Skip to main content
Log in

Traditional and geometric morphometrics supporting the differentiation of two new Retracrus (Phytoptidae) species associated with heliconias

  • Published:
Experimental and Applied Acarology Aims and scope Submit manuscript

Abstract

Cryptic diversity has been confirmed for several phytophagous mites in the Eriophyoidea superfamily previously considered as presenting low host specificity. Among generalist eriophyoids is the phytoptid Retracrus johnstoni Keifer, which has been reported in 19 palm species belonging to 11 genera, causing severe damage on some of them. Surprisingly this species was recently reported on another monocot family, Heliconiaceae, infesting Heliconia plants in Costa Rica and Brazil, being the only in the tribe Mackiellini to not be associated with palm trees. This study aimed to investigate the occurrence of cryptic species in R. johnstoni and to clarify the taxonomic status of populations associated with heliconias in the Americas. With this purpose traditional and geometric morphometric analyses were conducted as well as a detailed morphological study. Measurable trait data were analysed via univariate and multivariate analyses. Shapes of specimens from different populations were compared via geometric morphometric landmark methods. Morphometric analysis supported occurrence of at least two cryptic species previously identified as R. johsntoni and suggested occurrence of cryptic species among populations associated with different palm trees. Taxonomic descriptions of two new taxa associated with heliconias, namely Retracrus costaricensis n. sp. Ferreira and Navia and Retracrus heliconiae n. sp. Ferreira and Navia are presented. Morphometric traits that can be useful in the taxonomic identification are noted and their value is discussed. Results of the traditional morphometry and geometric methods were compared and the advantages of their joint use for Eriophyoidea systematics are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Abreu RLS (2004) Durabilidade natural do estipe de pupunha (Bactris gasipaes Kunth, Arecaceae) II: insetos. Acta Amaz 34:459–465

    Article  Google Scholar 

  • Adams DC, Rohlf FJ, Slice DE (2004) Geometric morphometrics: ten years of progress following the ‘revolution’. Ital J Zool 71:5–16. doi:10.1080/11250000409356545

    Article  Google Scholar 

  • Aguilar H, Murillo P (2012) Nuevos hospederos y registros de ácaros fitófagos para Costa Rica: período 2008–2012. Agron Costarric 36:11–28

    Google Scholar 

  • Amrine JW Jr, Manson DCM (1996) Preparation, mounting and descriptive study of eriophyoid mites. In: Lindquist EE, Sabelis MW, Bruin J (eds) Eriophyoid mites: their biology, natural enemies and control. Elsevier, The Netherlands, pp 388–396

    Google Scholar 

  • Amrine JW Jr, Stasny TAH (1994) Catalog of the Eriophyoidea (Acarina: Prostigmata) of the world. Indira Publishing House, West Bloomfield

    Google Scholar 

  • Armstrong KF, Ball SL (2005) DNA barcodes for biosecurity: invasive species identification. Philos Trans R Soc Lond B Biol Sci 360:1813–1823. doi:10.1098/rstb.2005.1713

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Arthur AL, Miller AD, Weeks AR (2011) Genetic markers indicate a new species complex of emerging pest mites in Australian grains. Ann Entomol Soc Am 104:402–415

    Article  Google Scholar 

  • Baker AS, Schwarz HH (1997) Morphological differences between sympatric populations of the Poecilochirus carabi complex (Acari: mesostigmata: Parasitidae) associated with burying beetles (Silphidae: Nicrophorus). Syst Parasitol 37:179–185

    Article  Google Scholar 

  • Baran S, Altun A, Ayyildiz N, Kence A (2011) Morphometric analysis of oppiid mites (Acari, Oribatida) collected from Turkey. Exp Appl Acarol 54:411–420

    Article  PubMed  Google Scholar 

  • Becerra JM, Valdecasas AG (2004) Landmark superimposition for taxonomic identification. Biol J Linn Soc 81:267–327

    Article  Google Scholar 

  • Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155

    Article  PubMed  Google Scholar 

  • Bookstein FL (1991) Morphometrics tools for landmark data: geometry and biology. EUA, New York

    Google Scholar 

  • Bookstein FL, Chernoff B, Elder RL, Humphries Jr JM, Smith GR, Strauss RE (1985) Morphometrics in evolutionary biology. Special publication 15. Academy of Natural Sciences Press, Philadelphia

  • Boykin LM, Armstrong KF, Kubatko L, Barro P (2012) Species delimitation and global biosecurity. Evol Bioinform 8:1–37

    Article  Google Scholar 

  • Carew M, Schiffer M, Umina P, Weeks A, Hoffmann A (2009) Molecular markers indicate that the wheat curl mite, Aceria tosichella Keifer, may represent a species complex in Australia. Bull Entomol Res 99:479–486

    Article  CAS  PubMed  Google Scholar 

  • Castagnoli M, Lewandowski M, Labanowski GS, Simoni S, Soika GM (2010) An insight into some relevant aspects concerning eriophyoid mites inhabiting forests, ornamental trees and shrubs. Exp Appl Acarol 51:169–189

    Article  PubMed  Google Scholar 

  • Chant DA, McMurtry JA (2007) Illustrated keys and diagnosis for the genera and subgenera of the Phytoseiidae of the world (Acari: Mesostigmata). Indira Publishing House, West Bloomfield

    Google Scholar 

  • Chetverikov PE, Sukhareva SI (2009) A revision of the genus Sierraphytoptus Keifer 1939 (Eriophyoidea, Phytoptidae). Zootaxa 2309:30–42

    Google Scholar 

  • Chetverikov PE, Craemer C, Vishnyakov AE, Sukhareva SI (2014) CLSM anatomy of internal genitalia of Mackiella reclinata n. sp. and systematic remarks on eriophyoid mites from the tribe Mackiellini Keifer, 1946 (Eriophyoidea: Phytoptidae). Zootaxa 3860:261–279

    Article  PubMed  Google Scholar 

  • Clarke FC, Pretorius E (2005) A comparison of geometric morphometric analyses and cross-breeding as methods to determine relatedness in three Amblyomma species (Acari: Ixodidae). Int J Acarol 31:393–405

    Article  Google Scholar 

  • de Castro CEI, May A, Gonçalves C (2007) Atualização da nomenclatura de espécies do gênero Heliconia (Heliconiaceae). Rev Bras Hort Ornam 13:38–62

    Google Scholar 

  • de Lillo E, Craemer C, Amrine JW Jr, Nuzzaci G (2010) Recommended procedures and techniques for morphological studies of Eriophyoidea (Acari: Prostigmata). Exp Appl Acarol 51:283–307

    Article  PubMed  Google Scholar 

  • Duso C, Castagnoli M, Simoni S, Angeli G (2010) The impact of eriophyoids on crops: recent issues on Aculus schlechtendali, Calepitrimerus vitis and Aculops lycopersici. Exp Appl Acarol 51:151–168

    Article  CAS  PubMed  Google Scholar 

  • El-Halawany ME, Abdel-Samad MA, El-Naggar ME (2001) Mites inhabiting date palms. In: Proceedings of second international conference on date palms, U.A.E. Al-Ain, pp 366–373

  • Furiatti RS (2001) Principais pragas da pupunheira. In: Kultchetscki L, Chaimsohn FP, Gardingo JR (eds) Palmito pupunha (Bactris gasipaes Kunth.): a espécie, manejo agronômico, usos e processamentos. Ponta Grossa, UEPG, pp 91–93

  • Genty P (1980) Estudios entomológicos com relacción a la palma africana em América Latina. Palmas (Colombia) 5:22–31

    Google Scholar 

  • Genty P, Reyes E (1977) Un nouvel acarien du palmier à huile: l’Eriophyidae Retracrus elaeis Keifer. Oléagineux 32:255–262

    Google Scholar 

  • Gondim Jr MGC (2000) Ácaros de palmeiras (Arecaceae) em áreas dos estados de São Paulo e Pernambuco. Thesis, Universidade de São Paulo, Piracicaba

  • Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci USA 101:14812–14817

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jagersbacher-Baumann J (2014) Species differentiation of scutacarid mites (Heterostigmatina) using multivariate morphometric methods. Exp Appl Acarol 62:279–292

    Article  PubMed  Google Scholar 

  • Keifer HH (1965) Eriophyid Studies B-16. Bureau of Entomology, California Department of Agriculture, 7–8

  • Keifer HH (1975) Eriophyid Studies C-10. Bureau of Entomology, California Department of Agriculture 3–4

  • Klimov PB, Bochkov AV, OConnor BM (2006) Host specificity and multivariate diagnostics of cryptic species in predacious cheyletid mites of the genus Cheletophyes (Acari: Cheyletidae) associated with large carpenter bees. Biol J Linn Soc 87:45–58

    Article  Google Scholar 

  • Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 11:353–357

    Article  PubMed  Google Scholar 

  • Lindquist EE, Amrine JW Jr (1996) Systematics, diagnoses for major taxa, and keys to families and genera with species on plants of economic importance. In: Lindquist EE, Sabelis MW, Bruin J (eds) Eriophyoid mites: their biology, natural enemies and control. Elsevier, The Netherlands, pp 33–87

    Chapter  Google Scholar 

  • Lindquist EE, Sabelis MW, Bruin J (1996) Eriophyoid mites: their biology, natural enemies and control. World Crop Pests, vol 6. Elsevier, The Netherlands

  • Marcus L F (1990) Traditional morphometrics. In: Rohlf FJ, Bookstein FL (eds) Proceedings of the Michigan morphometrics workshop. Spec. Publ. No. 2. University of Michigan Museum of Zoology, Ann Arbor, pp 77–122

  • Miller AD, Skoracka A, Navia D, Mendonça RS, Szydło W, Schultz MB, Smith CM, Truol G, Hoffmann AA (2013) Phylogenetic analyses reveal extensive cryptic speciation and host specialization in an economically important mite taxon. Mol Phylog Evol 66:928–940

    Article  Google Scholar 

  • Mosca LJ, Queiroz de MB, Almeida AS, Cavalcante RA, Alves RE (2004) Helicônia: Descrição, Colheita e Pós-Colheita (Documento 91). Fortaleza, Brazil

  • Navia D, Moraes GJ, Querino RB (2006) Geographic variation in the coconut mite, Aceria guerreronis Keifer (Acari: Eriophyidae): a geometric morphometric analysis. Int J Acarol 32:301–314

    Article  Google Scholar 

  • Navia D, Gondim MGC Jr, Moraes GJ (2007) Eriophyoid mites (Acari: Eriophyoidea) associated with palm trees. Zootaxa 1389:1–30

    Google Scholar 

  • Navia D, de Moraes GJ, Querino RB (2009) Geographic pattern of morphological variation of the coconut mite, Aceria guerreronis Keifer (Acari: Eriophyidae), using multivariate morphometry. Braz J Biol 69(3):773–783

    Article  CAS  PubMed  Google Scholar 

  • Navia D, Ochoa R, Welbourn C, Ferragut F (2010) Adventive eriophyoid mites: a global review of their impact, pathways, prevention and challenges. Exp Appl Acarol 51:225–255

    Article  PubMed  Google Scholar 

  • Ochoa R, Aguilar H, Vargas C (1991) Ácaros fitófagos de America Central: guia ilustrada. Catie, Turrialba

    Google Scholar 

  • Ochoa R, Aguilar H, Vargas C (1994) Phytophagous mites of Central America: an illustrated guide. Catie, Turrialba

    Google Scholar 

  • Oldfield GN (1996) Diversity and host plant specificity. In: Lindquist EE, Sabelis MW, Bruin J (eds) Eriophyid mites: their biology, natural enemies and control. Elsevier, Amsterdam, pp 199–216

    Chapter  Google Scholar 

  • Ozman-Sullivan SK, Amrine JW Jr, Walter DE (2006) A new species of eriophyoid mite (Acari: Eriophyidae) on sugarcane in Australia. Int J Acarol 32:387–395

    Article  Google Scholar 

  • Pfingstl T, Schäffer S, Krisper G (2010) Re-evaluation of the synonymy of Latovertex Mahunka, 1987 and Exocepheus Woolley and Higgins, 1968 (Acari: Oribatida: Scutoverticidae). Int J Acarol 36:327–342

    Article  Google Scholar 

  • Pretorius E, Clarke FC (2000) Geometric morphometric analyses of the male and female body shape of Hyalomma truncatum and H. marginatum rufipes (Acari: Ixodidae). Int J Acarol 26:229–238

    Article  Google Scholar 

  • Rafter MA, Hereward JP, Walter GH (2013) Species limits, quarantine risk and the intrigue of a polyphagous invasive pest with highly restricted host relationships in its area of invasion. Evol Appl 6:1195–1207

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Reis AC, Gondim MGG Jr, Navia D, Flechtmann CHW (2012) Eriophyoid mites (Acari: Prostigmata: Eriophyoidea) on palms (Arecaceae) from the Brazilian Amazon: a new genus and four new species. Zootaxa 3446:49–59

    Google Scholar 

  • Reis AC, Gondim MGC Jr, Ferragut FJ, Navia D (2014) New eriophyoid mites (Prostigmata: Eriophyoidea) associated with palm trees (Arecaceae) from South America. Int J Acarol 40:230–246

    Article  Google Scholar 

  • Rohlf FJ (1997) Program TPSSMALL. Department of Ecology and Evolution, State University of New York, Stony Brook 1v

    Google Scholar 

  • Rohlf FJ (1998) Program TPSRELW. Department of Ecology and Evolution, State University of New York, Stony Brook 1v

    Google Scholar 

  • Rohlf FJ (1999) Shape statistics: procrustes superimpositions and tangent spaces. J Classif 16:197–223

    Article  Google Scholar 

  • Rohlf FJ (2010) TpsDig, ver. 2.16. Ecology and evolution. SUNY at Stony Brook. http://life.bio.sunysb.edu/morph/

  • Rowell HJ, Chant DA, Hansell RIC (1978) The determination of setal homologies and setal patterns on the dorsal shield in the family Phytoseiidae (Acarina: Mesostigmata). Can Entomol 110:859–876

    Article  Google Scholar 

  • Santana DLQ, Flechtmann CHW (1998) Mite (Arthropoda: Acari) associates of palms (Arecaceae) in Brazil. I. Present status and new records. Rev Bras Zool 15:959–963

    Article  Google Scholar 

  • Santana DLQ, Flechtmann CHW, Lima MF (1994) Novos ácaros do coqueiro no Brasil. Aracaju, Brazil

  • SAS Institute (2002) SAS/STAT User’s guide, verson 9.0, T.S level 2 MO. SAS Institute Inc, Cary, NC

  • Skoracka A (2009) Description of Abacarus lolii n. sp. (Prostigmata: Eriophyoidea: Eriophyidae), a cryptic species within a grass-feeding Abacarus complex. Intern J Acarol 35:405–417

    Article  Google Scholar 

  • Skoracka A, Dabert M (2010) The cereal rust mite Abacarus hystrix (Acari: Eriophyoidea) is a complex of species: evidence from mitochondrial and nuclear DNA sequences. Bull Entomol Res 100:263–272. doi:10.1017/S0007485309990216

    Article  CAS  PubMed  Google Scholar 

  • Skoracka A, Kuczynski L (2006) Is the cereal rust mite, Abacarus hystrix really a generalist? Testing colonization performance on novel hosts. Exp Appl Acarol 38:1–13

    Article  PubMed  Google Scholar 

  • Skoracka A, Kuczynski L, Magowski W (2002) Morphological variation in different host populations of Abacarus hystrix (Acari: Prostigmata: Eriophyoidea). Exp Appl Acarol 26:187–193

    Article  PubMed  Google Scholar 

  • Skoracka A, Smith L, Oldfield G, Cristofaro M, Amrine JW Jr (2010) Host-plant specificity and specialization in eriophyoid mites and their importance for the use of eriophyoid mites as biocontrol agents of weeds. Exp Appl Acarol 51:93–110

    Article  PubMed  Google Scholar 

  • Skoracka A, Kuczynski L, Mendonça RS, Dabert M, Szydło W, Knihinicki D, Truol G, Navia D (2012) Cryptic species within the wheat curl mite Aceria tosichella (Keifer) (Acari: Eriophyoidea), revealed by mitochondrial, nuclear and morphometric data. Invertebr Syst 26:417–433

    Article  Google Scholar 

  • Skoracka A, Kuczyński L, Szydło W, Rector B (2013) The wheat curl mite Aceria tosichella (Acari: Eriophyoidea) is a complex of cryptic lineages with divergent host ranges: evidence from molecular and plant bioassay data. Biol J Linn Soc 109:165–180

    Article  Google Scholar 

  • Stekol’nikov AA (2008) Two new species of chigger mites (Acari: Trombiculidae) close to Neotrombicula minuta, application of nonlinear multivariate statistics. Acarina 16:21–29

    Google Scholar 

  • Stekol’nikov AA, Klimov PB (2010) A revision of chiggers of the minuta species-group (Acari: Trombiculidae: Neotrombicula Hirst, 1925) using multivariate morphometrics. Syst Parasitol 77:55–69

    Article  Google Scholar 

  • Sukhareva SI (1994) Family Phytoptidae Murray 1877 (Acari: Tetrapodili), its consisting, structure and suggested ways of evolution. Acarina 2:47–72

    Google Scholar 

  • Vidović B, Stanisavljevic L, Petanovic R (2010) Phenotypic variability in five Aceria spp. (Acari: Prostigmata: Eriophyoidea) inhabiting Cirsium species (Asteraceae) in Serbia. Exp Appl Acarol 52:169–181

    Article  PubMed  Google Scholar 

  • Vidović B, Jojić V, Marić I, Marinkovic S, Hansen R, Petanovic R (2014) Geometric morphometric study of geographic and hostrelated variability in Aceria spp. (Acari: Eriophyoidea) inhabiting Cirsium spp. (Asteraceae). Exp Appl Acarol 64:321–335. doi:10.1007/s10493-014-9829-4

    Article  PubMed  Google Scholar 

  • Wang CF, Kuo CC, Jeng ML, Huang KW (2011) Morphometric analyses reveal synonymy of two monotypic genera, Huangiella and Tumoris (Acari, Eriophyoidea, Eriophyidae). ZooKeys 102:1–11

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

To National Council for Scientific and Technological Development (CNPq), Brazil and FACEPE, Pernambuco, Brazil, by the financial support. Authors DN and MGC Gondim Jr. are also grateful to CNPq for research fellowships. We sincerely thank Prof. Dr. Hugo Aguilar (Universidad de Costa Rica, São José, Costa Rica) and Prof. Dr. Anibal Ramadan Oliveira (Universidade Estadual de Santa Cruz, Ilhéus, Bahia, Brazil) for being the first to discover the new species described in this manuscript, collecting and sending samples for identification. We also would like to thank Prof. Dr. Philipp Chetverikov (Saint-Petersburg State University, St. Petersburg, Russia) for examining and providing detailed information on Retracrus johnstoni specimens; Prof. Dr. José Wagner da Silva Melo (Federal University of Ceará, Ceará, Brazil), for statistical support and valuable suggestions for revision of the manuscript; and Dr. Norton Polo Benito (Embrapa Recursos Genéticos e Biotecnologia) for support in graphs edition.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Denise Navia.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Suppl. material 1

Deformation grids of the ventral region of Retracrus females from population associated with palm trees and heliconias in the Americas. a. Cocos nucifera, Alagoas, Brazil; b. Cocos nucifera, Paraíba, Brazil; c. Cocos nucifera, Pernambuco, Brazil; d. Cocos nucifera, Rio Grande do Norte, Brazil; e. Heliconia latispatha, San José, Costa Rica; f. Heliconia pendula, Bahia, Brazil; g. Syagrus romanzoffiana, São Paulo, Brazil (TIFF 1877 kb)

Suppl. material 2

Deformation grids of the coxigenital region of Retracrus females from population associated with palm trees and heliconias in the Americas. a. Cocos nucifera, Alagoas, Brazil; b. Cocos nucifera, Paraíba, Brazil; c. Cocos nucifera, Pernambuco, Brazil; d. Cocos nucifera, Rio Grande do Norte, Brazil; e. Heliconia latispatha, San José, Costa Rica; f. Heliconia pendula, Bahia, Brazil; g. Syagrus romanzoffiana, São Paulo, Brazil (TIFF 2335 kb)

Suppl. material 3

Deformation grids of the prodorsal shield of Retracrus females from population associated with palm trees and heliconias in the Americas. a. Cocos nucifera, Alagoas, Brazil; b. Cocos nucifera, Paraíba, Brazil; c. Cocos nucifera, Pernambuco, Brazil; d. Cocos nucifera, Rio Grande do Norte, Brazil; e. Heliconia latispatha, San José, Costa Rica; f. Heliconia pendula, Bahia, Brazil; g. Syagrus romanzoffiana, São Paulo, Brazil (TIFF 2127 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Navia, D., Ferreira, C.B.S., Reis, A.C. et al. Traditional and geometric morphometrics supporting the differentiation of two new Retracrus (Phytoptidae) species associated with heliconias. Exp Appl Acarol 67, 87–121 (2015). https://doi.org/10.1007/s10493-015-9934-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10493-015-9934-z

Keywords

Navigation