Impact of Parasites in Captive Birds: A Review

Impact of Parasites in Captive Birds: A Review


Ombugadu, A.1*, Echor, B. O.2, Jibril, A. B.1, Angbalaga, G. A.3, Lapang, M. P.4, Micah, E. M.1, Njila, H. L.2, Isah, L.4, Nkup, C. D.5, Dogo, K. S.1 and Anzaku, A. A.6 

1Department of Zoology, Faculty of Science, Federal University Lafia, P.M.B. 146, Lafia, Nasarawa State, Nigeria.
2Department of Science Laboratory Technology, Faculty of Natural Sciences, University of Jos, P.M.B. 2084, Jos, Plateau State, Nigeria.
3Department of Microbiology, Faculty of Science, Federal University Lafia, P.M.B. 146, Lafia, Nasarawa State, Nigeria.
4Department of Zoology, Faculty of Natural Sciences, University of Jos, P.M.B. 2084, Jos, Plateau State, Nigeria.
5Department of Biology, College of Arts, Science and Technology, Kurgwi, Qua’an Pan LGA,Plateau State.
6Institute of Human Virology, Nigeria, Plot 252 Herbert Macaulay Way, Maina Court, Central Business District, P.O. Box 9396, Garki-Abuja. 

Received Date: June 28, 2020; Accepted Date: July 14, 2020; Published Date: August 18, 2020
*Corresponding author: Akwashiki Ombugadu, Department of Zoology, Faculty of Science, Federal University Lafia, P.M.B. 146, Lafia, Nasarawa State, Nigeria Email: akwash24@gmail.com

Citation: Akwashiki Ombugadu (2020) Impact of Parasites in Captive Birds: A Review. Enviro Sci Pollu Res Mang: ESPRM-104.


Abstract
      Zoological gardens is an ex-situ form of conservation where animals are kept in cages or enclosures for aesthetic, educational or research and conservation purposes. Study of captive animals’ diseases is of continued veterinary importance.  Parasites are one of the major concerns in conservation of bird species. Parasitic infections are major cause of wildlife health complications and death. Captive birds are more prone to parasites as compared to wild birds who leave unfavorable environment and naturally handle health challenges as compared to captive birds which might suffer consequences of poor and inadequate management protocols. To this end, a review on the current knowledge of the impact of parasites in captive birds rather than in wild birds was done. The review covers aetiology, epidemiology, pathogenesis, clinical signs and lesions, diagnosis, treatment and prevention of the parasites. Also, parasitic load was considered in relation to feeding guilds, predilection sites and seasonality which may help in effective management practices.


Keywords: Captive birds, Parasites, Feeding guilds, Predilection sites, Seasonality.


Introduction
     Captive birds are important to human economically and to other animals and plants as they serve as source of food and pollinators [1]. Birds kept in captivity are sometimes released into the wild, when there is sufficient natural habitat to support new individuals or when the species in the wild suffer less threat or bought by individuals [2]. Captive breeding allows for a controlled environment within well-defined settings that facilitate biodiversity and may save species from extinction [3]. Captive breeding is employed by modern conservationists, and has saved a wide variety of species from extinction; the Pink Pigeon (Nesoenasmayeri) is one of such success stories, [2]. Captive birds are prone to attack by parasites which causes serious threats to birds. These might be so serious for growth, reproduction and long term survival. This is a major concern in conservation of endangered species as they can lead to mortality, dramatic population declines, and even contribute to local extinction events [4,5,6, 7]. These parasites are found on both wild and captive bird species which causes various diseases such as avian malaria, ornithosis or psittacosis and bird flu [8]. A parasite can either be an ectoparasite or endoparasite. Ectoparasitesinclude ticks, flies, mites[9]whereas endoparasites such as nematodes, trematodes, cestodes, acanthocephalans and protozoans were recorded by Rahimangaet al. (2002) [10].  Parasitic diseases often represent a major concern in zoo animals due to the poor maintenance of confined cages leading to high level of environmental contamination as well as a possible zoonotic potential [11,12].

                Hence, the current knowledge of the impact of parasites in captive birds rather than in wild birds was reviewed based on their biology and load in birds in relation to feeding guilds, predilection sites and seasonality that may help in effective management practices. 

Captive Birds and Parasites

Almost all species of captive birds suffer from parasite infestation [13]. Large populations of captive birds are exposed to many parasitic diseases. This may include feather chewing lice (Ischnocera, Amblycea) which destroy feathers to helminthic infections which may lead to death [14]. Ascardiagalliis the largest nematode of birds residing in the small intestine. It is the most prevalent and pathogenic parasite of domestic fowl.  Parasite infestation can also be observed in other species of birds which causes anorexia, weight loss, hemorrhages in the intestinal mucosa and obstruction in intestinal lumen [15]. Parasitic infections are among the most common sanitary problems affecting captive birds, especially in high density populations due to an increased risk of exposure.

Ectoparasites

Birds may harbor a great variety of ectoparasites[16]. These parasites have been noted to be responsible for restlessness, skin damage, restricted growth, loss of weights in birds, as a result of their bites [17]. Parasites show morphological and physiological adaptations to enhance their living and existence on their host [18]. Most ectoparasites possess tarsal claws at tips of their leg that enable them to hold grip on their hosts hairs and feathers. The shape and size of ectoparasites are also modified; some are microscopic (mites) while some are not microscopic for example ticks and lice [19]. Ectoparasites affect the health and productivity of many captive bird species [20]. Parasitic arthropods, including ticks, mites, flies, mallophages and fleas are often found on the skin or feathers of their hosts.

Ectoparasites such as: lice, fleas, ticks and mites have been reported by Balaet al. (2011) [21] to show morphological and physiological adaptations to enhance their living and existence on their host. This include piercing and sucking mouth parts, characteristics stylets enclosed in a sac beneath the head, as found in lice, mouth parts are also armed with barbs which may not allow forceful withdrawal from host flesh as found in ticks. Lice also possess longer jaw adapted for biting and fleas are laterally compressed, possessing comb that helps to retain them amongst the fur of their host [18]. Most ectoparasites also possess claws at tips of their leg that enable them to hold grip on their hosts hairs and feathers. The shape and size of ectoparasites are also modified.  They are mostly small, some so small that they require microscopic observation like mites. Others can however be seen with naked eyes since they are large enough like ticks and lice [19].

Bacterial and fungal infections caused by ectoparasites can occur in wounds, and many ectoparasites are vectors. Philips [22, 23, 24] reviewed the parasitic mites of raptors and the author maintains an online checklist of raptor hosts and their mite ectoparasites. Ectoparasites cause illness and sometimes death in many species, a few adult ticks feeding on a chick of the domestic fowl can cause anaemia, reduced growth, weight loss, and contribute to a depressed state of health [25, 26]. Fatal paralysis from bites of tick has been reported in numerous species of small birds [20, 27]. Recently, parasitic diseases have been increasing in incidence in captive birds, this is as a consequence of increased levels of exposure to the parasite as a consequence of increased contamination of the aviary by the parents. A large ectoparasites infestation on a bird is typically a sign of the bird being ill for other reasons, as any fit bird will usually control its own parasites rather than just treating the parasite it’s also important to deal with the root cause [20].

Effect of Ectoparasites on Bird Host

Ectoparasites affect the host in different ways. They cause damage to birds feathers and impair a host of physiological comfort [28]. Chewing lice (Ischnocera, Ambblycea) are permanent ectoparasites primarily of bird species and they feed on feathers and skin scales. These lice can be harmful to both captive and wild hosts as they deteriorate the quality of the plumage, provoke small holes on feathers (which diminishes the thermoregulatory capacity as well as increase feather breakage [29]. 

Lice

Lice are also a common ectoparasite of birds. Lice feed on skin debris and feathers, they do not however survive outside the host for long,they do not suckblood but they feed on feathers. It is difficult to spot them as they can easily vanish under feathers [30].

Lice of the genus Struthiolipeurus can cause intense pruritis, feather damage and feather loss. Both lice and mites can be found by examining the skin and feathers, especially around the vent, legs, wings and neck. Night time examination of birds may detect parasites that feed at night, but specific identification of the parasite requires microscopic examination [31]. Chewing (biting) lice (feather lice, ostrich lice), Struthiolipeurusstruthionis cause skin and feather damage (which diminish thermoregulatory capacity), and increase feather breakage [32]. The lice and eggs can be seen in feathers close to the skin around the vent, legs, wings and neck [33, 34]. They are narrow bodied lice with large heads, not sucking blood but feeding on feathers [34]. It is difficult to spot them as they can easily vanish under feathers. Struthiolipeurus eggs are deposited on feather barbs on both sides along the shaft [31]. Price et al. (2003) [35] provided a list of global avian lice, their hosts, and identification keys to genera by host. Chewing lice usually are transferred by direct contact and, less frequently, by louse flies. Their feeding can damage feathers, and scratching in response to infestation can cause additional damage [34, 36, 37, 38].

Mites

Mites are members of the spider family. They spend their entire life cycle on a bird. Mites spread from bird to bird as flock members make body contact. They are about 0.5 μm long [34]. Mites of the family Pterolichidae are known to infest ostriches. The feather (quill, shaft) mites Gabuciniabicaudata(Pterolichusbicaudatus) of ostriches live in the vein in the ventral groove of the feather shaft and feed on blood and gelatinous contents of feather sheath. They can be visualized as small, reddish, dust-like, elongated particles in the feather vent [33,34,39,40]. As ostriches molt continuously, there are always immature feathers for them to feed on, although when their population grows out of control they also attack the skin [39]. These microscopic mites live within the shaft of the feather. Damage is done to the feather when the mites pass through the quills during their life cycle [41].

Skin or tissue-eating mites reported on raptors include Pneumophagus in the lungs and air sacs, Ereynetidae in the nasal cavity, Turbinoptidae in the outer nares, Hypoderatidae under thigh and underbody skin, Syringophilidae in quills, and Analgidae, Cheyletiellidae, Epidermoptidae, Harpirhynchidae, Knemidocoptidae, and Trombiculidae (chiggers) on or in the skin. Cheyletiellid mites also feed on blood, and, as with epidermoptid and harpirhynchid mites, can cause edema, hyperkeratosis, and feather loss, with secondary infections in skin lesions. Knemidocoptes can cause development of scaly-face and scaly-leg encrustations. Females of Strelkoviacarus and Microlichus are phoretic on louse flies, whereas Myialges females lay their eggs on these flies. Hypoderatid mites reproduce in nests, but their adults are non-feeding and short-lived. Chiggers, often a cause of dermatitis, are larval mites whose nymphal and adult forms are soil predators. Many mites live on feathers where they scavenge fungi, lipids, bacteria, and feather fragments. A few live in the rachis and quill and eat medulla tissue. Feather and quill mites are most abundant on wing feathers. Feather mites can be collected by ruffling feathers dusted with insecticides [34, 37, 41]. Thus, Barbosa et al. (2002) [42] reported that the activity by such parasite have effect on the behavior of their host.

Ticks

Adult ticks all suck blood, often from different hosts. Individuals remain attached to hosts for as long as two days [43]. They feed for very brief period of time, spending most of their time in secluded areas. Eyelids and the bases of beaks are usual feeding sites. Most ticks are ambush parasites found in litter and soil that latch on to passing hosts. Just a few adult ticks feeding on a small bird can cause anemia, reduced growth, weight loss and contribute in other ways to a depressed state of health [44]. Avian soft ticks (Argasidaeargas and Ornithodoros) and some hard ticks (Ixodidae, Ixodes) live in nests and burrows. Ticks transmit avian spirochetosis and Lyme disease, and are vectors for Babesiaspecies, an anemia causing protozoan known to occur in Prairie Falcons [45]. They also transmit viruses and tularemia bacteria to birds. Some species produce a toxin in their saliva that induces paralysis. Ticks have killed nestling Prairie Falcons [46,47] and Peregrine Falcons F. peregrinus [48], and tick paralysis killed an adult Powerful Boobook (Ninoxstrenua) [49] in Australia.  Paralysis of birds voluntary muscles is a result of the argasidae species bites. Tick paralysis in songbirds has been associated with the bite of the hard bodied tick Ixodesbrunneus [50]. Ticks of various species and different life stages infest ostriches and high infestation is associated with areas of high rainfall and dense vegetation [33,51, 52].  The most common site of attack for ticks (80%) is the head and neck. A preferred site of attachment is under the chin [31].

Flies (Diptera) 

                Flies that parasitize birds externally include biting midges, blackflies, louse flies and mosquitoes.

Biting midges

Biting midges (Ceratopogonidae) which are often called “no-see-ums,” transmit filarial nematodes, blood protozoans Haemoproteus and Leucocytozoon, and the Thimiriarbo virus to birds [53]. Flies spending all or most of their adult life within the furor among the feathers of their hosts [54]. 

Blackflies (Simuliidae)

Crosskey and Howard (1997) [55] provided an inventory of the blackflies of the world. Blackflies are the main vectors of Leucocytozoon in birds, and also transmit Trypanosoma and filarial nematodes [56]. Adler et al. (2004) [57] listed North American blackfly species, their raptor and other hosts, and the species of Leucocytozoon they transmit. Blackflies have killed nestling Red-tailed Hawks B. jamaicensis [58, 59], nestling MerlinsFalco columbariu [60], and have weakened nestling Cape Vultures Gyps coprotheres [61]. Blackflies tend to feed on the crown, back, and shoulders of raptors. Biting occurs during the day in the open.

Louse Flies (Hippoboscidae)

                Maa (1963) [62] listed the louse flies of the world and provides genera and species group identification keys. Avian louse flies, often called flat flies, tend to remain on their host unless disturbed, and they sometimes bite humans that handle infested birds. Larvae develop in the female and pupate in birds nests and roosts immediately when born. Louse flies transmit the blood protozoans, Haemoproteus and Trypanosoma, through biting, and carry lice and the ectoparasitic skin mites, Strelkoviacarus, MicrolichusandMyialges on their exterior to new bird hosts [63,64]. Louse flies have tested positive for West Nile virus, but their role as vectors of this and other viruses is unconfirmed. Infestation of several dozen louse flies does not seem to harm raptors, but when levels exceed 80, raptors become emaciated and too weak to hunt [65]. 

Mosquitoes (Culicidae)

Mosquitoes transmit many viruses to birds, including encephalomyelitis viruses, West Nile virus, and poxvirus [66]. They are also vectors of avian malaria (Plasmodium) and filarial nematodes. After a blood meal, female mosquitoes lay eggs on water or wet surfaces under floating vegetation or in the walls of wet tree holes [67]. Mosquitoes (Diptera: Culicidae): Aedesspecies and Culex species of mosquitoes have been involved in the transmission of fowl pox caused by avian poxvirus [68]. Mosquitoes can harbor and transmit the virus for a month or longer after feeding on infected birds or by direct contact with infected birds [69]. Other insects, such as stable flies have also shown the capability of transmitting the poxvirus [69]. Mosquitoes are vectors of avian malaria (Plasmodium) and filarial nematodes [70].

General Control Measures for Ectoparasites

Sanitation and cleanliness are the keys to ectoparasite control in captive birds. Sanitation includes cleaning and disinfecting bird cages, facilities and equipments. Eliminating the contact between flocks and wild birds can reduce the potential transfer of external parasites a wide spectrum insecticide not harmful to birds containing 0.09% tetrametrin and 0.45 piperronyl is highly favored in use to pulverize on the feather or the predilection sites [71]. Since the life cycle of lice and mites is approximately 2 weeks, treatments should be repeated every 2 weeks as needed [72]. 

Endoparasites

Endoparasites such as single celled protozoa, worms (helminths), invade nearly all organs of their host. Endoparasitism is one of the major health problems in the companion birds and is on the top of the list of clinical problems considered for differential diagnosis, especially in newly acquired birds and in large aviary collections [22]. Greve (1996) [73] reported that gastro-intestinal parasitism ranked as the most frequent and important one in caged and aviary birds. Ramiszet al. (2014) [74] determined the parasitic species composition, prevalence and intensity of infection in selected parrots. Lee et al. (2005) [75] conducted a prevalence study of gastrointestinal parasites in Psittacine birds which while in groups were found to have a significant higher percentage of parasites than birds that are kept individually. 

Effect of endoparasites on the host

Parasitic diseases caused by endoparasites generally constitute major impediments on husbandry, productivity and welfare of captives birds particularly poultry. Extensive studies have been conducted on the endoparasites of captive birds. This disease conditions limit their production through retardation in growth, poor health conditions, reduced egg production, lowered and overall sustainability. Endoparasitism causes loss of appetite, changes in vocalization, ruffled plumage, breathing difficulties, weight loss, bloody diarrhea, and inability to survive [22,23]. 

Common Endoparasites Reported to infest Captive Birds

Avian trichomoniasis

Trichomonasgallinae is a protozoan parasite known to infect the upper digestive tract and various organs of several avian groups, including Columbiformes (i.e. pigeons and doves). The genome of parasites can be bigger than those of the free living parasite relatives and in some cases, bigger than those of the hosts they occupy [76].

Trichomoniasis is caused by a group of one celled protozoa and regularly affects many bird species. One strain of the parasite infects pigeons and doves and also, their predators, such as raptors. In some strains of the disease, birds develop sores in their mouths, throats or gastro-intestinal tract and upper respiratory tract of birds. Birds can be affected with Trichomonasgallinae by consuming contaminated food which has dropped by infected birds. Symptoms includes: reduce appetite, or a physical inability to eat, inability to swallow,vomiting, dehydration , weight loss, depression, weakness, diarrhea  and respiratory distress which makes it hard for the birds to breathe. Liver damage can occur if the liver is invaded byTrichomonasorganisms, resulting in green biliverdinemia [30, 36, 77].

Coccidiosis

Coccidiosis is a disease caused by Coccidia which are a group of protozoan parasites that are extremely common. Coccidia live in the intestinal tract and if they proliferate, or at times of stress, will also cause chronic bloody stools.An infection may be mild enough to go unnoticed while a large infective dose of coccidia may produce severe lesions that can cause death. Coccidians survive for long periods outside the bird's body, so infection can occur simply by keeping a bird in a contaminated cage or aviary. It is difficult, if not impossible, to prevent coccidiosis by sanitation alone. It is best prevented by addition of a drug (coccidiostat) to the feed that controls the growth of coccidia in the digestive tract [78].

Avian malaria

Avian malaria parasites of the taxa Plasmodium and Parahaemoproteus (order: Haemosporida) are ubiquitous parasites that may co-circulate with zoonotic pathogens for which birds are reservoir hosts[79]. These parasites have complex lifecycles that involve asexual reproduction in an avian host and sexual reproduction in a dipteran vector. Parahaemoproteus is vectored by Culicoides midges (Ceratopogonidae), whereas Plasmodium parasites are vectored by mosquitoes (Culicidae), including those of the genus Culex [80,81].

Avian Giardiasis

Giardiasis is a gastrointestinal parasite that can cause a number of problems in a bird's stomach and intestines, but affects the normal functions of other organs. Giardia is a singled celled microbe (protozoa) found in the intestines. Giardiasis generally affects cockatiels, budgerigars [82], lovebirds, and other birds of the parrot family, like macaws, parrots, and cockatoos [83].

Aspergillosis

Aspergillosis is a fungal infection caused by the Aspergillus fungus, which can be found in damp or wet seed mixtures, in birds' nesting materials, or in landfills. Spores inhaled into the lungs and air sacs of birds eventually cause pneumonia and bronchitis. Sick birds experience labored breathing, weakness, and diarrhea, but will continue to take food at feeding stations until they die [84].

Roundworms

           These are the largest and most significant group of endoparasites. The group includes the Syngamus trachea and Serratospiculumspp. which affect the wind pipe and air sacs respectively. Both will cause respiratory signs in infected birds, however in both cases it is particularly important that the diagnosis is made prior to treatment being given. In the case of Syngamus even after the worms are killed they will remain in the airways for up to six weeks slowly rotting away causing respiratory signs and occasionally pneumonia in the meantime [85].

General Control Measures for Endoparasites

          Contact with wild birds should be avoided because it increases the chances of attracting parasitic diseases. Parasitic diseases are difficult to avoid in totality, but may be controlled by the use of management and treatment strategies. Cleaning and disinfection procedures should be improved. Routine deworming programmes are usually advised. Each treatment with a drug will increase the selection pressure in the helminth population for development of anthelmintic resistance [86], and therefore parasitic control programmes should reduce the number of treatments to a minimum and rather increase other control measures. Nevertheless, some kinds of routine anthelmintic treatments are relevant in the control of nematodes in most management systems [87]. 

         Class I anthelmintics: Benzimidazoles and pro-benzimidazoles should be administered. These drugs exert their action on the intracellular polymerization of the tubulin molecules to microtubules. As the cellular functions are disrupted, the worms die. Brands such as albendazole, thiabendazole, fenbendazole, parbendazole, flubendazole, febantel, and thiophanate are generally effective against helminthic infections. Regular vaccination against viral infections are also recommended as well as anticoccidial drugs [88].

Parasitic Load in Captive Birds in Relation to Feeding Guilds and Predilection Sites

Ectoparasitic Load

 Studies by Omuduet al. (2011) [89] and Njilaet al. (2018) [90] on captive birds in the Makurdi Zoological Garden in Benue State and Jos Museum Zoological Garden respectively showed that the omnivores had the highest abundance of parasitized bird group with heavy ectoparasites load, followed by carnivores, while low infestation rate in frugivores [73, 91] as shown in Table 1.

Feeding guild Ectoparasite Load Endoparasite Load
Carnivores ++ +++
Frugivores + ++
Omnivores +++ +
Herbivores   +++

Table 1: Ecto-and-endoparasitic loads in captive birds in relation to feeding guilds

+++: Heavy parasite load
++: Moderate parasite load
+: Low parasite

[Source: 73, 81, 90, 91,92]

Table 2 showed that the predilection sites on the average mostly infested by ectoparasites was the head region [31, 34,39,40] followed by the neck, wing and feather region[89] whereas tail region had no ectoparasite attached on it.

Species Head Crown Wing Leg Tail Feather Eyelid Beaks Chin Neck Vent Thigh Body (Breast/ Stomach) Trunk Perenium Feet
Tick +++ - - + - ++ + ++ ++ +++ - - - - - -
Mite +++ ++ - - - - ++ + - - +++ - - - - +++
Lice - - +++ ++ - +++ - - - ++ - + +++ ++ + -
Fleas - - + - - - - - - - - - - - - -
%  of Preference Mean 50 12.5 31.25 18.75 0 37.5 18.75 18.75 12.5 37.5 25 6.25 25 12.5 6.25 25

Table 2: Ectoparasites load in relation to predilection sites

+++ (100%): Most preferred site
++ (50%): More preferred site
+ (25%): Preferred site
- (0%): Not preferred

[Source:31, 33,34,39,40]

 

  Parasite Blood Intestine Liver Lung Air sac Throat Crop
Trichomonas - - - - - +++ ++
Coccidia - + ++ - - - - -
Giardia - + ++ - - - - -
Aspergillus - - - +++ +++ - -
Plasmodium andHaemoproteusspp. +++            
Preference Mean (%) 20 40 0 20 20 20 10

Table 3: Endoparasites preference in relation to predilection sites

+++ (100%): Most preferred site
++ (50%): More preferred site
+ (25%): Preferred site
- (0%): Not preferred

[Source: 77, 81,92,93,94,95,96]

Ticks predominantly preferred the head and neck regions. Mites preferred the head, vent and feet regions. Lice preferred feather, body (breast/stomach) region while fleas were heavily loaded in wing region (Table 2).

  • Endoparasitic load

               The carnivores and herbivores were mostly infected as described by Santos et al. (2011) [92] in faecal specimens andas well as their blood specimens [81] respectively (Table 1).

            The intestine was the most preferred predilection site by endoparasites[77, 92, 93,94,95] and then in blood [81]. But, the liver was not a site of attachment for endoparasites (Table 3).

                The site most preferred by Trichomonaswas throat; both Coccidia and Giardia was intestine; Aspergilluswas lung/air sac [96]; and Plasmodium and Haemoproteus species was the blood [81].

Composition and abundance of parasites in captive birds in relation to seasonality

Numerous factors drive seasonalcomposition and abundance of parasites in captive birds. One of the major factor being climate [97]. An understanding of these processes increases our ability to predict when outbreaks are likely to occur and in what abundance [98,99].  Some drivers of seasonal infection involve vector behavior and population dynamics. Seasonal shifts in vector utilization of hosts for blood meals have been demonstrated in numerous mosquito species and populations, and these shifts may influence the incidence of vector-borne infectious disease [100]. Pest abundance and activity are associated with infection risk and are influenced by seasonal climate variation [101].Climate also influences seasonal changes in host behavior and physiology that affect pathogen transmission. Host reproduction is often seasonal and correlated with resource availability, which in turn may vary with weather and climate. Energetically expensive breeding activities may leave adults more susceptible to infection [102]. Most birds reproduce during the wet season when food is abundant in which their young immunologically naive juveniles increases the proportion of susceptible individuals in a population and promotes disease transmission [103].

Avian Plasmodium infections within hosts can be highly dynamic. Studies have revealed seasonal patterns in haemosporidian prevalence especially in temperate regions where variation in the annual climate cycle influences host and vector demography[104]. A classic model of temperate avian malaria infection posits an age-structured bimodal peak in the seasonal Plasmodium prevalence among hosts [105]. The model suggests that malaria prevalence drops in winter as infection causes mortality in some hosts while others clear infections from the blood stream through host defense mechanism. Stress associated with reproduction drives a recrudescence of dormant infections among adult birds, elevating the prevalence [105].

Cosgrove et al.(1971) [106] showed that the expected seasonal pattern of malaria infection among blue tits (Cyanistescaeruleus) in Oxford shire, United Kingdom, was absent in Plasmodium relictum and present only in hatch-year hosts for Plasmodium circumflexum.

The dry season period in tropical region is characterized by dry environment which have shown  lessectoparasites activities owing to poor resource availability and environmental conditions [107].


Conclusion
           Large populations of captive wild birds are exposed to many parasitic diseases, infectious diseases which are a major concern in conservation of endangered species as well as of public health concern. They can lead to mortality, dramatic population declines, and even contribute to local extinction events in the place of conservation. It would be of great benefit if more studies are channeled at this area to provide more insight and guide on how to manage such a challenge. The endoparasite load preference was highest incarnivorous and herbivorous birds, while the ectoparasites load was very high in omnivorebirds. The predilection site highly infested by ectoparasites was the head region, while the intestine was mostly infected by endoparasites.Seaonality influences the composition and distribution of parasites. Therefore, the likelihood of the occurrence of disease outbreak for birds in captivity is predictable.

                It would be of great conservation benefit and more economical if captive bird managers improve management and maintenance of the various captive birds and there environment, particularly in the area of sanitation condition.


References 

  1. Ruppert, E. E., Fox, R. S. and Barnes, R.D. (2014). Invertebrate zoology: a functional Evolutionary approach san diego (7th Edition). Belmot, 505 pp.
  1. Nesoenas, M. (2015). The IUCN Red List of Threatened Species. International Union for Conservation of Nature and Natural Resources.
  1. David's, D. (2015). Extinct in the Wild: Père". The Whisker Chronicles. Retrieved 10-05.
  1. Vilcin, I. M., Old, J. M., Korner, G. and Deane, E. M. (2003). Ectoparasites and Skin lesions in wilds-caught spotted- tailed (Quoll (Dasyarus maculates) (Marsupialia: Dasyuridae). Veterinary Parasitology, 107(1-2): 137-160.
  1. Smith, K. F., Sax, D. F. and Lafferty, K. D. (2006). Evidence for the role of infectious disease in species extinction and endangerment. Conservation biology.,20: 1349-1357.
  1. Pedersen A. B., Jones, K. E., Nunn, C. L. and Altizer, S. (2007). Infectious Diseases and Extinction Risk in Wild Mammals. Conservation Biology,21: 1269-1279. DOI: 10.1111/j.15231739.2007.00776.x
  1. Wisely, S. M., Howard, J., Williams, S. A., Bain, O., Santymire, R. M., Bardsley, K .D. and Williams, E. S. (2008). An unidentified filarial species and its impact on fitness in wild populations of the black-footed ferret (Mustelanigripes). J. Wildlife Diseases, 44: 53-64.
  1. BirdLife International (2012). Wild Birds and Avian Influenza, www.birdlife.org/action/science/species/avian-flu/birds-fag-html
  1. Schmaschke, R., Schse, M., Eulenberger, K., and Schon (2003). Quill mites little known parasites of Birds. Vesh. Er .Erkrg. Zootière.,41: 127-133.
  1. Rahimanga, V., Soula, F., Raherilalao, M. J., Goodman, S. M., Sadones, H., Tall, A., Randrianarivelojosia, M., Raharimalala, L., Duchemin, J. B., Ariey, F., Robert, V. 2002). Hémoparasites des oiseauxsauvages à Madagascar. Arch Inst Pasteur de Madagascar, 68(1&2): 90-99.
  1. Gracenea, M., Gomez, M. S., Torres, J., Carne, E. and Fernadez-Moran, J. (2002) Transmission dynamics of Cryptosporidium in primates and herbivores at the Barcelona Zoo: A long-term study. Vet. Parasitol.,104: 19-26.
  1. Citino, S. B. (2003). Bovidae (except sheep and goat) and antilocapridae. In: Fowler, M. E. and Miller, R. E., editors. Zoo & Wild Animal Medicine. 5th ed. Saunders, W. B., Philadelphia, PA, 672 pp.
  1. Loye, J. and Carroll, S., (1995). Birds, bugs and blood: Avian Parasitism and Conservation. Trends in Ecology and Evolution, 10: 232-235.
  1. Spassky, A., Arotellininae, A. and Subfam, N. (2003). A new subfamily of Dilepididcestodes. ActaZooligicaLituanica,13(3): 327-329.
  1. Permin, A., Magwisha, H., Kassuku, A. A., Nansen, P., Bisgaard, M., Frandsen, F. and Gibbons, L. (1997). A cross-sectional study of helminths in rural scavenging poultry in Tanzania in relation to season and climate. J. Helminthol.,71:233-240.
  2. Elizabeth, M. (1951). A survey of parasitism of the Starling, Slurnusoulgaris L. in North America. Journal. Pamsit.,37: 56-84.
  1. Fabiyi, J. P. (2008). Survey of lice infesting domestic fowls of the Jos Plateau, Northern Nigeria. Bull Animal Health Production, 28: 21–9.
  1. Ikeme, M. M. (2002). Parasites of poultry in Nigeria. Annual Report Federal department of Veterinary Reserve. 45 pp.
  1. Agbede, R. I. S. (2010).Survey of ectoparasites and their predilection site on chicken. Journal of Agricultural and Veterinary Sciences, 2: 70-74.
  1. Doyle, Ú., Halloran, J. andSmiddy, P. (2004). Records of the feather lice (Mallophaga) Philopteruscincli (Denny) and Myrsideafranciscoloi(Conci), two species new to Ireland. Irish Naturalists Journal,27: 440.
  1. Bala, A. Y., Anka, S. A., Waziri, A. and Shehu, H. (2011). Preliminary Survey of Ectoparasites Infesting Chickens (Gallus domesticus) in Four Areas of Sokoto Metropolis. Nigerian Journal of Basic and Applied Science, 19(2): 173-180.
  1. Philips, J. R., (2000). A review and checklist of the parasitic mites (Acarina) of the Falconiformes and Strigiformes. J. Raptor Res., 34: 210–231.
  1. Philips, J. R. (2006a). A list of the parasitic mites of the Falconiformes. http://raptormites.babson.edu/falcmitelist.htm (last accessed 8 August 2006).
  1. Philips, J. R. (2006b). A list of the parasitic mites of the Strigiformes. http://raptormites.babson.edu/owlmitelist.htm (last accessed 8 August 2006).
  1. Brooke, M. L., (1985). The effect of all preening on tick burdens of molting eudyptid Penguins. Auk.,102: 893-5.
  1. Bucher, E. H., (1988). Do birds use biological control against nest parasites? Parasitol. Today, 4: 1– 3.
  1. Kettle, D. S. (2000). Medical and Veterinary Entomology. 2nd Ed. CABI Publishing, New York. Pp 361- 385.
  1. Muhammad, S. and Nazia, E. (2017). Insect ectoparasites on wild migratory birds: A review. Animal Science Journal, 8(1): 01-08.
  1. Ahmat, O. G., Bilal, D. and Oya, G. (2013). Chewing Lice (Phthiraptera) species of wild birds in northwerstern turkey a new host record. International Journal for Parasites: Parasites and Wildlife, 2: 217-221.
  1. Deeming, D. C. (1999): The Ostrich - Biology, Production and Health. 1st edition, Cabi Publishing, London, 358 pp.
  1. Nemejc, K. and Lukesova, D. (2012). Parasite fauna of ostriches, emus and rheas. Agricul. Trop. Subtrop., 45(1): 45-50.
  1. Engelbrecht, A. and Cloete, S. W. P. (2012). Preliminary investigations into the effect of ostrich feather lice (Struthiolipeurusstruthionis) on production and leather quality. Animal production science, 52(5): 347-353.
  1. Van, N. D. J., Fourie, L. J. and Horak, I. G. (2006). Birds as hosts of immature ixodid ticks in Free State Province, South Africa, Onderstepoort Journal of Veterinary Research, 73(2): 123.
  1. Taylor, M. A., Coop, R. L. and Wall, R. L. (2007). Veterinary Parasitology. 3rd edition, Blackwell Publishing, Oxford. Pp 586–593.
  1. Price, R. D., Hellenthal, R. A., Palma, R. L., Johnson, K. P., and Clayton, D. H. (2003). The chewing lice: world checklist and biological overview. Illinois Natural History Survey, Champaign, Illinois.501pp.
  2. Jurajda, V. (2002). Chov a nemocipštrosů. 1st edition, Veterinární a farmaceutickáuniverzita Brno, Brno, 92 pp.
  1. Cooper, R. G. (2005). Bacterial, Fungal and Parasitic Infections in the Ostrich (Struthiocamelus var. domesticus). Animal Science Journal, 76: 97-106.
  1. Durgut, R., and Yaman M. (2005). Parasitic infestation in ostriches and therapy. Turkish Journal of Parasitology, 29: 103-109.
  1. Ederli, N. B. and Oliveira, F. C. R. D. (2014). Comparative morphology of the species of Libyostrongylus and Codiostomum, parasites from ostriches, Struthiocamelus, with a identification key to the species. Revistabrasileira deParasitologiaveterinária, 23(3): 291-300.
  1. Dalia, F., khater, H., Soultan, M. and Nadia, A. A. (2011). Hazard Evaluation of Some Insecticides and Heavy Metals Residues in Duck Carcasses, Benha Veterinary medical Journal, 22(2): 87-94.
  1. Cooper, R. G. and EI Doumani, H. A. A. (2006). The presence of quill mites.
  1. Barbosa, A. S., deLope, M. F. and Moller, A. P. (2002). Effects of feather chawing lice on flight behavior of male swallow (Hirundorustica). Auk, 119: 213-216.
  1. Sonenshine, D. E., Lane R. S. and Nicholson, W. I. (2002). Ticks (Ixodida). In: G.R. Mullen and L. Durden [EDS.], Medical and veterinary entomology. Academic Press, San Diego, CA U.S.A., Pp 517–558.
  1. Edosomwan, E. U. and Amadasun, E. (2008). Ectoparasites of some bird’s species in Ogba Zoo in Benin City, Nigeria. Bioscience Research Communication, 20(5): 231-235.
  1. Croft, R.E. and Kingston, N. (1975). Babesiamoshkovskii (Schurenkova 1938) Laird and Lari, 1957 from the Prairie Falcon, Falco mexicanus, in Wyoming; with comments on other parasites found in this host. J. Wildlife. Diseases, 11: 230–233.
  1. Webster, H. J. R. (1944). A survey of the Prairie Falcon in Colorado. Auk, 61: 609-616.
  1. Oliphant, L.W., Thompson, W. J. P., Donald, T. and Rafuse, R. (1976). Present status of the Prairie Falcon in Saskatchewan. Can. Field-Nat., 90:365–367.
  1. Schilling, F. M. Bottcher and Walter G., (1981). Probleme des ZeckenbefallsbeiNestlingen des Wanderfalken (Falco peregrinus). J. Ornithol., 122: 359–367.
  1. Fleay, D. (1968). Night watchmen of bush and plain. Taplinger, New York, NY U.S.A. 163pp.
  1. Gothe, R. and Neitz,A.W.H. (1991).TickParalyses: Pathogenesis and etiology. In: AdvancesinDiseaseandVectorResearch; Harris, K.F., Ed.; Springer: New York, NY, USA; Pp. 177–204, ISBN 978-1-4612-3110-3.
  1. Shanawany, M. M., (1999). Ostrich Production Systems.Food and Agricultural Organization (FAO), Animal Production and Health Paper.
  1. Heylen, D. J. A., and Matthysen, E. (2008). Effect of tick parasitism on the health status of a passerine bird. Functional Ecology, 22: 1099-1107.
  2. 53.Mullen, G. R. and Durden, L. A., (2002). Medical and veterinary entomology. 1st edition. San Diego, California: Academic Press.263 pp.
  1. Jelagat, C. V. (2009). Studies on the Possible Causes of Losses in Ostrich Production in Selected Ostrich Farms in Kenya, University of Nairobi (Msc thesis).
  1. Crosskey, R. W. and Howard, T. M. (1997). Anew taxonomic and geographical inventory of world blackflies (Diptera: Simuliidae). Natural History Museum, London, United Kingdom.
  1. Adler, P. H. and McCreadie, J. W. (2002). Blackflies (Simuliidae).In: Mullen, G. R. and Durden, L. [EDS.], Medical and veterinary entomology. Academic Press, San Diego, CA U.S.A., Pp 163–183.
  1. Adler, P. H, Currie, D. C. and Wood, D. M. (2004). Blackflies (Simuliidae) of North America. Comstock, Ithaca, NY U.S.A. 24(2):442-444
  1. Brown, L. and D. Amadon. (1968).Eagles,hawks and falcons of the world. Country Life Books, Feltham, United Kingdom, Vols. 1 & 2.
  1. Smith, R. N., Cain, S. L., Anderson, S. H., Dunk, J. R. and Williams, E. S.. (1998). Blackfly-induced mortality of nestling Red- tailed Hawks. Auk.,115: 369–375.
  1. Trimble, S. A. (1975). Habitat management series for unique or endangered species. Report 15. Merlin Falco columbarius. USDI Bureau of Land Management Tech Note 71.
  1. Boshoff, A. F. and Currie, M. H. (1981).Notes on the Cape Vulture colony at Potberg, Bredasdorp. Ostrich,52: 1–8.
  1. Maa, T. C. (1963). Genera and species of Hippoboscidae (Diptera): types, synonymy, habitats and natural groupings. Pac.Ins. Monogr.
  1. Philips, J. R., (1990). What’s bugging your birds? Avian parasitic arthropods. Wildl. Rehab.,8: 155–203.
  1. Lloyd, J. E. (2002). Louse flies, keds and related flies (Hippoboscoidea). In: G.R. Mullen and L. Durden [EDS.]. Medical and veterinary entomology. Academic Press, San Diego, CAU.S.A. Pp 349–362.
  1. Sabrosky, C. W., Bennett, G. F. and Whitworth, T. L. (1989). Bird blowflies (Protocalliphora) in North America (Diptera: Calliphoridae) with notes on the Palearctic species. Smithsonian Institution Press, Washington, DC U.S.A.
  1. Foster, W. A. and E. D. Walker. (2002). Mosquitoes (Culicidae). In: G.R. Mullen and L. Durden [EDS.], Medical and veterinary entomology. Academic Press, San Diego, CA U.S.A. Pp 203–262.
  1. Service, M. W. (1993). Mosquitoes (Culicidae). In Lane, R.P. and Crosskey, R.W. [EDS.], Medical insects and arachnids. Chapman and Hall, London, United Kingdom. Pp 120–240.
  1. Van, R. C. and Forrester, D. J. (2007). Avian pox. In: Thomas, N. J., Hunter, D. B. and Atkinson, C. T., editors. Infectious diseases of wild birds. Blackwell Publishing, Ames, Iowa, USA. Pp 136-176.
  1. Marshall, A. G. (1981). The Ecology of Ectoparasitic Insects. Academic press London. 459 pp.
  1. Whitworth, T. L. (2003). A key to the puparia of 27 species of orth American Protocalliphora Hough (Diptera: Calliphoridae) from bird nests and two new puparial descriptions. Proc. Entomol. Soc. Wash.,105: 995 – 1033.
  1. Clayton, D. H. and Drown, D. M. (2001). Critical evaluation of five methods of quantifying chewing lice (Phthiraptera; Insect). Journal Parasitole, 87: 1291-1300.
  1. Clayton, D. H., Koop, J. A. H., Harbison, C. W., Moyer, B. R. and Bush, S. E.  (2010). How Birds Combat Ectoparasites. The Open Ornithology Journal, 3:41-71.
  1. Greve, J. H. (1996). Gastrointestinal parasites and Parasites of the skin. In:Diseases of cage and aviary birds. 3rd Edn. Ed Rosskopf W. J. and Woerpel, R. W. Lea and Febiger. Baltimore. Pp 613-626.
  1. Ramisz, A. B., Marciniak, A. T. Pilarczyk, B. Dabrowska, M. W., Bakowska, R. E. E., Fox, R.S. and Barnes, R. D. (2014).  Invertebrate Zoology: a functional evolutionary approach. San Diego (7th Edition). Belmot. 505 pp.
  1. Lee, N. Y. P., Jalila A, and Babjee, S. M. A. (2005).Prevalence study of gastrointestinal parasites in psittacine birds in the KlangValley. The 17th Malaysian Veterinary Association Congres, 27-30 July, MIECC, Kuala Lumpur. Pp 77-79.
  1. Poulin, R. (1998). Evolutionary ecology of parasitism. Chapman & Hall, London, United Kingdom. 212 pp.
  1. www.pet informed veterinary advice-online.com/trihomonas.html. (2017)
  1. Dingle, J. and Shanawany, M. M. (1999). Ostrich Production Systems: FAO Animal Production and Health Paper 144. 1st edition, FAO, Rome, 256 pp.
  2. Valkiūnas, G., Bensch, S., Iezhova, T. A., Križanauskienė, A., Hellgren, O. andBolshakov, C. V. (2006). Nested cytochrome b PCR diagnostics underestimate mixed infections of avian blood hemosporidian parasites: microscopy is still essential. J Parasitol., 92:418–422.
  1. Valkiūnas, G. (2005). Avian malaria parasites and other haemosporidia. Systematic Biology, 54(5,1): 860 – 863.
  1. Chagas, C. R. F., Valkiūnas, G., Guimarães, L. O., Monteiro, E. F., Guida, F. J. V., Simões, R. F., Rodrigues, P. T., Luna, E. J. A. and Kirchgatter, K. (2017). Diversity and distribution of avian malaria and related haemosporidian parasites in captive birds from a Brazilian megalopolis. Malar. J., 16(83): 1-20.DOI 10.1186/s12936-017-1729-8.
  1. Presley, S. J., and Willig, M. R. (2008). Intraspecific Patterns of Ectoparasite Abundance on Paraguayan Bats: Effects of Host Sex and Body Size. Journal of Tropical Ecology, 24: 75-83.
  1. Fudge, A. M., McEntee, L. (1986). Avian giardiasis: Syndrome,diagnosis, and therapy. ProcAssoc Avian Vet. Pp 155-164.
  1. Redig, P. T. (1994). Diagnosis of avian aspergillosis. In:Kornelsen,M.J. (Ed.). Main Conference Proceedings of the Annual Conference of the Association of Avian Veterinarians Reno, NV, USA. Pp. 355.
  1. Davidson, W.R., and Nettles, V.F., 1997, Field manual of wildlife diseases in the Southeastern United States (2d ed.): Athens, Ga., University of Georgia, 417 pp.
  1. Chabaud, A. G. (1978). Keys to the genera of the supeifamiliesCosmocercoidea, Seuratoidea, Heterakoidea and Subuluroidea No. 6. In: Anderson et al. (Eds) Keys to the Nematode parasites of Vertebrates,CAB International. 71pp.
  1. Food and Agriculture Organization (FAO) of the United Nations (1997). FAO Yearbook, Production Vol. 49. FAO, Rome 1995.
  1. Anderson, R. C. (1992). Nematode Parasites of Vertebrates. Their development and Transmission. 578pp. CAB International. University Press, Cambridge, 'UK.
  1. Omudu, E. A., Iorlaha, G. T. and Adelusi, S. (2011). Medically Important Arthropods Infesting Some Exotic Birds and Mammals in the Makurdi Zoological Garden in Benue State, Nigeria. Scientific Journal of King Faisal University (Basic and Applied Sciences), 12: 239 – 249.
  1. Njila, H. L., Debi-Dore, J. D., Ombugadu, A., Dibal, M. and Mafuyai, M. J. (2018). Survey of Ectoparasites Infesting Captive Birds in the Jos Museum Zoological Garden, North Central, Nigeria. Journal of Natural Sciences Research,8(7): 36 – 40. ISSN 2224-3186 (Paper) ISSN 2225-0921 (Online). www.iiste.org
  1. Khan, M. A., Khan, M. S., Shafee M and Khan, J. A. (2010). Prevalence and chemotherapy of helminthiasis in parrots at Lahore zoo, Pakistan. The Journal of Animal and Plant Sciences. 20: 189-192.
  1. Santos, T., de Oliveira, J. B., Vaughan, C. and Santiago, H. (2011). Health of an ex situ population of raptors (Falconiformes and Strigiformes) in Mexico: diagnosis of internal parasites. Rev. Biol. Trop., 59: 1265-1274.
  1. Pérez Cordón, G., HitosPrados, A., Romero, D., Sánchez Moreno, M., Pontes, A., Osuna, A., et al. (2009). Intestinal and haematic parasitism in the birds of the Almu˜necar (Granada, Spain) ornithological garden. Vet. Parasitol.,165: 361–366.
  1. Prathipa, A., Jayathangaraj, M. G., Sankaralingam, G. and Thangavelu, A. (2013). Prevalence of Endoparasites in Captive Psittacine Birds Belonging to Pet Shops and Private Residences In and Around Chennai. International Journal of Veterinary Science, 2(2): 58-60.
  1. Lima, V. F. S., Bezerra, T. L., Andrade, A. F., Ramos, R. A. N., Faustino, M. A., Alves, L. C. and Meira-Santos, P. O. (2016). Gastrointestinal Parasites of exotic birds living in captivity in the state of Sergipe, Northeastern Brazil. Braz. J. Vet. Parasitol., 1-4. Doi:http//dx.doi.org/10.1590/S1984-29612016080
  1. Beernaert, L. A., Pasmans, F., Waeyenberghe, L. V., Haesebrouck, F. and Martel, A. (2010). Aspergillusinfections in birds: a review. Avian Pathology, 39(5): 325-331.
  1. Altizer, S., Dobson, A., Hosseini, P., Hudson, P., Pascual, M. and Rohani, P. (2006). Seasonality and the dynamics of infectious diseases. EcolLett, 9: 467–484.
  1. Focks, D. A., Daniels, E., Haile, D. G. and Keesling, J. E. (1995). A simulation model of the epidemiology of urban dengue fever: literature analysis, model development, preliminary validation, seasonal infection patterns in vectors and hosts and samples of simulation results. Am J Trop Med Hyg,53: 489–506.
  1. Ruiz, M. O., Chaves, L. F., Hamer, G. L., Sun, T., Brown, W. M., Walker, E. D., Haramis, L., Goldberg, T. L. and Kitron, U. D. (2010). Local impact of temperature and precipitation on West Nile virus infection in Culex species mosquitoes in northeast Illinois, USA. Parasit Vectors, 3: 19-22
  1. Burkett-Cadena, N. D., Hassan, H. K., Eubanks, M. D., Cupp, E. W. and Unnasch, T. R. (2012). Winter severity predicts the timing of host shifts in the mosquito Culexerraticus. BiolLett, 8: 567–569.
  1. Reisen, W. K., Cayan, D., Tyree, M., Barker, C. A., Eldridge, B. andDettinger, M. (2008). Impact of climate variation on mosquito abundance in California. J Vector Ecol., 33: 89-98.
  1. Allander, K. (1997). Reproductive investment and parasite susceptibility in the great tit. Funct Ecol., 11: 358–364.
  1. Hamer, G. L., Walker, E. D., Brawn, J. D., Loss, S. R., Ruiz, M. O., Goldberg, T. L., Schotthoefer, A. M., Brown, W. M., Wheeler, E. and Kitron U. D. (2008). Rapid amplification of West Nile virus: the role of hatch year birds. Vector Borne Zoonotic Dis,8: 57–67.
  1. Kim, K. S. and Tsuda, Y. (2010). Seasonal changes in the feeding pattern of Culexpipienspallens govern the transmission dynamics of multiple lineages of avian malaria parasites in Japanese wild bird community. Mol Ecol., 19: 5545–5554.
  1. Beaudoin, R. L., Applegate, J. E., Davis, D. E. and McLean, R. G. (1971). A model for the ecology of avian malaria. J Wildl Dis, 7: 5–13.
  1. Cosgrove, C. L., Wood, M. J., Day, K. P. and Sheldon, B. C., (2008). Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistescaeruleus. J Anim Ecol., 77: 540–548.
  1. Hamstra, T. L. and Badyaev, A. V. (2009). Comprehensive Investigation of Ectoparasite Community and Abundance across Life History Stages of Avian Host. Journal of Zoology, 3:1-9.