Sanguineus Populations Research Articles

The role of the phylogeographic distribution of Rhipicephalus sanguineuson the spread of Rocky Mountain spotted fever in Arizona and Mexico

Rocky Mountain spotted fever (RMSF) is a rapidly‐progressing, tick‐borne, zoonotic disease caused by the bacterium Rickettsia rickettsii. Most of the symptoms of RMSF are flu‐like in nature; including fever, nausea, fatigue, and muscle weakness. The one non‐specific symptom is the presence of petechiae, but by the time they appear it is often too late. Even with treatment, RMSF can have a fatality rate of up to 35% and if left untreated it can rise to as high as 80%. In 2003, a new vector for RMSF was identified; Rhipicephalus sanguineus, or the brown dog tick. Unlike its Dermacentor counterparts, R. sanguineus is found nationally, yet is only known to act as a vector in the Arizona region. The number of cases in Arizona has been on the rise year over year and, perhaps more troubling, just south of the Arizona border, the number of cases in Mexico has surpassed 4000 in the last three years, with an annual fatality rate as high as 47%. Recently, the brown dog tick was indicated as the vector for this outbreak in Mexico. Therefore, understanding why R. sanguineus can act as a vector for RMSF in the Arizona region, but not elsewhere has become more urgent.We propose three hypotheses for the recent emergence of R. sanguineus as a vector for RMSF: (1) there exists a distinct sub‐population of R. sanguineus which better transmits R. rickettsii, (2) a distinct strain of R. rickettsii maintains more favorably in the R. sanguineus populations in this region, and (3) changing environmental factors and dog‐keeping practices in the Arizona region have contributed to the spread of RMSF.To test these hypotheses, we have partnered with the Midwestern Veterinary Mobile Clinic as well as the Arizona Animal Welfare League to collect brown dog tick and serum samples from 16 locations spanning Arizona, New Mexico, and Mexico. We isolated and sequenced 12S, 16S, and COX‐1 tick mitochondrial genes and used a maximum likelihood phylogenetic method on the concatenated sequences. To determine rickettsial prevalence, we tested for the rickettsial‐specific, rOmpA gene and sequenced it. Furthermore, immunofluorescence assay (IFA) was conducted on canine serum samples to evaluate canine anti‐rickettsial antibody seroprevalence in these locations. Finally, all these data were mapped on a geographic climate model. Results indicate variation in tick phylogeographic distribution, rickettsial prevalence rates ranging from 18% to 64% among sub‐populations of R. sanguineus, and seroprevalence rates as high as 33%, indicating areas with endemic levels of RMSF (>15%). These data indicate that no single factor, but rather a confluence of factors drive the spread of RMSF in the region. With this data we can begin to predict and prevent future outbreaks of RMSF and improve canine and human health.Support or Funding InformationMWU One Health Award to JVB, MWU REAP Award to JVB, MWU CGS Funding to AO, Kenneth A. Suarez Award to SM

Invasive versus native brachyuran crabs in a European rocky intertidal: respiratory performance and energy expenditures

The invasive Asian shore crab Hemigrapsus sanguineus is now the second most abundant intertidal crab in the North Sea after the native European green crab Carcinus maenas. To compare their respiratory performance and energy expenditures, we measured standard respiration rates of both species from around the island of Helgoland, North Sea, Germany (54°11′N, 7°53′E) in 2015. Oxygen consumption was recorded in a flow-through setup between 5 and 20 °C. At lower temperatures, H. sanguineus had similar respiration rates as C. maenas, but approximately twofold higher rates at higher temperatures. Numerical models for the calculation of individual respiration rates were established and applied to the entire intertidal populations around Helgoland to compare the energy expenditures of both species. Abundance and biomass data recorded in August 2014 showed that H. sanguineus reached values as high as 21 and 59%, respectively, compared to those of C. maenas. Based on these data and the numerical respiration models, the energy expenditures of both populations were calculated for the whole year 2014. The H. sanguineus population reached, depending on the assumed diet of both species (complete herbivory versus complete carnivory), 86–135% of the expenditure value of C. maenas. As population densities of H. sanguineus are likely to increase in the North Sea, the energy expenditure of the invader and thus its impact on the energy flux in the intertidal habitat will further increase. Whether this will lead to an impact on the local intertidal community depends on species-specific dietary preferences and remains to be investigated.

Determination of metabolic resistance mechanisms in pyrethroid-resistant and fipronil-tolerant brown dog ticks.

Rhipicephalus sanguineus (Latreille) (Ixodida: Ixodidae) is a three-host dog tick found worldwide that is able to complete its' entire lifecycle indoors. Options for the management of R. sanguineus are limited and its' control relies largely on only a few acaricidal active ingredients. Previous studies have confirmed permethrin resistance and fipronil tolerance in R. sanguineus populations, commonly conferred by metabolic detoxification or target site mutations. Herein, five strains of permethrin-resistant and three strains of fipronil-tolerant ticks were evaluated for metabolic resistance using synergists to block metabolic enzymes. Synergist studies were completed with triphenyl phosphate (TPP) for esterase inhibition, piperonyl butoxide (PBO) for cytochrome P450 inhibition, and diethyl maleate (DEM) for glutathione-S-transferase inhibition. Additionally, increased esterase activity was confirmed using gel electrophoresis. The most important metabolic detoxification mechanism in permethrin-resistant ticks was increased esterase activity, followed by increased cytochrome P450 activity. The inhibition of metabolic enzymes did not have a marked impact on fipronil-tolerant tick strains.

Increase in density of genetically diverse invasive Asian shore crab (Hemigrapsus sanguineus) populations in the Gulf of Maine.

Hemigrapsus sanguineus, the Asian shore crab, has rapidly replaced Carcinus maenas, the green crab, as the most abundant crab on rocky shores in the northwest Atlantic since its introduction to the United States (USA) in 1988. The northern edge of this progressing invasion is the Gulf of Maine, where Asian shore crabs are only abundant in the south. We compared H. sanguineus population densities to those from published 2005 surveys and quantified genetic variation using the cytochrome c oxidase subunit I gene. We found that the range of H. sanguineus had extended northward since 2005, that population density had increased substantially (at least 10-fold at all sites), and that Asian shore crabs had become the dominant intertidal crab species in New Hampshire and southern Maine. Despite the significant increase in population density of H. sanguineus, populations only increased by a factor of 14 in Maine compared to 70 in southern New England, possibly due to cooler temperatures in the Gulf of Maine. Genetically, populations were predominantly composed of a single haplotype of Japanese, Korean, or Taiwanese origin, although an additional seven haplotypes were found. Six of these haplotypes were of Asian origin, while two are newly described. Large increases in population sizes of genetically diverse individuals in Maine will likely have a large ecological impact, causing a reduction in populations of mussels, barnacles, snails, and other crabs, similar to what has occurred at southern sites with large populations of this invasive crab species.

Lack of acquired resistance in dogs to successive infestations of Rhipicephalus sanguineus ticks from Brazil and Argentina

Comparative studies between brown dog tick Rhipicephalus sanguineus populations from Brazil (Jaboticabal, São Paulo) and Argentina (Rafaela, Santa Fé) showed significant biological, morphological and genetic differences between them. This work aimed to study, in a comparative way, the acquisition of resistance in domestic dogs to R. sanguineus from Jaboticabal and Rafaela, after successive and controlled infestations. Ticks were kept in a BOD incubator under controlled conditions (27 °C, 80 % relative humidity, 12-h photoperiod). Ten dogs, Dachshund breed, males and females, 6 months old, short- or long-haired, without prior contact with ticks, were used as hosts. They were distributed into two experimental groups composed of five animals each: G1 infested with ten adult couples of R. sanguineus (Jaboticabal) per animal, and G2 infested with ten adult couples of R. sanguineus (Rafaela) per animal. Ticks' biological parameters and titration of antibodies from the dogs' sera by ELISA test were used for comparison between the strains. Results of the biological parameters showed that the dogs did not acquire immunity to either of the R. sanguineus strains after repeated infestations. The ELISA test showed low antibody titers in sera of dogs from G2, in successive infestations, and higher antibody responses post second and third infestations in G1. It also demonstrated cross-reactivity between sera of dogs infested with R. sanguineus (Jaboticabal) and antigens from R. sanguineus (Rafaela) and vice versa. We conclude that Dachshund dogs did not develop resistance against neither Jaboticabal nor Rafaela strains of R. sanguineus.

Additional records and distribution (2011-2012) of Hemigrapsus sanguineus (De Haan, 1835) along the French coast of the English Channel

The invasion process can be described as a succession of stages initiated by the transport of organisms from their native range to a new area where they persist, proliferate and spread. It is important to monitor the demographic development of invaders for management purposes. This study focuses on the different stages of population development during the invasion process and underlines the importance of understanding and monitoring the ‘persistence phase’. The distribution of Hemigrapsus sanguineus (Asian shore crab) in the English Channel, along the French coast, was first undertaken in 2008. In 2010, 35 sites were surveyed and it appeared that the abundance of this species had already established a 2–5 fold increase since 2008. The present study presents the geographical distribution of H. sanguineus in 2011 and 2012 which includes a further 39 sites (72 sampling stations in 2012). All populations observed during previous years persisted in 2011 and 2012. In 2012, H. sanguineus was detected at 61 sites; 36 intensely colonised (including 3 newly colonised sites compared to 2011); 22 had trace numbers and 3 sites had ‘proven presence’. In addition to males with carapaces up to 39 mm width (CW), abundances increased by a factor of 2 since 2010, which testifies for the naturalized status of the species along the French coast of the English Channel. Since 2008, La Hougue proved to be the most abundantly colonised site along the French coast. By 2011 it had an average density of 101±19 ind.m -2 , with an abundance of 258±54 individuals (under 30 boulders). Populations were subsequently halved in 2012. Increasing densities and abundances recorded between 2008 and 2011 at la Hougue suggest that H. sanguineus had reached the ‘expansion phase’, but the dynamics of H. sanguineus populations at the most colonised sites (12 sampling sites with abundance >200 individuals under 30 boulders), suggest that maximum values had already peaked and that the ‘persistence phase’ was probably reached. The implementation of pluri-annual surveys seems of prime importance to correctly evaluate population dynamics of alien species.

Invasion dynamics on a temperate rocky shore: from early invasion to establishment of a marine invader

Populations of invading Asian shore crabs (Hemigrapsus sanguineus) and resident crabs (European green crab Carcinus maenas or species in the family Panopeidae) were monitored for up to 12 years along a south to north orientation on the open coast of Massachusetts and within the Narragansett Bay estuary, Rhode Island. At all sites, densities of resident crabs declined as H. sanguineus increased in abundance. Population dynamics were divided into 3 stages of the invasion (early, mid, late) based on statistically different densities of invading and resident crabs. Early in the invasion on the open coast, the relatively few H. sanguineus present had a wide range of individual sizes. By late in the invasion, relatively small crabs [ 10 mm CW were present late in the invasion. In Narragansett Bay, a recruitment peak of H. sanguineus occurred shortly before it surged in population size, and large crabs were abundant late in the invasion. Geographic comparisons of H. sanguineus populations in southern New England showed similar growth trajectories. Monitoring populations of resident and invading species at multiple locations from early invasion through clear establishment of the invader allows a more complete understanding of the population dynamics of marine species invasions.

Serological survey on Ehrlichia sp. among dogs in the central region of Rio Grande do Sul

A serological survey on Ehrlichia canis was conducted among dogs in the central area of the state of Rio Grande do Sul, where the tick Rhipicephalus sanguineus is a common parasite of dogs. Out of a total of 316 dogs attended at the veterinary teaching hospital in the municipality of Santa Maria, only 14 (4.43%) reacted positively to E. canis antigens in the indirect immunofluorescence assay, with the following endpoint titers: 80 (three dogs), 160 (five), 320 (four), 640 (one) and 1280 (one). Like in previous studies in other regions of the state of Rio Grande do Sul, only a very small portion of the dogs in Santa Maria presented antibodies reactive to E. canis, even though canine infestations due to R. sanguineus are very common in this study region. These results contrast with other regions of Brazil, where E. canis is endemic among canine populations, with seropositivity values generally higher than 30%. Genetic differences among the R. sanguineus populations in South America might be implicated in these contrasting results.

Cold-stress response of engorged females of Rhipicephalus sanguineus

We investigated the effect of prolonged exposure to low temperature on engorged females of Rhipicephalus sanguineus. Five groups of two females (F1-F5) were maintained at 8±2°C, 70±10% RH, and 24h scotophase, for 15, 30, 45, 60 and 75days. One group was maintained in the incubator (26±1°C, 70±10% RH, and 24h scotophase) as control. The results show that egg hatch rate, longevity and reproductive fitness of engorged females of R. sanguineus are negatively correlated with the duration of exposure to low temperature, whereas preoviposition period was positively correlated with exposure to the cold. This shows that the engorged female ticks are sensitive to prolonged exposure to low temperature, and it may explain why females of this tick species are not reproductively active during winter. Our results confirm that temperature is a major limiting factor for the establishment of stable R. sanguineus populations in cold temperate regions of Europe.

Possible temperature limits to range expansion of non-native Asian shore crabs in Maine

The intertidal Asian shore crab, Hemigrapsus sanguineus (De Haan, 1835), recently (2001) appeared in very low densities along the southern Maine (USA) coast. Indigenous to Russia and Japan, this species arrived in New Jersey around 1988 and rapidly expanded south to the Carolinas and north to southern New England (CT, RI, MA) by the early 1990s. We examined the characteristics of a non-native species invasion by surveying over 30 intertidal sites in Maine from 2002 to 2005. We found relatively low population densities, slow rates of geographic expansion and virtually no colonization northeast of Penobscot Bay on the central coast of Maine. We hypothesized that further geographic expansion of sustaining populations of H. sanguineus in Maine may be limited by coastal temperatures colder than in its native range. To examine this, we deployed recording thermistors at 11 strategic sites and integrated those data with three oceanographic observation buoys and with satellite thermal images of the coastal zone for the period between 2003 and 2005. We found that Maine's H. sanguineus population densities in the intertidal peaked during the warmest months (July–September) and were lowest during the coldest months (January–March) when the crabs retreated to the subtidal zone. Densities were also greater in warmer localities (southern Maine) than in cooler localities (central and eastern Maine). In fact, populations were absent from areas with mean summer temperatures cooler than 13 °C. In southern Maine, seasonal population densities and reproductive periodicity corresponded to periods with mean temperatures warmer than 15° and 12 °C, respectively. There are many physical and biological factors that could limit this invasion. However, our temperature and demographic data are consistent with the thesis that the H. sanguineus invasion has stalled at the terminus of the Gulf of Maine's cold, Eastern Maine Coastal Current. We compared published mean summer and winter SST data for coastal waters in the western North Atlantic and in the native Asian range of H. sanguineus, and we quantified and compared H. sanguineus abundance in Maine with thermal microenvironments at these sites. From this, we speculate that future distribution of this crab may be limited to the warmer areas of the Maine coast (south and west of Penobscot Bay) and up estuaries that warm every summer. Thus, it may be possible for managers to gauge future risks of marine species invasion from vectors such as ships based on the thermal biogeographic match or mismatch between their ports of origin and their destinations. Such information could be useful for focused monitoring and enforcement of existing laws designed to prevent future introductions of non-native marine species. As coastal waters warm, invasion opportunities could increase from cold-limited species.

Foraging by Two Estuarine Fishes, Fundulus heteroclitus and Fundulus majalis, on Juvenile Asian Shore Crabs (Hemigrapsus sanguineus) in Western Long Island Sound

The Asian shore crab, Hemigrapsus sanguineus, is a recent and particularly successful introduction to the east coast of the USA. Little research has been done on the utilization of Asian shore crabs for food by native species, a potential form of biocontrol. Over a 4-year period, we examined the gut contents of cogeners, Fundulus heteroclitus and Fundulus majalis, collected from two embayments in western Long Island Sound for the presence of juvenile H. sanguineus. Frequency (percent) of occurrence of food items in the guts of both species varied over year and study site. Asian shore crabs were consumed more often by F. heteroclitus than by F. majalis, but predation pressure by both species was low. Only 13% of F. heteroclitus and 7.7% of F. majalis found with food in their guts had ingested Asian shore crab remains. Of those, 1/3 had consumed whole crabs; the rest had only autotomized appendages in their guts. The mean carapace width of juvenile Asian shore crabs ingested by F. heteroclitus was 3.59 ± 2.22 mm (N = 33). Results of our study on killifish predation support the hypothesis that H. sanguienus abundance is partly explained by reduced impact of native predators (i.e., the “enemy release hypothesis”). Predation pressure of other potential enemies on both planktonic and benthic stages of the Asian shore crab must be investigated, however, to understand the full impact of predation on H. sanguineus population dynamics.

SPECIES INVASION SHIFTS THE IMPORTANCE OF PREDATOR DEPENDENCE

The strength of interference between foraging individuals can influence per capita consumption rates, with important consequences for predator and prey populations and system stability. Here we demonstrate how the replacement of a previously established invader, the predatory crab Carcinus maenas, by the recently invading predatory crab Hemigrapsus sanguineus shifts predation from a species that experiences strong predator interference (strong predator dependence) to one that experiences weak predator interference (weak predator dependence). We demonstrate using field experiments that differences in the strength of predator dependence persist for these species both when they forage on a single focal prey species only (the mussel Mytilus edulis) and when they forage more broadly across the entire prey community. This shift in predator dependence with species replacement may be altering the biomass across trophic levels, consistent with theoretical predictions, as we show that H. sanguineus populations are much larger than C. maenas populations throughout their invaded ranges. Our study highlights that predator dependence may differ among predator species and demonstrates that different predatory impacts of two conspicuous invasive predators may be explained at least in part by different strengths of predator dependence.

Biological and DNA evidence of two dissimilar populations of the Rhipicephalus sanguineus tick group (Acari: Ixodidae) in South America

In this work, the biology, mitochondrial DNA and fertility of hybrids from two strains of Rhipicephalus sanguineus, from Brazil and Argentina, were compared. Engorged larvae, nymphs and adults from Argentina weighed more and the engorgement period of adult females was significantly longer than those of their Brazilian counterparts, whereas adult female tick yield rate was higher for the Brazilian strain. High intraspecific divergence of mitochondrial DNA was detected between R. sanguineus from Brazil and Argentina. On the other hand, a strong genetic relationship was detected between European and Argentinean R. sanguineus populations while the Brazilian population appeared to be related to the African Rhipicephalus turanicus. Adult hybrid females laid eggs, which were mostly unviable, whereas a mean of more than 1400 larvae hatched per egg mass from pure Brazilian and Argentinean strains. These results showed that differences between these strains are greater than previously assumed and that the biosystematic status of R. sanguineus ticks from South America should be re-evaluated. Wide variations, such as these might account for the reported worldwide differences in biology and vector capacity of this species.

Amitraz: a tick and flea repellent and tick detachment drug.

A topical formulation of amitraz (Mitaban Liquid Concentrate, The Upjohn Company, Kalamazoo, Michigan, U.S.A.) was evaluated as a tick repellent and detachment agent, and flea repellent. The diluted liquid concentrate (250 p.p.m. active drug) was topically applied as a single treatment to dogs; the concentration was identical to the rate recommended for treatment of demodicosis and scabies. Brown dog tick (Rhipicephalus sanguineus) and American dog tick (Dermacentor variabilis) populations were eliminated and repelled. Repellent activity (92-95%) was observed against R. sanguineus for 2 weeks post-treatment; the treatment was moderately active (63%) during the third week, and at 4 weeks post-treatment the drug was inactive. Established R. sanguineus populations were also treated, and the diluted liquid concentrate had 100% tick-detachment efficacy. Repellent activity (99%) was also detected against D. variabilis; the activity was monitored for only 7 days. The ectoparasiticide had low to moderate flea (Ctenocephalides felis) repellent activity (42%) for 4 days post-treatment; thereafter the treatment was ineffective. Side-effects were not observed in any of the dogs treated with amitraz, or the placebo.

Population differences in the timing of diapause: adaptation in a spatially heterogeneous environment.

Populations of the planktonic copepod, Diaptomus sanguineus, live in permanent and temporary freshwater ponds in Rhode Island. All ponds in which they occur become uninhabitable at some time during the year, but the nature and timing of the harsh period varies both spatially and temporally. Females produce discrete clutches either of subitaneous eggs which hatch immediately or of diapausing eggs which hatch the following season. The two egg types show distinct chorion morphologies under transmission electron microscopy. In permanent ponds the copepods start making diapausing eggs in March, one month before rising water temperatures induce planktivorous sunfish to become active. In temporary ponds diapausing eggs are produced, in a complex pattern from May to July, before the water disappears in late summer or early fall.We investigated the spatial scale at which D. sanguineus is adapted to this complex environment. In a reciprocal transfer experiment between temporary and permanent bodies of water, female copepods placed in new ponds made subies of water, female copepods placed in new ponds made subitaneous and diapausing eggs in the same sequence as control females retained in their home ponds. The copepod populations enter diapause at times appropriate for the local habitat conditions they experience, but inappropriate for other, nearby ponds. Transplanted females were unable to sense a change in pond type or to adjust egg production accordingly. We conclude that D. sanguineus populations are adapted to the specific conditions of isolated ponds rather than to a broader geographical region containing several pond types.