1Departamento de Investigación en Entomología Médica, Instituto Conmemorativo Gorgas de Estudios de la Salud. Panamá, Panamá.
2Departamento de Investigación en Entomología Médica, Instituto Conmemorativo Gorgas de Estudios de la Salud. Panamá, Panamá.
3Departamento de Investigación en Parasitología, Instituto Conmemorativo Gorgas de Estudios de la Salud. Panamá, Panamá.
4Departamento de Investigación en Entomología Médica, Instituto Conmemorativo Gorgas de Estudios de la Salud. Panamá, Panamá.
5✉ Departamento de Investigación en Entomología Médica, Instituto Conmemorativo Gorgas de Estudios de la Salud. Panamá, Panamá & Estación Científica Coiba, Coiba AIP, Ciudad del Saber, Panamá.
2020 - Volume: 60 Issue: 1 pages: 40-44https://doi.org/10.24349/acarologia/20204356
Lizards in the family Iguanidae are commonly parasitized by different groups of ectoparasites, mainly mites and ticks (Corn et al., 2011; Martínez-Salazar et al., 2015). In these reptiles, mites of the genera Geckobiella (Pterygosomatidae) and Amblyomma (Ixodidae) ticks are among the most frequently observed (Guglielmone et al., 2003; Corn et al., 2011; Paredes-León et al., 2012; Murgas et al. 2013). To date, Geckobiella comprises 12 species, which parasitize lizards in the families Iguanidae, Phrynosomatidae, Crotaphytidae and Tropiduridae (Paredes-León et al., 2012; Paredes-León and Guzmán-Cornejo, 2015), although individual species often have restricted host ranges. At least 13 species of Amblyomma are regular parasites of Neotropical cold-blooded terrestrial vertebrates (Guglielmone et al., 2003). Both types of ectoparasite feed on host blood.
Geckobiella stamii appears to be a specific parasite of iguanas and has been reported from green iguanas (Iguana iguana) in captivity in the Netherlands (Jack, 1961), United States (Corn et al., 2011), Mexico (Paredes-León et al., 2012), Panama (Murgas et al., 2013) and Italy (Mendoza-Roldán et al., 2019), and from Iguana delicatissima from the Dominican Republic (Knapp et al., 2012). With the exception of some information on taxonomy, hosts and/or distribution, little is known about the biology of G. stamii. Amblyomma dissimile is among the main parasites of reptiles and amphibians in the Americas, and the green iguana is among its main hosts, although it has also been reported from diverse birds and mammals (Guglielmone et al., 2003).
In this paper, we show interactions between G. stamii and A. dissimile in different localities of Panama and present some hypotheses on the nature of this association. During a review of the ticks from the Ectoparasite Collection of the Zoological Collection ''Dr. Eustorgio Méndez'', Gorgas Memorial Institute of Health Studies (CoZEM-ICGES), specimens of A. dissimile were found with mites and/or mite egg covers attached to the idiosoma. Non-adhered mites with similar morphology were also found loose in the vials.
These data corresponded to the following locations: 1 ♀. PANAMÁ: Prov. Chiriquí. Bugaba. 2 April 2015. Ex: Iguana iguana. Col: Juan Bernal. 21 ♀, 4 ♂, 1 larva. PANAMÁ: Prov. Panamá. Corozal. 25 October 2018-30 January 2019. Ex: Iguana iguana. Col: Indra Rodríguez. 1 ♀. PANAMÁ: Prov. Los Santos. Tonosí, La Honda. 25 March 2019. Ex: Iguana iguana. Col: Daniel González. The geographical location of each site is presented in Figure 1.
The ticks were examined individually using a Leica MZ125 stereomicroscope and photographed with a Leica DFC500 digital camera, and the images were processed with the IM50 and Combine ZP photography software. The mites removed from the ticks were mounted on slides with Hoyer solution and observed with a Leica DME. The morphological identification of G. stamii was based on the characters described by Jack (1961), Paredes-León et al. (2012) and Paredes-León and Guzmán-Cornejo (2015). Mite vouchers were deposited in CoZEM-ICGES.
From a total of 3042 examined A. dissimile ticks (1454 larvae, 768 nymphs, 215 females and 605 males), two females, one male and one larva had mites adhering to different parts of the idiosoma. Twenty-three females and 3 males had with white finger-like covers on the ventral surface of the idiosoma, that protected eggs. The number of covers per tick varied from 1 to several tens (Figures 2 and 3).
This is the first interaction report between G. stamii and A. dissimile and is one of the few records of mites associated with ticks. The findings obtained from three locations, separated by hundreds of kilometers, suggests that this association is not a local event. Until now, the known interactions between mites and other arthropods include predation, parasitism, hyperparasitism (parasitism of parasites) and phoresy, and there are few reports of mite-tick interactions (Walter and Proctor, 1999; Durden et al., 2018).
With exception of quiescent instars (protonymph and tritonymph), all stages of Geckobiella are parasites of reptiles, and there are no suggested instances of predation or hyperparasitism for this species. Reports of tick hyperparasites have been mainly reported when ticks parasitize other ticks (Bhat, 1968; Labruna et al., 2007; Durden et al., 2018). To our knowledge, the only report of mites parasitizing ticks was reported by Durden et al. (2015), who found a larva of Leptus (Erythraeidae) on Amblyomma torrei in the Bahamas. In that paper, the authors showed a picture where one larva is attached to the leg articulation of the tick, allowing ingestion of hemolymph. Unlike Geckobiella, larvae of Leptus are known parasites of arthropods (Southcott, 1999; Haitlinger, 2000; Mcaloon and Durden, 2000; Miranda and Bermúdez, 2008).
Many details on the biology of Geckobiella remain unknown, especially relating to oviposition and host questing behaviors. Murgas et al. (2013) reported eggs of G. stamii placed on the scales of I. iguana, suggesting that G. stamii is a permanent parasite. Our observations, however, show that female G. stamii can deposit her eggs on A. dissimile, secreting a protective cover, similar to that described by Goodwin (1953) for G. texana. Thus, it is possible that G. stamii use A. dissimile as a surrogate substrate for oviposition.
Since the females of A. dissimile detach from the iguana host to oviposit in the soil and subsequently die, using the tick as substrate for oviposition could represent a disadvantage for G. stamii if the tick dies far from a new host. However, if the tick female detaches into nesting or resting sites of the iguana, it would facilitae mite larvae accessing another iguana host. In this sense, G. stamii ''gains'' mobility by placing its eggs on a species (e.g. A. dissimile) with a higher dispersial capacity. This reasoning could also be assumed for male or immature ticks, since it is possible that their movements allow transportation to other parts of the iguana. Thus, it is possible that G. stamii uses A. dissimile as a way to reach new potential hosts (in the case of larvae and female of A. dissimile) or other parts of the body of the iguana (in the case of the male of A. dissimile).
These observations present an interesting interaction between these two parasites of green iguanas. Despite the wide distribution of A. dissimile in the Americas, this type of behavior has not been previously recorded, which could mean that a unique example of phoresy or hyperparasitism has gone unnoticed for now. Further observations are now necessary to improve our understanding of the nature and frequency of this association.
We would like to thank Daniel González for sending the specimens of Amblyomma dissimile from Los Santos, Santiago Nava (Instituto Nacional de Tecnología Agropecuaria, Argentina) for his comments on an early version of the manuscript, and Joao Varela-Petrucelli (Ministerio de Desarrollo Agropecuario, Panamá) for English corrections.
Bermúdez S., Apanaskevich D., Domínguez L. 2018. Garrapatas Ixodidae de Panamá. ISBN 978-9962-699-25-5. pp. 129.
Bhat V. 1968. Parasitism of males of Ornithodoros (Pavlovskyella) tholozani var. crossi (Laboulene & Megnin 1882) Argasidae: Ixodoidea, on fed nymps and females of the same species. J. Bombay Nat. Hist. Soc. 66(2): 401-403.
Corn J., Mertins J., Hanson B., Snow S. 2011. First reports of ectoparasites collected from wild-caught exotic reptiles in Florida. J. Med. Entomol. 48(1): 94-100. doi:10.1603/ME10065
Durden L. A., Knapp C. R., Beati L., Dold S. 2015. Reptile-Associated ticks from Dominica and the Bahamas with notes on hyperparasitic Erythraei Mites. J. Parasitol. 102(1): 24-27. doi:10.1645/14-602.1
Durden L. A., Gerlach R. F., Beckmen K. B., Greiman S. E. 2018. Hyperparasitism and Non-Nidicolous Mating by Male Ixodes angustus Ticks (Acari: Ixodidae). J. Med. Entomol. 55(3): 766-768. doi:10.1093/jme/tjy012
Goodwin M. H Jr.1954. Observations on the biology of the lizard mite Geckobiella texana (Banks) 1904 (Acarina: Pterygosomidae). J. Parasitol. 40(1): 54-59. doi:10.2307/3274256
Guglielmone A. A., Estrada-Peña A., Keirans J. E., Robbins R. G. 2003. Ticks (Acari: Ixodida) of the Neotropical zoogeographic region. Spec. Publ. Inter. Cons. Ticks and Tick-Borne Dis., Atalanta, Houten, The Netherlands. p. 173.
Haitlinger R. 2000. Four new species of Leptus Latreille, 1796 (Acari: Prostigmata: Erythraeidae) from Central America. Syst. Appl. Acarol. 5(1): 131-142.
Jack K. M. 1961. A re-examination of the genera Pimeliaphilus Trägårdh 1905 and Hirstiella Berlese 1920 (Acari; Prostigmata). Ann. Mag. Nat. History. 4: 305-314. doi:10.1080/00222936108651109
Knapp C., Durden L., Klompen H. 2012. Natural History Notes, Iguana delicatissima (Lesser Antillean Iguana). Herpetological Review. 43: pp. 134.
Labruna M., Ahid S., Soares H., Suassuna A. 2007. Hyperparasitism in Amblyomma rotundatum (Acari: Ixodidae). J. Parasitol. 93(6): doi:10.1645/GE-1277.1
Martínez-Salazar M, García L, Vélez-Hernández L, Mendoza-Martínez G, López-Pozos R. 2015. La iguana verde (Iguana iguana) y sus parásitos en una unidad de manejo intensivo en la costa de Oaxaca. Tem. Cien. Tecnol. 19(55): 43-52.
McAloon, F. M., Durden L. A. 2000. Attachment sites and frequency distribution of erythraeid mites, Leptus indianensis (Acari: Prostigmata), ectoparasitic on harvestmen Leiobunum formosum (Opiliones). Exp. Appl. Acarol. 24(7): 561-567. doi:10.1023/A:1026554308826
Mendoza-Roldán J., Colella V., Lia R., Nguyen V., Barros-Battesti D., Latta R., Dantas-Torres F., Otranto D. 2019. Borrelia burgdorferi (sensu lato) in ectoparasites and reptiles in southern Italy. Parasites & Vectors. doi:10.1186/s13071-019-3286-1
Miranda R, Bermúdez S. 2008. Ácaros (Arachnida: Acari) asociados con moscas Calliphoridae (Diptera: Oestroidea) en tres localidades de Panamá. Rev. Colomb. Entomol. 34(2): 192-196.
Murgas D., Dutary S., Miranda R. 2013. First report of Geckobiella stamii (Acari: Pterygosomatidae) parasitizing Iguana iguana (Squamata: Iguanidae in Panama. Rev. Ibér. Aracnol. 22: 97-98
Paredes-León R., Klompen H., Pérez T. 2012. Systematic revision of the genera Geckobiella Hirst, 1917 and Hirstiella Berlese, 1920 (Acari: Prostigmata: Pterygosomatidae) with description of a new genus for American species parasites on geckos formerly placed in Hirstiella. Zootaxa. 3510: 1-40. doi:10.11646/zootaxa.3510.1.1
Paredes-León R., Guzmán-Cornejo C. 2015. A new species of pterygosomatid mite and its phylogenetic position within the genus Geckobiella (Acariformes: Prostigmata: Pterygosomatidae). Int. J. Acarol. 41(1): 19-30. doi:10.1080/01647954.2014.988642
Southcott, R. V. 1992. Revision of the larvae of Leptus Latreille (Acarina: Erythraeidae) of Europe and North America, with descriptions of post-larval instars. Zool. J. Linnean Soc.105(1): 1-153. doi:10.1111/j.1096-3642.1992.tb01228.x
Walter, D. E., Proctor H. 1999. Mites. Ecology, evolution and behavior. Everbest Print. Hong Kong. p. 321.