Integrative taxonomy demonstrates the unexpected synonymy between two predatory mite species: Cydnodromus idaeus and C. picanus (Acari : Phytoseiidae)
Marie-Stéphane Tixier A C , Haralabos Tsolakis B , Salvatore Ragusa B , Alix Poinso A , Maxime Ferrero A , Mireille Okassa A and Serge Kreiter A
+ Author Affiliations
- Author Affiliations
A Montpellier SupAgro, UMR CBGP INRA/IRD/CIRAD/SupAgro, Campus International de Baillarguet, CS 30 016, 34988 Montferrier sur Lez cedex, France.
B University of Palermo, Department DEMETRA, Laboratory of Applied Acarology ‘Eliahu Swirski’, Viale delle Scienze 13, 90128 Palermo, Italy.
C Corresponding author. Email: tixier@supagro.inra.fr
Invertebrate Systematics 25(4) 273-281 https://doi.org/10.1071/IS11025
Submitted: 2 June 2011 Accepted: 23 September 2011 Published: 22 December 2011
Abstract
Species of the mite family Phytoseiidae are well known as predators of mite pests all over the world. Their identification is thus of great interest for biological control. The specimens examined in this study belong to the species Cydnodromus idaeus (described from Brazil) and C. picanus (described from Chile). They were collected together on the same plant in Argentina. These species are mainly differentiated by the presence/absence of the dorsal solenostomes (gland openings) gd2. Some morphometric differences were observed between the Argentinian specimens and the type material of C. idaeus and C. picanus; however, they were not sufficient to support a species separation. Morphological and molecular analyses with two mtDNA (12S rRNA, CytB) and a nuclear DNA (ITS) marker showed no difference between Argentinian specimens with and without the solenostome gd2. Also, molecular differentiation between these latter specimens, C. picanus and C. idaeus, was very low, suggesting that all these individuals belong to the same species. Biological experiments confirm these results, as 75% of the progeny resulting from females with gd2 had gd2 present whereas all the descendants resulting from the females without gd2 had gd2 present too. The presence/absence of this solenostome seems thus to be variable within a species and cannot be used diagnostically. We conclude that all specimens from Argentina belong to C. idaeus and that C. picanus is a junior synonym of C. idaeus. The present results were unexpected as the presence/absence of solenostomes is used in Phytoseiidae identification keys and as one of a suite of diagnostic characters for discriminating between species. The consequences of these findings for the taxonomy of Phytoseiidae are discussed.
Additional keywords: 12S rRNA, CytB mtDNA, ITS, morphology, solenostome.
References
Athias-Henriot, C. (1969). Les organes cuticulaires sensoriels et glandulaires des Gamasides. Poroidotaxie. Bulletin de la Société Zoologique de France 94, 485–492.Athias-Henriot, C. (1971). Nouvelles notes sur les Amblyseiini (Gamasides Podospermiques, Phytoseiidae) I.La dépilation des génuaux et tibias des pattes. Acarologia 13, 4–15.
Athias-Henriot, C. (1974). Un problème arachnologique: l’interprétation phylogénétique des deux états idiosomaux des gamasides – protoadénie et eunéoadénie (Parasitiformes). In ‘Proceedings of the 4th International Congress of Acarology, Budapest’. pp. 443–445. (Pub. House of the Hungarian Academy of Science.)
Athias-Henriot, C. (1975). Nouvelles notes sur les Amblyseiini. II. Le relevé organotaxique de la face dorsale adulte (Gamasides, Protoadéniques, Phytoseiidae). Acarologia 27, 20–29.
Athias-Henriot, C. (1977). Nouvelles notes sur les Amblyseiini. III. Sur le genre Cydnodromus: Redéfinition, composition (Parasitiformes, Phytoseiidae). Entomophaga 22, 61–73.
| Nouvelles notes sur les Amblyseiini. III. Sur le genre Cydnodromus: Redéfinition, composition (Parasitiformes, Phytoseiidae).Crossref | GoogleScholarGoogle Scholar |
Chant, D. A. (1955). Notes on mites of the genus Typhlodromus Scheuten, 1857 (Acarina: Laelaptidae), with descriptions of the male of some species and the female of a new species. Canadian Entomologist 87, 496–503.
| Notes on mites of the genus Typhlodromus Scheuten, 1857 (Acarina: Laelaptidae), with descriptions of the male of some species and the female of a new species.Crossref | GoogleScholarGoogle Scholar |
Chant, D. A., and McMurtry, J. A. (1994). A review of the sub-families Phytoseiinae and Typhlodrominae (Acari: Phytoseiidae). International Journal of Acarology 20, 223–310.
| A review of the sub-families Phytoseiinae and Typhlodrominae (Acari: Phytoseiidae).Crossref | GoogleScholarGoogle Scholar |
Chant, D. A., and McMurtry, J. A. (2003). A review of the subfamily Amblyseiinae Muma (Acari: Phytoseiidae): Part 1. Neoseiulini new tribe. International Journal of Acarology 29, 3–46.
| A review of the subfamily Amblyseiinae Muma (Acari: Phytoseiidae): Part 1. Neoseiulini new tribe.Crossref | GoogleScholarGoogle Scholar |
Chant, D. A., and McMurtry, J. A. (2007). ‘Illustrated Keys and Diagnoses for the Genera and Subgenera of the Phytoseiidae of the World (Acari: Mesostigmata).’ (Indira Publishing House.) pp. 220.
Chant, D. A., and Yoshida-Shaul, E. (1987). A world review of the pyri species group in the genus Typhlodromus Scheuten (Acari: Phytoseiidae). Canadian Journal of Zoology 65, 1770–1804.
| A world review of the pyri species group in the genus Typhlodromus Scheuten (Acari: Phytoseiidae).Crossref | GoogleScholarGoogle Scholar |
Collier, K. F. S., De Lima, J. O. G., and Albuquerque, G. S. (2004). Predacious mites in papaya (Carica papaya L.) orchards: in search of a biological control agent of phytophagous mite pests. Neotropical Entomology 33, 799–803.
| Predacious mites in papaya (Carica papaya L.) orchards: in search of a biological control agent of phytophagous mite pests.Crossref | GoogleScholarGoogle Scholar |
Coons, L. B., and Alberti, G. (1999). Acari - Ticks. In ‘Microscopic Anatomy of Invertebrates. Vol. 8b’. (Ed. F. W. Harrison.) pp. 267–514. (Wiley–Liss: New York.)
Cuellar, M. E., Calatayud, P.-A., Melo, E. L., Smith, L., and Bellotti, A. C. (2001). Consumption and oviposition rates of six phytoseiid species feeding on eggs of the cassava green mite Mononychellus tanajoa (Acari: Tetranychidae). The Florida Entomologist 84, 602–607.
| Consumption and oviposition rates of six phytoseiid species feeding on eggs of the cassava green mite Mononychellus tanajoa (Acari: Tetranychidae).Crossref | GoogleScholarGoogle Scholar |
de Moraes, G. J., McMurtry, J. A., Denmark, H. A., and Campos, C. B. (2004). A revised catalog of the mite family Phytoseiidae. Zootaxa 434, 1–494.
Denmark, H. A. (1992). A revision of the genus Typhlodromus Scheuten (Acari: Phytoseiidae). Occasional Papers of the Florida State Collection of Arthropods, USA 7, 1–43.
Dermauw, W., Vanholme, B., and Van Leeuwen, T. (2010). Mitochondrial genome analysis of the predatory mite Phytoseiulus persimilis and a revisit of the Metaseiulus occidentalis mitochondrial genome. Genome 53, 285–301.
| Mitochondrial genome analysis of the predatory mite Phytoseiulus persimilis and a revisit of the Metaseiulus occidentalis mitochondrial genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlslCqsb0%3D&md5=d914f98c7a9050696b25cd8652751950CAS |
Evans, G. O. (1992). ‘Principles of Acarology.’ (CAB International: Cambridge.)
Faraji, F., Roig, J., and Bakker, F. (2011). Some new records of Phytoseiidae from southwest Europe with description of a new species from Spain (Acari: Mesostigmata). International Journal of Acarology 37, 331–346.
| Some new records of Phytoseiidae from southwest Europe with description of a new species from Spain (Acari: Mesostigmata).Crossref | GoogleScholarGoogle Scholar |
Ferrero, M., Gigot, C., Tixier, M.-S., Van Houten, Y., and Kreiter, S. (2010). Egg hatching response to a range of relative humidities for six species of predatory mites. Entomologia Experimentalis et Applicata 135, 237–244.
| Egg hatching response to a range of relative humidities for six species of predatory mites.Crossref | GoogleScholarGoogle Scholar |
Guanilo, A. D., de Moraes, G. J., Toledo, S., and Knapp, M. (2008). Phytoseiid mites (Acari: Phytoseiidae) from Argentina, with description of a new species. Zootaxa 1884, 1–35.
Jafari, S., Fathipour, Y., and Faraji, F. (2011). Re-descriptions of Amblyseius meghriensis Arutunjan and Typhlodromus haiastanius (Arutunjan) with discussion on using preanal pores as a character in the subgenus Anthoseius (Mesostigmata: Phytoseiidae). International Journal of Acarology 37, 244–254.
| Re-descriptions of Amblyseius meghriensis Arutunjan and Typhlodromus haiastanius (Arutunjan) with discussion on using preanal pores as a character in the subgenus Anthoseius (Mesostigmata: Phytoseiidae).Crossref | GoogleScholarGoogle Scholar |
Jeyaprakash, A., and Hoy, M. A. (2002). Mitochondrial 12S rRNA sequences used to design a molecular ladder assay to identify six commercially available phytoseiids (Acari: Phytoseiidae). Biological Control 25, 136–142.
| Mitochondrial 12S rRNA sequences used to design a molecular ladder assay to identify six commercially available phytoseiids (Acari: Phytoseiidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotVCqsbg%3D&md5=d8b06ada9df43a7eac58325a93c967c6CAS |
Kanouh, M., Tixier, M.-S., Okassa, M., and Kreiter, S. (2010a). Phylogenetic and biogeographic analysis of the genus Phytoseiulus (Acari: Phytoseiidae). Zoologica Scripta 39, 450–461.
| Phylogenetic and biogeographic analysis of the genus Phytoseiulus (Acari: Phytoseiidae).Crossref | GoogleScholarGoogle Scholar |
Kanouh, M., Tixier, M.-S., Guichou, S., Cheval, B., and Kreiter, S. (2010b). Two synonymy cases within the genus Neoseiulella (Acari: Phytoseiidae): is the molecular evidence so evident? Biological Journal of the Linnean Society. Linnean Society of London 101, 323–344.
| Two synonymy cases within the genus Neoseiulella (Acari: Phytoseiidae): is the molecular evidence so evident?Crossref | GoogleScholarGoogle Scholar |
Krantz, G. W., and Redmond, B. L. (1987). Identification of glandular and poroidal idionotal systems in Macrocheles perglaber F. & P. (Acari: Macrochelidae). Experimental & Applied Acarology 3, 243–253.
| Identification of glandular and poroidal idionotal systems in Macrocheles perglaber F. & P. (Acari: Macrochelidae).Crossref | GoogleScholarGoogle Scholar |
Lindquist, E., and Evans, G. W. (1965). Taxonomic concepts in the Ascidae, with a modified setal nomenclature for the idiosoma of the Gamasina Acarina: Mesostigmata. Memoirs of the Entomological Society of Canada 47, 1–64.
McMurtry, J. A., and Croft, B. A. (1997). Life-styles of phytoseiid mites and their roles in biological control. Annual Review of Entomology 42, 291–321.
| Life-styles of phytoseiid mites and their roles in biological control.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjvFWiug%3D%3D&md5=e43044a218de7915da6fdd8465b4672fCAS |
Meshkov, Yu. I. (1991). Euseius amissibilis sp. n. (Parasitiformes, Phytoseiidae), a new species of mite from Tadjikistan. Zoologicheskij Zhurnal 70, 138–140.
Murrell, A., Campbell, N. J., and Barker, S. C. (2001). A total-evidence phylogeny of ticks provides insights into the evolution of life cycles and biogeography. Molecular Phylogenetics and Evolution 21, 244–258.
| A total-evidence phylogeny of ticks provides insights into the evolution of life cycles and biogeography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXotVynurc%3D&md5=6d8692c35659f22ba560667f5718d7afCAS |
Navajas, M., Lagnel, J., Fauvel, G., and de Moraes, G. J. (1999). Sequence variation of ribosomal Internal Transcribed Spacer (ITS) in commercially important Phytoseiidae mites. Experimental & Applied Acarology 23, 851–859.
| Sequence variation of ribosomal Internal Transcribed Spacer (ITS) in commercially important Phytoseiidae mites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtFCnug%3D%3D&md5=3061d413b1b48bf061b7be9755afa7baCAS |
Okassa, M., Tixier, M.-S., Cheval, B., and Kreiter, S. (2009). Molecular and morphological evidence for a new species status within the genus Euseius (Acari: Phytoseiidae): consequences for taxonomy. Canadian Journal of Zoology 87, 689–698.
| Molecular and morphological evidence for a new species status within the genus Euseius (Acari: Phytoseiidae): consequences for taxonomy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFyit7fN&md5=11ecbd0001b2fd35aaa96731da210972CAS |
Okassa, M., Tixier, M.-S., and Kreiter, S. (2010). The use of two mitochondrial DNA fragments (12S rDNA and Cytb mtDNA) for assessing the diagnosis of Phytoseiulus persimilis Athias-Henriot and Phytoseiulus macropilis (Banks) (Acari: Phytoseiidae). Experimental & Applied Acarology 52, 291–303.
| The use of two mitochondrial DNA fragments (12S rDNA and Cytb mtDNA) for assessing the diagnosis of Phytoseiulus persimilis Athias-Henriot and Phytoseiulus macropilis (Banks) (Acari: Phytoseiidae).Crossref | GoogleScholarGoogle Scholar |
Ragusa, S. (2000). A new Cydnodromus (Parasitiformes, Phytoseiidae), from the desert of northern Chile. Phytophaga 10, 3–10.
Ragusa, S., and Athias-Henriot, C. (1983). Observations on the genus Neoseiulus Hughes (Parasitiformes, Phytoseiidae). Redefinition. Composition. Geography. Description of two new species. Revue Suisse de Zoologie 90, 657–678.
Ragusa, S., and Tsolakis, H. (1994). Revision of the genus Kampimodromus Nesbitt 1951 (Parasitiformes, Phytoseiidae), with a description of a new species. Acarologia 35, 305–322.
Ragusa, S., and Vargas, R. (2002). On some phytoseiid mites (Parasitiformes, Phytoseiidae) from Chile. Phytophaga 12, 129–139.
Rioja, T. S., and Vargas, R. M. (2009). Life table parameters and consumption rate of Cydnodromus picanus ragusa, Amblyseius graminis Chant, and Galendromus occidentalis (Nesbitt) on avocado red mite Oligonychus yothersi (McGregor) (Acari: Phytoseiidae, Tetranychidae). Chilean Journal of Agricultural Research 69, 160–170.
Ragusa, S., Vargas, R., Tsolakis, H., and Ashbrach, R. (2000). Laboratory studies on the influence of various food substances on some biological and life-table parameters of Cydnodromus picanus Ragusa (Parasitiformes, Phytoseiidae) associated with citrus trees in the Chilean desert. Phytophaga 10, 11–23.
Rowell, H. J., Chant, D. A., and Hansell, R. I. C. (1978). The determination of setal homologies and setal patterns on the dorsal shield in the family Phytoseiidae (Acarina: Mesostigmata). Canadian Entomologist 110, 859–876.
| The determination of setal homologies and setal patterns on the dorsal shield in the family Phytoseiidae (Acarina: Mesostigmata).Crossref | GoogleScholarGoogle Scholar |
StatSoft France (2008). STATISTICA version 7.1. www.statsoft.fr.
Swofford, D. L. (2002). ‘PAUP - Phylogenetic analysis using parsimony (*and other methods), Ver. 4. 0.’ Beta. (Sinauer Associates: Sunderland, MA.)
Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.
| MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVGrsL8%3D&md5=353e41e981e4ccb0f2f9b19980971a0fCAS |
Tello, V., Vargas, R., Araya, J., and Cardemil, A. (2009). Biological parameters of Cydnodromus picanus and Phytoseiulus persimilis raised on the carmine spider mite, Tetranychus cinnabarinus (Acari: Phytoseiidae, Tetranychidae). Ciencia Invertebrate Agraria 36, 277–290.
Tixier, M. S., Kreiter, S., Barbar, Z., Ragusa, S., and Cheval, B. (2006a). The status of two cryptic species: Typhlodromus exhilaratus Ragusa and Typhlodromus phialatus Athias-Henriot (Acari: Phytoseiidae): consequences for taxonomy. Zoologica Scripta 35, 115–122.
| The status of two cryptic species: Typhlodromus exhilaratus Ragusa and Typhlodromus phialatus Athias-Henriot (Acari: Phytoseiidae): consequences for taxonomy.Crossref | GoogleScholarGoogle Scholar |
Tixier, M.-S., Kreiter, S., Ferragut, F., and Cheval, B. (2006b). The suspected synonymy of Kampimodromus hmiminai and Kampimodromus adrianae (Acari: Phytoseiidae): morphological and molecular investigations. Canadian Journal of Zoology 84, 1216–1222.
| The suspected synonymy of Kampimodromus hmiminai and Kampimodromus adrianae (Acari: Phytoseiidae): morphological and molecular investigations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlelsbvP&md5=680823bf3e5d6322a4197a5174ce932cCAS |
Tixier, M.-S., Kreiter, S., Croft, B. A., and Cheval, B. (2008a). Kampimodromus aberrans (Acari: Phytoseiidae) from USA: morphological and molecular assessment of its density. Bulletin of Entomological Research 98, 125–134.
| Kampimodromus aberrans (Acari: Phytoseiidae) from USA: morphological and molecular assessment of its density.Crossref | GoogleScholarGoogle Scholar |
Tixier, M.-S., Guichou, S., and Kreiter, S. (2008b). Morphological variation of the species Neoseiulus californicus (McGregor) (Acari: Phytoseiidae): importance for diagnostic reliability and synonymies. Invertebrate Systematics 22, 453–469.
| Morphological variation of the species Neoseiulus californicus (McGregor) (Acari: Phytoseiidae): importance for diagnostic reliability and synonymies.Crossref | GoogleScholarGoogle Scholar |
Tixier, M.-S., Ferrero, M., Okassa, M., Guichou, S., and Kreiter, S. (2010a). On the specific identity of specimens of Phytoseiulus longipes Evans (Mesostigmata: Phytoseiidae) showing different feeding behaviours: morphological and molecular analyses. Bulletin of Entomological Research 17, 1–11.
Tixier, M.-S., Okassa, M., Liguori, M., Poinso, A., Salerno, B., and Kreiter, S. (2010b). Voucher specimens for DNA sequences of phytoseiid mites (Acari: Mesostigmata). Acarologia 50, 487–494.
| Voucher specimens for DNA sequences of phytoseiid mites (Acari: Mesostigmata).Crossref | GoogleScholarGoogle Scholar |
Tsolakis, H., Tixier, M.-S., Kreiter, S., and Ragusa, S. (2011). The genus concept within the family Phytoseiidae (Acari: Parasitiformes). Historical review and phylogenetic analyses of the genus Neoseiulus Hughes. Zoological Journal of the Linnean Society , .
Wang, Y. M., and Xu, J. (1987). A new species of the genus Amblyseius Berlese (Acarina: Phytoseiidae). Entomotaxonomia 9, 153–155.
Wiens, J. J., and Servedio, M. R. (2000). Species delimitation in systematics: inferring “fixed” diagnostic differences between species. Proceedings. Biological Sciences 267, 631–636.
| Species delimitation in systematics: inferring “fixed” diagnostic differences between species.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3czovFagtQ%3D%3D&md5=c9bf77d0449eac32a6807606862b7f38CAS |
Wharton, G. W., Parrish, W., and Johnston, D. E. (1968). Observations on the fine structure of the cuticle of the spiny rat mite, Laelaps echidnina (Acari-Mesostigmata). Acarologia 10, 206–214.
