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Hindawi Publishing Corporation ISRN Parasitology Volume ;<=>, Article ID C=<;C;, C pages http://dx.doi.org/=<.HI<;/;<=>/C=<;C;

Research Article Host-Parasite Relationship of (: and Argasidae) and Feral Pigs ( Sus scrofa ) in the Nhecolândia Region of the Pantanal Wetlands in Mato Grosso do Sul

P. H. D. Cançado, 1 J. L. H. Faccini, 2 H. M. Herrera, 3 L. E. R. Tavares, 4 G. M. Mourão, 5 E. M. Piranda, 4 R. C. S. Paes, 6 C. C. D. U. Ribeiro, 2 T. C. Borghesan, 7 A. K. Piacenti, 8 M. A. Kinas, 9 C. C. Santos, 10 T. M. Ono, 8 and F. Paiva 4

, Embrapa Beef Cattle, Av. R adio´ Maia ;<=, >?==@-?>= Campo Grande, MS, Brazil @ Departamento de Parasitologia , Universidade Federal Rural do Rio de Janeiro, @<;?=-=== Serop edica,´ RJ, Brazil < Universidade Cat olica´ Dom Bosco, >?,,>-=,= Campo Grande, MS, Brazil M Centro de Ci enciasˆ Biol ogicas´ e da Sa ude,´ Universidade Federal de Mato Grosso do Sul, >?=;=-,?= Campo Grande, MS, Brazil O Brazilian Agricultural Research Corporation-CPAP, Wild Life Laboratory, >?<@=-?== Corumb a,´ MS, Brazil S Ag enciaˆ Estadual de Defesa Sanit aria´ Animal e Vegetal de Mato Grosso do Sul-IAGRO, >?=>M-?=@ Campo Grande, MS, Brazil > Programa de P os-Graduac¸´ ao˜ em Biologia da Relac¸ao˜ Pat ogeno-Hospedeiro-ICB/USP,´ =OO=;-=== S ao˜ Paulo, SP, Brazil ; Programa de P os-Graduac¸´ ao˜ em Ci enciaˆ Animal-UFMS, >?=;=-,?= Campo Grande, MS, Brazil ? Programa de P os-Graduac¸´ ao˜ em Ecologia e Conservac¸ao-UFMS,˜ >?=;=-,?= Campo Grande, MS, Brazil ,= Associac¸ao˜ de Propriet arios´ de RPPN do MS, >?==@ ==M Campo Grande, MS, Brazil

Correspondence should be addressed to P. H. D. Canc¸ado; [email protected]

Received =; March ;<=>; Accepted == April ;<=>

Academic Editors: M. Florin-Christensen, N. T. Huy, G. Lochnit, and J. M. Perez

Copyright © ;<=> P. H. D. Canc¸ado et al. Xis is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Feral pigs ( S. scrofa ) were introduced to the Pantanal region around ;<< years ago and the population appears to be in expansion. Its eradication is considered to be impossible. Xe population of feral pigs in the Pantanal wetlands is currently estimated at one million. Two scienti]c excursions were organized. Xe ]rst was conducted during the dry season, when ;= feral pigs were captured and the second was during the wet season, when ;> feral pigs were captured. Ticks were collected and the oviposition and hatching process were studied to con]rm the biological success of each . Xree tick species were found to be feeding on feral pigs: cajennense , A. parvum , and rostratus . During the dry season, =^_ adult A. cajennense were collected, contrasting with =;^ A. cajennense specimens in the wet season. Xis suggests that the seasonality of these ticks in the Brazilian Pantanal wetlands could be diaerent from other regions. Xe results indicate that A. parvum and A. cajennense are biologically successful parasites in relation to feral pigs. A. cajennense appears to have adapted to this tick-host relationship, as well as the areas where feral pigs are abundant, and could play a role in the ampli]cation of this tick population.

1. Introduction worldwide [ I–^]. Xe most common tick species reported in association with domestic pigs in Brazil is Amblyomma Ticks have coevolved with various wild animal hosts which cajennense (Fabricius, =^_^), an eclectic tick that has a broad are reservoir hosts for pathogens such as fungi, bacteria, range of hosts and widespread distribution [ _–=< ]. In Brazil, viruses, rickettsiae, and protozoan which can be transmitted this hard tick is an important vector of Rickettsia rickettsii to domestic mammals and humans [ =–>]. to humans [ == ]. A second reported in association with Ticks that feed on feral or domestic pigs ( Sus scrofa ) Brazilian pigs is the genus Ornithodoros , which has two and their tick-borne diseases have been previously studied species: O. rostratus and O. brasiliensis . Both of these species ; ISRN Parasitology have also been reported in association with wild native pigs were captured. Xe pigs were captured by fence traps or (Tayassu sp.) [ _, e]. by cowboys who used a lasso to catch them. All captured Xe Pantanal ecosystem is considered to be one of the pigs were tranquilized (tiletamine and Zolazepam—Zoletil) most well-preserved biomes in Brazil and was added to prior to examination and tick collection. All trapping and the UNESCO World Heritage List in ;<<<. Xe Brazilian handling procedures were conducted in accordance with Pantanal has been described as a “biological hotspot” for the authorization of the Brazilian Environment Institute conservation and one of the richest and the most diverse (IBAMA) (license no. =_>/;<

Tstuv =: Mean, standard deviation (SD), and number of adult Amblyomma ticks collected from feral pigs in the Nhecol andiaˆ sub-region of the Pantanal between July ;<

Wet season Dry season Parasites Males Females Total Mean ± SD Males Females Total Mean ± SD A. cajennense ^_ Ie =;^ H.H; ± >.;< ==e He =^_ _.I_ ± I.>C A. parvum < I I <.=^ ± <.Ie _ I =; <.H^ ± =.^_

Tstuv ;: Prevalence (P), mean abundance (MA), and mean intensity of Amblyomma cajennense and A. parvum parasites feeding on Sus scrofa from " and % in the state of Mato Grosso do Sul, Brazil. Possible diaerences are tested with Fisher’s exact test (prevalence) and Student’s t- test (mean intensity).

Wet season Dry season Diaerences Parasites P% MA ± SD MI ± SD P% MA ± SD MI ± SD P t A. cajennense D CH.; ;.=> ± ;.C^ >.;^ ± ;.Ce eH.; H.C^ ± I.e_ H.eH ± I.eI <.<; ;._e ∗ A. cajennense C eH.^ >.>e ± ;.H; >.HH ± ;.IC _H.^ ;._= ± =.eI >.;_ ± =.C^ <.>> <._C A. parvum D — — — =I.> =.=C ± ;.C^ ;.C^ ± ;.<_ — — A. parvum C => <.=^ ± <.Ie =.>> ± <.H^ e.H <.=e ± <.C_ ; ± =.I= = −<.

40 O. rostratus was only collected on one occasion (I 35 2 nymphs) during the wet season, feeding on the belly region 30 (Figure ;(c)). Xree nymphs molted to adults (two females 25 and one male) in the laboratory. Xese were experimentally 20 fed to domestic pigs. Xe larvae obtained under labora- 15 10 tory conditions were identi]ed as O. rostratus [;^ ]. Xe 5 1 ecchymosis-like lesions observed in experimentally infested 0 domestic pigs were similar to those found in naturally 0 5 10 15 20 25 30 35 40 45 infested feral pigs. Although O. rostratus was not found, similar lesions were observed on domestic dogs and humans Fwxyzv =: Sample scores of the ]rst two discriminant axes for in the studied area (Figures ;(a), ;(b) and ;(c)). tick infracommunities of Sus scrofa (feral pigs) from the southern Pantanal wetlands in the State of Mato Grosso do Sul, Brazil. Xe numbers represent seasons: (=) wet season and (;) dry season, whereas the circles around the group represent the eH.^% tolerance 4. Discussion region (e.g., eH.^% of the observations in a group are expected to lie Xe prevalence and intensity of A. cajennense infestation inside the respective circle). found to be feeding on feral pigs, based on the observation that all engorged females laid viable eggs with a good hatching percentage ( >e<%), strongly suggest that this introduced Xe values of prevalence, mean abundance, and mean mammal species is a very adequate host for this hard tick in intensity of infestations and their possible diaerences can the southern Pantanal region. Considering that feral pigs rep- be seen in Table ;. Both Amblyomma species exhibited the resent one of the major biomass free-living mammals in the typical aggregated pattern of distribution (Table >). studied area, as well as the fact that A. cajennense is a multi- Xe ticks did not exhibit a preference for any region of the host parasite, its ampli]cation through feral pigs may play pig’s body and were collected from the rostrum, head, ears, an important role in the health conditions of local wildlife, neck, thorax, back, and members. All A. cajennense (;>) or domestic animals, and people. In fact, a number of mammal A. parvum (H) engorged females laid eggs with good hatch species commonly found in the southern Pantanal have pre- (>e<%). viously been naturally infested by A. cajennense : the collared Xe ]rst discriminant function explained =<<% of the peccary ( Pecari tajacu ); the white-lipped peccary ( Tayassu variance (eigenvalue = <.>>). Dimensionality tests for group pecari ); the giant anteater ( Myrmecophaga tridactyla ); the separation revealed two distinct host groups (' 2 = 11.31; * = collared anteater ( Tamandua tetradactyla ); the coati ( Nasua 0.02) . A signi]cant overall eaect was observed (Wilk’slambda nasua ); the capybara ( Hydrochaeris hydrochaeris ); the marsh = <.^H; ,4,39 , * = 0.02 ). Each host specimen was ^<.>% deer ( Blastocerus dichotomus ); and the brown brocket deer well classi]ed in the two distinct groups (Table I). Xe (Mazama gouazoubira ) [ ;_ –>< ]. Xe crab-eating fox ( Cer- diaerence of prevalence and intensity for A. cajennense male docyon thous ), the ocelot ( Leopardus pardalis ), and certain infestation between the seasons was the most signi]cant small rodents are examples of other wild mammals that have (eH.^%) in determining the position of hosts among the been infested by A. cajennense in the same studied area groups (Figure =). (ongoing unpublished research). Xis situation is a very good I ISRN Parasitology

Tstuv >: Dispersion index (ID) and index of discrepancy ( D) for Amblyomma cajennense and A. parvum feeding on Sus scrofa from " and % in the state of Mato Grosso do Sul, Brazil. Wet season Dry season Parasites ID D ID D Amblyomma cajennense D >.>I <.He I.>_ <.I A. cajennense C =.>^ <.>^ =.>I <.>C Amblyomma parvum D — — >.HI <._C A. parvum C =.>e <._H ;.I; <._e C: female; D: male.

(a)

(b) (c)

Fwxyzv ;: (a) Nymph of O. rostratus feeding on a feral pig ( Sus scrofa ) and ecchymosis-like lesions; (b) skin lesion (ecchymosis) caused by nymph of Ornithodoros rostratus feeding on a dog; (c) ecchymosis-like lesions caused by nymphs of O. rostratus feeding on a human leg.

Tstuv I: Discriminant analysis showing the number and percentage the dry season. In total, ^<% of the feral pigs examined were of well-classi]ed feral pigs in the dry and wet seasons. correctly classi]ed according to the seasons, considering the distribution of male A. cajennense to be responsible for this Number of well-classi]ed pigs Season % diaerence. Xese results are not in accordance with previously Dry season Wet season published studies. According to a number of studies, adult A. !" ∗ "# ∗ Dry season C cajennense are more prevalent during the wet season [ ;e , >= – !# ∗ $" ∗ Wet season ^ >C ] because the annual water cycle in the Pantanal region is Total ;I ;< "% ∗ unique and diaers from other Brazilian regions. Since this ∗Correctly classi]ed. research comprises only one dry or wet season, more research concerning A. cajennense seasonality should be conducted example of man-made opportunities for neo-tropical tick before any solid conclusion. development [ =e ]. Xe same author describes the expansion Xe higher intensity of infestation of male A. cajennense of the cayenne tick’s ( A. cajennense ) geographical range as in relation to females in naturally infested feral pigs was a result of its association with feral pigs, which are a highly probably due to the longer parasitic period of males. Xis has mobile host. previously been suggested by Pinter et al. [ >; ]. Xe discriminant analysis con]rmed that A. cajennense Xe results of the present study also suggest that feral was more abundant in the Nhecol andiaˆ sub-region during pigs seem to be a good host for A. parvum in the southern ISRN Parasitology H

Pantanal because (a) the prevalence was =H% and (b) all [;] P. Parola and D. Raoult, “Ticks and tickborne bacterial diseases engorged females that were collected from feral pigs laid in humans: an emerging infectious threat,” Clinical Infectious viable eggs from which hatched larvae were used to start a Diseases , vol. >;, no. C, pp. _e^–e;_, ;<<=. laboratory colony. Considering the constant environmental [>] F. Jongejam and G. Uilemberg, “Xe global importance of ticks,” modi]cations by human activities in the Pantanal region and Parasitology , vol. =;e, pp. S>–S=I, ;<< , >^ , >_ ], feral pigs might be also an important in Florida,” Journal of Wildlife Diseases , vol. ;<, no. ;, pp. ==I–==e, source of infestation in domestic animals and humans. Xe =e_I. recent discovery of a novel spotted fever group, Rickettsia sp., [H] S. B. Kleiboeker, G. A. Scoles, T. G. Burrage, and J. H. 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Xe state of Rio Grande do Sul, Southern Brazil,” multiplicity suggests the existence of a complex network in Memorias do Instituto Oswaldo Cruz , vol. eH, no. I, pp. IH>–I^<, the eco-epidemiology of these ticks in the Pantanal region. ;<<<. Finally, one of the main causes of disease emergence [=<] M. B. Labruna, L. M. A. Camargo, T. T. S. Schumaker, and or reemergence is environmental alterations that increase E. P. Camargo, “Parasitism of domestic swine ( Sus scrofa ) by the contact between wildlife and domestic animals and its Amblyomma ticks (Acari: Ixodidae) on a farm at Monte Negro, consequent modi]cation of epidemiological pro]les [ I; ]. Western Amazon, Brazil,” Journal of Medical Entomology , vol. Xese feral pigs are an alien species which became greatly >e, no. =, pp. ;I=–;I>, ;<<;. abundant and share the same habitat as autochthone wildlife [==] E. Guedes, R. C. Leite, M. C. A. Prata, R. C. Pacheco, D. H. and livestock. 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