Cajennense Complex Research Articles

Impact of climate change on the geographical distribution of ticks of public health significance in Colombia: Amblyomma ovale (Ixodida: Ixodidae), the Amblyomma maculatum (Ixodida: Ixodidae) complex and the Amblyomma cajennense (Ixodida: Ixodidae) complex.

Ticks of the Amblyomma maculatum (Ixodida Ixodidae) complex, the Amblyomma cajennense (Ixodida Ixodidae) complex and Amblyomma ovale (Ixodida Ixodidae) are known to transmit various Rickettsia species in Colombia, but their exact distribution is unknown. We built several models based on current climate and projected future climate changes using a maximum entropy approach. A total of 314 records of the A. cajennense complex (65.9%; n = 207), A. ovale (22.9%; n = 72), and the A. maculatum complex (11.1%; n = 35) were obtained. Amblyomma ovale has a current distribution in the Pacific, Caribbean and Andean regions and could be potentially found in the Amazon. Amblyomma maculatum has a current distribution in the Andean and could potentially be found in the Caribbean and Orinoco regions. Amblyomma mixtum can be found near the Caribbean Sea and in the Pacific region, and A. patinoi is likely to be found in the Andean region and the Caribbean. In 2070, it will be possible to find an expansion of A. ovale and A. maculatum and a decrease of A. mixtum and A. patinoi. The variables that best predict the distribution of these species are isothermality (small fluctuations in temperature) and annual precipitation. Amblyomma cajennense s.l and A. ovale, A. cajennese s.l and A. patinoi, as well as A. maculatum and A. patinoi, have an important environmental sympatry. Epidemiological and acarological surveillance is crucial to investigate rickettsiosis caused by R. parkeri in A. ovale regions, by R. rickettsii in A. patinoi and A. mixtum areas, and by R. parkeri s.s in A. maculatum regions.

First report of Amblyomma sculptum (Amblyomma cajennense complex) in a Brazilian state classified as a silent area for human rickettsiosis.

Studies on ticks of public health concern in equine husbandry are scarce in the Northeastern region of Brazil. This study aimed to investigate the presence of ticks on horses in the State of Alagoas, which is classified as a silent area for human rickettsiosis. Ticks infesting horses were collected using anatomical tweezers or a commercial hook and kept in ethanol-labeled tubes for taxonomic identification. A total of 2,238 ticks were found. Ticks were identified as 2,215 (98.89%, 95% CI: 98.41-99.28) Dermacentor nitens, 19 (0.98%, 95% CI: 0.05-1.38) Amblyomma sculptum, and 4 (0.18%; 95% CI: 0.007-0.46) Rhipicephalus microplus. This is the first study to report A. sculptum and D. nitens in the State of Alagoas. The presence of A. sculptum should draw the attention of public health managers once Alagoas State is considered a silent area for rickettsial diseases, which means the absence of local surveillance programs for these pathogens.

First isolation of Rickettsia amblyommatis from Amblyomma mixtum in Colombia

BackgroundRickettsiae are obligate intracellular Gram-negative bacteria that are the causative agent of rickettsioses and are spread to vertebrate hosts by arthropods. There are no previous reports of isolation of Rickettsia amblyommatis for Colombia.MethodsA convenience sampling was executed in three departments in Colombia for direct collection of adult ticks on domestic animals or over vegetation. Ticks were screened for the presence of Rickettsia spp. by real-time polymerase chain reaction (qPCR) amplifying the citrate synthase gene (gltA), and the positive sample was processed for isolation and further molecular characterization by conventional PCR. The absolute and relative frequencies were calculated for several tick species variables. All products from conventional PCR were further purified and sequenced by the Sanger technique. Representative sequences of 18 Rickettsia species were downloaded from GenBank. Consensus phylogenetic trees were constructed for the gltA, ompB, ompA, and htrA genes with 1000 replicates, calculating bootstrap values through the maximum likelihood method and the generalized time reversible substitution model in the MEGA 7.0 software program.ResultsOne female Amblyomma mixtum collected on vegetation was amplified by qPCR (gltA), indicating a frequency of 1.6% (1/61) for Rickettsia spp. infection. Sequence analysis of a rickettsial isolate from this tick in BLASTn showed 100% identity with gltA (340 base pairs [bp]), 99.87% for ompB (782 bp), 98.99% for htrA (497 bp), and 100% for ompA (488 bp) to R. amblyommatis. Concatenated phylogenetic analysis confirmed these findings indicating that the isolate is grouped with other sequences of Amblyomma cajennense complex from Panama and Brazil within the R. amblyommatis clade.ConclusionsThis paper describes the isolation and early molecular identification of a R. amblyommatis strain from A. mixtum in Colombia.Graphical

Phylogenetic relationships of the Amblyomma cajennense complex (Acari: Ixodidae) at mitogenomic resolution

The genus Amblyomma is the third most diverse in the number of species within the Ixodidae, with practically half of its species distributed in the Americas, though there are also species occurring in Africa, Asia, and Australia. Within the genus, there are several species complexes with veterinary and public health importance. The Amblyomma cajennense complex, in the Americas, is represented by six species with a wide distribution, from Texas to northern Argentina. We combined two sequencing techniques to generate complete mitogenomes of species belonging to the Amblyomma cajennense complex: genome skimming and long-range PCRs sequencing methods. Thus, we generated seven new mitochondrial genomes for all species of the Amblyomma cajennense complex, except for Amblyomma interandinum. Genetic distances between the mitogenomes corroborate the clear differentiation between the five species of the Amblyomma cajennense complex. The phylogenetic relationships of these species had previously been evaluated by combining partial nuclear and mitochondrial genes and here these relationships are corroborated with a more robust framework of data, which demonstrates that the conjunction of mitochondrial and nuclear partial genes can resolve close relationships when entire genes or genomes are unavailable. The gene order, structure, composition, and length are stable across these mitogenomes, and they share the general characteristics of Metastriata. Future studies should increase the number of available mitogenomes for this genus, especially for those species from the Indo-Pacific region and Africa, by means of a better understanding of their relationships and evolutionary process.

Presence of two species of the Amblyomma cajennense complex (Acari: Ixodidae) and probable zones of sympatry in northwestern Colombia

The A. cajennense tick complex has been thought to be the main vector of Rickettsia rickettsii in Central and South America. Studies in Colombia have determined the presence of species A. patinoi and A. mixtum of the A. cajennense complex, but it is unknown which species of this complex exist in northwestern Colombia. Our aim was to identify the species of the A. cajennense complex that are present in northwestern Colombia. We sampled ticks of A. cajennense sensu lato infesting equids. Females identified according to the morphology of their genital pore were selected for genetic confirmation. Specimens from each locality were selected to perform molecular and genetic analysis. Specimens were analyzed from five departments (Antioquia, Bolívar, Córdoba, Magdalena, and Sucre). Morphologically 65 specimens were identified as A. patinoi and 5 as A. mixtum. Molecular analysis allowed to confirm the morphological identification of 27 specimens. In this study A. patinoi was widely distributed in the departments of Antioquia, Bolívar, and Córdoba with allopatric and sympatric distribution in some places. These two species in the region could have unexpected effects on the epidemiology of rickettsiosis.

Morphometrics of Amblyomma mixtum in the State of Veracruz, Mexico.

The tick Amblyomma mixtum is an ectoparasite of veterinary and public health importance because of its role as a vector of zoonotic pathogens. However, little is known about A. mixtum intraspecific variability and if morphological differentiation exists between populations across its geographic range. This study aimed to determine by electron microscopy the morphological variability of A. mixtum populations in the state of Veracruz, which has a large livestock population among states in Mexico. Forty male and 40 female A. mixtum collected from the 10 natural regions of Veracruz state were analyzed microscopically to accomplish main component analysis for each sex. Clusters were calculated with the out-tree method and a dendrogram produced to group the specimens according to their morphometric characteristics. Using 10 main components, 77% of the morphological variation of the ticks was explained. This is a reflection of scarce intraspecific variation between females. The dendogram for females grouped six clusters of specimens with similar characteristics. Morphometric variability in males was described using eight main components. Limited intraspecific variation was also observed between males. In males, the dendogram yielded six groups with similar morphometric characteristics. Morphometric analyses confirmed that the only species from the Amblyomma cajennense complex that are parasites to livestock in Veracruz state is A. mixtum. The eryxenous nature of A. mixtum combined with the frequent movement of livestock hosts may contribute to the apparent homogeneous phenotype of this tick species in Mexico.

Bats used as hosts by Amblyomma sculptum (Acari: Ixodidae) in Northeastern Brazil and its implications on tick-borne diseases

Amblyomma Koch, 1844 is distributed worldwide, with ca. 130 species currently recognized. These ticks are vectors of pathogens to animals and humans, including the causative agent of the New World Rocky Mountain spotted fever. Species of the Amblyomma parasitize a wide range of organisms, especially medium and large terrestrial mammals. Here we report for the first time the association of Myotis lavali Moratelli, Peracchi, Dias & Oliveira, 2011, Noctilio albiventris Desmarest, 1818 and Noctilio leporinus (Linnaeus, 1758) as hosts for Amblyomma sculptum Berlese, 1888. The ticks were originally identified as Amblyomma cajennense (Fabricius, 1787), in 2011. However, a later taxonomic review indicated that the species of the A. cajennense complex occurring in the Caatinga is A. sculptum. We also discuss the ecoepidemiological implications of this association.

Morphological and molecular characterization supporting Amblyomma mixtum presence in Cuba

Amblyomma cajennense Fabricius, 1787 (Acari: Ixodidae) is a widely distributed tick taxon. Recent studies have reassessed this taxon as a complex of six species. Amblyomma mixtum Koch, 1844 has been suggested by some authors as the only species of this complex that is present in Cuba. Other authors have pointed a niche overlapping for A. mixtum and A. cajennense s.s. in the country. Detailed taxonomic studies on the Cuban species belonging to this complex are needed in order to evaluate their current distribution according to the recent classification. This study aimed to characterize Cuban populations from the A. cajennense complex by using tick samples obtained from 3 occidental provinces and 1 central province of the country. Morphological identification and measurements of the main relevant taxonomic structures were conducted by using Scanning Electron Microscopy. Phylogenetic analyzes were carried out with 16S ribosomal RNA, internal transcribed spacer 2 and the subunit I of mitochondrial cytochrome c oxidase gene sequences. The results of these studies demonstrated that all samples belonged to the species A. mixtum (Koch, 1844). This study constitutes the first molecular characterization of this Amblyomma species in Cuba. Further studies will be necessary in order to corroborate if A. cajennense s.s. is also present in the island.

Germ cells: a useful tool for the taxonomy of Rhipicephalus sanguineus s.l. and species of the Amblyomma cajennense complex (Acari: Ixodidae).

The systematics of several ticks species (Acari: Ixodidae) remains controversial. Many species, including those of the Amblyomma cajennense complex and Rhipicephalus sanguineus s.l., are given special attention since they are cryptic species complexes and are also important in human and veterinary medicine. The A. cajennense complex was recently reorganized into six valid species, among which Amblyomma patinoi and Amblyomma mixtum have been confirmed in Colombia. On the other hand, the taxonomic status of R. sanguineus s.l. is controversial since it is a cosmopolitan cryptic species complex with a high reproductive capacity and a broad range of hosts (including man). To address this challenge, the germ cells of male ticks display a diverse morphology that offers novel opportunities for taxonomy. This study describes the events of spermatogenesis in A. mixtum and R. sanguineus s.l. individuals collected during active feeding on domestic hosts in the department of Caldas, Colombia. The individuals were identified using dichotomous keys and through PCR amplification of a fragment of the mitochondrial 16S ribosomal DNA gene. The male reproductive systems of A. mixtum and R. sanguineus s.l. were fixed in 2.5% glutaraldehyde for 48h and dehydrated in increasing dilutions of ethanol. The samples were then embedded and mounted in historesin to obtain sections of 3μm that were stained with hematoxylin-eosin (HE), photographed, and visualized through optical microscopy. The results show that the morphology of mature germ cells displays excellent diagnostic traits that can be used for tick taxonomy.

Integrated tick control on a farm with the presence of capybaras in a Brazilian spotted fever endemic region.

Ticks of the Amblyomma cajennense complex present high infestation rates. These ticks transmit the bacterium Rickettsia rickettsii, which causes Brazilian Spotted Fever. For this reason, an integrated tick control system was adopted on a farm in the municipality of Itu, state of São Paulo. On this farm, which borders the Tietê river, domestic animals are in contact with populations of capybaras. Six locations were monitored and evaluated between the years of 2015 and 2017. During this work 1271 nymphs and adult ticks were caught, all of them from the Amblyomma sculptum species, except for a single individual from the Amblyomma dubitatum species. The integrated tick management reduced the overall infestation levels to zero. Adult tick population dropped in the first year of the study, while larvae population dropped in the second year. Nymph population dropped in both years, decreasing in higher numbers in the first year. The estimated mean infestation levels for all of the tick's life cycle forms in the six monitored spots did not reach one individual in the end of the study. Estimated mean infestation levels for nymphs in these places equaled zero.

Fiebre manchada en Argentina. Descripción de dos casos clínicos

Rickettsioses are zoonotic tick-borne diseases. In Argentina, there are two epidemiological scenarios: jungle of Salta and Jujuy, involving vectors from the “Amblyomma cajennense Complex” (A. sculptum, and A. toneliae) and Rickettsia rickettsii as the main etiological agent; and the second scene to Delta del Rio Paraná and Samborombón Bay, where Amblyomma triste acts as a vector; and the provinces of Córdoba, La Rioja, San Luis and La Pampa where Amblyomma tigrinum is the vector. In this second scenario, Rickettsia parkeri is the causal agent. The spotted fever (SF) due to R. rickettsii is responsible for a severe cutaneous and systemic disease. Contrarily, R. parkeri produces benign and self-limited clinical manifestation. Here we describe a fatal SF case by R. rickettsii, in El Tunal, Salta and the first SF case due to R. parkeri in San Juan.

Occurrence of Amblyomma mixtum on the water buffalo (Bubalus bubalis) in Mexico.

The water buffalo (Bubalus bubalis) is an Asian species of bovine that was introduced in Mexico in 1992 as an alternative for milk and meat production. To date, no surveys have been conducted to identify ticks acquired by water buffaloes since their arrival in the country. Here we report, for the first time, the presence of Amblyomma mixtum, a neotropical tick in the Amblyomma cajennense complex, found on water buffaloes from Mexico and discuss its possible implications in veterinary public health for the region.

Diversity of rickettsiae and potential vectors of spotted fever in an area of epidemiological interest in the Cerrado biome, midwestern Brazil.

The Brazilian state of Goiás, untouched by spotted fever (SF) until 2012, has subsequently reported cases of the disease in several regions. This study aimed to survey the diversity of potential vectors and rickettsia in areas of Goiás under environmental surveillance or case investigation for SF. Collected specimens were assayed with molecular biology technology using DNA extraction, amplification and sequencing of fragments of the genes gltA, ompA, ompB and sca4 to detect rickettsia in ticks and fleas. Amplification of cytochrome oxidase subunit II and 16S rRNA was performed to assist tick identification. Rickettsia felis (Rickettsiales: Rickettsiaceae) was found in Ctenocephalides felis (Bouché, 1835) (Siphonaptera: Pulicidae). Rickettsia bellii was found in Amblyomma rotundatum Koch, 1844 (Ixodida: Ixodidae) and in Amblyomma cajennense sensu lato. Rickettsia sp. strain NOD was found in Amblyomma nodosum Neumann, 1899. Of the Amblyomma cajennense complex, Amblyomma sculptum Berlese, 1888 was confirmed in the northern, northeast, midwest and southeast regions of Goiás, whereas Amblyomma cajennense sensu stricto (Fabricius, 1787) was found only in the northern region of the state. Amblyomma dubitatum Neumann, 1899 associated with a species of the A.cajennense complex was the most common epidemiological finding, although Rickettsia rickettsii was not detected. This is the first report of Rickettsia sp. strain NOD in Goiás.

Modelos potenciales de distribución geográfica y climática del complejo Amblyomma cajennense (Acari: Ixodidae), potencial vector de Rickettsia rickettsii en Colombia

Introduction: The species of the Amblyoma cajennense complex, potential vectors involved in the transmission of Rickettsia rickettsii in Central and South America, have a wide geographical distribution in the Neotropics. In Colombia, the knowledge about these species, their distribution, and many aspects of their ecology is still limited. Objective: To explore the ecology of A. cajennense complex in Colombia based on the study of its habitat selection, as well as the generation of potential geographic and climatic distribution models. Materials and methods: We used unique records of these ticks to study the selection patterns of the climatic habitat using the Ecological Niche Factor Analysis (ENFA), and we built distribution models using the MaxEnt and GARP algorithms. Results: The record of distributions showed that A. cajennense complex is present in all five natural regions of Colombia with 64.71% of the records found in the departments of Antioquia, Cundinamarca, and Huila. The analysis of their habitat selection showed that these ticks preferably select geographical areas (ENFA: 96.03%) according to the isothermality conditions and the precipitation of the driest quarter of the year. The potential distribution models indicated habitat suitability in 31 to 51% of the area of the country depending on the algorithm. Conclusions: The distribution of A. cajennense complex in Colombia is highly influenced by a climatebased habitat selection, a characteristic that favored the creation of distribution models. Field studies will allow the validation of the potential distribution models and further genetic studies will be required in the country to identify species within the complex and study their potential hybridization areas.

Sequencing and comparative analysis of the Amblyomma sculptum mitogenome

The mitogenome of Amblyomma sculptum was sequenced, providing important information for understanding the evolutionary relationships among species of the A. cajennense complex. The mitochondrial genome has a circular structure with 37 genes, including 13 coding DNA sequences, two ribosomal RNA genes (12S rRNA and 16S rRNA) and 22 tRNA genes. Comparative analysis with the mitogenomes of six reference species of the genus Amblyomma revealed that the ND5 gene, which is related to energy metabolism, and control regions 1 and 2 of the mitogenomes have polymorphisms that can be exploited as molecular markers to differentiate A. sculptum from other tick species in the Amblyomma cajennense complex as well as other Amblyomma species.

Life cycle of Amblyomma mixtum (Acari: Ixodidae) parasitizing different hosts under laboratory conditions.

Amblyomma mixtum is a tick species in the Amblyomma cajennense complex. The known geographic range of A. mixtum extends from Texas in the USA to western Ecuador and some islands in the Caribbean. Amblyomma mixtum is a vector of disease agents of veterinary and public health importance. The objective of this study was to describe the life cycle of A. mixtum under laboratory conditions. Bovines, rabbits and sheep were infested with larvae, nymphs, and adult ticks under controlled conditions to assess several biological parameters. Eggs, larvae, nymphs and adults were kept in an incubator (27°C temperature and 80% relative humidity) when they were off the host. The average life cycle of A. mixtum was 88 and 79days when fed on rabbits and cattle, respectively. Sheep were found to be unsuitable because no ticks attached. The rabbit is a more practical host to maintain a colony of A. mixtum under laboratory conditions. The data from this study can be considered as an example for the life cycle of A. mixtum. However, caution must be exercised when making comparisons to the biology of A. mixtum in its natural habitat.

Amblyomma ticks and future climate: Range contraction due to climate warming

Ticks of the Amblyomma cajennense species complex are important vectors of spotted fever in Latin America. Environmental conditions determine the geographic distribution of ticks, such that climate change could influence the distribution of tick-borne diseases. This study aimed to analyze the potential geographic distribution of A. cajennense complex ticks in a Brazil region under present-day and future climate models, assuming dispersal limitations and non-evolutionary adaptation of these tick populations to climate warming. Records of A. cajennense sensu stricto (s.s.) and Amblyomma sculptum were analyzed. Niche models were calibrated using Maxent considering climate variables for 1950–2000 and projecting models to conditions anticipated for 2050 and 2070 under two models of future climate (CCSM4 and HadGEM2-AO). Broad suitable areas for A. cajennense s.s. and A. sculptum were found in present-day climate models, but suitability was reduced when models were projected to future conditions. Our exploration of future climates showed that broad areas had novel climates not existing currently in the study region, including novel extremely high temperatures. Indeed, predicted suitability in these novel conditions would lead to biologically unrealistic results and therefore incorrect forecasts of future tick-distribution. Previous studies anticipating expansions of vectors populations due to climate change should be considered with caution as they assume that model extrapolation anticipates that species would evolve rapidly for adaptation to novel climatic conditions.

Molecular Detection and Identification of Rickettsia Species in Ticks (Acari: Ixodidae) Collected From Belize, Central America.

Little is known about tick-borne rickettsial pathogens in Belize, Central America. We tested ixodid ticks for the presence of Rickettsia species in three of the six northern and western Belizean districts. Ticks were collected from domestic animals and tick drags over vegetation in 23 different villages in November 2014, February 2015, and May 2015. A total of 2,506 collected ticks were identified to the following species: Dermacentor nitens Neumann (46.69%), Rhipicephalus sanguineus (Latreille) (19.55%), Rhipicephalus microplus (Canestrini) (19.47%), Amblyomma cajennense complex (9.74%), Amblyomma maculatum Koch (3.47%), Amblyomma ovale Koch (0.68%), Ixodes nr affinis (0.16%), Amblyomma nr maculatum (0.12%), and Amblyomma nr oblongoguttatum (0.12%). Ticks were pooled according to species, life stage (larva, nymph, or adult), and location (n = 509) for DNA extraction and screened for genus Rickettsia by quantitative real-time polymerase chain reaction (qPCR). All 42 positive pools were found to be positive for spotted fever group (SFG) Rickettsia in pools of A. cajennense complex (n = 33), A. maculatum (n = 4), A. nr maculatum (n = 1), A. ovale (n = 1), R. sanguineus (n = 1), and I. nr affinis (n = 2). Rickettsia amblyommatis was identified from A. cajennense complex and A. nr maculatum. Rickettsia parkeri was found in A. maculatum, and Rickettsia sp. endosymbiont was detected in I. nr affinis. The presence of infected ticks suggests a risk of tick-borne rickettsioses to humans and animals in Belize. This knowledge can contribute to an effective tick management and disease control program benefiting residents and travelers.

Ambush behavior of the tick Amblyomma sculptum (Amblyomma cajennense complex) (Acari: Ixodidae) in the Brazilian Pantanal

We herein describe the ambush behavior of Amblyomma sculptum (Berlese 1888), a widespread and epidemiologically important tick in Brazil. Along two years of sampling by visual search in the Brazilian Pantanal, A. sculptum ticks were observed on the vegetation and in the leaf litter. Most of the ticks were observed between 10 and 50cm above ground level and less than five percent of the total were positioned below 10cm, indicating that they are seeking for middle or large-sized hosts. In both seasons, vapor saturation deficit was low during the morning. No significant relationship was found between questing ticks and daytime interval of observation or saturation deficit. However, questing tick numbers seem be higher in the end of the morning, when saturation deficit reaches its peak. Behavioral patterns of A. sculptum ticks observed in Pantanal underscore the occurrence of this tick and human contact at green anthropogenic sites. Considering A. sculptum questing behavior, inferences on human behavioral patterns that enhance or avoid contact with ticks are discussed.

Amblyomma sculptum (Amblyomma cajennense complex) tick population maintained solely by domestic pigs

In Brazil Amblyomma sculptum from Amblyomma cajennense complex is a tick species with a rather broad distribution encompassing the Cerrado Biome and devastated areas of the Atlantic rainforest. This species is also the major vector to humans of Rickettsia rickettsii, agent of the Brazilian spotted fever. Main primary hosts for the adult stage and frequently associated to high environmental infestation levels are the native capybaras and tapirs and a domestic host, the horse. Recent, however, solely circumstantial evidence, has shown that pigs (Sus scrofa) domestic, feral or exotic (wild boars) as well as wild suidae may maintain A. sculptum populations as well. We herein describe the maintenance of an A. sculptum tick population by domestic pigs for three years when raised in paddocks. Observations herein described occurred in the facilities of an intensive outdoor pig production system within a farm in Uberaba municipality southeast Brazil. Initial evaluation was done upon request due to human tick-bite complains in June 2013. Later tick infestations were evaluated at each of eight consecutive seasons from August 2014 to May 2016. In the first evaluation, 104 nymphs and one female A. sculptum were collected from four pigs and 269 nymphs of A. sculptum and 12 Amblyomma spp larva clusters from the paddocks. Only one A. sculptum nymph was found in each of the surrounding bovine pasture and a nearby riparian forest. Seven Rhipicephalus spp and three Amblyomma spp larva were found in the former as well. Infestations were greatly reduced with elimination of the two most infested paddocks and mowing of vegetation. Still along the inspection of eight consecutive seasons A sculptum ticks were collected overwhelmingly adults from pigs. Thus, observations herein described show that outdoor pig raising may provide both a permissive environment and adequate host allowing for a minimal threshold for the maintenance of A. sculptum populations. Since raising domestic pigs in paddocks to increase animal welfare is an increasing practice, it may indicate a new trend in this parasitism, with yet an unknown effect upon animal and human health.