these endoparasites, thus maintaining a healthy status.
Since the production systems being suggested for the agouti are similar to those of rabbits (Oryctolagus cuniculus), and their digestive systems are also similar (Brown-Uddenberg et al 2004; Garcia 2000), it was necessary to also look at the internal parasites of the domestic rabbit. However, little work has been reported on the gastrointestinal parasites of the rabbits in Trinidad and Tobago and the wider Caribbean. The gastrointestinal nematodes reported in the rabbits included:Obeliscoides cuniculi, Graphidium strigosum, Trichostrongylus spp., Strongyloides spp., Passalarus ambiguous andTrichuris leporis. Cestodes included: Mosgovoyia pectinate and Cysticercus pisiformis and coccidia present in rabbits at slaughter (Szkucik et al 2014).
Digestive disorders in rabbits were responsible for significant morbidity characterized by a decrease in weight gain and poor feed conversion. These digestive disorders were due to pathogens such as Eimeria spp, Escherichia coli and Clostridium perfringens (Licois 2004). Most Eimeria species reported in rabbits occupied the small intestine except for Eimeria stiedai which occupied the bile duct in the liver and Eimeria performis which occupied cells in the crypts of the colon (Pakandl 2009; Rutherford 1943). Rabbits raised on the ground had increased problems with coccidiosis due to the direct exposure to the infectious agent (Lukefahr and Cheeke 1990).
The rabbit, which is a hindgut fermenter and practices caecotrophy, similar to the agouti, when infected with endoparasites suffer ill health as a result of these parasites. Rabbits suffer from a wide array of gastrointestinal parasites (Trichostrongylus retortaeformis,Mosgovoyia ctenoides,Graphidium strigosum and Nematodirodes zembrae). Those which had high numbers of these endoparasites had dereased body conditions, diarrhoea and ruffled hair coats (Eira et al 2007; Molina et 1999).
The literature showed that rabbits which were treated with anthelminthics and coccidiostats produced more offspring per female as compared to the untreated group (Yuill 1864). Trichostrogylus larvae migrate from the stomach wall of the rabbit to the small intestines via its blood vessels. The larvae enter blood vessels by damaging enterocytes and its basement membrane causing severe inflammation of the gastrointestinal tract and a decrease in the absorptive capacity of the animals’ gastrointestinal tract (Aurbert et al 2003). Coccidia are intracellular parasites that account for the major parasitic disorders in rabbits causing diarrhea, decreased feed conversion and mortality (Aubert et al 2003).
The presence of coccida seen in the rabbits used in this study is similar to the findings of Pakandl (2009). The impact of endoparasites in the rabbit seems to have a greater impact on health and production than in the agouti with similar levels of endoparasites. In the rabbits, coccidia oocysts were present even though they were treated every three months with a coccidiostat (Anchoban®)) at the SFC. This can be attributed to the dosage regime used at SFC.Therefore the coccidiosis protocol used at the SFC should be revised to use the coccidiostat more frequently or change from Anchoban® to another coccidiostat. In this sudy it was found that none of the gastrointestinal parasites which were present in the agouti was found in the rabbit.
Future work on the gastrointestinal parasites of the agouti should be done to get a better understanding of the role of these organisms on the health of the host and to understand what role management can play in controlling these pathogenic agents. This should entail the understanding of the actual level of endoparasites these animals can withstand. This should be quantified and compared with the rabbit which will be considered the control animal. This must be done in order to determine if these endoparasites have a parasitic or mutualistic function in the gastrointestinal tract of the agouti.
The authors would like to thank Emeritus Professor Holman Eugine Williams for critically reviewing this paper. Special thanks must also go out to the technical staff at the UWI UFS, the SFC, The Agriculture Education Unit of the University of Trinidad and Tobago [UTT] and Mr. Miguel Reece. Without your animals and help this research would not have been possible.
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Received 31 July 2017; Accepted 14 September 2017; Published 3 October 2017