Abstracts
Ctenocephalides felis felis is one of the most important ectoparasites of dogs and cats throughout the world, because of its geographical distribution, dual parasitological action as an infesting agent and a vector of diseases, the economic losses and the acquired resistance against common insecticides. In Brazil, it surpasses Ctenocephalides canis in distribution, number of host species infested, prevalence and epidemiological importance. However, in some studies the species have been misidentified on the basis of their morphological characters included in taxonomic keys. The morphological variations of chaetotaxy, especially those on the dorsal margin of the hind tibia and lateral metanotal area (LMA), found in certain specimens, have sometimes been erroneously treated as hybrids, in spite of the nonexistence of the two species of Ctenocephalides in the same municipality or region. This review focuses on the characteristics used for interspecific diagnosis and intraspecific variations found between the species. Data on distribution, hosts, prevalence and parasitological action are also presented as an auxiliary means for recognizing the species.
Ctenocephalides felis felis; Ctenocephalides canis; Siphonaptera; fleas; taxonomy; morphological variation
Ctenocephalides felis felis é um dos mais importantes ectoparasitos de cães e gatos no mundo inteiro, em virtude de sua distribuição geográfica, dupla ação parasitológica como agente infestante e vetor de doenças, perdas econômicas e resistência adquirida contra inseticidas comuns. No Brasil, ela sobrepuja Ctenocephalides canis em distribuição, número de espécies de hospedeiros infestadas, prevalência e importância epidemiológica. Todavia, em alguns estudos, as espécies têm sido incorretamente identificadas pelos caracteres morfológicos incluídos em chaves taxonômicas. As variações morfológicas de quetotaxia, especialmente aquelas da margem dorsal da tibia posterior e área metanotal lateral (LMA) encontradas em certos exemplares, algumas vezes têm sido erroneamente consideradas como híbridas, a despeito da inexistência das duas espécies em um mesmo município ou região. Esta revisão aborda as características utilizadas para o diagnóstico interespecífico e variações intra-específicas encontradas entre as espécies. Dados sobre distribuição, hospedeiros, prevalência e atuação parasitológica são também apresentados como um meio auxiliar para o reconhecimento das espécies.
Ctenocephalides felis felis; Ctenocephalides canis; Siphonaptera; pulgas; taxonomia; variações morfológicas
REVIEW ARTICLE
Ctenocephalides felis felis vs. Ctenocephalides canis (Siphonaptera: Pulicidae): some issues in correctly identify these species
Ctenocephalides felis felis vs. Ctenocephalides canis: (Siphonaptera: Pulicidae): algumas questões para identificar corretamente estas espécies
Pedro Marcos LinardiI; Juliana Lúcia Costa SantosI, II
IDepartamento de Parasitologia, Instituto de Ciências Biológicas - ICB, Universidade Federal de Minas Gerais - UFMG, Belo Horizonte, MG, Brasil
IIEscola de Saúde Pública do Estado de Minas Gerais - ESP-MG, Belo Horizonte, MG, Brasil
Correspondence to Correspondence to: Pedro Marcos Linardi Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais - UFMG CP 486 CEP 31270-901, Belo Horizonte, MG, Brasil e-mail: linardi@icb.ufmg.br
ABSTRACT
Ctenocephalides felis felis is one of the most important ectoparasites of dogs and cats throughout the world, because of its geographical distribution, dual parasitological action as an infesting agent and a vector of diseases, the economic losses and the acquired resistance against common insecticides. In Brazil, it surpasses Ctenocephalides canis in distribution, number of host species infested, prevalence and epidemiological importance. However, in some studies the species have been misidentified on the basis of their morphological characters included in taxonomic keys. The morphological variations of chaetotaxy, especially those on the dorsal margin of the hind tibia and lateral metanotal area (LMA), found in certain specimens, have sometimes been erroneously treated as hybrids, in spite of the nonexistence of the two species of Ctenocephalides in the same municipality or region. This review focuses on the characteristics used for interspecific diagnosis and intraspecific variations found between the species. Data on distribution, hosts, prevalence and parasitological action are also presented as an auxiliary means for recognizing the species.
Keywords:Ctenocephalides felis felis, Ctenocephalides canis, Siphonaptera, fleas, taxonomy, morphological variation.
RESUMO
Ctenocephalides felis felis é um dos mais importantes ectoparasitos de cães e gatos no mundo inteiro, em virtude de sua distribuição geográfica, dupla ação parasitológica como agente infestante e vetor de doenças, perdas econômicas e resistência adquirida contra inseticidas comuns. No Brasil, ela sobrepuja Ctenocephalides canis em distribuição, número de espécies de hospedeiros infestadas, prevalência e importância epidemiológica. Todavia, em alguns estudos, as espécies têm sido incorretamente identificadas pelos caracteres morfológicos incluídos em chaves taxonômicas. As variações morfológicas de quetotaxia, especialmente aquelas da margem dorsal da tibia posterior e área metanotal lateral (LMA) encontradas em certos exemplares, algumas vezes têm sido erroneamente consideradas como híbridas, a despeito da inexistência das duas espécies em um mesmo município ou região. Esta revisão aborda as características utilizadas para o diagnóstico interespecífico e variações intra-específicas encontradas entre as espécies. Dados sobre distribuição, hospedeiros, prevalência e atuação parasitológica são também apresentados como um meio auxiliar para o reconhecimento das espécies.
Palavras-chave:Ctenocephalides felis felis, Ctenocephalides canis, Siphonaptera, pulgas, taxonomia, variações morfológicas.
Introduction
Within the family Pulicidae of the order Siphonaptera, the genus Ctenocephalides Stiles & Collins, 1930, includes 13 species and subspecies (BEAUCOURNU; MÉNIER, 1998), but only two, respectively the dog flea Ctenocephalides canis (Curtis, 1826) and the cat flea Ctenocephalides felis felis (Bouché, 1835), are cosmopolitans that have been recorded in South America. C. felis felis is more adaptable than C. canis, since it infests more host species and has therefore become established in more extensive areas (HOPKINS et al., 1953). According to KOUTINAS et al. (1995), the distribution of these species is related to environmental factors that influence their survival, development and reproduction.
Although the two species of Ctenocephalides can occur in the same Brazilian geographical region and infest the same host species, C. felis felis is more important in disease transmission. Moreover, C. felis felis has also already shown resistance to common insecticides for two decades (EL-GAZZAR et al., 1986). For this reason, correct species identification is essential for control measures and genetic inferences.
The two species are usually separated according to the shape of the head, length of the first spine of the genal comb, number of bristles on the lateral metanotal area (LMA) (Figures 1, 2) and the number of short stout bristles in the interval between the postmedian and apical long bristles of the dorsal margin of the hind tibia (HOPKINS et al., 1953; JOHNSON, 1957; AMIN, 1976; MÉNIER; BEAUCOURNU, 1998; BEAUCOURNU; MÉNIER, 1998; LINARDI; GUIMARÃES, 2000) (Figures 3, 4; Table 1). Males can be further identified by the shape of the manubrium of the clasper (HOLLAND, 1949) (Figures 5, 6) and the size of the hamulus on the aedeagus (Figures 2 and 3 of MÉNIER; BEAUCOURNU, 1998). However, in spite of these differences, some variations in the chaetotaxy and the number of spines in the genal comb have been found (AMIN, 1976; AMIN et al., 1974). Some misidentifications have also been noticed: in the Afrotropical zone, C. felis strongylus has often been identified incorrectly as C. canis based on the sole criterion of the cephalic profile; and likewise, C. orientis in Asia (BEAUCOURNU; KOCK, 1990). Ctenocephalides collected from epidemiological investigations, particularly in relation to plague in the Palaearctic and Nearctic regions, were often named according to their hosts, although urban dogs are much more infested with C. felis felis than with C. canis (BEAUCOURNU, 1973). On the other hand, some characteristics have been improperly interpreted when using certain taxonomic keys.
Hosts of Ctenocephalides
Ctenocephalides species infest carnivores, edentates, lagomorphs, marsupials, primates, rodents and ungulates, and can also be found in the nests, burrows, trails and tracks of their hosts, as well as indoors, where they colonize profusely (LINARDI; GUIMARÃES, 2000). Brazilian host species recorded for species of Ctenocephalides include seven orders and 41 species of mammals, as well as one species of bird infested by C. felis felis (Table 2). Although carnivores can be considered to be the true or primary hosts, infestations on Brazilian carnivores and rodents represent respectively 26.8% and 43.9% of the findings. The cat flea is commonly collected on opossums because of the varied habitats that they use (LINARDI, 2006). On the contrary, C. canis is only seen on domestic carnivores.
Ctenocephalides Species as Vectors of -Diseases
Amongst the arthropods, C. felis felis is the most important ectoparasite of dogs and cats throughout the world, causing annoyance to the animals and acting as a vector of diseases (RUST; DRYDEN 1997). It causes allergic dermatitis (HALLIWELL, 1979) and in heavy infestations can also cause iron deficiency anemia in young animals (HARVEY et al., 1982). More than twenty different types of endosymbionts or pathogens have been found to be associated with species of Ctenocephalides as biological vectors or intermediate hosts, including bacteria, protozoa and helminths, thus representing a potential health risk for humans (JELLISON, 1959; JENKINS, 1964; BEARD et al., 1990; KRÄMER; MENCKE, 2001; LINARDI; GUIMARÃES, 2000; LINARDI, 2001). The cat flea also lodges other monoxenic organisms, such as gregarines, microsporidians and trypanosomatids. The endosymbionts or pathogens found in Ctenocephalides species in Brazil are shown in Table 3. According to De Avelar et al. (2007, 2008), these endosymbionts might be useful for biological control of C. felis felis in environments exhibiting high levels of infestation. Also using molecular techniques, Coutinho and Linardi (2007) and Ferreira et al. (2009a) recognized DNA of Leishmania chagasi in C. felis felis, thus opening new perspectives for mechanical transmission of canine visceral leishmaniasis.
De Avelar et al. (2011) raised the possibility that Leptomonas of fleas may be pathogenic to humans and dogs because some people crush dog fleas between their fingers and carry them to their mouths. Besides, dogs are likely to ingest flea gut contents or entire fleas when crushing the insects between their teeth or licking their own fur or that of other dogs. According to Garin et al. (2001), it is possible that the numbers of human cases of infection with lower trypanosomatids is underestimated because of the morphological similarity to and cross-reactivity with Leishmania infantum chagasi.
In addition to the role as a transmitter of diseases, C. felis felis provokes allergic dermatitis and has been reported to produce anemia in dogs, cats, goats, cattle and sheep (OBASAJU; OTESILE, 1980; YERUHAM et al., 1989).
Geographical Distribution
C. felis felis was most prevalent species in studies on companion animals in Argentina (LOMBARDDERO; SANTA-CRUZ, 1986), Australia (CORNACK; O'ROURKE, 1991), Denmark (KRISTENSEN et al., 1978), Egypt (AMIN, 1966), Germany (LIEBISCH et al., 1985), Puerto Rico (FOX, 1952), South Africa (HORAK, 1982), United Kingdom (BERESFORD-JONES, 1981; COWARD, 1991; CHESNEY, 1995) and USA (AMIN, 1976; MUNSEE, 1985; HARMAN et al., 1987). Otherwise, C. canis was the commonest species found on dogs in Austria (RESSL, 1963), Greece (KOUTINAS et al., 1995), Ireland (BAKER; HATCH, 1972), New Zealand (GUZMAN, 1984) and Poland (PIOTROWSKI; POLOMSKA, 1975).
In Brazil, C. felis felis is also the most common flea of Canidae and has been found in 17 states: Alagoas, Amazonas, Bahia, Ceará, Espírito Santo, Goiás, Mato Grosso, Minas Gerais, Paraíba, Paraná, Pernambuco (including the territory of Fernando de Noronha), Rio de Janeiro, Rio Grande do Norte, Rio Grande do Sul, Roraima, Santa Catarina and São Paulo. On the other hand, C. canis occurs less frequently, mainly in areas with high or low temperatures (LINARDI; NAGEM, 1973). Up until now, infestations by C. canis on companion animals have been recorded only in nine states: Amazonas, Bahia, Maranhão, Minas Gerais, Paraná, Pernambuco, Rio Grande do Sul, Santa Catarina and São Paulo. In relation to the state of Paraná, out of the 2,676 fleas recovered by Unti (1935) on several dogs in the municipalities of Curitiba, Araucária, Marechal Mallét, Pirahy, Mafra, Rio Negro, Ponta Grossa, Paranaguá and Colombo, 53.5% were C. canis and 40.6% C. felis felis. Also in Florianópolis, state of Santa Catarina, C. canis and C. felis felis were found in respectively, 54% and 38% of the samples. The data concerning the prevalence of these two species on Brazilian domestic carnivores are shown in Table 4.
Morphological Variations
In Ctenocephalides spp., the most frequent morphological variations are observed in the combs and chaetotaxies of LMA (erroneously referred to as the metepisternum by some authors) and in hind tibia (AMIN et al., 1974; AMIN, 1976). In Canada, Holland (1949) found certain nontypical specimens, usually females, which were difficult to identify with certainty. Because of this, the two species were treated collectively in those localities where they were collected.
Alterations in chaetotaxy on the LMA and metatibia might suggest hybridization between the two species, as previously proposed by Holland (1949), Fox (1952), Amin et al. (1974) and Amin (1976). According to Benton (1998), hybrids depend upon occurrence of two closely related species in close association, such as in fleas of the genus Ceratophyllus Curtis, 1832, which share the same bird nests in North America. However, the hypothesis of hybridization between C. felis felis and C. canis must be rejected because good species do not cross with each other, as reinforced by Beaucournu and Guiller (2006).
In Brazil, altered chaetotaxies on the LMA or hind tibia of Ctenocephalides spp. were also observed by Nagem (1977) when examining fleas from dogs in the municipality of São João d'El Rei, state of Minas Gerais, and by Fernandes et al. (1996) in fleas from dogs and cats in the municipality of Rio de Janeiro, state of Rio de Janeiro. However, in these surveys, they were named C. felis felis. Other variations concerning the chaetotaxy of these species were unduly designated hybrids in some studies (RODRIGUES et al., 2008; SANTOS, 2008; STALLIVIERE et al., 2009).
In a sample of 87 fleas collected from 33 dogs in the rural zone of the municipality of Jaboticatubas, around Serra do Cipó National Park (19° 30' S and 43° 44' W), state of Minas Gerais, Brazil, Santos (2008) found that all the dogs were infested by C. f. felis, and 18 of them (54.5%) by specimens presenting variations in the number of bristles on the LMA and/or metatibia. Out of the 87 specimens of C. f. felis examined, 27 (31.0%) presented variations both on the LMA and hind tibia (Table 5). Separately by sex, the variations represented 40.7% in females and 15.1% in males, with a significant difference between them when compared using the chi-square test (χ2 = 6.26; p < 0.05). Also in this sample, 15 specimens (17.2%) presented variations only on one side (asymmetrical), while in four (4.6%) the alterations were observed on both sides of the thorax (symmetrical) (Table 6). About 21.8% of the alterations from the standard numbers consisted of an increase of at least one bristle. Alterations occurred significantly more frequently in females (33.3%) than in males (6.1%) (χ2 = 7.1; p < 0.01). Figure 7 shows the variation of the number of bristles on the left side of the LMA. The variations of chaetotaxy of the hind tibia among the sampled specimens of C. f. felis are indicated in Table 7; 12.7% of the specimens examined presented such variations. Figure 8 illustrates one of these variations. Contrary to the characteristics of the LMA, the chaetotaxy of the hind tibia was approximately equally variable in both sexes. Asymmetrical variations (9.2%) were more frequent than symmetrical ones (3.4%). Likewise, variations involving increased numbers of bristles were more frequently found (9.2%) than ones relating to decreased numbers (3.4%) (Table 7).
Although the total numbers of variations (Table 5) and the ones concerning the LMA (Table 6) in the present study were more significant in females, and a great number of females were collected (62.1%), Amin (1976) found similar results when studying dog and cat fleas from Wisconsin, USA. Interestingly, both variations of bristles on the LMA (Table 6) and hind tibia (Table 7) were more significant in relation to increased numbers of bristles, rather than decreased numbers.
Final Remarks
Given the enormous epidemiological and economical importance of these fleas, correct identification of species is indispensable. Pet flea-related diseases account for over 50% of the dermatological cases reported to veterinarians (BEVIER-TOURNAY, 1989). Moreover, the annual expenditure by pet owners on flea control products in the United States exceeds $ 1 billion (CONNIFF, 1995). Besides the economical aspect, C. felis felis has been reported to have developed resistance to at least five different categories of insecticides, including carbamates, organophosphates, pyrethroids, pyrethrins and organochlorines (WHO, 1992).
In Brazil, C. felis felis is the most important flea species on pets because of its geographical distribution, number of other hosts parasitized and vector competence. It is more euryxenous than C. canis, having been recorded on 41 different host species (Table 2) and 17 states, as well as being found naturally infected by eight different species of endosymbionts (Table 3). The infestations are more prevalent in southeastern states (Table 4). In all states, cats exclusively harbored C. felis felis. Except for Manaus and Salvador, where only small numbers of few dogs were sampled, the prevalence of infestation by C. canis seems to increase from north to south. Interestingly, Castro and Rafael (2006) found no specimens of C. canis on dogs in Manaus, whereas previously Gordon and Young (1922) observed dogs infested only by this species. It remains unclear as to whether this finding was geographically isolated or whether, in fact, this species is truly decreasing in numbers towards extinction; or else, whether it was incorrectly identified.
It is important to stress that the head curvature is highly different between males and females of C. felis felis; however, this characteristic may be unclear for separating males of the two species. Consequently, in some studies, males of C. felis felis have been incorrectly diagnosed as C. canis.
Morphological variations among fleas do not always result from interbreeding between species (TIPTON; MACHADO-ALISSON, 1972; AMIN; SEWELL, 1977; AMIN et al., 1974; LINARDI, 1984), but they must be used carefully for taxonomic purposes. Since the chaetotaxies of the hind tibia and LMA showed significant intraspecific variations, these two characteristics must be cautiously used for interspecific diagnoses. Sometimes, specimens exhibiting variations have been improperly treated as hybrids, in spite of the nonexistence of the two species in the same municipality or region.
It is concluded that separation of the two species of Ctenocephalides must be done while considering all characteristics. Data on hosts, geographical distribution and prevalence of infestation may support identification of the species.
ACKNOWLEDGEMENTS
In this research, the data on chaetotaxy variations constituted part of the MSc thesis of JLCS on Parasitology, produced within the Postgraduate Parasitology Program, Institute of Biological Sciences, Federal University of Minas Gerais (UFMG), and was partially supported by the Research Support Foundation of the State of Minas Gerais (FAPEMIG), Brazil). PML is a research fellow supported by the National Council for Scientific and Technological Development (CNPq), Brazil.
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Horak IG. Parasites of domestic and wild animals in South Africa. XIV. The seasonal prevalence of Rhipicephalus sanguineus and Ctenocephalides spp. on kennelled dogs in Pretoria North. Onderstepoort J Vet Res 1982; 49(1): 63-68. PMid:7122067.
Horta MC, Chiebao DP, De Souza DB, Ferreira F, Pinheiro SR, Labruna MB, et al. Prevalence of Rickettsia felis in the fleas Ctenocephalides felis felis and Ctenocephalides canis from two Indian villages in São Paulo municipality, Brazil. Ann N Y Acad Sci 2006; 1078: 361-363. PMid:17114741. http://dx.doi.org/10.1196/annals.1374.071
Horta MC, Labruna MB, Pinter A, Linardi PM, Schumaker TTS. Rickettsia infection in five areas of the state of São Paulo, Brazil. Mem Inst Oswaldo Cruz 2007; 102(7): 793-801. PMid:18094887. http://dx.doi.org/10.1590/S0074-02762007000700003
Jellison WL. Fleas and disease. Annu Rev Entomol 1959; 4: 389-414. http://dx.doi.org/10.1146/annurev.en.04.010159.002133
Jenkins DW. Pathogens, parasites and predators of medically important arthropods. Anotated list and bibliography. Bull World Health Organ 1964; 30 (Suppl): 1-30. PMid:14245244.
Johnson PT. A classification of the Siphonaptera of South America with description of new species. Mem Ent Soc Wash 1957; 5: 1-298.
Koutinas AF, Papazahariadou MG, Rallis TS, Tzivara NH, Himonas CA. Flea species from dogs and cats in northern Greece: environmental and clinical implications. Vet Parasitol 1995; 58(1-2): 109-115. http://dx.doi.org/10.1016/0304-4017(94)00706-I
Krämer F, Mencke N. Flea biology and control. Berlin: Springer-Verlag; 2001. http://dx.doi.org/10.1007/978-3-642-56609-7
Kristensen S, Haarlov V, Mourier H. A study of skin diseases in dogs and cats. IV. Patterns on flea infestation in dogs and cats in Denmark. Nord Vet Med 1978; 30(10): 401-413. PMid:714660.
Liebisch A, Brandes R, Hoppenstedt KI. Zum Befall Von Hunden und Katzen MIT Zecken und Flöhen in Deutschland. Prakt Tierarzt 1985; 66: 817-824.
Linardi PM. Utilização de algumas estruturas na caracterização de espécies da ordem Siphonaptera. II. A quetotaxia da margem posterior da tíbia posterior na separação de espécies de Polygenis Jordan, 1939. Rev Brasil Ent 1984; 28(1): 115-119.
Linardi PM. Pulgas. In: Marcondes CB. Entomologia médica e veterinária. São Paulo: Atheneu; 2001. p. 157-181.
Linardi PM. Endoparasitos de Ctenocephalides felis felis (Siphonaptera: Pulicidae) em Belo Horizonte, MG. O Biológico 2002; 64(1): 65.
Linardi PM. Os ectoparasitos de marsupiais brasileiros. In: Cáceres NC, Monteiro Filho ELA. Os marsupiais do Brasil: Biologia, ecologia e evolução. Campo Grande: Editora UFMS; 2006. p. 37-52.
Linardi PM, Nagem RL. Pulicídeos e outros ectoparasitos de cães de Belo Horizonte e municípios vizinhos. Rev Bras Biol 1973; 33(4): 529-537. PMid:4804478.
Linardi PM, Guimarães LR. Sifonápteros do Brasil. São Paulo: Museu de Zoologia USP/FAPESP; 2000.
Lombarddero OJ, Santa-Cruz AM. Parasites of stray dogs in the city of Corrientes (Argentina). Changes over a 25 year-period. Vet Argent 1986; 3: 888-892.
Lustosa ES, Carneiro JR, Carvalho MED, Jardim JHV. Ectoparasitos de cães vadios de Goiânia. Rev Patol Trop 1973; 2(4): 397-379.
Menezes OB. Parasitos de Canis familiaris em Salvador. Bol Inst Biol Bahia 1954; 1(1): 75-78.
Ménier K, Beaucournu JC. Taxonomic study of the genus Ctenocephalides Stiles & Collins, 1930 (Insecta: Siphonaptera: Pulicidae) by using aedeagus characters. J Med Entomol 1998; 35(5): 883-890. PMid:9775624.
Munsee JR. Annual changes in flea populations on three domestic pets, 1978-1984. Proc Indiana Acad Sci 1985; 94: 329-334.
Nagem RL. Sifonápteros da Coleção UFMG: sistemática, relações estruturais, adaptativas e entre hospedeiro/parasito [ Dissertação]. Belo Horizonte: Universidade Federal de Minas Gerais; 1977.
Obasaju MF, Otesile EB. Ctenocephalides canis infestation of sheep and goats. Trop Anim Health Prod 1980; 12(2): 116-118. PMid:7414697. http://dx.doi.org/10.1007/BF02242620
Oliveira CMB, Ribeiro PB. Espécies de pulgas que parasitam cães em Porto Alegre e suas prevalências mensais. Arq Fac Vet UFRGS 1982/83; 10-11: 29-33.
Oliveira RP, Galvão MAM, Mafra CL, Chamone CB, Calic SB, Silva SU, et al. Rickettsia felis in Ctenocephalides spp. fleas, Brazil. Emerg Infect Dis 2002; 8(3): 317-319. PMid:11927031 PMCid:2732462. http://dx.doi.org/10.3201/eid0803.010301
Piotrowski F, Polomska J. Ectoparasites of the dog (Canis familiaris L.) in Gdansk. Wiad Parazytol 1975; 21(3): 441-451. PMid:1146337.
Raszl SM, Cabral DD, Linardi PM. Notas sobre sifonápteros (Pulicidae, Tungidae e Rhopalopsyllidae) de carnívoros domésticos brasileiros. Rev Bras Entomol 1999; 43(1-2): 95-97.
Ressl F. Die Siphonapterenfauna dês Verwaltungsbezirkes Scheibbs (Niederösterreich). Z F Parasitenkunde 1963; 23: 470-490.
Rodrigues AFSF, Daemon E, D'Agosto M. Investigação sobre alguns ectoparasitos em cães de rua no município de Juiz de Fora. Minas Gerais. Rev Bras Parasitol Vet 2001; 10(1): 13-19.
Rodrigues DF, Daemon E, Rodrigues AFSF. Caracterização da população de ectoparasitos em cães de núcleos de expansão urbana de Juiz de Fora, Minas Gerais, Brasil. Rev Bras Parasitol Vet 2008; 17(4): 185-188. PMid:19265575.
Rust MK, Dryden MW. The biology, ecology, and management of the cat flea. Annu Rev Entomol 1997; 42: 451-473. PMid:9017899. http://dx.doi.org/10.1146/annurev.ento.42.1.451
Santos JLC. Parasitos de canídeos domésticos e silvestres da região do Parque Nacional da Serra do Cipó, Minas Gerais, Brasil [ Dissertação]. Belo Horizonte: Universidade Federal de Minas Gerais; 2008.
Santos MF, Miranda CVB, Lima NA, Da Silva SB. Dados preliminares sobre levantamento da população de ectoparasitos e hemoparasitos em cães capturados pelo Centro de Zoonoses no município de Imperatriz-MA. In: Anais da 11ª. Semana de Integração de Ciências Agrárias; 2011, Altamira. Altamira: UFPA, 2011
Stalliviere FM, Bellato V, De Souza AP, Sartor AA, De Moura AB, Neidermaier L. Ectoparasitos em Canis familiaris da cidade de Lages, SC, Brasil e aspectos sócio-econômicos e culturais das famílias dos proprietários dos animais. Rev Cienc Agrovet 2009; 8(2): 179-183.
Teixeira VP, Silva NN. Sobre a ocorrência de pulicídeos e outros ectoparasitos de Felis felis do município de Juiz de Fora (Siphonaptera, Mallophaga, Ixodidea). Bol Inst Cienc Biol Geocienc 1975; 16:1-12.
Tipton VJ, Machado-Allison CE. Fleas of Venezuela. Brigham Young Univ Sc Bull Biol Ser 1972; 17(6): 1-115.
Torres FD, Figueiredo LA, Faustino MAG. Ectoparasitos de cães provenientes de alguns municípios da região metropolitana do Recife, Pernambuco, Brasil. Rev Bras Parasitol Vet 2004; 13(4): 151-154.
Unti O. Dados estatísticos relativos a alguns pulicídeos dos estados do Paraná e Santa Catarina. Rev Biol Hyg S. Paulo 1935; 6: 31-35.
World Health Organization - WHO. Present status of pesticide resistance. Tech Rep Ser 1992; 818:2-17.
Yeruham I, Rosen S, Hadani A. Mortality in calves, lambs and kids caused by severe infestation with the cat flea Ctenocephalides felis felis (Bouché, 1835) in Israel. Vet Parasitol 1989; 30(4): 351-356. http://dx.doi.org/10.1016/0304-4017(89)90105-2
Received August 28, 2012
Accepted December 4, 2012
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- Holland GP. The Siphonaptera of Canada. Can Dept Agric Tech Bul 1949; 70: 1-306.
- Hopkins GHE, Rothschild M, Mardon DK. An illustrated catalogue of the Rothschild collection of fleas (Siphonaptera) in the British Museum Natural History: Tungidae and Pulicidae. Cambridge; London: British Museum; 1953.
- Horak IG. Parasites of domestic and wild animals in South Africa. XIV. The seasonal prevalence of Rhipicephalus sanguineus and Ctenocephalides spp. on kennelled dogs in Pretoria North. Onderstepoort J Vet Res 1982; 49(1): 63-68. PMid:7122067.
- Horta MC, Chiebao DP, De Souza DB, Ferreira F, Pinheiro SR, Labruna MB, et al. Prevalence of Rickettsia felis in the fleas Ctenocephalides felis felis and Ctenocephalides canis from two Indian villages in São Paulo municipality, Brazil. Ann N Y Acad Sci 2006; 1078: 361-363. PMid:17114741. http://dx.doi.org/10.1196/annals.1374.071
- Horta MC, Labruna MB, Pinter A, Linardi PM, Schumaker TTS. Rickettsia infection in five areas of the state of São Paulo, Brazil. Mem Inst Oswaldo Cruz 2007; 102(7): 793-801. PMid:18094887. http://dx.doi.org/10.1590/S0074-02762007000700003
- Jellison WL. Fleas and disease. Annu Rev Entomol 1959; 4: 389-414. http://dx.doi.org/10.1146/annurev.en.04.010159.002133
- Jenkins DW. Pathogens, parasites and predators of medically important arthropods. Anotated list and bibliography. Bull World Health Organ 1964; 30 (Suppl): 1-30. PMid:14245244.
- Johnson PT. A classification of the Siphonaptera of South America with description of new species. Mem Ent Soc Wash 1957; 5: 1-298.
- Koutinas AF, Papazahariadou MG, Rallis TS, Tzivara NH, Himonas CA. Flea species from dogs and cats in northern Greece: environmental and clinical implications. Vet Parasitol 1995; 58(1-2): 109-115. http://dx.doi.org/10.1016/0304-4017(94)00706-I
- Krämer F, Mencke N. Flea biology and control. Berlin: Springer-Verlag; 2001. http://dx.doi.org/10.1007/978-3-642-56609-7
- Kristensen S, Haarlov V, Mourier H. A study of skin diseases in dogs and cats. IV. Patterns on flea infestation in dogs and cats in Denmark. Nord Vet Med 1978; 30(10): 401-413. PMid:714660.
- Liebisch A, Brandes R, Hoppenstedt KI. Zum Befall Von Hunden und Katzen MIT Zecken und Flöhen in Deutschland. Prakt Tierarzt 1985; 66: 817-824.
- Linardi PM. Utilização de algumas estruturas na caracterização de espécies da ordem Siphonaptera. II. A quetotaxia da margem posterior da tíbia posterior na separação de espécies de Polygenis Jordan, 1939. Rev Brasil Ent 1984; 28(1): 115-119.
- Linardi PM. Pulgas. In: Marcondes CB. Entomologia médica e veterinária São Paulo: Atheneu; 2001. p. 157-181.
- Linardi PM. Endoparasitos de Ctenocephalides felis felis (Siphonaptera: Pulicidae) em Belo Horizonte, MG. O Biológico 2002; 64(1): 65.
- Linardi PM. Os ectoparasitos de marsupiais brasileiros. In: Cáceres NC, Monteiro Filho ELA. Os marsupiais do Brasil: Biologia, ecologia e evolução. Campo Grande: Editora UFMS; 2006. p. 37-52.
- Linardi PM, Nagem RL. Pulicídeos e outros ectoparasitos de cães de Belo Horizonte e municípios vizinhos. Rev Bras Biol 1973; 33(4): 529-537. PMid:4804478.
- Linardi PM, Guimarães LR. Sifonápteros do Brasil. São Paulo: Museu de Zoologia USP/FAPESP; 2000.
- Lombarddero OJ, Santa-Cruz AM. Parasites of stray dogs in the city of Corrientes (Argentina). Changes over a 25 year-period. Vet Argent 1986; 3: 888-892.
- Lustosa ES, Carneiro JR, Carvalho MED, Jardim JHV. Ectoparasitos de cães vadios de Goiânia. Rev Patol Trop 1973; 2(4): 397-379.
- Menezes OB. Parasitos de Canis familiaris em Salvador. Bol Inst Biol Bahia 1954; 1(1): 75-78.
- Ménier K, Beaucournu JC. Taxonomic study of the genus Ctenocephalides Stiles & Collins, 1930 (Insecta: Siphonaptera: Pulicidae) by using aedeagus characters. J Med Entomol 1998; 35(5): 883-890. PMid:9775624.
- Munsee JR. Annual changes in flea populations on three domestic pets, 1978-1984. Proc Indiana Acad Sci 1985; 94: 329-334.
- Nagem RL. Sifonápteros da Coleção UFMG: sistemática, relações estruturais, adaptativas e entre hospedeiro/parasito [
- Obasaju MF, Otesile EB. Ctenocephalides canis infestation of sheep and goats. Trop Anim Health Prod 1980; 12(2): 116-118. PMid:7414697. http://dx.doi.org/10.1007/BF02242620
- Oliveira CMB, Ribeiro PB. Espécies de pulgas que parasitam cães em Porto Alegre e suas prevalências mensais. Arq Fac Vet UFRGS 1982/83; 10-11: 29-33.
- Oliveira RP, Galvão MAM, Mafra CL, Chamone CB, Calic SB, Silva SU, et al. Rickettsia felis in Ctenocephalides spp. fleas, Brazil. Emerg Infect Dis 2002; 8(3): 317-319. PMid:11927031 PMCid:2732462. http://dx.doi.org/10.3201/eid0803.010301
- Piotrowski F, Polomska J. Ectoparasites of the dog (Canis familiaris L.) in Gdansk. Wiad Parazytol 1975; 21(3): 441-451. PMid:1146337.
- Raszl SM, Cabral DD, Linardi PM. Notas sobre sifonápteros (Pulicidae, Tungidae e Rhopalopsyllidae) de carnívoros domésticos brasileiros. Rev Bras Entomol 1999; 43(1-2): 95-97.
- Ressl F. Die Siphonapterenfauna dês Verwaltungsbezirkes Scheibbs (Niederösterreich). Z F Parasitenkunde 1963; 23: 470-490.
- Rodrigues AFSF, Daemon E, D'Agosto M. Investigação sobre alguns ectoparasitos em cães de rua no município de Juiz de Fora. Minas Gerais. Rev Bras Parasitol Vet 2001; 10(1): 13-19.
- Rodrigues DF, Daemon E, Rodrigues AFSF. Caracterização da população de ectoparasitos em cães de núcleos de expansão urbana de Juiz de Fora, Minas Gerais, Brasil. Rev Bras Parasitol Vet 2008; 17(4): 185-188. PMid:19265575.
- Rust MK, Dryden MW. The biology, ecology, and management of the cat flea. Annu Rev Entomol 1997; 42: 451-473. PMid:9017899. http://dx.doi.org/10.1146/annurev.ento.42.1.451
- Santos JLC. Parasitos de canídeos domésticos e silvestres da região do Parque Nacional da Serra do Cipó, Minas Gerais, Brasil [
- Santos MF, Miranda CVB, Lima NA, Da Silva SB. Dados preliminares sobre levantamento da população de ectoparasitos e hemoparasitos em cães capturados pelo Centro de Zoonoses no município de Imperatriz-MA. In: Anais da 11Ş. Semana de Integração de Ciências Agrárias; 2011, Altamira. Altamira: UFPA, 2011
- Stalliviere FM, Bellato V, De Souza AP, Sartor AA, De Moura AB, Neidermaier L. Ectoparasitos em Canis familiaris da cidade de Lages, SC, Brasil e aspectos sócio-econômicos e culturais das famílias dos proprietários dos animais. Rev Cienc Agrovet 2009; 8(2): 179-183.
- Teixeira VP, Silva NN. Sobre a ocorrência de pulicídeos e outros ectoparasitos de Felis felis do município de Juiz de Fora (Siphonaptera, Mallophaga, Ixodidea). Bol Inst Cienc Biol Geocienc 1975; 16:1-12.
- Tipton VJ, Machado-Allison CE. Fleas of Venezuela. Brigham Young Univ Sc Bull Biol Ser 1972; 17(6): 1-115.
- Torres FD, Figueiredo LA, Faustino MAG. Ectoparasitos de cães provenientes de alguns municípios da região metropolitana do Recife, Pernambuco, Brasil. Rev Bras Parasitol Vet 2004; 13(4): 151-154.
- Unti O. Dados estatísticos relativos a alguns pulicídeos dos estados do Paraná e Santa Catarina. Rev Biol Hyg S. Paulo 1935; 6: 31-35.
- World Health Organization - WHO. Present status of pesticide resistance. Tech Rep Ser 1992; 818:2-17.
- Yeruham I, Rosen S, Hadani A. Mortality in calves, lambs and kids caused by severe infestation with the cat flea Ctenocephalides felis felis (Bouché, 1835) in Israel. Vet Parasitol 1989; 30(4): 351-356. http://dx.doi.org/10.1016/0304-4017(89)90105-2
Publication Dates
-
Publication in this collection
02 Jan 2013 -
Date of issue
Dec 2012
History
-
Received
28 Aug 2012 -
Accepted
04 Dec 2012