Eur. J. Entomol. 118: 31-45, 2021 | DOI: 10.14411/eje.2021.004

Ecological niche modelling of species of the rose gall wasp Diplolepis (Hymenoptera: Cynipidae) on the Iberian PeninsulaOriginal article

Sara SARDÓN-GUTIÉRREZ1, Diego GIL-TAPETADO1,2, José F. GÓMEZ1, José L. NIEVES-ALDREY2
1 Departamento de Biodiversidad, Ecología y Evolución, Facultad de Ciencias Biológicas, Universidad Complutense de Madrid, 28040 Madrid, Spain; e-mails: sarasard@ucm.es; diego.gil@ucm.es; jf.gomez@bio.ucm.es
2 Museo Nacional de Ciencias Naturales (CSIC), José Gutiérrez Abascal 2, 28006 Madrid, Spain; e-mail: mcnna38@mncn.csic.es

Diplolepis (Hymenoptera: Cynipidae) are gall wasps that induce conspicuous galls on Rosa spp. (Rosaceae). These species are distributed globally and in Europe some are especially common and are founder organisms of biological communities composed of different insects. However, the ecological niches of these species have not been studied in detail. We modelled the potential distributions of these species using the locations of the galls of the four most abundant species of Diplolepis on the Iberian Peninsula (Diplolepis mayri, Diplolepis rosae, Diplolepis eglanteriae and Diplolepis nervosa, the galls of latter two are indistinguishable) using four different algorithms and identified the resulting consensus for the species. We compared the potential distributions of these species, considering their spatial complementarity and the distributions of their host plants. We found that D. mayri and D. eglanteriae/nervosa have complementary distributions on the Iberian Peninsula. The former species is found in the Mediterranean region, while D. eglanteriae and D. nervosa are distributed mainly in the Eurosiberian region. Diplolepis rosae has the widest distribution on the Iberian Peninsula. Our models constitute the first effort to identify suitable areas for species of Diplolepis species on the Iberian Peninsula and could be useful for understanding the evolutionary ecology of these species throughout their distribution in the western Palearctic.

Keywords: Hymenoptera, Cynipidae, Diplolepis, species distribution modelling, gall-inducing wasps, Spain, Rosaceae, habitat complementarity

Received: June 9, 2020; Revised: December 16, 2020; Accepted: December 16, 2020; Published online: February 5, 2021  Show citation

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SARDÓN-GUTIÉRREZ, S., GIL-TAPETADO, D., GÓMEZ, J.F., & NIEVES-ALDREY, J.L. (2021). Ecological niche modelling of species of the rose gall wasp Diplolepis (Hymenoptera: Cynipidae) on the Iberian Peninsula. EJE, 118, Article 31-45. https://doi.org/10.14411/eje.2021.004
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    References

    1. Abe Y., Melika G. & Stone G.N. 2007: The diversity and phylogeography of cynipid gallwasps (Hymenoptera: Cynipidae) of the oriental and eastern Palearctic regions, and their associated communities. - Orient. Insects 41: 169-212. Go to original source...
    2. Araújo M.B. & Guisan A. 2006: Five (or so) challenges for species distribution modelling. - J. Biogeogr. 33: 1677-1688. Go to original source...
    3. Askew R.R. 1960: Some observations on Diplolepis rosae (L.) (Hym. Cynipidae) and its parasites. - Entomol. Mon. Mag. 95: 191-192.
    4. Austin M.P. 2007: Species distribution models and ecological theory: a critical assessment and some possible new approaches. - Ecol. Model. 200: 1-19. Go to original source...
    5. Barbet-Massin M., Rome Q., Muller F., Perrard A., Villemant C. & Jiguet F. 2013: Climate change increases the risk of invasion by the yellow-legged hornet. - Biol. Conserv. 157: 4-10. Go to original source...
    6. Belizin V.I. 1957: Gall wasps (Hymenoptera: Cynipidae) in the USSR fauna developed on roses. - Entomol. Obozr. 36: 925-934.
    7. Bergqvist E. 2010: Sawflies and Wasps Attacking Roses. First cycle, G1E. Department of Plant Protection Biology, Swedish University of Agricultural Sciences, Alnarp, 42 pp. [in Swedish].
    8. BVdb (Biodiversidad Virtual Database) 2016: Insectarium Virtual. Genus Diplolepis. URL: http://www.biodiversidadvirtual.org/insectarium (last accessed 20 Sep. 2016).
    9. Breiman L. 2001: Random forests. - Machi. Learn. 45: 5-32. Go to original source...
    10. Breiman L., Cutler A., Liaw A. & Wiener M. 2015: Breiman and Cutler's Random Forests for Classification and Regression (R Package Ver. 4.6-12). URL: https://cran.r-project.org/web/packages/randomForest/.
    11. Burks B.D. 1979: Superfamily Cynipoidea. In Krombein K.V., Hurd P.D., Smith Jr. D.R. & Burks B.D. (eds): Catalog of Hymenoptera in America North of Mexico, Vol. 1. Smithsonian Institution Press, Washington, pp. 1045-1107.
    12. Calvo J. & Ross-Nadié E. 2016: Rosas silvestres ibéricas. Guía de identificación. Consejo Superior de Investigaciones Científicas, Madrid, 70 pp.
    13. Castroviejo S., Muñoz Garmendia F. & Navarro C. 1998: Flora Ibérica: Plantas vasculares de la Península Ibérica e Islas Baleares. Vol. VI. Rosaceae. Real Jardín Botánico, CSIC, Madrid, 592 pp.
    14. Chefaoui R.M., Hortal J. & Lobo J.M. 2004: Potential distribution modelling, niche characterization and conservation status assessment using GIS tools: a case study of Iberian Copris species. - Biol. Conserv. 122: 327-338. Go to original source...
    15. Codina A. 1920: Recull de zoocecidies catalanes. - Butl. Inst. Catalana Hist. Nat. 20: 178-187 [in Catalan].
    16. Cogolludo J. 1921: Contribución al conocimiento de las zoocecidias de España. - Trab. Mus. Nac. Cienc. Nat. (Ser. Bot.) 16: 1-117.
    17. Csóka G., Stone G.N. & Melika G. 2005: The biology, ecology and evolution of gall wasps. In Raman A., Schaefer C.W. & Withers T.M. (eds): Biology, Ecology and Evolution of Gall-Inducing Arthropods. Science Publisher, Enfield, New Hampshire, pp. 573-642.
    18. Cueto M. & Giménez E. 2009: Family Rosaceae. In Blanca G., Cabezudo B., Cueto M., Fernández López C. & Morales Torres C. (eds): Flora Vascular de Andalucía Oriental. Universidades de Almería, Jaén y Málaga, Granada, pp. 869-904.
    19. De Smedt P., Wuyts K., Baeten L., De Schrijver A., Proesmans W., De Frenne P., Ampoorter E., Remy E., Gijbels M., Hermy M. et al. 2016: Complementary distribution patterns of arthropod detritivores (woodlice and millipedes) along forest edge-to-interior gradients. - Insect Conserv. Divers. 9: 456-469. Go to original source...
    20. EEA (European Environment Agency) 2009: WISE Large Rivers and Lakes Raster Data. URL: https://www.eea.europa.eu/data-and-maps/data/wise-large-rivers-and-large-lakes (last accessed Jan. 2018).
    21. EEA (European Environment Agency) 2012: Corine Land Cover 2006 Raster Data. URL: https://www.eea.europa.eu/data-and-maps/data/clc-2006-raster (last accessed Jan. 2018).
    22. ESDB (European Soil Database) 2004: The European Soil Database Distribution Ver. 2.0. URL: https://esdac.jrc.ec.europa.eu/content/european-soil-database-v20-vector-and-attribute-data#tabs-0-description=0 (last accessed Jan. 2018).
    23. ESRI (Environmental Systems Research Institute) 2011: Arc-Gis 10.1 Geographical Information System. URL: https://www.esri.com/es-es/home (last accessed Jan. 2018).
    24. Fernández de Gata M. 1901: Nuevos estudios sobre las agallas. - Bol. R. Soc. Esp. Hist. Nat. 1: 194-199, 231-331, 345-353, 385-402.
    25. Folliot R. 1964: Contribution à l'étude de la biologie des cynipides gallicoles (Hymenoptères, Cynipoidea). - Ann. Sci. Nat. (Zool. Sér. 12) 6: 402-564.
    26. Franklin J. 2009: Mapping Species Distributions: Spatial Inference and Prediction. Cambridge University Press, Cambridge, UK, 320 pp. Go to original source...
    27. GBIF Data Portal 2016: Genus Diplolepis. URL: https://www.gbif.org/ (last accessed 20 Sep. 2016).
    28. Gil-Tapetado D., Gómez J.F., Cabrero-Sañudo F.J. & Nieves-Aldrey J.L. 2018: Distribution and dispersal of the invasive Asian chestnut gall wasp, Dryocosmus kuriphilus (Hymenoptera: Cynipidae), across the heterogeneous landscape of the Iberian Peninsula. - Eur. J. Entomol. 115: 575-586. Go to original source...
    29. Goula M., Sesma J.M. & Vivas L. 2013: Photosharing websites may improve Hemiptera biodiversity knowledge and conservation. - ZooKeys 319: 93-105. Go to original source...
    30. Guisan A. & Zimmermann N.E. 2000: Predictive habitat distribution models in ecology. - Ecol. Model. 135: 147-186. Go to original source...
    31. Guisan A., Lehmann A., Ferrier S., Austin M., Overton J.M.C., Aspinall R. & Hastie T. 2006: Making better biogeographical predictions of species' distributions. - J. Appl. Ecol. 43: 386-392. Go to original source...
    32. Güçlü S., Hayat R., Shorthouse J.D. & Tozlu G. 2008: Gall-inducing wasps of the genus Diplolepis (Hymenoptera: Cynipidae) on shrub roses of Turkey. - Proc. Entomol. Soc. Wash. 110: 204-217. Go to original source...
    33. Hastie T.J. & Tibshirani R.J. 1990: Generalized Additive Models. Chapman & Hall, London, 335 pp.
    34. Heiberger R.M. & Holland B. 2015: Statistical Analysis and Data Display: An Intermediate Course with Examples in R (1st and 2nd ed.). Springer Text in statistics. URL: https://cran.r-project.org/web/packages/HH/index.html Go to original source...
    35. Hewitt G.M. 1999: Post-glacial re-colonization of European biota. - Biol. J. Linn. Soc. 68: 87-112. Go to original source...
    36. Hijmans R.J., Cameron S.E., Parra J.L., Jones P.G. & Jarvis A. 2005: Very high resolution interpolated climate surfaces for global land areas. - Int. J. Climatol. 25: 1965-1978. Go to original source...
    37. Hijmans R.J., Phillips S., Leathwick J. & Elith J. 2015: Dismo. Species Distribution Modeling. (R Package Ver. 1.1-1). URL: https://CRAN.R-project.org/package=dismo.
    38. Hoffmeyer E.B. 1925: Remarks on Danish gall wasps. - Entomol. Medd. 16: 1-8 [in Danish].
    39. IGME (Instituto Geográfico y Minero Español) 2020: Lithology Layer. URL: http://info.igme.es/catalogo/catalog.aspx?portal=1&catalog=3&ctt=1⟨=spa&dlang=eng&llt=dropdown&master=infoigme&shdt=false&shfo=false&types=3 (last accessed 6 June 2020).
    40. Jiménez-Valverde A., Peterson A.T., Soberón J., Overton J.M., Aragón P. & Lobo J.M. 2011: Use of niche models in invasive species risk assessments. - Biol. Invas. 13: 2785-2797. Go to original source...
    41. Jiménez-Valverde A., Peña-Aguilera P., Barve V. & Burguillo-Madrid L. 2019: Photo-sharing platforms key for characterising niche and distribution in poorly studied taxa. - Insect Conserv. Divers. 12: 389-403. Go to original source...
    42. Katilmis Y. & Kiyak S. 2010: Distribution, phenology and effects of Diplolepis spp. (Hymenoptera: Cynipidae) on Rosa canina in the Inland Western Anatolian. - J. Entomol. Res. Soc. 12(2): 31-36.
    43. Kohnen A., Wissemann V. & Brandl R. 2011: No host associated differentiation in the gall wasp Diplolepis rosae (Hymenoptera: Cynipidae) on three dog rose species. - Biol. J. Linn. Soc. 102: 369-377. Go to original source...
    44. Koopman W.J.M., Wissemann V., De Cock K., Van Huylenbroeck J., De Riek J., Sabatino G.J.H., Visser D., Vosman B., Ritz C.M., Maes B. et al. 2008: AFLP markers as a tool to reconstruct complex relationships: a case study in Rosa (Rosaceae). - Am. J. Bot. 95: 353-366. Go to original source...
    45. Kutner M.H., Nachtsheim C., Neter J. & Li W. 2004: Applied Linear Regression Models. McGraw Hill, New York, 1396 pp.
    46. László Z. & Tóthmérész B. 2011: Parasitism, phenology and sex ratio in galls of Diplolepis rosae in the Eastern Carpathian Basin. - Entomol. Romanica 16: 33-38.
    47. László Z., Rákosy L. & Tóthmérész B. 2018: The simpler the better: when decreasing landscape complexity increases community stability. - Ecol. Indic. 84: 828-836. Go to original source...
    48. Lázaro e Ibiza B. 1917: Noticias de algunas agallas de España. In Asociación Española para el Progreso de las Ciencias, Congreso de Valladolid, Sección 4, Ciencias Naturales. Imprenta de Fortanet, Madrid, pp. 5-55.
    49. Lin D., Foster D.P. & Ungar L.H. 2011: VIF-Regression: A fast regression algorithm for large data. - J. Am. Stat. Assoc. 493: 232-247. Go to original source...
    50. Looney C. & Eigenbrode S.D. 2010: Landscape-level effects of cynipid component communities of "orphaned" native shrubs. - J. Insect Conserv. 15: 695-706. Go to original source...
    51. Lotfalizadeh H., Rasplus J.Y. & Delvare G. 2006: Rose gall wasps and their associated fauna (Hymenoptera) in Iran. -Redia 89: 73-85.
    52. Markoviæ È. 2015: Contribution to knowledge of the cynipid gall wasp (Hymenoptera: Cynipidae) fauna of Mt. Rtanj (Serbia). - Acta Entomol. Serb. 20: 137-143.
    53. McCullagh P. & Nelder J.A. 1989: Generalized Linear Models. Chapman & Hall, London, 532 pp. Go to original source...
    54. Melika G. 2006: Gall wasps of Ukraine. Cynipidae. - Vestn. Zool. 21: 301-644.
    55. Mete Ö & Demirsoy A. 2012: A preliminary study on the gallwasp fauna of Kemaliye (Erzincan, Turkey) and a new record for Turkey. - Hacettepe J. Biol. Chem. (Suppl.) 2012: 351-363.
    56. Mifsud S. 2016: Rediscovery of a rare gall on Rosa sempervirens induced by Diplolepis eglanteriae (Hartig, 1840) (Hymenoptera, Cynipidae) in Malta. - Bull. Entomol. Soc. Malta 8: 39-45.
    57. Nieves-Aldrey J.L. 1981: Datos sobre Diplolepis rosae (L.) (Hym., Cynipidae) y su fauna de himenópteros parásitos en Salamanca. - Boln. Asoc. Esp. Entomol. 4: 107-113.
    58. Nieves-Aldrey J.L. 1984: Contribución al conocimiento de la fauna de himenópteros inquilinos y parásitos en las agallas de Diplolepis mayri (Schlechtendal) y Diplolepis eglanteriae (Hartig) (Hym., Cynipidae). - Graellsia 39: 93-102.
    59. Nieves-Aldrey J.L. 1985: Notas sobre los Aylaxini (Hym., Cynipidae, Cynipinae) de la Península Ibérica, con descripción de una nueva especie de Isocolus. - Eos 60: 235-250.
    60. Nieves-Aldrey J.L. 1986: La colección de cinípidos gallícolas (Hym., Cynipidae, Cynipinae) del Instituto Español de Entomología. - Graellsia 41: 113-124.
    61. Nieves-Aldrey J.L. 1989: Los cinípidos gallícolas e inquilinos de la Sierra de Guadarrama y zonas adyacentes (Hym., Cynipidae). - Eos 64: 125-163.
    62. Nieves-Aldrey J.L. 1995: Abundancia, diversidad y dinámica temporal de cinípidos en dos hábitats del centro de España (Hymenoptera, Cynipidae). In Avances en Entomología Ibérica: VI Congreso Ibérico de Entomología. Museo Nacional de Ciencias Naturales (CSIC), Universidad Autónoma de Madrid, Madrid, pp. 113-136.
    63. Nieves-Aldrey J.L. 2001a: Fauna Ibérica, Vol. 16, Hymenoptera: Cynipidae. Consejo Superior de Investigaciones Científicas (CSIC), Madrid, 636 pp.
    64. Nieves-Aldrey J.L. 2001b: Nuevos datos faunísticos, corológicos y biológicos sobre los cinípidos del ámbito íbero-balear (Hymenoptera, Cynipidae). - Graellsia 57: 39-72. Go to original source...
    65. Nieves-Aldrey J.L. 2012: Two new herb gall wasps from Spain, including the description of a new species of Aulacidea Ashmead, 1897 (Hymenoptera, Cynipidae, "Aylacini") inducing galls on Serratula nudicaulis L. DC (Asteraceae). - Graellsia 68: 325-339. Go to original source...
    66. Nieves-Aldrey J.L., Gómez J.F., Hernández Nieves M. & Lobo J.M. 2006: Los Cynipidae (Hymenoptera) de la Comunidad de Madrid: lista anotada, mapas de distribución, riqueza y estatus de conservación. - Graellsia 62: 371-403. Go to original source...
    67. O'Brien R.M. 2007: A caution regarding rules of thumb for variance inflation factors. - Qual. Quant. 41: 673-690. Go to original source...
    68. Pérez V. 2013: Bombus (Bombus) terrestris (Linnaeus, 1758) (Hymenoptera: Apidae) introduction in the Magellan region: potential risk for the native bees. - An. Inst. Patagon. 41: 147-152. Go to original source...
    69. Peterson A.T. 2006: Uses and requirements of ecological niche models and related distributional models. - Biodiv. Informatics 3: 59-72. Go to original source...
    70. Peterson A.T., Soberón J., Pearson R.G., Anderson R.P., Martínez-Meyer E., Nakamura M. & Araújo M.B. 2011: Ecological Niches and Geographical Distributions: A Modeling Perspective. Princeton University Press, Princeton, 328 pp. Go to original source...
    71. Phillips S.J. & Dudik M. 2008: Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. - Ecography 31: 161-175. Go to original source...
    72. Phillips S.J., Anderson R.P. & Schapire R.E. 2006: Maximum entropy modelling of species geographic distributions. - Ecol. Model. 190: 231-259. Go to original source...
    73. Plantard O., Shorthouse J.D. & Rasplus J.Y. 1997: Molecular phylogeny of the genus Diplolepis (Hymenoptera: Cynipidae). In Csóka G., Mattson G., Stone W.J. & Price P.W. (eds): The Biology of Gall Inducing Arthropods. USDA Forest Service, North Central Forest Experiment Station, Saint Paul, MN, pp. 247-260.
    74. Prázsmári H., Mátis A. & László Z. 2017: Eurytoma caninae (Hymenoptera: Eurytomidae) in the parasitoid community of unilocular Diplolepis galls in the Carpathian Basin. - Folia Entomol. Hung. 78: 91-96. Go to original source...
    75. Pujade-Villar J. 1983: Algunas consideraciones sobre Diplolepis rosae y Diplolepis mayri (Schlechtendal) en Cataluña (Hymenoptera, Cynipoidea, Cynipidae, Cynipinae). In: Actas del Primer Congreso Ibérico de Entomología, León 2. Servicio de Publicaciones de la Universidad de León, pp. 613-622.
    76. Pujade-Villar J. 1987: Organografía i malalties del cecidi de Diastrophus rubi (Bouché, 1834) Harting, 1840 (Hymenoptera: Cynipoidea) a la tija d'esbarzer, Rubus caesius L. (Rosaceae). - Butll. Inst. Catal. Hist. Nat. 54(6): 65-71 [in Catalan].
    77. Pujade-Villar J. 1991: Contribució al coneixement dels cinípids cecidógens dels arbres i arbusts de Catalunya dels cinípids associats a aquests i dels seus paràsits. PhD thesis, Universidad de Barcelona, Barcelona, 1128 pp. [in Catalan].
    78. Pujade-Villar J. 1993: Revisió de les espècies del gènere Diplolepis de l'Europa centro-occidental (Hym., Cynipidae) amb una especial atenció a la Península Ibérica. - Historia Animalium 2: 57-76 [in Catalan].
    79. Pujade-Villar J. 1996: Zoocecids presents a les fulles de fagàcies andorranes, causats per cinípids (Hym., Cynipidae). - Annals Inst. Estud. Andorrans (Centre de Barcelona) 1994: 79-102 [in Catalan].
    80. Pujade-Villar J., Wang Y., Zhang W., Mata-Casanova N., Lobato-Vila I., Dénes A.L. & László Z. 2020: A new Diplolepis Geoffroy (Hymenoptera, Cynipidae, Diplolepidini) species from China: a rare example of a rose gall-inducer of economic significance. - ZooKeys 904: 131-146. Go to original source...
    81. R Development Core Team 2008: R: A Language and Environment for Statistical Computing R Foundation for Statistical Computing. URL: https://www.r-project.org/ (last accessed Jan. 2018).
    82. Rizzo M.C. & Massa B. 2006: Parasitism and sex ratio of the bedeguar gall wasp Diplolepis rosae (L.) (Hymenoptera: Cynipidae) in Sicily (Italy). - J. Hymenopt. Res. 15: 277-285.
    83. Rodríguez A., Gómez J.F. & Nieves-Aldrey J.L. 2015: Modeling the potential distribution and conservation status of three species of oak gall wasps (Hymenoptera: Cynipidae) in the Iberian range. - J. Insect Conserv. 19: 921-934. Go to original source...
    84. Rokas A., Atkinson R.J., Webster L.M.I., Csöka G. & Stone G.N. 2003: Out of Anatolia: longitudinal gradients in genetic diversity support an eastern origin for a circum-Mediterranean oak gall wasp Andricus quercustozae. - Mol. Ecol. 12: 2153-2174. Go to original source...
    85. Ronquist F. 1999: Phylogeny, classification and evolution of the Cynipoidea. - Zool. Scr. 28: 139-164. Go to original source...
    86. Ronquist F. & Liljeblad J. 2001: Evolution of the gall wasp host plant association. - Evolution 55: 2503-2522. Go to original source...
    87. RStudio Team 2016: RStudio: Integrated Development for R RStudio. URL: https://www.rstudio.com/ (last accessed Jan. 2018).
    88. Sánchez-Vialas A., García-París M., Ruiz J.L. & Recuero E. 2020: Patterns of morphological diversification in giant Berberomeloe blister beetles (Coleoptera: Meloidae) reveal an unexpected taxonomic diversity concordant with mtDNA phylogenetic structure. - Zool. J. Linn. Soc. 20: 1-64. Go to original source...
    89. Scherrer D. & Körner C. 2010: Infra-red thermometry of alpine landscapes challenges climatic warming projections. - Glob. Chang. Biol. 16: 2602-2613. Go to original source...
    90. Scherrer D. & Körner C. 2011: Topographically controlled thermalhabitat differentiation buffers alpine plant diversity against climate warming. - J. Biogeogr. 38: 406-416. Go to original source...
    91. Scherrer D., Schmid S. & Korner C. 2011: Elevational species shifts in a warmer climate are overestimated when based on weather station data. - Int. J. Biometeorol. 55: 645-654. Go to original source...
    92. Schilthuizen M. & Stouthamer R. 1998: Distribution of Wolbachia among the guild associated with the parthenogenetic gall wasp Diplolepis rosae. - Heredity 81: 270-274. Go to original source...
    93. Shorthouse J.D. 1973: The insect community associated with rose galls of Diplolepis polita (Cynipidae, Hymenoptera). -Quaest. Entomol. 9: 55-98.
    94. Shorthouse J.D., Zuchlinski J.A. & Courtin G.M. 1980: Influence of snow cover on the overwintering of three species of gallforming Diplolepis (Hymenoptera: Cynipidae). - Can. Entomol. 112: 225-229. Go to original source...
    95. Shorthouse J.D. & Rohfritsch O. 1992: Biology of Insect-Induced Galls. Oxford University Press, London, 296 pp.
    96. Sømme L. 1964: Effects of glycerol on cold-hardiness in insects. - Can. J. Zool. 42: 87-101. Go to original source...
    97. Stille B. 1984: The effect of host plant and parasitoids on the reproductive success of the parthenogenetic gall wasp Diplolepis rosae (Hymenoptera: Cynipidae). - Oecologia 63: 364-369. Go to original source...
    98. Stille B. 1985: Population genetics of the parthenogenetic gall wasp Diplolepis rosae (Hymenoptera, Cynipidae). - Genetica 67: 145-151. Go to original source...
    99. Stone G.N., Atkinson R., Rokas A., Csóka G. & Nieves-Aldrey J.L. 2001: Differential success in northwards range expansion between ecotypes of the marble gallwasp Andricus kollari: a tale of two lifecycles. - Mol. Ecol. 10: 761-778. Go to original source...
    100. Taberlet P., Fumagalli L., Wust-Saucy A.G. & Cosson J.F. 1998: Comparative phylogeography and postglacial colonization routes in Europe. - Mol. Ecol. 7: 453-464. Go to original source...
    101. Tavares J. da S. 1931a: Cynipidae Peninsulae Ibericae, I. By the author, Lisboa, 5 + 315 pp. [in Portuguese].
    102. Tavares J. da S. 1931b: Cynipidae Peninsulae Ibericae, II. By the author, Lisboa, 4 + 131 pp. [in Portuguese].
    103. Todorov I., Stojanova A., Parvanov D. & Boyadzhiev P. 2012: Studies on the gall community of Diplolepis rosae (Hymenoptera: Cynipidae) in Vitosha Mountain, Bulgaria. - Acta Zool. Bulg. 4: 27-37.
    104. Tomljenovic N. & Pejiæ I. 2018: Taxonomic review of the genus Rosa. - Agric. Conspec. Sci. 83: 139-147.
    105. Ventalló D. 1905: Algunas zoo-cecidias de Tarrassa. - Butll. Inst. Catal. Hist. Nat. 1905(5): 65 [in Catalan].
    106. Vilarrúbia A. 1936: Les zoocecidies de les plantes de Catalunya. - Trevalls Mus. Cienc. Natl. Barcelona 11(10): 1-106 [in Catalan].
    107. Vilarrúbia A. & Vilarrúbia L. 1933: Recull de zoocedies vigatanes. - Butll. Inst. Catal. Hist. Nat. 33: 232-240 [in Catalan].
    108. Vyrzhikovskaya A.V. 1963: New gall wasps (Hymenoptera: Cynipidae) from Dog-rose in Central Asia and Kazakhstan. - Entomol. Obozr. 42: 651-659 [in Russian].
    109. Williams J.B., Shorthouse J.D. & Lee R.R. Jr. 2003: Deleterious effects of mild simulated overwintering temperatures on survival and potential fecundity of rose-galling Diplolepis wasps (Hymenoptera: Cynipidae). - J. Exp. Zool. 298: 23-31. Go to original source...
    110. Wood S.N. 2016: mgcv: Mixed GAM Computation Vehicle with GCV/AIC/REML Smoothness Estimation (R Package Ver. 1.8-12). URL: http://CRAN.R-project.org/package=mgcv
    111. Yan Z.F., Dolstra O., Hendriks T., Prins T.W., Stam P. & Visser P.B. 2005: Vigour evaluation for genetics and breeding in rose. - Euphytica 145: 339-347. Go to original source...
    112. Yee T.W. & Mitchell N.D. 1991: Generalized additive models in plant ecology. - J. Veg. Sci. 2: 587-602. Go to original source...
    113. Zimmermann N.E., Edwards T.C., Graham C.H., Pearman P.B. & Svenning J.C. 2010: New trends in species distribution modeling. - Ecography 33: 985-989. Go to original source...
    114. Zhang D. & Gandelin M.H. 2003: Cultivar identification by image analysis. In Roberts A.V., Debener T. & Gudin S. (eds): Encyclopedia of Rose Science. Vol. 1. Elsevier, London, pp. 124-135. Go to original source...
    115. Zhang Y.M., Lászlo Z., Looney C., Dénes A.L., Hanner R. & Shorthouse J.D. 2019: DNA barcodes reveal inconsistent species boundaries in Diplolepis rose gall wasps and their Periclistus inquilines (Hymenoptera: Cynipidae). - Can. Entomol. 151: 717-727. Go to original source...

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