Coendangered hard-ticks: threatened or threatening?

Andrei Daniel Mihalca 0 Clin Mircea Gherman 0 Vasile Cozma 0 0 Department of Parasitology and Parasitic Diseases, University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca , Calea Manastur 3-5, Cluj- Napoca, 400372 , Romania The overwhelming majority of animal conservation projects are focused on vertebrates, despite most of the species on Earth being invertebrates. Estimates state that about half of all named species of invertebrates are parasitic in at least one stage of their development. The dilemma of viewing parasites as biodiversity or pest has been discussed by several authors. However, ticks were omitted. The latest taxonomic synopses of non-fossil Ixodidae consider valid 700 species. Though, how many of them are still extant is almost impossible to tell, as many of them are known only from type specimens in museums and were never collected since their original description. Moreover, many hosts are endangered and as part of conservation efforts of threatened vertebrates, a common practice is the removal of, and treatment for external parasites, with devastating impact on tick populations. There are several known cases when the host became extinct with subsequent coextinction of their ectoparasites. For our synoptic approach we have used the IUCN status of the host in order to evaluate the status of specifically associated hardticks. As a result, we propose a number of 63 coendangered and one extinct hard-tick species. On the other side of the coin, the most important issue regarding tick-host associations is vectorial transmission of microbial pathogens (i.e. viruses, bacteria, protozoans). Tick-borne diseases of threatened vertebrates are sometimes fatal to their hosts. Mortality associated with pathogens acquired from ticks has been documented in several cases, mostly after translocations. Are ticks a real threat to their coendangered host and should they be eliminated? Up to date, there are no reliable proofs that ticks listed by us as coendangered are competent vectors for pathogens of endangered animals. - Extant or extinct? Ticks (suborder Ixodida) are obligate blood-sucking acarines attacking a wide variety of hosts from all tetrapod vertebrate classes (Amphibia, Reptilia, Aves and Mammalia). Three families are currently recognized: Ixodidae (hard ticks), Argasidae (soft ticks) and Nuttalliellidae. The latest taxonomical synopses of the group [10-12] updated by [13] consider valid 700 non-fossil species in Ixodidae (for a review of fossil ticks see [14]). Though, how many of the non-fossil species are still extant is almost impossible to tell, as many of them are known only from type specimens in museums and were never collected since their original description. Generally, extinction is considered to have four main causes: habitat loss, species invasion, overkill and cascades of extinctions [15]. Cascades of extinctions (or coextinctions) are in most situations cases of habitat loss in species for which the habitat is another species, like the case of mutualists, commensals and parasites. In the case of most symbiotic interactions the extinction of the host could result in the extinction of several associated species [16]. Ticks are no exception. Narrow host specificity makes ticks coendangered After the concept of coextinction was intuited by Darwin in 1862 and introduced in scientific literature in 1993 [17], the term coendangered arose logically within the next years [18], when estimates stated that 6300 symbiotic species are coendangered with their associated organisms. Nevertheless, the review omitted several groups of parasites like protozoans, cestodes, trematodes, most nematodes, acanthocephalans, fleas, ticks, whale lice etc. Therefore, the number of coendangered parasites could be much higher. For ectoparasites, including ticks, not only the endangered status of the host makes them endangered. As part of conservation efforts of threatened vertebrates, actions often involve artificial breeding, re-introduction or relocations. During these processes, a common practice is the removal of external parasites, with devastating impact on their population [19]. Several cases are documented. One relevant example is of the louse Colpocephalum californici (now extinct) which were intentionally removed from the endangered California condor, Gymnogyps californianus during the captive breeding project at Los Angeles Zoo [20]. In the case of parasites, the coendangered status applies with predilection to species with high host-specificity. Ticks are distributed worldwide from the Arctic to tropical regions. Their geographical distribution is related to the range of their host(s) with the highest diversity in tropical regions. Host specificity in ticks is still a debated issue. In some tick species, the host specificity was evaluated by more or less complex experimental trials, but in the majority of the situations this label comes solely from field reports on tick-host associations. In the first situation, one of the most studied species is the cattle tick, Rhipicephalus (Boophilus) microplus. Several hypotheses were incriminated to explain host specificity in ticks: adaptation by the tick to the particular properties of hosts skin, specific sensory stimulus to attachment, specific ability of the tick to evade the hosts immune responses or dietary specificity [21-23]. Based on a review of experimental evidence or ecological observations, about 85% of the tick species are considered to have a certain degree of host specificity, especially in their adult stage [1]. However, sometimes ecological specificity (habitat dependence) could explain the apparent specific host association in ticks, reducing the access of certain tick species to a limited number of vertebrate species [24]. The first and single review so far on tick conservation [19] proposed 42 species of Ixodidae as candidates for the endangered status. Following this idea, the echidna tick Bothriocroton oudemansi was listed as coendangered with its host [25]. Similar opinions are available for other groups of parasites. The conservation status of myiasis causing Oestrid flies was discussed recently in detail [6]. In this review, the authors grouped the endangered parasitic flies into three categories, by the cause of possible extinction: treatment-induced, coextinction and neglected, listing a total number of 39 bot-flies. A synoptic review on coextinct lice of birds and mammals is also available [26]. A synopsis of ticks proposed for coendangered status The International Union for Conservation of Nature (IUCN) classifies organisms into seven categories, according to their conservation status [27]. Additionally, some species have entries in the red list database, but their status is listed as data deficient. Furthermore, many species are not present at all in the IUCN database, meaning they have not been evaluated to date. For our synoptic approach we have used the IUCN status (...truncated)