Skip to main content Accessibility help
×
×
Home

A paradise for parasites? Seven new haemogregarine species infecting lizards from the Canary Islands

  • Beatriz Tomé (a1) (a2), Ana Pereira (a1) (a2), D. James Harris (a1), Miguel A. Carretero (a1) and Ana Perera (a1)...
Abstract

Oceanic islands are hotspots of biodiversity due to their high levels of endemism, with the Canary Islands being a notable example. A previous molecular study on the biogeography and host associations of haemogregarines (Apicomplexa: Adeleorina) infecting lizards from this archipelago detected seven parasite haplogroups. These haplogroups exhibited high host-specificity and geographical structure, suggesting that they might correspond to distinct biological identities. In this study, along with sequencing a longer fragment of the 18S rRNA, we further explore the distinctiveness of these parasites by analysing their morphology, effects on host erythrocytes and parasitaemia levels. These lines of evidence together with their genetics, host associations, frequency of occurrence and geographical distribution support them as different biological entities. As such, we describe seven new species: Karyolysus canariensis sp. nov., Karyolysus galloti sp. nov., Karyolysus stehlini sp. nov., Karyolysus gomerensis sp. nov., Karyolysus atlanticus sp. nov., Karyolysus tinerfensis sp. nov. and Karyolysus makariogeckonis sp. nov. These new taxa are further examples of endemic diversity in the Canarian archipelago. They also contribute to clarify the taxonomy within the Apicomplexa, a phylum estimated to have one of the lowest percentages of described species.

Copyright
Corresponding author
Author for correspondence: Beatriz Tomé, E-mail: beatome@cibio.up.pt
References
Hide All
Abràmoff, MD, Magalhães, PJ and Ram, SJ (2004) Image processing with ImageJ. Biophotonics International 11, 3641.
Amo, L, López, P and Martín, J (2005) Prevalence and intensity of haemogregarine blood parasites and their mite vectors in the common wall lizard, Podarcis muralis. Parasitology Research 96, 378381.
Ancochea, E, Hernán, F, Huertas, MJ, Brändle, JL and Herrera, R (2006) A new chronostratigraphical and evolutionary model for La Gomera: implications for the overall evolution of the Canarian Archipelago. Journal of Volcanology and Geothermal Research 157, 271293.
Anderson, MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 3246.
Arbizu, PM (2017) pairwiseAdonis: Pairwise multilevel comparison using adonis. Version 0.0.1. Retrieved from: https://github.com/pmartinezarbizu/pairwiseAdonis (accessed 1 March 2018).
Bannert, B (1992) Sarcocystis simonyi sp. nov. (Apicomplexa: Sarcocystidae) from the endangered Hierro giant lizard Gallotia simonyi (Reptilia: Lacertidae). Parasitology Research 78, 142145.
Bannert, B, Lux, E and Sedlaczek, J (1995) Studies on endo- and ectoparasites of Canarian Lizards. Scientia Herpetologica 1995, 293296.
Bannert, B, Karaca, HY and Wohltmann, A (2000) Life cycle and parasitic interaction of the lizard-parasitizing mite Ophionyssus galloticolus (Acari: Gamasida: Macronyssidae), with remarks about the evolutionary consequences of parasitism in mites. Experimental and Applied Acarology 24, 597613.
Barry, M, Peirce, MA, Heath, ACG, Brunton, DH and Barraclough, RK (2011) A new blood parasite within the relict endemic New Zealand gecko Hoplodactylus duvaucelii. Veterinary Parasitology 179, 199202.
Bertrand, M, Pfliegler, WP and Sciberras, A (2012) Does the African native host explain the African origin of the parasite? The Maltese Geckobia estherae n. sp. parasitic on Tarentola mauritanica (Acari: Raphignathoidea: Pterygosomatidae). Acarologia 52, 353366.
Carranza, S, Arnold, EN, Mateo, JA and Geniez, P (2002) Relationships and evolution of the North African geckos, Geckonia and Tarentola (reptilia: Gekkonidae), based on mitochondrial and nuclear DNA sequences. Molecular Phylogenetics and Evolution 23, 244256.
Carranza, S, Arnold, EN, Geniez, P, Roca, J and Mateo, JA (2008) Radiation, multiple dispersal and parallelism in the skinks, Chalcides and Sphenops (squamata: Scincidae), with comments on Scincus and Scincopus and the age of the Sahara Desert. Molecular Phylogenetics and Evolution 46, 10711094.
Caudell, JN, Whittier, J and Conover, MR (2002) The effects of haemogregarine-like parasites on brown tree snakes (Boiga irregularis) and slatey-grey snakes (Stegonotus cucullatus) in Queensland, Australia. International Biodeterioration and Biodegradation 49, 113119.
Clement, M, Posada, D and Crandall, KA (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 16571659.
Cook, CA, Netherlands, EC and Smit, NJ (2016) Redescription, molecular characterisation and taxonomic re-evaluation of a unique African monitor lizard haemogregarine Karyolysus paradoxa (Dias, 1954) n. comb. (Karyolysidae). Parasites & Vectors 9, 347.
Cox, SC, Carranza, S and Brown, RP (2010) Divergence times and colonization of the Canary Islands by Gallotia lizards. Molecular Phylogenetics and Evolution 56, 747757.
Criado-Fornelio, A, Ruas, JL, Casado, N, Farias, NAR, Soares, MP, Müller, G, Brumt, JGW, Berne, MEA, Buling-Saraña, A and Barba-Carretero, JC (2006) New molecular data on mammalian Hepatozoon species (Apicomplexa: Adeleorina) from Brazil and Spain. Journal of Parasitology 92, 9399.
Damas-Moreira, I, Harris, DJ, Rosado, D, Tavares, I, Maia, JP, Salvi, D and Perera, A (2014) Consequences of haemogregarine infection on the escape distance in the lacertid lizard. Podarcis vaucheri. Acta Herpetologica 9, 119123.
Fain, A and Bannert, B (2000) Two new species of Ophionyssus megnin (Acari: Macronyssidae) parasitic on lizards of the genus Gallotia boulenger (Reptilia: Lacertidae) from the Canary Islands. International Journal of Acarology 26, 4150.
Fain, A and Bannert, B (2002) New observations on species of the genus Ophionyssus Mégnin (Acari: Macronyssidae) parasitic on lizards of the genus Gallotia boulenger (Reptilia: Lacertidae) from the Canary Islands, Spain with description of a new species. International Journal of Acarology 28, 361366.
Fajfer, M (2012) Acari (Chelicerata) – parasites of reptiles. Acarina 20, 108129.
Feliu, C, López, M, Gómez, MS, Torres, J, Sánchez, S, Miquel, J, Abreu-Acosta, N, Segovia, JM, Martín-Alonso, A, Montoliu, I, Villa, M, Fernández-Álvarez, Á, Bakhoum, AJS, Valladares, B, Orós, J and Foronda, P (2012) Parasite fauna of rodents (Murinae) from El Hierro (Canary Islands, Spain): a multidisciplinary approach. Acta Parasitologica 57, 171178.
Foronda, PR, Figueruelo, EO, Ortego, AR, Abreu, NA and Casanova, JC (2005) Parasites (viruses, coccidia and helminths) of the wild rabbit (Oryctolagus cuniculus) introduced to Canary Islands from Iberian Peninsula. Acta Parasitologica 50, 8084.
Foronda, P, Santana-Morales, MA, Orós, J, Abreu-Acosta, N, Ortega-Rivas, A, Lorenzo-Morales, J and Valladares, B (2007) Clinical efficacy of antiparasite treatments against intestinal helminths and haematic protozoa in Gallotia caesaris (lizards). Experimental Parasitology 116, 361365.
Foronda, P, López-González, M, Hernández, M, Haukisalmi, V and Feliu, C (2011) Distribution and genetic variation of hymenolepidid cestodes in murid rodents on the Canary Islands (Spain). Parasites & Vectors 4, 185.
García-Ramírez, A, Delgado-García, JD, Foronda-Rodríguez, P and Abreu-Acosta, N (2005) Haematozoans, mites and body condition in the oceanic island lizard Gallotia atlantica (Peters and Doria, 1882) (Reptilia: Lacertidae). Journal of Natural History 39, 12991305.
Haklová-Kočíková, B, Hižňanová, A, Majláth, I, Račka, K, Harris, DJ, Földvári, G, Tryjanowski, P, Kokošová, N, Malčeková, B and Majláthová, V (2014) Morphological and molecular characterization of Karyolysus – a neglected but common parasite infecting some European lizards. Parasites & vectors 7, 555.
Hassl, A (2012) Blood parasitism by hemogregarines in Central European lizards. Herpetozoa 25, 8386.
Hatcher, MJ, Dick, JTA and Dunn, AM (2012) Diverse effects of parasites in ecosystems: linking interdependent processes. Frontiers in Ecology and the Environment 10, 186194.
Hudson, PJ, Dobson, AP and Lafferty, KD (2006) Is a healthy ecosystem one that is rich in parasites? Trends in Ecology and Evolution 21, 381385.
Illera, JC, Fernández-Álvarez, Á, Hernández-Flores, CN and Foronda, P (2015) Unforeseen biogeographical patterns in a multiple parasite system in Macaronesia. Journal of Biogeography 42, 18581870.
Illera, JC, Spurgin, LG, Rodriguez-Exposito, E, Nogales, M and Rando, JC (2016) What are we learning about speciation and extinction from the Canary Islands? Ardeola 63, 523.
Johnson, EM, Allen, KE, Panciera, RJ, Ewing, SA and Little, SE (2009) Experimental transmission of Hepatozoon americanum to New Zealand White rabbits (Oryctolagus cuniculus) and infectivity of cystozoites for a dog. Veterinary Parasitology 164, 162166.
Jorge, F, Perera, A, Carretero, MA, Harris, DJ and Roca, V (2013) Cryptic species unveiled: the case of the nematode Spauligodon atlanticus. Journal of Zoological Systematics and Evolutionary Research 51, 187202.
Jorge, F, Perera, A, Poulin, R, Roca, V and Carretero, MA (2018) Getting there and around: host range oscillations during colonization of the Canary Islands by the parasitic nematode Spauligodon. Molecular Ecology 27, 533549.
Juan, C, Emerson, BC, Oromí, P and Hewitt, GM (2000) Colonization and diversification: towards a phylogeographic synthesis for the Canary Islands. Trends in Ecology and Evolution 15, 104109.
Karadjian, G, Chavatte, JM and Landau, I (2015) Systematic revision of the adeleid haemogregarines, with creation of Bartazoon n. g., reassignment of Hepatozoon argantis Garnham, 1954 to Hemolivia, and molecular data on Hemolivia stellata. Parasite 22, 31.
Katoh, K and Standley, DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772780.
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 18701874.
Kvičerová, J, Hypša, V, Dvořáková, N, Mikulíček, P, Jandzik, D, Gardner, MG, Javanbakht, H, Tiar, G and Široký, P (2014) Hemolivia and Hepatozoon: haemogregarines with tangled evolutionary relationships. Protist 165, 688700.
Maia, JPMC, Harris, DJ and Perera, A (2011) Molecular survey of Hepatozoon species in lizards from North Africa. Journal of Parasitology 97, 513517.
Maia, JPMC, Perera, A and Harris, DJ (2012) Molecular survey and microscopic examination of Hepatozoon miller, 1908 (Apicomplexa: Adeleorina) in lacertid lizards from the western Mediterranean. Folia Parasitologica 59, 241248.
Maia, JP, Álvares, F, Boratyński, Z, Brito, JC, Leite, JV and Harris, DJ (2014) Molecular assessment of Hepatozoon (Apicomplexa: Adeleorina) infections in wild canids and rodents from North Africa, with implications for transmission dynamics across taxonomic groups. Journal of Wildlife Diseases 50, 837848.
Maia, JP, Carranza, S and Harris, DJ (2016 a) Comments on the systematic revision of adeleid haemogregarines: is more data needed? Journal of Parasitology 102, 549552.
Maia, JP, Harris, DJ, Carranza, S and Goméz-Díaz, E (2016 b) Assessing the diversity, host-specificity and infection patterns of apicomplexan parasites in reptiles from Oman, Arabia. Parasitology 143, 17301747.
Mangiafico, S (2018) rcompanion: Functions to Support Extension Education Program Evaluation. Version 1.13.0. https://CRAN.R-project.org/package=rcompanion (accessed 1 March 2018).
Martínez-Silvestre, A, Mateo, JA, Silveira, L and Bannert, B (2001) Presencia de protozoos intraeritrocitarios en el lagarto gigante de La Gomera. Boletin de la Asociacion Herpetologica Española 12, 9092.
Matuschka, FR and Bannert, B (1987) Cannibalism and autotomy as predator-prey relationship for monoxenous sarcosporidia. Parasitology Research 74, 8893.
Matuschka, FR and Bannert, B (1989) Recognition of cyclic transmission of Sarcocystis stehlinii n. sp. in the Gran Canarian giant lizard. Journal of Parasitology 75, 383387.
Medlin, L, Elwood, HJ, Stickel, S and Sogin, ML (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71, 491499.
Megía-Palma, R, Martínez, J and Merino, S (2016) A structural colour ornament correlates positively with parasite load and body condition in an insular lizard species. The Science of Nature 103, 52.
Modrý, D, Beck, R, Hrazdilová, K and Baneth, G (2017) A review of methods for detection of Hepatozoon infection in carnivores and arthropod vectors. Vector-Borne and Zoonotic Diseases 17, 6672.
Morrison, DA (2009) Evolution of the Apicomplexa: where are we now? Trends in Parasitology 25, 375382.
Múrias Dos Santos, A, Cabezas, MP, Tavares, AI, Xavier, R and Branco, M (2015) TcsBU: a tool to extend TCS network layout and visualization. Bioinformatics (Oxford, England) 32, 627628.
Myers, N, Mittermeier, RA, Mittermeier, CG, Da Fonseca, GAB and Kent, J (2000) Biodiversity hotspots for conservation priorities. Nature 403, 853.
Netherlands, EC, Cook, CA, Du Preez, LH, Vanhove, MPM, Brendonck, L and Smit, NJ (2018) Monophyly of the species of Hepatozoon (adeleorina: Hepatozoidae) parasitizing (African) anurans, with the description of three new species from hyperoliid frogs in South Africa. Parasitology, 145, 10391050.
O'Dwyer, LH, Moço, TC, Paduan, KDS, Spenassatto, C, da Silva, RJ and Ribolla, PEM (2013) Description of three new species of Hepatozoon (apicomplexa, Hepatozoidae) from Rattlesnakes (Crotalus durissus terrificus) based on molecular, morphometric and morphologic characters. Experimental Parasitology 135, 200207.
Oppliger, A, Vernet, R and Baez, M (1999) Parasite local maladaptation in the Canarian lizard Gallotia galloti (Reptilia: Lacertidae) parasitized by haemogregarian blood parasite. Journal of Evolutionary Biology 12, 951955.
Padilla, DP, Illera, JC, Gonzalez-Quevedo, C, Villalba, M and Richardson, DS (2017) Factors affecting the distribution of haemosporidian parasites within an oceanic island. International Journal for Parasitology 47, 225235.
Pérez-Rodríguez, A, Ramírez, Á, Richardson, DS and Pérez-Tris, J (2013) Evolution of parasite island syndromes without long-term host population isolation: parasite dynamics in Macaronesian blackcaps Sylvia atricapilla. Global Ecology and Biogeography 22, 12721281.
Prenter, J, MacNeil, C, Dick, JTA and Dunn, AM (2004) Roles of parasites in animal invasions. Trends in Ecology and Evolution 19, 385390.
Rabie, SAH and Hussein, ANA (2014) A description of haemogregarina species naturally infecting white-spotted gecko (Tarentola annularis) in Qena, Egypt. Journal of the Egyptian Society of Parasitology 44, 351358.
R Core Team (2017) R: A language and environment for statistical computing. Version 3.4.3. Retrieved from: https://www.R-project.org/ (accessed 1 March 2018).
Reyes-Betancort, JA, Santos Guerra, A, Guma, IR, Humphries, CJ and Carine, MA (2008) Diversity, rarity and the evolution and conservation of the Canary Islands endemic flora. Anales del Jardín Botánico de Madrid 65, 2545.
Roca, V, Carretero, M, Llorente, G, Montori, A and Martin, J (2005) Helminth communities of two lizard populations (Lacertidae) from Canary Islands (Spain): host diet-parasite relationships. Amphibia-Reptilia 26, 535542. doi: 10.1163/156853805774806160.
Roca, V, Jorge, F and Carretero, MA (2012) Synopsis of the helminth communities of the lacertid lizards from the Balearic and Canary Islands. Basic and Applied Herpetology 26, 107116.
Sanmartín, I, Van Der Mark, P and Ronquist, F (2008) Inferring dispersal: a Bayesian approach to phylogeny-based island biogeography, with special reference to the Canary Islands. Journal of Biogeography 35, 428449.
Saoud, MFA, Ramadan, NF, Mohammed, SH and Fawzi, SM (1995) Haemogregarines of geckos in Egypt, together with a description of Haemogregarina helmymohammedi n. sp. Qatar University Science Journal 15, 131146.
Sloboda, M, Kamler, M, Bulantová, J, Votýpka, J and Modrý, D (2008) Rodents as intermediate hosts of Hepatozoon ayorgbor (Apicomplexa: Adeleina: Hepatozoidae) from the African ball python, Python regius? Folia parasitologica 55, 1316.
Smith, TG (1996) The genus Hepatozoon (apicomplexa: Adeleina). Journal of Parasitology 82, 565585.
Svahn, K (1975) Blood parasites of the genus Karyolysus (coccidia, Adeleidae) in Scandinavian lizards. Description and life cycle. Norwegian Journal of Zoology 23, 277295.
Telford, SR (2009) Hemoparasites of the Reptilia: Color Atlas and Text. Boca Raton, USA: CRC Press.
Tomé, B, Maia, JPMC and Harris, DJ (2013) Molecular assessment of apicomplexan parasites in the snake Psammophis from North Africa: do multiple parasite lineages reflect the final vertebrate host diet? Journal of Parasitology 99, 883887.
Tomé, B, Maia, JP, Salvi, D, Brito, JC, Carretero, MA, Perera, A, Meimberg, H and Harris, DJ (2014) Patterns of genetic diversity in Hepatozoon spp. infecting snakes from North Africa and the Mediterranean Basin. Systematic Parasitology 87, 249258.
Tomé, B, Rato, C, Perera, A and Harris, DJ (2016) High diversity of Hepatozoon spp. in geckos of the genus Tarentola. Journal of Parasitology 102, 476480.
Tomé, B, Pereira, A, Jorge, F, Carretero, MA, Harris, DJ and Perera, A (2018) Along for the ride or missing it altogether: exploring the host specificity and diversity of haemogregarines in the Canary Islands. Parasites & Vectors 11, 113.
Ujvari, B, Madsen, T and Olsson, M (2004) High prevalence of Hepatozoon spp. (Apicomplexa, Hepatozoidae) infection in water pythons (Liasis fuscus) from tropical Australia. Journal of Parasitology 90, 670672.
Van As, J, Davies, AJ and Smit, NJ (2013) Hepatozoon langii n. sp. and Hepatozoon vacuolatus n. sp. (Apicomplexa: Adeleorina: Hepatozoidae) from the crag lizard (Sauria: Cordylidae) Pseudocordylus langi from the North Eastern Drakensberg escarpment, Eastern Free State, South Africa. Zootaxa 3608, 345356.
Venables, WN and Ripley, BD (2002) Random and mixed effects. In Venables, WN and Ripley, BD (eds), Modern Applied Statistics with S. New York, USA: Springer, pp. 271300.
Votýpka, J, Modrý, D, Oborník, M, Šlapeta, J and Lukeš, J (2017) Apicomplexa. In Archibald, JM, Simpson, AGB and Slamovits, CH (eds), Handbook of the Protists. New York, USA: Springer, pp. 567624.
Wheeler, B and Torchiano, M (2016) lmPerm: Permutation Tests for Linear Models. Version 2.1.0. Retrieved from: https://CRAN.R-project.org/package=lmPerm (accessed 1 March 2018).
Zapatero-Ramos, LM, Gonzalez-Santiago, PM, Solera-Puertas, MA and Carvajal-Gallardo, MM (1989) Estudio de nuevas especies de Pterigosomidae (Acari: Antinedida) sobre Gekkonidos de las Islas Canarias. Descripción de Geckobia canariensis n. sp. y de Geckobia tinerfensis n. sp. Revista Iberica de Parasitologia 49, 5164.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Type Description Title
UNKNOWN
Supplementary materials

Tomé et al. supplementary material
Tomé et al. supplementary material 1

 Unknown (80 KB)
80 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed