Coendangered hard-ticks: threatened or threatening?

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 hard-ticks. 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.

Biodiversity or pest?

In their review on tick-host specificity from 1982, Hoogstraal & Aeschlimann wrote: "As biomedical researchers, we are charged with the task of improving the quality of human life and welfare precisely, reducing risks of disease, irritation, and debilitation resulting from parasitism by ticks" [1]. From strict medical point of view they might be questionably right. But, ticks, as all parasitic species, are part of global biodiversity which according to current trends should be preserved.

The overwhelming majority of conservation projects in the animal kingdom 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 [2]. The dilemma of viewing parasites as biodiversity or pest has been discussed by several authors, regardless if it is about animal parasites [3-8]. General human perception of parasites is usually negative and several dictionaries derogatorily associate this concept with exploitation. Among all parasites, ticks, along with other ectoparasites seem to have one of the most negative reputations [9].

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 co-endangered

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 host's skin, specific sensory stimulus to attachment, specific ability of the tick to evade the host's 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 of the host in order to evaluate the status of specifically associated tick parasites, following the algorithm in Table 1. The list of valid ticks species used was according to the latest taxonomical reviews of the group [10,11,13].

Table 1

Algorithm used for proposal of tick conservation status

Proposed status of the tick	IUCN status of the host
Extinct	EX, EW
Coendangered	CR, EN, VU

EX - Extinct; EW - Extinct in the Wild; CR - Critically Endangered; EN - Endangered; VU - Vulnerable

Extinction of single host species could result in the immediate extinction of several associated species (parasites, commensals, mutualists) [16]. In the case of Ixodidae, there are certain threatened vertebrates which host more than one tick species. For instance, the extinction of the sambar deer (Rusa unicolor) could lead to the coextinction of four specifically associated ticks. Moreover, ticks harbor themselves internal symbiotic microorganisms, most of them not studied. Thus, the resulted chain of extinctions is much more complex and difficult to estimate.

Our synoptic evaluation of ticks specifically associated with their threatened host revealed a number of 63 coendangered species (Tables 2 and 3).

Table 2

Summary of Ixodidae (hard ticks) proposed to be considered coendangered

Genus	Number of valid species	Number of coendangered species	Host cathegory
			Reptiles	Birds	Mammals
Amblyomma	130	31	19	1	11
Anomalohimalaya	3	0	-	-	-
Bothriocroton	7	1	-	-	1
Cosmiomma	1	1	-	-	1
Dermacentor	34	3	-	-	3
Haemaphysalis	166	9	-	-	9
Hyalomma	27	2	1	-	1
Ixodes	243	16a	-	4	12
Margaropus	3	0	-	-	-
Nosomma	2	0	-	-	-
Rhipicentor	2	0	-	-	-
Rhipicephalus	82	0	-	-	-
TOTAL	700	63	20	5	38

a - Ixodes nitens which we list as extinct is not included

Table 3

Host associations of Ixodidae proposed to be coendangered

Species	Distribution	Main hosts	IUCN status of host
Ixodes anatis Chilton, 1904	New Zeeland	Apteryx mantelli	EN
		Apteryx australis	VU
I. dendrolagi Wilson, 1967	New Guinea	Dendrolagus matschiei	EN
		Dendrolagus dorianus	VU
I. diomedeae Arthur, 1958	Tristan da Cunha Islands	Thalassarche chlororhynchos	EN
I. galapagoensis Clifford and Hoogstraal, 1980	Galapagos	Aegialomys galapagoensis	VU
I. lemuris Arthur, 1958	Madagascar	Eulemur macaco	VU
I. montoyanus Cooley, 1944K	South America	Pudu puda	VU
I. moscharius Teng, 1982	Tibet	Moschus berezovskii	EN
I. moschiferi Nemenz, 1968	Nepal, China	Moschus berezovskii	EN
I. murreleti Cooley and Kohls, 1945	Coronados Islands	Synthliboramphus hypoleucus	VU
I. percavatus Neumann, 1906	Tristan da Cunha Islands	Thalassarche chlororhynchos	EN
I. schillingsi Neumann, 1901	Africa	Colobus polykomos	VU
I. stilesi Neumann, 1911	Chile	Pudu puda	VU
I. taglei Kohls, 1969	Chile	Pudu puda	VU
I. tapirus Kohls, 1957	Central and South America	Tapirus pinchaque	EN
		Tapirus bairdii	EN
I. vestitus Neumann, 1908	Australia	Myrmecobius fasciatus	EN
I. zaglossi Kohls, 1960	New Guinea	Zaglossus bruijni	CR
Haemaphysalis borneata Hoogstraal, 1971	Malaysia	Rusa unicolor	VU
H. capricornis Hoogstraal, 1966	Thailand	Capricornis sumatraensis	VU
H. goral Hoogstraal, 1970	China	Nemorhaedus griseus	VU
H. kopetdaghica Kerbabaev, 1962	Asia	Capra aegagrus	VU
H. moschisuga Teng, 1980	China	Moschus berezovskii	EN
H. pentalagi Pospelova-Shtrom, 1935	Japan	Pentalagus furnessi	EN
H. psalistos Hoogstraal, Kohls and Parrish, 1967	Philippines	Rusa unicolor	VU
H. sambar Hoogstraal, 1971	India	Rusa unicolor	VU
H. vietnamensis Hoogstraal and Wilson, 1966	Asia	Rusa unicolor	VU
Dermacentor circumguttatus Neumann, 1897	Africa	Loxodonta africana	VU
D. latus Cooley, 1937	Central America	Tapirus bairdii	EN
D. rhinocerinus (Denny, 1843)	Africa	Diceros bicornis	CR
		Ceratotherium simum	NT
Hyalomma aegyptium (Linnaeus, 1758)	Africa, Eurasia	Testudo graeca	VU
		Testudo horsfieldi	VU
H. rhipicephaloides Neumann, 1901	Middle East	Gazella gazella	VU
Bothriocroton oedemansi (Neumann, 1910)	New Guinea	Zaglossus bruijni	CR
Cosmiomma hippopotamensis (Denny, 1843)	Africa	Hippopotamus amphibius	VU 0.
		Diceros bicornis	CR
Amblyomma albopictum Neumann, 1899	West Indies	Cyclura lewisi	CR
		Cyclura cornuta	VU
A. antillorum Kohls, 1969	West Indies	Cyclura pinguis	CR
		Iguana delicatissima	VU
		Cyclura carinata	EN
A. argentinae Neumann, 1905	Argentina	Chelonoidis chilensis	VU
A. boeroi Nava et al., 2009	Argentina	Catagonus wagneri	EN
A. chabaudi Rageau, 1964	Madagascar	Pyxis arachnoides	EN
		Astrochelys radiata	EN
A. clypeolatum Neumann, 1899	Asia	Geochelone platynota	EN
		Indotestudo elongata	EN
A. coelebs Neumann, 1899	Central and South America	Tapirus bairdii	EN
		Tapirus terrestris	VU
A. crassum Robinson, 1926	South America	Chelonoidis denticulata	VU
A. crenatum Neumann, 1899	Java	Rhinoceros sondaicus	CR
A. cruciferum Neumann, 1901	West Indies	Cyclura cornuta	VU
A. darwini Hirst and Hirst, 1910	Galapagos	Amblyrhynchus cristatus	VU
A. geochelone Durden, Keirans and Smith, 2002	Madagascar	Astrochelys yniphora	CR
A. humerale Koch, 1844	South America	Chelonoidis denticulata	VU
A. incisum Neumann, 1906	Central and North America	Tapirus terrestris	VU
A. javanense (Supino, 1897)	Asia	Manis javanica	EN
		Manis pentadactyla	EN
A. komodoense (Oudemans, 1929)	Indonesia	Varanus komodoensis	VU
A. latepunctatum Tonelli-Rondelli, 1939	South America	Tapirus terrestris	VU
A. macfarlandi Keirans, Hoogstraal and Clifford, 1973	Galapagos	Chelonoidis nigra	VU
A. multipunctum Neumann, 1899	South America	Tapirus sp.	EN/VU1
A. papuanum Hirst, 1914	Australia	Casuarius casuarius	VU
A. personatum Neumann, 1901	Africa	Diceros bicornis	CR
A. pilosum Neumann, 1899	Galapagos	Chelonoidis nigra	VU
A. postoculatum Neumann, 1899	Australia	Lagostrophus fasciatus	EN
A. rhinocerotis (de Geer, 1778)	Africa	Diceros bicornis	CR
		Ceratotherium simum	NT
A. robinsoni Warburton, 1927	Indonesia	Varanus komodoensis	VU
A. supinoi Neumann, 1905	Asia	Indotestudo elongata	EN
		Heosemys spinosa	EN
		Heosemys depressa	CR
A. tholloni Neumann, 1899	Africa	Loxodonta africana	VU
A. torrei Perez Vigueras, 1934	West Indies	Cyclura lewisi	CR
A. tuberculatum Marx, 1894	USA	Gopherus polyphemus	VU
A. usingeri Keirans, Hoogstraal and Clifford, 1973	Galapagos	Chelonoidis nigra	VU
A. williamsi Banks, 1924	Galapagos	Conolophus subcristatus	VU

1 - The host for A. multipunctum was listed only as Tapirus sp. Only four species of genus Tapirus are known, three of which are endangered and one vulnerable.

CR - Critically Endangered; EN - Endangered; VU - Vulnerable; NT - Near Threatened

Most species included in our review (n = 31) belong to genus Amblyomma Koch, 1844. Their host specificity is high, especially in their adult stage [1] which makes them candidates for extinction if their hosts become extinct. Within the genus Ixodes, we propose 16 species, parasitic on tropical birds or mammals, as coendangered. All coendangered species (n = 9) from the genus Haemaphysalis Koch, 1844 are restricted to Asian threatened mammals. Only three species of the genus Dermacentor Koch, 1844 are included in our synopsis. The genus Hyalomma Koch, 1844, parasitic on mammals and tortoises includes two coendangered species. The genus Bothriocroton Keirans, King and Sharrad, 1994, recently erected to genus level, was initially described as a subgenus of the former genus Aponomma (now synonym of Amblyomma) [12]. Seven species are currently included here, all with Australian distribution, with a single species coendangered (B. oedemansi). The monospecific genus Cosmiomma Schulze, 1919 is found on large threatened mammals from Africa, hence its single species, Cosmiomma hippopotamensis is considered coendangered.

Coendangered ticks of reptiles

Twenty species of coendangered ticks are proposed from those specifically associated with reptiles (Tables 2 and 3). Threatened chelonians harbor 12 of them (11 in the genus Amblyomma and 1 in the genus Hyalomma). Ten of these chelonian ticks are specifically associated with terrestrial species of the Testudinidae family. On the other hand, Amblyomma supinoi, which seems to have less host specificity, has all reported hosts being threatened chelonians (Testudinidae, Geoemydidae) from Asia. The only coendangered tick species of chelonians from Eurasia and Northern Africa is Hyalomma aegyptium, parasitic on tortoises of the genus Testudo. We can group the eight coendangered ticks of lizards into two major groups (all in the genus Amblyomma), based on the taxonomic and biogeographic data of their host: (i) ticks of Iguanidae endemic to West Indies and Galapagos and (ii) ticks of Varanidae from Indonesia.

Coendangered ticks of birds

Birds harbor five species which we list as coendangered. Four of them belong to the genus Ixodes and are non-questing nest ticks parasitic on endangered or vulnerable birds; they were reported exclusively from island habitats (Tables 2 and 3). The Atlantic yellow-nosed albatross (Thalassarche chlororhynchos), which nests solely on a few islands from the Atlantic Ocean. is the only recorded host for two species of coendangered ticks. Two species of threatened kiwi birds (genus Apteryx) are the only known hosts of Ixodes anatis in New Zeeland. The fourth bird-associated Ixodes listed here as coendangered is Ixodes murreleti found specifically on the Xantus's murrelet (Synthliboramphus hypoleucus) in the Coronados Islands. The principal host of Amblyomma papuanum is the vulnerable flightless Southern cassowary (Casuarius casuarius) from Papua New Guinea.

Coendangered ticks of mammals

The 38 species of coendangered ticks associated with mammals belong to several genera (Table 2): Ixodes, Haemaphysalis, Dermacentor, Hyalomma, Bothriocroton, Cosmiomma and Amblyomma.

Two species are parasitic on an egg-laying mammal, the critically endangered Western long-beaked echidna (Zaglossus bruijnii) in New Guinea. The other three species are found on threatened marsupials from Australia or New Guinea. South and Central American tapirs (genus Tapirus) are hosts to six coendangered ticks in the genera Ixodes, Dermacentor and Amblyomma. Seven species of ticks are specific parasites of elephants, rhinoceros and hippopotamus. Although the distribution range of these hosts is still wide, antiparasitic treatments during translocations pose a large problem to the survival of associated ticks [19]. Several threatened South American and Asian even-toed ungulates (order Artiodactyla) are specific hosts to 15 species of coendangered ticks. Five additional coendangered tick species are each parasitic on species from five other mammalian orders. Ixodes galapagoensis on a rodent in Galapagos, Ixodes lemuris on a lemur in Madagascar, Ixodes schillingsi on a primate in Africa, Haemaphysalis pentalagi on a lagomorph in Japan and Amblyomma javanense on pangolins in Asia.

Extinct ticks

Ticks described from fossil deposits are omitted. We consider extinct one species, namely Ixodes nitens, described from two female ticks collected on Rattus macleari on Christmas Island. The last report of the host species was in 1903 [28]. As the other endemic rat species Rattus nativitatis (sympatric with R. macleari), did not harbor I. nitens, we can assume this tick was specifically associated with its type host. Thus, we exclude the possibility that I. nitens might have re-adapted as a parasite of the introduced black rats, Rattus rattus [29]. However, no direct evidence is available.

Are endangered hosts endangered because of ticks?

Probably the most important issue regarding tick-host associations is vectorial transmission of microbial pathogens. Ticks are able to transmit viruses, bacteria and protozoans to a variety of hosts. One of the most pathogenic tick-borne microbes are piroplasms (genera Babesia and Theileria). The potential impact of babesiosis on conservation actions was discussed mainly as a consequence of stress-mediated relapse of chronic infections during translocation [30]. Otherwise, tick-borne diseases of threatened vertebrates are rarely fatal to their hosts. The following accounts consider only reports from hosts of coendangered ticks. Mortality associated with pathogens (Babesia bicornis and Theileria bicornis) acquired from ticks has been documented in black rhinoceros in Tanzania and South Africa [31-34]. The specific vector for these two haemoprotozoans is not known, but Dermacentor rhinocerinus and Amblyomma rhinocerotis were suggested [34]. Hence, extinction of these ticks is expected to result in the eradication of disease caused by B. bicornis and T. bicornis. A recent study from South Africa showed that 36.41% white rhinoceros were infected with Theileria bicornis and 9.23% with Theileria equi [35]. However, no pathology associated with the infection was recorded in white rhinoceros. Babesia loxodontis was described from asymptomatic African elephants, Loxodonta africana [36]; babesiosis in Asian elephants can be associated with weakness, fever, jaundice, constipation and haemoglobinuria [37]. Babesia pattoni was reported in Rusa unicolor but no associated pathology was described [38].

So far, no tick-borne diseases with impact on the health of threatened birds or reptiles have been described. Asymptomatic infections with Hemolivia mauritanica have been reported in Testudo graeca over its distribution range [39]. The zoonotic bacterial pathogen Anaplasma phagocytophilum have been isolated in ticks Amblyomma flavomaculatum collected on monitor lizards (Varanus exanthematicus) [40]. Although neither the host nor the ticks are endangered, there is high probability that other Amblyomma species could transmit Anaplasma to lizards of genus Varanus.

Conclusions

Expectedly or not, we came back to the question of Hoogstraal and Aeschlimann from the beginning of this paper. Should we decide on conservation of rare ticks? Or are they a real threat to their coendangered host and should be eliminated? Ticks as such are not dangerous. Disease, if present, is in most of the situations caused by vectored microbes. Moreover, pathology induced by tick-borne diseases in wild animals is seldom dangerous and is usually related to supplemental stressing factors (i.e. translocation). Last but not least, there is no proof to date that ticks listed by us as coendangered are competent vectors for pathogens of endangered animals.

Nevertheless, IUCN should reconsider the criteria of indexing species in its database as threatened. All symbiotic species (mutuals, commensals, parasites) specifically associated with their host should be listed as co-endangered. As previously suggested [3], some host-specific parasites are more endangered than their host. Moreover, parasites have their own evolutionary importance, and as suggested even in the early 1990's, parasites should have equal rights with their host [3,5].

Competing interests

The authors declare that they have no competing interests.

Authors' contributions

ADM - the idea of the manuscript, the intellectual content and wrote the text, reference on reptiles; CMG - reference research on part of the mammals and birds; VC - reference research on mammals and contributed to the text writing, mainly the piroplasm related paragraphs. All authors read and approved the final manuscript.