Article available at http://www.parasite-journal.org or http://dx.doi.org/10.1051/parasite/2009163191
BIOLOGICAL AND ECOLOGICAL CHARACTERISTICS OF SOFT TICKS (IXODIDA: ARGASIDAE) AND THEIR IMPACT FOR PREDICTING TICK AND ASSOCIATED DISEASE DISTRIBUTION VIAL L.*
Summary: Résumé : CARACTÉRISTIQUES BIOLOGIQUES ET ÉCOLOGIQUES DES TIQUES MOLLES (IXODIDA: ARGASIDAE) ET IMPLICATIONS QUANT À LA As evidence of global changes is accumulating, scientists are PREDICTION DE LEUR DISTRIBUTION ET DES MALADIES ASSOCIÉES challenged to detect distribution changes of vectors, reservoirs and pathogens caused by anthropogenic and/or environmental Dès lors que des preuves du changement global s’accumulent, les changes. Statistical and mathematical distribution models are scientifiques se doivent de détecter les changements de distribution emerging for ixodid hard ticks whereas no prediction has ever de vecteurs, de réservoirs et de pathogènes causés par des been developed for argasid ones. These last organisms remain modifications anthropogéniques ou environnementales. Alors que unknown and under-reported; they differ from hard ticks by many des modèles de distribution statistiques ou mathématiques, structural, biological and ecological properties, which complicate commencent à émerger pour les tiques dures (ixodidés), aucune direct adaptation of hard tick models. However, investigations on prédiction n’est disponible pour les tiques molles (argasidés). Ces bibliographic resources concerning these ticks suggest that organismes restent inconnus et sous-estimés; ils diffèrent des tiques distribution modelling based on natural niche concept and using dures par leurs propriétés structurales, biologiques et écologiques, environmental factors especially climate is also possible, bearing qui compliquent la simple adaptation de modèles initialement in mind the scale of prediction and their specificities including their développés pour les tiques dures. Toutefois, l’étude des données nidicolous lifestyle, an indiscriminate host feeding and a short bibliographiques concernant ces tiques suggère qu’il est possible bloodmeal duration, as well as a flexible development cycle de prédire leur distribution basée sur le concept de niche naturelle through diapause periods. en fonction de variables environnementales essentiellement climatiques. Il est alors nécessaire de choisir correctement l’échelle KEY WORDS : Argasidae, soft tick, Ornithodoros, biology, ecology, d’étude et de considérer leurs spécificités incluant leur statut geographical distribution, natural niche, predictive modelling nidicole, leur opportunisme pour les hôtes et la faible durée de gorgement sur hôte, ainsi que la flexibilité du cycle de développement par l’entrée en diapause.
MOTS CLÉS : Argasidae, tique molle, Ornithodoros, biologie, écologie, distribution géographique, niche naturelle, modélisation prédictive.
INTRODUCTION tors and reservoirs of pathogens (Jonjegan & Uilenberg, 2004). Illustrations of the diseases transmitted by soft rgasid (or soft) ticks differ from ixodid (or hard) ticks include: 1) human tick-borne relapsing fever (TBRF) ticks by many structural, biological and ecolo- transmitted worldwide by Ornithodoros ticks and cau- Agical properties. They lack a dorsal scutum in sed by spirochetes of the genus Borrelia, 2) viral ence- adult and nymphal stages as the most discriminating phalitis transmitted by ticks infesting seabirds, shore morphological feature and always exhibit a nidicolous birds and roosting birds, 3) the african swine fever virus to endophilous lifestyle as their major ecological attri- (ASFV) transmitted by O. moubata and O. porcinus in bute (Pospelova-Shtrom, 1969). Their specialization to Africa, 4) fowl spirochetosis or anaplasmosis-like infec- sheltered microhabitats and their characteristic short tions caused by B. anserina and Aegyptianella pullo- blood feeding duration usually hides their presence rum, respectively, and transmitted by Argas persicus such that their role in human and animal health is worldwide, and 5) epizootic bovine abortion caused by generally ignored (Hoogstraal, 1985). However, they B. coriaceae and transmitted by O. coriaceus in North can cause toxicosis, paralysis, irritation, allergies and America. Argasid ticks of recognized medical and vete- exsanguination, and can play an important role as vec- rinary importance typically belong to the genera Argas, Ornithodoros and Otobius (Jonjegan & Uilenberg, 2004). * Centre de Coopération Internationale en Recherche Agronomique As evidence of global climate change accumulates (Inter- pour le Développement (CIRAD), BIOS UMR15 (TA A-15/G), Campus governmental Panel on Climate Change, synthesis report, International de Baillarguet, 34398 Montpellier cedex 5, France 2007: http://www.ipcc.ch/ipccreports/ar4-syr.htm), so Correspondence: Laurence Vial. Tel.: +33 (0)4 67 59 38 21 – Fax: +33 (0)4 67 59 37 98. does recognition of its potential consequences for E-mail: [email protected] human and animal health. Scientists are challenged to
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detect changes in the distribution of vectors, reservoirs wing soft ticks to survive at high temperatures and and pathogens, and to attribute these shifts to anthro- under relatively dry conditions (Lees, 1947). For exam- pogenic and/or environmental changes (McMichael et ple, O. moubata and O. savignyi tolerate air tempera- al., 2006). As a consequence, it is essential to reveal any ture up to 63 °C and 75 °C, respectively (Morel, 1969). of biological and ecological characteristics of soft ticks, This phenomenon results in the common presence of in contrast to those of the ixodid line, to understand their soft ticks in tropical and subtropical zones and their peculiar distribution patterns and habitat preferences and spread into arid areas of Central Asia and Africa (Sahara) their specific role as parasites, vectors and pathogen (Morel, 1969). reservoirs (Hoogstraal, 1985; Sonenshine, 1993). However, the success of their developmental cycle The present paper aims i) to review such characteris- depends on cooler conditions, which are provided by tics of soft ticks, with a special emphasis on the genus the sheltered microhabitats they colonize. Most argasid Ornithodoros; ii) to present their epidemiological impact ticks are nidicolous living in the nests, burrows, and in terms of risk for tick and associated disease distri- caves of vertebrate animals or in human and livestock bution; and iii) to propose new research priorities to habitations, where they survive in cracks, crevices, improve model predictions on changes in the distri- under rock ledges, among nest fibres, or in sandy, bution of soft ticks and tick-borne diseases. rocky, or dusty ground surface (Sonenshine, 1993). Some, known as endophilous nidicoles like many Ornithodoros tick species (Figs 1A, B, C, D) live inside BIOLOGICAL AND ECOLOGICAL these microhabitats while geophilous nidicoles prefer CHARACTERISTICS OF SOFT TICKS harborages nearby host habitations. In addition to intrinsic microclimatic conditions of shelters, body heat and moisture from the respiration and excrement of IDICOLOUS LIFESTYLE N the host within the microhabitat help establish the he peculiar nature of oilskin and cement com- atmospheric conditions required for the development ponents of argasid ticks’ cuticle makes it highly of these ticks (Sonenshine, 1993). Soft ticks show Tresistant and reduces water evaporation, allo- strict, narrowly defined temperature and humidity tole-
Fig. 1. – Examples of typical microhabitats for endophilous Ornithodoros soft ticks, including (1A) warthog burrows infested by O. moubata spp. in Mozambique, (1B) crevices colonized by O. porcinus domes- ticus and opening inside human and pig buildings in Madagascar, (1C) mud nests of rocky cliff swallows inhabited by O. concanensis in the United-States, or (1D) rodent burrows infested by O. sonrai and opening inside human houses in Senegal.
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rances for development and activity, reflecting the considered less efficient than that of a hard tick. How- conditions of their microhabitat. These optima are dis- ever, its total duration may be optimized thanks to short tinct for closely related species and may be so specific pre- and post-feeding delays, as well as short moul- as to be included in the species definition (Morel 1969). ting periods and rapid feeding (see below). Set apart from possible interrupted seasonal development, Argas DEVELOPMENTAL CYCLE persicus or Otobius megnini showing only 2-3 nymphal In contrast to ixodid ticks, soft ticks present many nym- instars complete their development in 49-118 days, phal instars (2-8) between the larval and adult stages whereas more O. moubata and O. porcinus, with 4-7 nym- (Fig. 2). Each immature stage requires at least one blood- phal instars require 76-155 days. Developmental cycles meal on a vertebrate host prior to moulting, except of 80-120 days for one-host hard ticks like Boophilus larvae of some Ornithodoros species like O. moubata microplus or of 80-300 days for three-host hard ticks (Fig. 2). The number of nymphal moults varies from like Dermacentor andersoni or Amblyomma america- two to nine according to species; the quality and the num are usually reported (Loomis, 1961; Morel, 1969). amount of blood ingested also influence this number Regardless of interspecific variability, the global dura- (Morel, 1969). When emerging, soft tick adults are long- tion and success of the developmental cycle of soft lived, with a maximum life span as great as 25 years ticks depend on the efficiency of blood feeding and for some species (Sonenshine, 1993), and are able to on climatic conditions. High to significantly high effects feed several times when hosts are available (1-10) of temperature and humidity are noticed on mean egg (Morel, 1969). In argasid females, each bloodmeal is incubation period and hatching success, larval and generally followed by egg laying, with or without a nymphal prefeeding/premoulting durations and adult previous copulation because females are able to retain preoviposition/oviposition duration (Cunliffe, 1921; Whee- sperms within endospermatophores (Fig. 2). Compared ler, 1943; Loomis, 1961; Hafez et al., 1971; Balashov, to hard ticks, soft tick clutches are small (5-500) but, 1972; El Shoura, 1987; Endris et al., 1991; Olmedo et al., a given female can produce from two to five clutches 1995). over her lifetime. This iteroparous strategy could be seen as an adaptation to host scarcity and/or climatic BLOOD FEEDING variability; however, even with multiple clutches, soft ticks never achieve the amount of eggs produced by A major characteristic of soft ticks is the short dura- some ixodid ticks (Morel, 1969). tion of bloodmeal, particularly for nymphs and adults Regarding this aspect, as well as the multiplicity of (15-60 minutes). The duration is typically longer for nymphal instars, the life-cycle of a soft tick could be larvae (12 hours to several days) (Fig. 2). This feature
Fig. 2. – A typical life-cycle of a soft tick indicating the different deve- lopmental instars, the crucial steps between instars and, in grey For each nymphal instar: boxes, the duration of each step for the species O. moubata (accor- Emergence to feeding: 3 days [1-7] ding to Morel, 1969; Cunliffe, 1921; Loomis, 1961). Nymphal bloodmeal: 15-60 min Nymphal moulting: 11 days [8-13] Number of nymphal instars: 4-7
Last nymphal moulting to
adult: 11 days [7-23] ³
Adult bloodmeal: 15-60 min Number of adult bloodmeals: 1-10 No moulting for O. moubata adults Duration feeding-oviposition: 13 days [7-24]
Several laying outs after a single copulation 1 bloodmeal for each laying bout Number of eggs/bloodmeal: 111 [28-318] Number of eggs/female: 350 [108-488]
Larval moulting (true metamorphosis): 5 days [3-6] Embryogenesis on the No larval bloodmeal for O. moubata ground: 10 days [8-13]
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may be seen as an adaptation to their nidicolous life- recently found infected by B. duttonii in a region where style; they reduce possible exposure to unfavourable no animal reservoir is known (McCall et al., 2007). external conditions by detaching rapidly from their ver- tebrate hosts before these hosts leave the microhabitat SEASONAL POPULATION DYNAMICS in search of food or a sexual partner (Sonenshine, 1993). Soft ticks have developed physiological strategies to As a possible adaptation to a nidicolous lifestyle and favour such rapid blood feeding, including high tegu- host scarcity, argasid ticks, especially adults, are very ment distension during blood feeding and excretion of resistant to starvation for several years and are able to excess water and ions via coxal glands as soon as enter a quiescent phase for two to eight months (Morel, blood is ingested or just after detachment (Hoogstraal, 1969). Seasonal morphogenetic diapause is usually 1985). Many pathogens maintained in soft tick reser- correlated to host availability and delays develop- voirs like Borrelia or ASFV are excreted in coxal fluid, mental activity such that the expansion of the tick which increases their transmission capacity through population is optimized during the seasonal period when tick-to-tick transfers (Gaber et al., 1984; Kleiboeker et hosts are present (Sonenshine, 1993). However, host al., 1998). seeking activity is not directly affected by this diapause. Soft ticks are commonly polyphagous, that is changing For example, O. kelleyi feeds seasonally during the host for each bloodmeal, except for some species like spring on bats returning from winter caves to aban- doned buildings or cracks infested by ticks; these Ot. megnini where larvae and nymphs engorge and moult ticks, collected in winter when bats are absent, feed on the same ungulate (Morel, 1969). Argasid ticks seem readily when offered these hosts in laboratory (Sonen- to exhibit varying degrees of host preference, ranging shine & Anastos, 1960). In Egypt, A. arboreus infesting from strict specificity, as for certain bat-parasitizing tick the nests of herons and other roosting birds delays ovi- species of the genera Ornithodoros, Antricola, Nothoas- position until the following spring when it feeds during pis, Carios, Chiropterargas or Secretargas, to little or the fall, but oviposits without delay when it feeds in no described specificity for burrow-inhabiting endophi- July (Khalil, 1974; Khalil & Shanbaky, 1976). Conver- lous Ornithodoros species (Sonenshine, 1993). Indeed, sely, soft ticks infesting nest or burrows of non-migra- it has been suggested that most soft ticks actually tory hosts are not considered to exhibit seasonal acti- show indiscriminate host feeding and that apparent vity, especially when they are indiscriminate feeders variation in host preference likely reflects microhabitat (Sonenshine, 1993). In many cases, this may be due preference and host availability within the microhabitat to the fact that these ticks inhabit microhabitats where (Morel, 1969). As a consequence of their nidicolous climatic conditions are buffered all along the year lifestyle, soft ticks may simply choose hosts that are (Sonenshine, 1993). However, diapause remains an inhe- directly available in their favourable microhabitat, resul- rent attribute of the biology of many nidicolous ticks ting in an apparent selection of small vertebrate hosts, and seasonal climate changes can impact feeding acti- domestic livestock and humans. However, host prefe- vity and the consequent reproductive and develop- rences are difficult to investigate in soft ticks because mental cycle (Morel, 1969). Nevertheless, such patterns they feed rapidly and are thus difficult to find on the are most often observed at the geographic limits of the host; only PCR amplification of host genes within tick species’ distribution, in temperate or sub-Saharan areas midgut may allow us to detect such relationships where ticks carry out feeding or ovipositional diapause (Kent, 2009). during winter or dry season, and not at the center of Indiscriminate host feeding was clearly demonstrated the distribution in tropical or subtropical areas. For exam- for some Ornithodoros tick species, including: i) O. tar- ple, O. tholozani from Central Asia does not feed on takovskyi transmitting TBRF in Central Asia and able cattle during winter and shows a diapause of six months, to feed on terrapin, skink, agama, gecko, sand snake, while the same species is active during the whole year toad, hedgehog, dog, mouse, bee-eater, roller and spar- in Israel (Moskvin, 1927; Avivi, 1967). Similar obser- row (Vasil’eva, 1971); ii) O. verrucosus and O. alacta- vations have been reported in Spain for O. erraticus galis in Soviet Georgia that feed on tortoise, snake, that does not feed on its common pig host until pig- toad, burrow-inhabiting bird, fox and bird, rodent, pens reach a temperature of 13-15 °C (Oleaga-Perez et fox, respectively (Gughusvili 1980); iii) O. sonrai in al., 1990). In Egypt, the same species (actually its Senegal, which is able to feed on many rodent and small variant O. sonrai) inhabiting rodent burrows shows insectivore species that are naturally infected by TBRF the highest densities of adults during the summer and (Trape et al., 1996) and which occasionally feeds on early fall and the lowest during the winter months, sug- pigs living close to small mammal burrows and is thus gesting a seasonal decline in successful feeding and contaminated by ASFV (Vial et al., 2007), iv) O. mou- moulting. The rodent hosts in this area have been bata spp. transmitting TBRF in Tanzania that is able found in burrows throughout the year (Khalil et al., to feed on pigs and chickens, and which has been 1984).
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PREDICTIONS ON SOFT TICK introduced to the barns since 2004 (Vial, personal communication); ii) in Senegal, O. sonrai was present AND DISEASE DISTRIBUTION in 1991 and 2002 in same human buildings of Dielmo village, and corresponded to two permanently positive clusters of disease transmission (significantly more TBRF THE CONCEPT OF THE NATURAL NICHE cases detected in humans throughout the study period) redictions of vector and vector-borne disease (Vial, 2005; Vial et al., 2006a); iii) for O. tartakovskyi occurrence are based on two major concepts: ranging from Turkmenia to Kazakhstan and O. errati- P1) the natural nidality of transmissible diseases cus with its large variant in North Africa and its small meaning that, independent of humans, infectious disea- one in West Africa (renamed O. sonrai), a positive cor- ses exist in nature under a combination of local condi- relation has been obtained between decreased fertility tions and in the presence of vertebrates and arthropods or complete sterility and the geographical distance that act as vectors and/or reservoirs of the pathogenic between cross-bred tick populations (Chabaud, 1954; agent (Pavlovsky, 1966), and 2) the fundamental eco- Balashov, 1971), suggesting low or insignificant gene logical niche of a species, defined as a set of environ- flow between natural populations within a described mental conditions within which a species can survive species range. and persist. This niche consists of an “n-dimensional Being nidicolous, especially endophilous, consists of hypervolume” that determines suitable habitat for the adding an intermediate environmental layer between species but is distinct from the distribution of the spe- the external conditions outside the microhabitat, rea- cies plotted in the geographical space (Hutchinson, 1957). dily measurable and commonly used for species dis- Under the first concept, and provided strict assump- tribution models (e.g. air temperature, air humidity and tions on disease transmission dynamics, it is possible evaporation, sunshine, wind, altitude, hydrography, to approximate disease distribution using some indices, landscape and land use), and the internal conditions such as those based on vector presence and/or abun- of the microhabitat that directly influence soft tick sur- dance. According to the second concept, such poten- vival, development and dynamics (e.g. temperature, tial vector presence and/or abundance should be pre- moisture, darkness, host presence). Internal conditions dicted instead of being described, in order to extend depend on external ones, but the specific organization predictions into non sampled areas or future periods. of the microhabitat and the structure of the interme- This method uses habitat suitability based on favou- diate layer (e.g. depth and width of the opening, nature rable or tolerable environmental conditions for a spe- and size grading of soil, etc.) buffer outside conditions. cies survival, development and dynamics. This buffering effect should be taken into account for soft tick distribution models. For instance, a few studies RELEVANT CHARACTERISTICS OF SOFT TICKS have investigated the relationships between the internal TO PREDICT THEIR NICHE and external conditions of different microhabitats inha- bited by endophilous ticks or closely-related arthro- Considering the peculiar biology and ecology of arga- pods, but it is already possible to extract some general sid ticks, it seems difficult to adapt predictions of sui- patterns (Table I). Niche temperature and relative humi- table habitats for hard ticks to soft ticks. The major fea- dity usually show lower amplitude than outside air ture that often discriminates these groups of organisms conditions, determining the lower and upper limits of in relation to their environment is the nidicolous life- optimal conditions for tick survival and development. style of argasid ticks. These ticks, especially endophi- According to the spatial scale considered, the influence lous ones, are limited to specialized niches and have of landscape, hydrography and anthropogenic activi- developed well-adapted life history traits that insure ties on the organisation of the microhabitat and the their persistence in their microhabitat. For example, the structure of the intermediate layer will be more or less short blood feeding period for nymphs and adults important for predictions. At regional scale, as for hard may result in low dispersal capacity, or at least “step ticks, it is possible to consider that most distribution by step” dispersion, and thus in a more limited distri- patterns can be extracted from climatic conditions (Cum- bution of soft tick species and their associated patho- ming, 2002), except at range margins where the pre- gens (Sonenshine, 1993). Such patterns have been sence of rivers or mountains may change the micro- illustrated by different field and experimental studies: climate and allow the presence of soft ticks in seemly i) in Madagascar, O. p. domesticus was present over an unsuitable habitats. Conversely, at local scale, diffe- eight year period (2000-2008) at the same pig barn, but rences in the distributional patterns may depend mainly was absent in neighbouring farms at both sampling on pedology, hydrography, landscape composition or occasions (Ravaomanana, personal communication). organization, and vegetation. For example, Ornitho- Natural infection by ASFV was still detectable in ticks doros species belonging to the now obsolete group in 2008 whereas no potentially infected pig had been Theriodoros Pospelova-Shtrom 1953, are located in dif-
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Arthropod Temperature Authors Climatic zone Microhabitat species and humidity relationships
Pospelova-Shtrom, Temperate continental Gerbil burrow O. tartakovskyi In summer: ≈ 1953 climate (Turkmenistan) Tint Mean or MaxText < 26 °C ≈ MaxRHint MaxRHext MinRHint > 70 % Cave (fox den) O. verrucosus Similar moisture deficit but with lower amplitude inside microhabitat Avivi, 1967 Temperate mediterranean Sand-stone caves O. tholozani In summer: ≈ climate (Israël) Tint MaxText – [19-20] < 26 °C ≈ MaxRHint MaxRHext MinRHint > 60 % In winter: ≈ Tint MinText + [3-4] ≈ MaxRHint MaxRHext ≈ MinRHint MinRHext ≈ Butler et al., 1984 Temperate to subtropical Gopher-tortoise burrow O. turicata Tint Text – [4-7] < 25 °C ≈ oceanic climate (Florida) RHint MeanRHext + [40-55] > 8 % Yunker & Guirgis, Sub-saharan desert or Gerbil burrow Hyalomma spp. In summer: ≈ 1970 semi-desert (Egypt) Tint MaxText < 30 °C ≈ RHint MeanRHext + [30-60] > 80 % In winter: ≈ Tint MinText < 15 °C ≈ RHint MeanRHext + [30-60] > 80 % ≈ Heger et al., 2006 Sub-tropical to tropical Wall crack of human Rodnius prolixus Tint MeanText climate (Venezuela) houses Ampl Tint << Ampl Text Similar moisture deficit but with lower amplitude inside microhabitat
Table I. – Mathematical relationships (extracted from various studies) linking internal and external temperature and humidity of varied microhabitats inhabited by different endophilous tick species, or closely-related arthropods, in distinct climatic zones.
ferent continents but within the same eco-climatic distribution than for hard tick species. However, at region showing continental or Mediterranean tempe- local scale, the nature of the host community may act rate to sub-tropical climates and vegetation characte- as an evolutionary driver of tick populations. For exam- rized by low grasslands, steppes and semi-deserts ple, three genetically distinct tick populations have been (Morel, 1969). All of these species likely colonize detected within the distribution range of O. sonrai in rodent or reptile burrows and are directly in contact Senegal, Mali and Mauritania, using PCR amplifications with soil, which highly depends on the external cli- of the 16S rDNA gene (Vial et al., 2006b). Although mate. However, one of these species O. sonrai (for- no cause has been clearly identified, the geographical merly O. erraticus small variant) is present in Egypt, distribution of these three clusters apparently corres- despite the fact that global temperature and humidity ponded to rodent community zoning, with a predo- in most areas of the country seem unsuitable for its minance of Gerbillinae species associated with group survival and development; its presence is mainly due 3 in northern Saharan to Sahelo-Sudanan regions, a to an equilibrium of sufficiently dry areas and proxi- predominance of Murinae species associated with mity to a water source (the Nile Valley or local oases) group 1 in south-western Senegal, and the presence of that maintains a minimum relative soil humidity inside Mus musculus in Richard-Toll associated with group 2 microhabitats (Hoogstraal et al., 1954). At local scale, (Duplantier et al., 1997). pedology is responsible of local heterogeneity, with a high infestation of burrows composed by silt, silt-sand CURRENT ADVANCES or sand-clay soil and a complete absence of O. sonrai FOR PREDICTING SOFT TICK DISTRIBUTION from pure sand situations, even when open to humid For now, no distributional model has been developed sea or river breezes, as well as wet ground of extre- for any argasid tick. The only reference for soft ticks mely saline areas (Hoogstraal et al., 1954). is from Cumming & Van Vuuren (2006) who modelled Finally, regarding the common indiscriminate host pre- continental changes of geographical range for 73 African ference lifestyle of many soft ticks, host availability tick species, dealing with O. moubata and Ot. megnini seems to be less important to predict their geographical in the same way as for hard ticks. While results seemed
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conclusive for Ot. megnini that shows life history traits data for African ticks (http://www.wec.ufl.edu/faculty/ close to exophilous hard ticks, the model could not cummingg/TickDiP.htm). However, such data may show explain the high variability of O. moubata presence some biases: i) they essentially correspond to historical data, suggesting an influence of other, still unidenti- data from the 1930s to the 1960s when many field col- fied, environmental factors acting on its distribution. lection campaigns were organized. Since this time dis- Presence data are available for many species from past tribution patterns may have changed; ii) they may field studies and could be used for modelling or as pre- show a bias in sampling because information comes liminary assessments of soft tick distributions. For exam- from distinct collectors using different protocols and ple, Morel (1969) devoted part of his career to recording techniques and samplings may have been done in the results of hard and soft tick sampling conducted accessible areas only, for example along the main by various scientists in Africa and Mediterranean Basin roads, which is not representative of realized distri- starting at the beginning of the twentieth century. For bution; iii) they only correspond to presence data each record, he specified the location, date, host or because some scientists did not document absences or habitat, stages and verified the identification by obser- because records come from museum collections where ving original specimens if available. These data are only specimens that were found are stored; iv) they available on a CDrom published by CIRAD in 2003 and are subjected to misidentification according to the exper- an example application of this data is given in Figure 3. tise and the sense of responsibility of the collector and More recently, the Integrated Consortium on Ticks because of complexity and ambiguity of the morpho- and Tick-borne Diseases (ICTTD) (http://www.icttd.nl/) logical keys used at this period for tick identification. proposed to produce and update a worldwide tick pre- Other available resources on soft tick biology and eco- sence database associating each record with GPS coor- logy can be obtained through: i) field observations of dinates and Cumming has already published some habitat/microhabitat preferences or the seasonal dyna-
Fig. 3. – Geographical location of Morel’s presence data for several species of Orni- thodoros ticks transmitting TBRF and/or ASFV in Eurasia and Africa. 1052 records were reported and 865 were geographi- cally localized using the US Army Gazeeter (http://tomcat-dmaweb1.jrc.it/fuzzyg/ query/).
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mics of tick populations; and ii) laboratory experiments statistical or associative) models. These models match investigating the influence of climatic conditions (e.g. observed distributions to various current environment temperature, humidity and sunshine) on survival, life variables in a statistical framework and apply spatial cycle and feeding success. Such data may be useful, or temporal projected changes in environmental varia- as a preliminary approach, to predict the possible relation- bles, especially climate, to the distribution by interpo- ship between geographical range of soft ticks and lation or extrapolation (Kitron & Mannelli, 1994). Bea- some environmental factor. For example, the African ring in mind the potential biases of presence datasets, subgenus Ornithodoros sensu stricto Koch 1944 was such models enable one to predict a species’ range without highly documented in the 1960s by Walton who clearly knowing how each biological parameter is affected by demonstrated that O. moubata consisted of a complex the environment and are easily adapted to risk map- of species and subspecies, each showing distinct mor- ping (Rogers & Randolph, 2006). However, bibliogra- phological, biological and ecological features (Walton, phic resources on soft ticks remain essential to assess 1979). His 20 years of intensive research on TBRF in the ecological significance of such models. Another pre- East Africa provided new insights on O. p. domesticus, liminary approach would be to directly use resources suggesting the existence of at least four different ecolo- on soft tick biology and ecology under specific envi- gical “races” locally adapted to different regions and pre- ronmental constraints to implement distribution models. senting distinct temperature and humidity optima (Wal- Because available data on soft ticks are heterogeneous ton, 1962, 1964, 1979). During the same period, Pierce according to tick species and the environmental impact (1974) investigated O. p. porcinus distributional patterns of conditions on soft tick survival, development and according to climate, soil, vegetation, host and season. dynamics are only partially documented, an alternative Within the same subgenus, the biology of O. moubata would be the use of intermediate approaches like sensu stricto from Southern Africa was investigated in fuzzy knowledge-based models (Zadeh, 1965). This the laboratory by Cunliffe (1921), Jobling (1925) and approach has been developed for artificial intelligence Loomis (1961) according to temperature and humidity techniques and is emerging in ecology for predicting conditions. The subgenus Theriodoros Pospelova-Shtrom species distributional ranges and population dynamics 1950 was studied both in Central Asia and Middle East, (Bock & Salski, 1998; Kampichler et al., 2000; Mackin- for the group Pavlovskyella Pospelova-Shtrom 1953, son, 2000; Adriaenssens et al., 2006). It is based on expert and in Africa and the Mediterranean Basin for the or bibliographic knowledge that is represented by a group Theriodoros sensu stricto Pospelova-Shtrom 1953. set of logic linguistic rules in the form: IF
Parasite, 2009, 16, 191-202 198 Mise au point CHARACTERISTICS OF SOFT TICKS AND THEIR DISTRIBUTION Pospelova-Shtrom 1950 in Theriodoros > 17 °C Field data Field data altitude annual Highlands Moderate altitude T altitude Moderate altitude Alt > 1,000 m Alt > 1,500 m Houses Rain < 1,250-1,500 mm apers and unpublished reports. sensu stricto Koch 1944 and Ornithodoros Life-cycle (days) ? Higher T amplitude burrows too low 51too low 158 157 50 < Rain 750 mm 184 Rodent burrows/humid cracks or too low 250 < Rain 500 mm Caves and lairs/human herd 153 260 Rain mean: 350 mm Caves or reptile small mammal ext ext ext june-sept No 8 months low T amplitude 6 months (oct-june) rain max > 500 mm burrows 4-5 months Supposed in Rain < 900-1,000 mm Warthog burrows Min? Sea level Fowl buildings Min? Alt < 2,100-3,000 m Max? Max: 90 (5-8 °C) shelters ? 1,200 < Alt 1,500 m Houses and fowl buildings ? Min? dry season Min: 0 Max: 90 80 95 100 < Rain 300 mm Reptile and small mammal Min: 5 Min: 34 If T Min: 10 Min: 15 If T Max: 43 Max? (13-15 °C) No altitude burrows in houses Max: 37 (3-4NN) No altitude houses Min: 5-8 Max: 80 ? 36 113 Rain < 500 mm Warthog burrows/dry cracks in 0 0 0 0 0 0 0 0 0 microhabitat microhabitat Possible conditions Optima inside Critical inside for optimum 25 [16-29] 75 [70-80] 24 [20-27] 62 [50-96] 25 [16-29] 75 [70-80] 26 [20-31]30 [25-35] 77 [67-96] 90 [75-95] 16 [15-18] 90 [80-100] Min: 10 Min? If T 23 [22-24] 52 [50-55] 22 [17-26] 92 [72-96] (25 [22-32] 50 [50-60] (25 [24-25] 83 [77-83] O. tartakovskyi Opd (race 2) O. tholozani Table II. – Optimal and critical conditions for the survival development of species from subgenus Africa, the Mediterranean Basin, Central Asia and Middle East. These data were extracted from historical scientific published p Species/subsp.O. moubata T (°C) RH (%) T (°C) RH (%) diapauseOpd (race 4) O. erraticus Min Max distibutionO. asperus microhabitat Opd (race 3) O. sonrai O. p. porcinus O. p. domesticus (race 1)
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which seek to describe each biological parameter and Dr Karen McCoy (CNRS/IRD, Montpellier) for editing mechanism underlying a phenomenon and how these the English manuscript; Dr Renaud Lancelot (CIRAD, aspects can be affected by the environment (Kitron & Montpellier) for institutional support and scientific advi- Mannelli, 1994). Such approaches are more accurate ces. Some original syntheses presented in the review for modelling complex, weak or temporary processes were supported by the European Centre for Diseases like seasonal reproduction or blood feeding according Control and Prevention (ECDC public tender– OJ/ to host dynamics (Randolph et al., 2002; Ogden et al., 2007/04/13 – PROC/2007/003) and the European Food 2005, 2006) and are able to deal with environmental Safety Authority (CFP/EFSA/AHAW/2007/02). I grate- factors other than climate or vegetation, such as anthro- fully thank the editorial board of Parasite to propose pogenic effects, landscape uses or species competition/ my oral presentation in the CIRDES International exclusion (Sumilo et al., 2007). By using equations that Conference, Ouidah Benin 2008, for publication. describe the growth patterns of a tick population, the infectious status of individuals, their contact with sus- ceptible hosts and host immunity can be easily integra- REFERENCES ted to obtain disease transmission models (Kitron & ABIDOV Z.I., VASIL’EVA I.S., RAKHIMOV N.R., GUTOVA V.P. & PAR- Mannelli, 1994). However, the application of such models PIEV A.M. Tick-borne relapsing fever morbidity in Naman- to soft ticks will require the collection of detailed bio- gan. 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Ecolological his paper reviewed the peculiar biological and Modelling, 2006, 195, 3-10. ecological characteristics of argasid ticks to be AVIVI A. Biology of the relapsing-fever tick, Ornithodoros tho- Ttaken into account to enhance predictions concer- lozani, (Laboulbene & Megnin, 1882) in Israel. World Health ning soft tick and associated disease distribution, with Organization Seminar on the Ecology, Biology and Control a special emphasis on Ornithodoros ticks. These cha- of Ticks and Mites of Public Health Importance, 11-15 racteristics included: i) nidicolous lifestyle, ii) indiscri- December 1967, Geneva. minate host feeding and short bloodmeal duration, and BALASHOV Y.S. Genotypic differences between populations of iii) flexible developmental cycles via diapause periods. Ornithodoros tartakovskyi (Ixodoidea, Argasidae) [Rus- Contrary to the common belief that it may be difficult sian]. 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