Mini review
Systematics and ecology of the brown dog tick, Rhipicephalus sanguineus

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Abstract

Rhipicephalus sanguineus, the brown dog tick, kennel tick, or pan-tropical dog tick, is probably the most widespread ixodid tick, colonising both human and canine dwellings. It is of great significance in both human and veterinary medicine as a vector of several important pathogens and can also cause clinical illness in heavy infestations of dogs. However, there are still significant taxonomic uncertainties, and it is probable that some records of this tick refer to other species. Most past reviews have been broad-ranging or have focused on the pathogens that R. sanguineus transmits, and relatively few have considered its biology in detail or the issues around its true identity. The present review has paid most attention to the taxonomy of R. sanguineus and to the ecological factors that influence tick survival and distribution, particularly in a climate change context. It is evident that more research is required on the systematics of the R. sanguineus species complex, in order to elucidate the epidemiology and prevention of the diseases that it transmits, and to provide the relevant biological data required for development of predictive models of future tick distribution in a climate change scenario.

Introduction

Rhipicephalus sanguineus, the brown dog tick, kennel tick, or pan-tropical dog tick, probably evolved as a parasite of burrowing carnivores in warm climates and with the domestication of the dog has been able to colonise both human and canine dwellings over a wide range of habitats. It is therefore, as a result of human activities, probably the most widespread of all ticks and has a global distribution, but is most prevalent in tropical and subtropical regions. This metastriate ixodid (Fig. 1) is a relatively small member of the genus and is usually yellow to mid-brown in colour. It can easily be confused with several other species, such as R. camicasi and R. turanicus, that are morphologically very similar (Estrada-Peña et al., 2004), but have different behavioural, ecological, and vector characteristics (Walker et al., 2000).

R. sanguineus is of great significance in both veterinary and human medicine, primarily because of its role as a vector of several pathogens, though the ticks themselves can cause clinical illness in heavy infestations of dogs (Fig. 2) giving rise to anaemia, skin abscesses, and as recently described to tick paralysis (Otranto et al., 2012). The most important dog diseases transmitted by this tick are babesiosis, caused by Babesia vogeli and ehrlichiosis caused by Ehrlichia canis. The most important human pathogens are Rickettsia conorii, the cause of Mediterranean spotted fever, and Ri. rickettsii, which causes Rocky Mountain spotted fever (Dantas-Torres et al., 2012a).

Most past reviews on R. sanguineus have either focused on the tick in relation to particular disease agents (Schoeman, 2009, Parola et al., 2009, Nicholson et al., 2010) or have been broad ranging, focusing on the practicalities of identification, prevention, and control, as well as on transmitted diseases (Palmas et al., 2001, Dantas-Torres, 2008, Dantas-Torres, 2010). In view of the uncertainties concerning R. sanguineus taxonomy (Walker et al., 2000, Dantas-Torres, 2010) and of the predicted effects of global warming on ticks and tick-borne diseases, the present review has paid most attention to taxonomy and systematics and to the ecological factors that influence tick survival and distribution, particularly in a climate change context.

Section snippets

Taxonomy and systematics

R. sanguineus was first described by Latreille (1806) as Ixodes sanguineus and later placed in the genus Rhipicephalus (Koch, 1884). Neumann (1911) was the first to critically study this group of species, and he synonymised several species and sub-species named at that time under the name of R. sanguineus (see Camicas et al., 1998; for a complete list of synonymies). A second attempt to revise the group of species was made by Zumpt, 1939, Zumpt, 1940. The contemporary concept of the group R.

Population genetics

As indicated above, the detailed taxonomy of R. sanguineus is a subject of an ongoing debate and a number of morphologically and biologically similar species, which were originally described under different names in different locations around the world, have been synonymised with R. sanguineus (Pegram et al., 1987a, Pegram et al., 1987b, Pegram et al., 1989, Camicas et al., 1998, Walker et al., 2000). The resulting joint taxon is the type species of the R. sanguineus group.

Accurate

Habitat

R. sanguineus is nidicolous and exhibits behaviour that can be classified as endophilous (inhabiting burrows, artificial shelters etc.) or harbourage (sequestered in the immediate vicinity of host dwellings). In some humid habitats it may be exophilic and ambush its hosts from vegetation in the open, usually in areas frequented by dogs (Demma et al., 2005, Parola et al., 2008). It is considered to have originally been a parasite of burrowing carnivores, such as foxes and mustelids (Morel, 2003

Life cycle

R. sanguineus is a three-host tick, with larvae, nymphs, and adults all usually feeding on a dog. The feeding periods of R. sanguineus are directly influenced by biotic (e.g. host species) and abiotic (e.g. pre-feeding light cycles and ambient temperature) factors (Dantas-Torres, 2008, Dantas-Torres et al., 2011) and are not dissimilar to those of many non-nidicolous species of this genus. In a recent study using R. sanguineus ticks from southern Italy, the feeding period of larvae varied from

Host specificity

Strong though incomplete monoxeny (use of a single host species) is exhibited by all stages of R. sanguineus in that they prefer dogs as hosts, and there is also good evidence that some dog breeds are preferred to others (Louly et al., 2009). These preferences appear to be based on distinct behavioural preferences influencing host contact and attachment, and also by physiological factors that come into play during feeding, including modulation of the host's immune response (Dantas-Torres, 2010

Population growth and abundance

R. sanguineus can cause heavy infestations on dogs and very high numbers can build up in kennels, especially in those that house several dogs (Fig. 4). Garcia et al. (2007) counted a total of 16,065 specimens of all developmental stages in veterinary kennels from October 2000 to September 2001 in Venezuela, whereas only 21 were found in the external environment. It has been noted that tick burdens on dogs vary greatly within kennels (Dantas-Torres, 2010), which indicates that individual host

Seasonality

In some parts of its geographical range, particularly in the tropics, R. sanguineus shows no distinct seasonality, but where seasonal activity is evident, such as in the southern USA, in temperate South America and southern Europe, the ticks tend to show reduced activity in the winter which then rises in spring as the temperatures increase, and in some areas there may be a resurgence of activity in the autumn (Arthur, 1963, Venzal et al., 2007, Dantas-Torres, 2010). However, a study in Agra,

Climate change and geographical distribution

It is generally acknowledged that climate change, particularly increases in temperature, but also changes in rainfall patterns, are likely to affect tick distribution and the epidemiology of the diseases they transmit (Gray et al., 2009). Potential changes in the distribution of ticks have been investigated for some tick species, such as Ixodes ricinus (Hancock et al., 2011, Estrada-Peña and Venzal, 2006), I. scapularis (Ogden et al., 2004), and Hyalomma marginatum (Estrada-Peña et al., 2011),

Role as a disease vector

R. sanguineus is the vector of several pathogens to both dogs and humans. The most important pathogens that it transmits to dogs are the protozoan parasites Babesia vogeli (possibly also B. gibsoni), Hepatozoon canis, and the rickettsia Ehrlichia canis, all of which can cause significant morbidity and mortality. B. vogeli, H. canis, and E. canis occur throughout the areas of distribution of the vector. In human medicine, R. sanguineus is the main vector of Ri. conorii conorii, the cause of

Future research requirements

It is evident that more research is required on the taxonomy of the R. sanguineus species complex. Correct vector identification underpins the epidemiology and prevention of the diseases transmitted by R. sanguineus and also the biological data required for development of predictive models of future tick distribution in a climate change scenario. There is a need to redescribe R. sanguineus, to sequence DNA fragments and to name a neotype that stabilises the research on this topic. From such a

Acknowledgment

Parts of this work were supported by the project AGL2009-10797, funded by the Ministry of Science and Technology of Spain.

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