|Livestock Research for Rural Development 27 (8) 2015||Guide for preparation of papers||LRRD Newsletter||
Citation of this paper
Ectoparasite serves as vector of zoonotic and economic diseases, and degrades the welfare of animal. A gap of knowledge concerning ectoparasite fauna has remained in livestock, poultry, companion and exotic animals in Philippines where limited record existed and none in remote regions such as in Leyte Island, Philippines. The present study was carried out to determine the species of lice, fleas and ticks infesting various animals in Baybay, Leyte. A total of 577 ectoparasites were collected, processed and identified morphologically. There were 19 different species identified: 14 lice, 2 fleas, and 3 ticks. Chicken lice recorded were Goniocotes gallinae, Goniodes dissimilis, Lipeurus caponis, Oxylipeurus dentatus, Menopon gallinae, and Menacanthus stramineus. Lice isolated from rock pigeon and turkey were Columbicola columbae and Chelopistes meleagridis, respectively. Damalinia caprae and Linognathus spp. were observed in goats; D. ovis in sheep; Heterodoxus spinigera in dog; Haematopinus tuberculatus in both carabao and cattle; and H. suis in pig. Fleas isolated from dogs were Ctenocephalides felis and Pulex irritans, the former was also seen in cat. Rhipicephalus sanguineus, R. microplus and Aponomma spp. were recorded from dog, large ruminant and reticulated python, respectively. Knowledge in ectoparasite distribution and taxonomic composition will lead to better understanding of vector and vector-borne diseases. This will result in the improvement of diagnosis, prevention and control strategies in the region.
Keywords: arthropod vector, ectoparasite, tropical parasite
Ectoparasites affect the well-being of animals and serve as vector of zoonotic and economic diseases. Three of these important ectoparasites belong to suborder Ixodida (ticks), and orders Siphonaptera (fleas) and Phthiraptera (lice) (Bowman 2009). Ticks and tick-borne diseases can cause major production losses in ruminant and threat to public health by transmitting zoonotic bacteria, viruses and protozoa (Ahmed et al 2007). They are also nuisance to companion animals causing skin damage and irritation. Meanwhile, fleas serve as carrier of known human and animal pathogenic microorganisms such as Yersinia, Rickettsia and Bartonella. They are annoying biters leading to discomfort, secondary infection and skin allergy (Dieme et al 2015; Wall and Shearer 1997). Lice transmit and serve as reservoir of pathogens like swinepox and Rickettsia (Wolf 2010).Their chewing and blood feeding habit will result to anaemia, skin irritation and decrease in production capacity among poultry and livestock (Wall and Shearer 1997). Therefore, ectoparasites are serious pest with vital role in disseminating vector-borne diseases, decreasing animal production and debilitating animal welfare (Campbell-Lendrum et al 2015; Fuehrer et al 2012).
The distribution of ectoparasites certainly varies by location and climate. Tropical and subtropical climates favour good habitat for parasite survival and reproduction, thus infestations are common in Southeast Asian countries (Changbunjong et al 2009; Petney et al 2007). In the Philippines, published reports of ectoparasites fauna in domestic and exotic animals are very few especially in the islands of Visayas. Profile of ectoparasites species (i.e. lice, fleas and ticks) has focused mainly in wild animals from Luzon Island, the northern part of the country.
Researchers have isolated lately some old and new arthropod parasite from Philippine wild birds and small mammals. Common avian lice of the genus Menacanthus, Goniocotes, Menopon and Lipeurus were reported from wild birds in a rescue center (Sia Su et al 2013). Lice of the genus Columbicola, Auricotes, Strigiphilus, Colpocephalum, Kurodaia, Pseudomenopon, Rallicola, and Eulaemobothrion were found in selected Philippine wild birds, in which novel lice species were identified (Eduardo 2014; Eduardo 2012; Desemero and Eduardo 2011). Fleas collected from small mammals belonging to genus Polyplax, Xenopsyllia, Lentistivalius, Thaumapsylla, Ischnopsyllus, Sigmactenus, and Medwayella with new characterized species were also reported (Hastriter and Bush 2014; Durden and Beaucournu 2000; Luyon and Salibay 2007). Moreover, old reports of tick’s species isolated among Philippine wild pigs, Philippine deer and varanid lizards were from the genus Dermacentor, Haemaphysalis and Amblyomma, respectively (Auffenberg 1988; Wassef and Hoogstraal 1988). On the other hand, species of ectoparasites identified from domestic animals in Luzon were limited to Haematopinus tuberculatus (sucking louse of buffalo), Ctenocephalides felis (cat flea), Rhipicephalus sanguineus (brown dog tick) and R. microplus (tropical cattle tick) (Wolf 2010). Avian lice species documented from domestic chickens in the country were M. gallinae, L. caponis, M. pallidullus, G. dissimilis, and O. dentatus (Manuel and Anceno 1981).
Studies that address identification and distribution of parasite fauna in remote regions of developing countries, like in Leyte Island, are very limited and not given enough attention. Given their ability to transmit dreadful human and animal diseases, the need for profiling is therefore urgent. Ectoparasites distribution and taxonomic compositions are key points to improve the diagnosis, prevention and control programs in an area for zoonotic pathogens, as well as for economically important vector-borne diseases (Fuehrer et al 2012). Hence, this paper presents a list of morphologically identified ectoparasites from different animals in Baybay, Leyte, Philippines.
The study was carried out in Baybay, Leyte Island which is located in the eastern Visayas, central part of the Philippines at coordinate 10.6521412 °N, 124.8525626 °E. The climate is characterized by high humidity (80-90%) and temperature (27.2 to 28.2°C). There’s no seasonal demarcation in the area, but possessed high rainfall throughout the year (annual average = 2,500 mm). The eastern part is forested and highly elevated with gradual decrease in elevation to the west towards the shore. Farming and fishing are the two common livelihood of the local people, though some are involved in hunting and collecting forest resources (LGU-Baybay 2013).
Ectoparasites were collected in different villages of Baybay, Leyte, Philippines and processed at the Parasitology Laboratory of the College of Veterinary Medicine, Visayas State University. External parasites were removed manually from the body of the host using forceps and placed in vials containing Alcohol-Formalin-Acetic acid (AFA) for preservation. Afterwards, they were processed and mounted in the slide following the technique described by previous studies (Eduardo 2012; Palma 1978). Identification of the parasite to the genus and species level was carried out using holistic approach, which includes the parasitized hosts, location and finally the morphological key of ectoparasite identification (Wall and Shearer 1997; Pratt and Stojanovich 1992; Stojanovich and Pratt 1992; Soulsby 1982; Emerson 1956).
A total number of 577 ectoparasite were collected from avian, ruminant, swine, canine, feline and reptile in Baybay, Leyte, Philippines (Table 1). This constitutes 322, 71 and 184 numbers of lice, fleas and ticks, respectively. We have identified a total of 19 different species (lice = 14 species; fleas= 2 species; and ticks = 3 species).
Among the 322 number of lice, 14 species were morphologically identified with 11 chewing type (8 species from order Ischnocera; and 3 species from order Amblycera), and 3 sucking type (order Anoplura). Chewing type lice were mainly observed in avian hosts, whereas sucking type lice were only seen in mammalian. Species of chewing lice found to infest chickens in the study area were Goniocotes gallinae (n=6), Goniodes dissimilis (n=4), Lipeurus caponis (n=24), Oxylipeurus dentatus (n=25), Menopon gallinae (n=15), and Menacanthus stramineus (n=10) (Fig. 1). Large numbers of ectoparasite in chicken were identified as L. caponis and O. dentatus. Columbicola columbae (n=50) and Chelopistes meleagridis (n=6), which are both chewing lice, were observed from rock pigeon and turkey, respectively.
In mammalian host, 3 species of chewing lice and 2 species of sucking lice were identified. Goats were infested by Damalinia caprae (n=21) and Linognathus spp. (n=23). Sheep were solely infested by D. ovis (n= 19), while dogs were infested by Heterodoxus spinigera (n=32). Furthermore, the sucking louse of buffalo (H. tuberculatus) were found in both carabao (n=70) and cattle (n=12). In pigs, H. suis (n=5) was observed (Fig. 2).
The study has found 71 numbers of fleas infesting dogs and cats, these are Ctenocephalides felis (n=70) and Pulex irritans (n=1) (Table 1). Majority of the fleas were C. felis which was found to infest both dogs and cats. Pulex irritans (human flea) was recorded in dog (Fig 3). On the other hand, the study was not able to find C. canis.
A total of 184 hard ticks from 3 different species were found in dogs, cattle, carabao and reticulated python (Table 1). Brown dog ticks (Rhipicephalus sanguineus) (n=93) were the only species identified in dogs. The tropical cattle ticks (R. microplus) (n=89) were found in both cattle and carabao. The study has found Aponomma spp. (n=2) in reticulated python (Fig. 4).
|Table 1. List of species of lice, fleas and ticks found in domestic and exotic animals in Baybay, Leyte, Philippines.|
|Ectoparasite||Scientific Name||Host||Ecto (n)*|
|Columbicola columbae||Rock Pigeon (Columba livia)||50|
|Chelopistes meleagridis||Turkey (Meleagris gallopavo)||6|
|Goniocotes gallinae||Chicken (Gallus g. domesticus)||6|
|Goniodes dissimilis||Chicken (Gallus g. domesticus)||4|
|Lipeurus caponis||Chicken (Gallus g. domesticus)||24|
|Oxylipeurus dentatus||Chicken (Gallus g. domesticus)||25|
|Damalinia caprae||Goat (Capra hircus)||21|
|Damalinia ovis||Sheep (Ovies aries)||19|
|Menopon gallinae||Chicken (Gallus g. domesticus)||15|
|Menacanthus stramineus||Chicken (Gallus g. domesticus)||10|
|Heterodoxus spinigera||Dog (Canis l. familiaris)||32|
|Haematopinus tuberculatus||Carabao (Bubalus b. carabanensis)||70|
|Cattle (Bos indicus)||12|
|Haematopinus suis||Pig (Sus s. domesticus)||5|
|Linognathus spp.||Goat (Capra hircus)||23|
|Ctenocephalides felis||Dog (Canis l. familiaris)||51|
|Cat (Felis catus)||19|
|Pulex irritans||Dog (Canis l. familiaris)||1|
|Rhipicephalus sanguineus||Dog (Canis l. familiaris)||93|
|Rhipicephalus microplus||Cattle (Bos indicus)||78|
|Carabao (Bubalus b. carabanensis)||11|
|Aponomma spp.||Reticulated Python (Python reticulatus)||2|
|* Ecto (n) = Number of ectoparasites|
|Figure 1. Avian lice collected in Baybay, Leyte, Philippines. (A) Columbicola columbae, (B) Lipeurus caponis, (C) Oxylipeurus spp., (D) Menacanthus stramineus, (E) Chelopistes meleagridis, (F) Menopon gallinae, (G) Goniodes dissimilis, (H) Goniocotes gallinae. Magnification: 100x|
|Figure 2. Ruminant and swine sucking lice collected in Baybay, Leyte, Philippines. (A) Haematopinus tuberculatus, (B) Linognathus spp., (C) H. suis. Magnification: 100x|
|Figure 3. Fleas and lice found in dog and cat. (A) Ctenocephalides felis, (B) Pulex irritans, (C) Heterodoxus spinigera. Magnification: 100x|
|Figure 4. Ticks found in domestic and exotic animal in Baybay, Leyte, Philippines. (A) Rhipicephalus sanguineus, (B) R. microplus, (C) Aponomma spp. Magnification: 40x|
The present list of ectoparasite under the orders Pthiraptera (lice) and Siphonaptera (fleas), and suborder Ixodida (ticks) were identified based on holistic approach, taking into account initially the host and location where the parasites were collected, and finally according to morphological keys for diagnosis published by different authors (Wall and Shearer 1997; Pratt and Stojanovich 1992; Stojanovich and Pratt 1992; Soulsby 1982; Emerson, 1956). Identifying parasites in holistic way usually give an efficient process and reliable result when confirmed by microscopy. Through this, morphological identification becomes straightforward.
The present study reported 8 species of avian lice from Baybay, Leyte, Philippines (Figure 1). Lice identified from chicken confirms the study of Manuel and Anceno (1981) who reported M. gallinae, L. caponis, M. pallidullus, G. dissimilis, and O. dentatus in northern Philippines. Interestingly, common lice from domestic chickens such as M. stramineus, Goniodes spp., Goniocotes spp., M. gallinae and L. caponis were observed in wild birds kept in rescue center in Quezon City, Philippines (Sia Su et al 2013) despite the relative host specificity of many lice species. Though this is possible when wild birds are in contact with infested chickens since the degree of host specificity among lice is dictated by its ability to disperse among multiple host species (Brooke and Nakamura 1998). Furthermore, 3 lice species (L. caponis, G. dissimilis and M. gallinae)) observed in Tak Province, Thailand were also observed in the study area (Changbunjong et al 2009). We have identified C. columbae as main lice infesting rock pigeons and C. meleagridis infesting turkey. Their occurrence has also been reported in many parts of the world causing host debilitation (Galloway and Lamb 2015; Radfar et al 2011).
The identified lice from ruminants include D. caprae, D. ovis, H. tuberculatus, Linognathus spp. and H. spinigera. In the Philippines, other species of Damalinia was found to infest Philippine deer (Eduardo 2000) and H. tuberculatus usually infest carabao (Del Rosario and Manuel 1983). In terms of public health concern, a study conducted by Wolf (2010) showed that H. tuberculatus collected from carabao in Luzon was positive for Rickettsia felis, the causative agent of human spotted fever. We also recorded another sucking louse (Linognathus spp.) that infests goat. This ectoparasite morphologically differ from Haematopinus by the presence of smaller first pair of legs with stout claws compared to the second and third pairs (Wall and Shearer, 1997). The three known lice to infest dogs are Linognathus setosus, Trichodectes canis and H. spinigera. According to Thompson (1939), it is rare to find these 3 species co-occurring in one dog. However, there’s a great chance that the occurrence of H. spinigera in dogs in Southeast Asian countries will persist due to better lice adaptability, increase population of stray dogs, and pet popularity (Irwin and Jefferies 2004).
Two species of fleas were recorded in our study. We found C. felis in both dog and cat, and P. irritans in dogs. Dogs are not the common host of the two identified fleas. C. felis is more common in cat. Similarly, P. irritans (human flea) infest mainly pigs and jump to human in contact. Indeed, fleas are facultative parasites capable of infesting multiple host. A study in Israel showed that these two species could transmit zoonotic diseases such as Bartonella risking human having pet dogs (Sofer et al 2015). In fact, fleas are transmitter of numerous parasites, bacteria and virus to animals and humans (Bowman 2009).
In Southeast Asia, R. sanguineus and R. microplus are the most common ticks in dog and large ruminant, respectively (Changbunjong et al 2009). While in reptiles, Aponomma spp. has also been recorded some Asian countries (Petney et al 2007). Likewise, our study found these three species infesting dog, ruminant and reticulated python. In central Philippines, R. sanguineus and R. microplus were reported to carry zoonotic microorganisms (e.g. Anaplasma platys) (Ybañez et al 2012). Also, Aponomma spp. has been reported to transmit the pathogens Cowdria and Rickettsia, which causes Heartwater disease in ruminant and spotted fever in human, respectively (Burridge et al 2000).
The result of our study offers the first list of ectoparasite fauna in Baybay, Leyte, Philippines. Knowing their distribution and taxonomic composition means a better understanding in terms of diagnosis, prevention and control of vector and vector-borne diseases. Further studies are needed to evaluate their spatiotemporal pattern and analyse its direct impact to animals and human in remote and agricultural regions of the country.
We thank the owner of the animals and the clinicians/staff of the College of Veterinary Medicine, Visayas State University for the cooperation and assistance during the conduct of the study.
Ahmed J, Alp H, Aksin M and Seitzer U 2007 Current status of ticks in Asia. Parasitology Research 101(2): 159–162.
Auffenberg T 1988 Amblyomma helvolum (Acarina: Ixodidae) as a parasite of varanid and scincid reptiles in the Philippines. International Journal for Parasitology 18(7): 937-945.
Bowman D D 2009 Georgis’ Parasitology for Veterinarians. 9th edn. Saunders Elsevier, USA.
Brooke M D L and Nakamura H 1998 The acquisition of host-specific feather lice by common cuckoos (Cuculus canorus). Journal of Zoology 244 (02): 167-173.
Burridge M J, Simmons L A and Allan S A 2000 Introduction of potential heartwater vectors and other exotic ticks into Florida on imported reptiles. Journal of Parasitology 86(4): 700-704
Campbell-Lendrum D, Manga L, Bagayoko M and Sommerfeld J 2015 Climate change and vector-borne diseases: what are the implications for public health research and policy?. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 370(1665): 20130552. doi: 10.1098/rstb.2013.0552
Changbunjong T, Buddhirongawatr R, Suwanpakdee S, Siengsanan J, Yongyuttawichai P, Cheewajorn K, Jangjaras J, Sangloung C and Ratanakorn P A 2009 Survey of ectoparasitic arthropods on domestic animals in Tak Province, Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 40: 435-442.
Del Rosario M C and Manuel M F 1983 Sucking louse Haematopinus tuberculatus Burmeister, 1838: morphology and distribution on the body of Philippine swamp buffalo. Philippine Journal of Veterinary Medicine 12: 126-183.
Desamero M M and Eduardo S L 2011 Some Ectoparasites from Philippine Owls (Strigiformes: Strigidae) with Description of a New Louse Species, Kurodaia (Conciella) theresamunditae Desamero & Eduardo (Amblycera: Menoponidae). Philippine Journal of Veterinary Medicine 48 (1): 27-34
Dieme C, Parola P, Guernier V, Lagadec E, Le Minter G, Balleydier E, Pagès F, Dellagi K, Tortosa P, Raoult D and Socolovschi C 2015 Rickettsia and Bartonella species in fleas from Reunion Island. The American Journal of Tropical Medicine and Hygiene 92(3): 617-619.
Durden L A and Beaucournu J C 2000 The flea genus Sigmactenus (Siphonaptera: Leptopsyllidae): a new species from Timor and new material from New Guinea and the Philippines.Journal of Parasitology 86(3): 32-437.
Eduardo S L 2000 Damalinia cordillerai n. sp. (Mallophaga: Trichodectidae) and two other previously known arthropod parasites of the Luzon sambar deer, Cervus (Rusa) philippinus Smith, 1827 (Mammalia: Artiodactyla: Ruminantia). Philippine Journal of Veterinary Medicine 37(2): 72-81.
Eduardo S L 2012 Species of the Genus Pseudomenopon Mjöberg, 1910 (Mallophaga: Amblycera: Menoponidae) Occurring on Philippine Rallidae (Aves: Gruiformes) With Description of a New Species, Pseudomenopon micosai. Philippine Journal of Veterinary Medicine 49(1): 21-29
Eduardo S L 2014 Rallicola Johnston and Harrison 1911 and Eulaemobothrion Ewing 1929 species (Mallophaga) found on some Philippine Rallidae (Aves: Gruiformes) with description of a new species. Philippine Journal of Veterinary Medicine 51(2): 107-106: 107-106
Emerson K C 1956 Mallophaga (chewing lice) occurring on the domestic chicken. Journal of the Kansas Entomological Society 29(2): 63-79
Fuehrer H P, Igel P, Treiber M, Baumann T A, Riedl J, Swoboda P, Joachim A and Noedl H 2012 Ectoparasites of livestock, dogs, and wild rodents in the Chittagong Hill Tracts in southeastern Bangladesh. Parasitology research 111(4): 1867-1870.
Galloway T D and Lamb R J 2015 Seasonal population dynamics of four species of chewing lice (Phthiraptera: Menoponidae, Philopteridae) on feral pigeons (Aves: Columbiformes: Columbidae). The Canadian Entomologist 1-11. available on CJO2015. doi:10.4039/tce.2014.84.
Hastriter M W and Bush S E 2014 Description of Medwayella independencia (Siphonaptera, Stivaliidae), a new species of flea from Mindanao Island, the Philippines and their phoretic mites, and miscellaneous flea records from the Malay Archipelago. Zookeys. (408): 107–123.doi: 0.3897/zookeys.408.7479
Irwin P J and Jefferies R 2004 Arthropod-transmitted diseases of companion animals in Southeast Asia. Trends in Parasitology 20(1): 27-34.
LGU-Baybay 2013 Local Government Unit of Baybay City, Leyte. Accesed on April 30, 2015 https://lgubaybay.wordpress.com/
Luyon H A V and Salibay C 2007 Ectoparasites on murid rodents caught in Mts. Palay-palay/Mataas Na Gulod National park, Luzon Island, Philippines. Southeast Asian Journal of Tropical Medicine and Public Health 38(1): 194-202
Manuel M F and Anceno T A 1981 Distribution of biting lice Mallophaga on the body of native chickens Gallus domesticus. Philippine Journal of Veterinary Medicine 20(1): 50-57
Palma R L 1978 Slide-mounting of lice: a detailed description of the Canada balsam technique. New Zealand Entomologist 6(4): 432-436.
Petney T N, Kolonin G V and Robbins R G 2007 Southeast Asian ticks (Acari: Ixodida): a historical perspective. Parasitology Research 101(2): 201-205.
Pratt H D and Stojanovich C J 1992 Fleas: Illustrated Key to Species Found During Plague Investigations. In. CDC pictorial keys, arthropods, reptiles, birds and mammals of public health significance US Department of Health Education and Welfare. Public Health Service. Reprinted in, 171-174.
Radfar M H, Fathi S, Asl E N, Dehaghi M and Seghinsara H R 2011 A survey of parasites of domestic pigeons (Columba livia domestica) in South Khorasan. Iranian Journal of Veterinary Research 4(1): 18-23.
Sia Su GI, Amil C J A, San Juan J AP, Sia Su M L, Maguad G S, Salinas R A, Ragragio EM, Santiago AA and Ramos G B 2013 Ectoparasite Survey of Quarantined Animals in a Wildlife Rescue Center in Quezon City, Philippines. World Journal of Agricultural Research 1(3): 44-47.
Sofer S, Gutiérrez R, Morick D, Mumcuoglu K Y and Harrus S 2015 Molecular detection of zoonotic bartonellae (B. henselae, B. elizabethae and B. rochalimae) in fleas collected from dogs in Israel. Medical and Veterinary Entomology DOI: 10.1111/mve.12116
Soulsby E J L 1982 Helminths, Arthropods and Protozoa of Domesticated Animals. 7thEdn. Bailliere Tindall, London, Great Britain pp. 366-383
Stojanovich CJ and Pratt HD 1992 Anoplura and Mallophaga: Pictorial Key to Some Common Genera of Sucking Lice. In. CDC pictorial keys, arthropods, reptiles, birds and mammals of public health significance US Department of Health Education and Welfare. Public Health Service. Reprinted in, 68-91.
Thompson G B 1939 The distribution of Heterodoxus spiniger (Enderlein). In Papers and Proceedings of the Royal Society of Tasmania pp. 27-32.
Wall R and Shearer D 1997 Veterinary Ectoparasites: Biology, Pathology and Control. 2nd Edn. Blackwell. Ames, Iowa, USA.
Wassef H Y and Hoogstraal H 1988 Dermacentor (Indocentor) steini (Acari: Ixodoidea: Ixodidae): hosts, distribution in the Malay Peninsula, Indonesia, Borneo, Thailand, the Philippines, and New Guinea. Journal of Medical Entomology 25(5): 315-320.
Wolf M S 2010 Air Force Entomology Efforts during Operation Pacific Angel: Philippines, 2010. Proceedings of the Department of Defense (DoD) Symposium “DoD Entomology: Global, Diverse, and Improving Public Health”. Entomological Society of America. San Diego, CA. pp 47-51.
Ybañez A P, Perez Z O, Gabotero S R, Yandug R T, Kotaro M and Inokuma H 2012 First molecular detection of Ehrlichia canis and Anaplasma platys in ticks from dogs in Cebu, Philippines. Ticks and Tick-borne diseases 3(5): 288-293.
Received 18 May 2015; Accepted 25 May 2015; Published 1 August 2015
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