Arthropod-Plant Interactions

, Volume 13, Issue 3, pp 477–488 | Cite as

Life inside a gall: diversity, phenology and structure of Portuguese gall communities, their hosts, parasitoids and inquilines

  • Francisco A. López-NúñezEmail author
  • Sérgio Ribeiro
  • Hélia Marchante
  • Ruben H. Heleno
  • Elizabete Marchante
Original Paper


Plant galls sustain diverse and complex communities of gallers, parasitoids and inquilines that provide exceptional systems to explore evolutionary, ecological and conservation questions. However, the structure and phenology of such communities are still largely unknown. In order to fill these gaps, we sampled plant galls along the Portuguese coast aiming to (1) characterize the diversity of gall-associated communities (plants, gallers, their parasitoids, and inquilines); (2) evaluate how richness and abundance of gallers are shaped by plant life-form; and (3) explore the phenology (i.e. emergence time) of the different guilds. For 1 year, we collected 31,737 galls from 33 plant species, revealing remarkably diverse communities centred on 49 gallers, 65 parasitoids and 88 inquiline species. The plant families with more galls were Fabaceae, Fagaceae and Cistaceae, while most gallers were Cynipidae and Cecidomyiidae. Regarding parasitoids, Torymidae and Eulophidae were the richest families, and most inquilines belonged to the families Cecidomyiidae, Thripidae, Aphidiidae and Psocoptera. Shrubs hosted a significantly greater abundance and richness of gallers. Overall community composition was highly variable in time, frequently with turnover rates greater than 50% between consecutive months. An asynchrony between life cycles of each guild could be explained by the sequential availability of resources for gallers and parasitoids and by the relaxed physiological constraints between galls and inquilines. This baseline information is vital for revealing a hidden component of biodiversity and shedding light on its community structure and resilience.


Gall-inducing insects Iberia Multitrophic relationships Parasitoids Inquilines Hidden biodiversity 



We are grateful for the commitment of many dedicated field personnel: P. Castro, S. Carvalho, L. Barrico, N. César de Sá, J. Cerca, J. Costa, A. Martins, D. Alves, E. Almeida and D. Barros-García; and the professional taxonomist consulted for arthropods identification, including N. Dorchin, L. Friedman, L. Crespo, J.L. Grosso-Silva, M. Alonso-Zarazaga, F. Di Giovanni, G. Broad, A. Polaszek, H. Vardal, A. Franquinho Aguiar, F. Chichorro, C. Prado e Castro, A. M. Ortega, A. R. Gonçalves, and the involved institutions such as Natural History Museum of London and National Research College of Veterinary and Agronomy of Portugal. RHH was funded by grant IF/00441/2013 of the Portuguese Foundation for Science and Technology (FCT). This research and FLN were supported by FCT and COMPETE/FEDER, through project “INVADER-B–INVAsive plant species management in Portugal: from early Detection to Remote sensing and Biocontrol of Acacia longifolia” (PTDC/AAGREC/4896/2014).

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11829_2018_9655_MOESM1_ESM.docx (430 kb)
Online Resource 1 (DOCX 430 KB)
11829_2018_9655_MOESM2_ESM.docx (107 kb)
Online Resource 2 (DOCX 107 KB)


  1. Aebi A, Schönrogge K, Melika G, Quacchia A, Alma A, Stone GN (2007) Native and introduced parasitoids attacking the invasive chestnut gall wasp Dryocosmus kuriphilus. EPPO Bull 37:166–171CrossRefGoogle Scholar
  2. Amrine JW, Stasny TA (1994) Catalog of the Eriophyoidea (Acarina: Prostigmata) of the World. Indira Publishing House, West BloomfieldGoogle Scholar
  3. Ananthakrishnan TN (1998) Insect gall systems: patterns, processes and adaptive diversity. Curr Sci 75:672–676Google Scholar
  4. Askew RR (1961) A study of the biology of species of the genus Mesopolobus (Hymenoptera: Pteromalidae) associated with cynipid galls on oaks. Trans R Entomol Soc Lond 113:155–173CrossRefGoogle Scholar
  5. Askew RR, Plantard O, Gómez JF, Nieves MH, Nieves-Aldrey JL (2006) Catalogue of parasitoids and inquilines in galls of aylacini, diplolepidini and pediaspidini (Hym., Cynipidae) in West Palearctic. Zootaxa 1301:1–60Google Scholar
  6. Askew RR, Melika G, Pujade-Villar J, Schönrogge K, Stone GN, Nieves-Aldrey JL (2013) Catalogue of parasitoids and inquilines in cynipid oak galls in the Western Palaearctic. Zootaxa 3643(1):1–133CrossRefGoogle Scholar
  7. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using {lme4}. J Stat Softw 67:1–48CrossRefGoogle Scholar
  8. Begon M, Harper JL, Townsend CR (1999) Ecología: individuos, poblaciones y comunidades. Omega, BarcelonaGoogle Scholar
  9. Bellido D, Pujade-Villar J (1999) Aproximació al coneixement de la biogeografia de la tribu Cynipini (Hymenoptera: Cynipoidea: Cynipidae) a la Regió Paleàrtica. Ses entom ICHN-SCL 11:67–79Google Scholar
  10. Bingre P, Aguiar C, Espírito-Santo D, Arsénio P, Monteiro-Henriques T (2007) Guia de campo: árvores e arbustos de Portugal Continental. Fundação Luso-Americana para o Desenvolvimento/ Liga para a Protecção da Natureza, Jornal Público, LisboaGoogle Scholar
  11. Blanche R (2012) Life in a gall: the biology and ecology of insects that live in plant galls. CSIRO Publishing, CollingwoodCrossRefGoogle Scholar
  12. Branco M, Franco JC, Valente C, Mendel Z (2006) Survey of Eucalyptus gall wasps (Hymenoptera: Eulophidae) in Portugal. Boletin Sanidad Plagas Vegetales 32:199–202Google Scholar
  13. Branco M, Boavida C, Durand N, Franco JC, Mendel Z (2009) Presence of the Eucalyptus gall wasp Ophelimus maskelli and its parasitoid Closterocerus chamaeleon in Portugal: first record, geographic distribution and host preference. Phytoparasitica 37:51–54CrossRefGoogle Scholar
  14. Brian MV (2012) Social insects: ecology and behavioural biology Springer, BerlinGoogle Scholar
  15. Brooks SE, Shorthouse JD (1998) Developmental morphology of stem galls of Diplolepis nodulosa (Hymenoptera:Cynipidae) and those modified by the inquiline Periclistus pirata (Hymenoptera:Cynipidae) on Rosa blanda (Rosaceae). Can J Bot 76(3):365–381Google Scholar
  16. Brussino G, Bosio G, Baudino M, Giordano R, Ramello F, Melika G (2002) Pericoloso insetto esotico per il castagno europeo. L’Informatore Agrario 37:59–62Google Scholar
  17. Bunnefeld L, Hearn J, Stone GN, Lohse K (2018) Whole-genome data reveal the complex history of a diverse ecological community. PNAS 115:E6507–E6515CrossRefGoogle Scholar
  18. Chinery M (2013) Britain’s plant galls: a photographic guide. Princeton University Press, HampshireCrossRefGoogle Scholar
  19. Collins S, Suding KN, Cleland EE, Batty M, Pennings SC, Gross KL, Grace JB, Gough L, Fargione JE, Clark CM (2008) Rank clocks and plant community dynamics. Ecology 89:3534–3541CrossRefGoogle Scholar
  20. Copping LG (2009) The manual of biocontrol agents: a World compendium. Ed. 4. British Crop Production Council, LondonGoogle Scholar
  21. Csóka G, Stone GN, Melika G (2005) The biology, ecology and evolution of gall wasps. In: Raman A, Schaeffer CW, Withers TM. Biology, ecology and evolution of gall-inducing arthropods. Science Publishers Inc., Enfield. pp 573–642Google Scholar
  22. Csóka G, Stone N, Melika GG (2017) Non-native gall-inducing insects on forest trees: a global review. Biol Invasions 19:3161–3181CrossRefGoogle Scholar
  23. Cuevas-Reyes P, Quesada M, Hanson P, Dirzo R, Oyama K (2004) Diversity of gall-inducing insects in a Mexican tropical dry forest: the importance of plant species richness, life-forms, host plant age and plant density. J Ecol 92:707–716CrossRefGoogle Scholar
  24. Dorchin N, Hoffmann JH, Stirk WA, Novák O, Strnad M, Van Staden J (2009) Sexually dimorphic gall structures correspond to differential phytohormone contents in male and female wasp larvae. Physiol Entomol 34:359–369CrossRefGoogle Scholar
  25. EPPO Reporting Service no. 06-2014; Num. article: 2014/103, First report of Dryocosmus kuriphilus in Portugal Google Scholar
  26. Fernandes GW, Price PW (1992) The adaptive significance of insect gall distribution: survivorship of species in xeric and mesic habitats. Oecologia 90:14–20CrossRefGoogle Scholar
  27. Fisher RA, Corbet AS, Williams CB (1943) The relation between the number of species and the number of individuals in a random sample of an animal population. J Anim Ecol 12:42–58CrossRefGoogle Scholar
  28. Fisher TW, Bellows TS, Caltagirone LE, Dahlsten DL, Huffaker CB, Gordh G (1999) Handbook of biological control: principles and applications of biological control. Elsevier, New YorkGoogle Scholar
  29. Franco JA (1971) Nova Flora de Portugal Continental (Continente e Açores), (Licopodiaceae–Umbelliferae). Vol. I LisboaGoogle Scholar
  30. Franco JA (1984) Nova Flora de Portugal Continental (Continente e Açores), (Clethraceae–Compositae). Vol. II, LisboaGoogle Scholar
  31. Franco JA, Rocha Afonso M (1994) Nova Flora de Portugal (Continente e Açores), vol.III (fascículo I), Alismataceae–Iridaceae. Escolar Editora, LisboaGoogle Scholar
  32. Franco JA, Rocha Afonso M (1998) Nova Flora de Portugal (Continente e Açores), vol.III (fascículo II), GRAMINEAE. Escolar Editora, LisboaGoogle Scholar
  33. Franco JA, Rocha Afonso M (2003) Nova Flora de Portugal (Continente e Açores), vol.III (fascículo III), JUNCACEAE–ORCHIDACEAE. Escolar Editora, LisboaGoogle Scholar
  34. Garbin L, Díaz N, Pujade-Villar J (2008) Experimental study of the reproductive cycle of Plagiotrochus amenti Kieffer, 1901 (Hymenoptera, Cynipoidea, Cynipidae), with comments on tis taxonomy. Boletin Asociación Española de Entomología 32:341–349Google Scholar
  35. Giron D, Huguet E, Stone GN, Body M (2016) Insect-induced effects on plants and possible effectors used by galling and leaf-mining insects to manipulate their host-plant. J Insect Physiol 84:70–89CrossRefGoogle Scholar
  36. Goulet H, Huber J (1993) Hymenoptera of the World: an Identification guide to families 1. In: Goulet H, Huber J (eds), Ottawa: Agriculture Canada. Research BranchGoogle Scholar
  37. Grissell EE (1995) Toryminae (Hymenoptera: Chalcidoidea: Torymidae): a redefinition, generic classification, and annotated world catalog of species. vol 2. Associated Publishers, Washington, DCGoogle Scholar
  38. Hallett L, Jones SK, MacDonald AA, Flynn DFB, Slaughter P, Ripplinger J, Collins SL, Gries CJ, Matthew B (2016) {codyn}: Community Dynamics Metrics. Accessed 23 July 2016
  39. Hawkins BA, Goeden RD (1984) Organization of a parasitoid community associated with a complex of galls on Atriplex spp. in southern California. Ecol Entomol 9:271–292CrossRefGoogle Scholar
  40. Hayward A, Stone GN (2005) Oak gall wasp communities: evolution and ecology. Basic Appl Ecol 6:435–443CrossRefGoogle Scholar
  41. Heslenfeld P, Jungerius PD, Klijn JA (2004) European coastal dunes: Ecological values, threats, opportunities and policy development. In: Martínez ML, Psuty NP (eds) Coastal dunes: ecology and conservation. Springer, Berlin, pp 335–351Google Scholar
  42. Hewitt GM (2011) Mediterranean peninsulas: the evolution of hotspots. In: Zachos FE, Habel JC (eds) Biodiversity hotspots: distribution and protection of conservation priority areas. Springer, Berlin, pp 123–147CrossRefGoogle Scholar
  43. Hoffmann JH, Impson FAC, Moran VC, Donnelly D (2002) Biological control of invasive golden wattle trees (Acacia pycnantha) by a gall wasp, Trichilogaster sp. (Hymenoptera:Pteromalidae), in South Africa. Biolog Control 25:64–73CrossRefGoogle Scholar
  44. Holt RD, Lawton JH (1993) Apparent competition and enemy-free space in insect host-parasitoid communities. Am Nat 142:623–645CrossRefGoogle Scholar
  45. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical J 50:346–363CrossRefGoogle Scholar
  46. Impson FAC, Kleinjan CA, Hoffmann JH, Post JA (2008) Dasineura rubiformis (Diptera:Cecidomyiidae), a new biological control agent for Acacia mearnsii in South Africa. S Afr J Sci 104:247–250Google Scholar
  47. Inácio ML, Naves P, Moreira M, Sousa EM (2002) Gall inducing insects associated with oak trees (Quercus spp.) in Portugal. Integrated Protect Oak Forests IOBC/wprs Bull 25:159–162Google Scholar
  48. Joseph MB, Gentles M, Pearse IS (2011) The parasitoid community of Andricus quercuscalifornicus and its association with gall size, phenology, and location. Biodivers Conserv 20:203–216CrossRefGoogle Scholar
  49. Jürgen Buhr H (2012) Webseite der Fotogalerie Pflanzengallen. Accessed 1 Jan 2014
  50. Kaartinen R, Stone GN, Hearn J et al (2010) Revealing secret liaisons: DNA barcoding changes our understanding of food webs. Ecol Entomol 35:623–638CrossRefGoogle Scholar
  51. László Z, Tóthmérész B (2006) Inquiline effects on a multilocular gall community. Acta Zool Academiae Sci Hungaricae 52:373–383Google Scholar
  52. Lawton JH (1983) Plant architecture and the diversity of phytophagous insects. Annu Rev Entomol 28:23–39CrossRefGoogle Scholar
  53. López-Núñez FA, Heleno RH, Ribeiro S, Marchante H, Marchante E (2017) Four-trophic level food webs reveal the cascading impacts of an invasive plant targeted for biocontrol. Ecology 98:782–793CrossRefGoogle Scholar
  54. Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. Bioscience 56:311CrossRefGoogle Scholar
  55. Marchante H, López-Núñez FA, Freitas H, Hoffmann JH, Impson FAC, Marchante E (2017) First report of the establishment of the biocontrol agent Trichilogaster acaciaelongifoliae for control of invasive Acacia longifolia in Portugal. EPPO Bull Scholar
  56. Moran PJ, Goolsby JA (2009) Biology of the galling wasp Tetramesa romana, a biological control agent of giant reed. Biol Control 49:169–179CrossRefGoogle Scholar
  57. Nafría JMN, Durante MPM (2002) Hemiptera: aphididae II. Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Científicas, MadridGoogle Scholar
  58. Nieves-Aldrey JL (2001a) Fauna Iberica: 16: Hymenoptera:Cynipidae. Consejo Superior de Investigaciones Científicas, MadridGoogle Scholar
  59. Nieves-Aldrey JL (2001b) Nuevos datos faunísticos, corológicos y biológicos sobre los cinípidos del ámbito Íbero-Balear. Graellsia 57:39–72CrossRefGoogle Scholar
  60. Nieves-Aldrey JL, Askew RR (2002) Calcidoideos (Hym., Chalcidoidea) asociados a agallas de Aylacini y Diplolepidini (Hym., Cynipidae) en España. Boletin Asociación Española de Entomología 26:11–37Google Scholar
  61. Noyes JS (2016) Universal Chalcidoidea Database. World Wide Web electronic publication. Accessed 1 Jan 2016
  62. Ogle DH (2016) FSA: Fisheries Stock Analysis. R package version 0.8.11. Accessed 23 July 2016
  63. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H (2013) vegan: Community ecology package. Accessed 23 July 2016
  64. Paniagua MR, Medianero E, Lewis OT (2009) Structure and vertical stratification of plant galler-parasitoid food webs in two tropical forests. Ecol Entomol 34:310–320CrossRefGoogle Scholar
  65. Preston FW (1948) The commonness, and rarity, of species. Ecology 29:254–283CrossRefGoogle Scholar
  66. Price PW, Fernandes GW, Lara ACF, Brawn J, Barrios H, Wright MG, Ribeiro SP, Rothcliff N (1998) Global patterns in local number of insect galling species. J Biogeogr 25:581–591CrossRefGoogle Scholar
  67. Pujade-Villar J, Ros-Farré P (1998) Inquilinos y parasitoides de las agallas del género Plagiotrochus Mayr colectadas en el Nordeste de la Península Ibérica. Boletin Asociación Española de Entomología 22:115–143Google Scholar
  68. Quacchia A, Ferracini C, Nicholls JA, Piazza E, Saladini MA, Tota F, Melika G, Alma A (2013) Chalcid parasitoid community associated with the invading pest Dryocosmus kuriphilus in north-western Italy. Insect Conserv Diver 6:114–123CrossRefGoogle Scholar
  69. R Development Core Team (2011) R: A Language and environment for statistical computing, Vienna, Austria: the R Foundation for Statistical Computing. Accessed 24 July 2011
  70. Redfern M (2011) Plant galls, 1st edn. Harper Collins Publishers, LondonGoogle Scholar
  71. Redfern M, Shirley P (2002) British plant galls. Identification of galls on plants and fungi, 2nd edn. Field Studies Council Publication, LondonGoogle Scholar
  72. Redfern M, Shirley P (2011) British plant galls 2nd ed., Field Studies Council Publication, LondonGoogle Scholar
  73. Ronquist F, Liljeblad J (2001) Evolution of the gall wasp-host plant association. Evolution 55:2503–2522Google Scholar
  74. Ronquist F, Nieves-Aldrey JL, Buffington ML, Liu Z, Liljeblad J, Nylander JAA (2015) Phylogeny, evolution and classification of gall wasps: the plot thickens. PLOS ONE 10:1–40CrossRefGoogle Scholar
  75. Ros-Farré P, Pujade-Villar J (1998) Estudio mediante una trampa Malaise de la comunidad de cinipidos cecidógenos e inquilinos de Santa Coloma, Andorra (Hymenoptera, Cynipidae). Ecologia 12:441–454Google Scholar
  76. Russo R (2006) Field guide to plant galls of California and other Western states. University of California Press, OaklandGoogle Scholar
  77. Sanver D, Hawkins BA (2000) Galls as habitats: the inquiline communities of insect galls. Basic Appl Ecol 1:3–11CrossRefGoogle Scholar
  78. Shorthouse JD (1998) Role of Periclistus (Hymenoptera:Cynipidae) inquilines in leaf galls of Diplolepis (Hymenoptera:Cynipidae) on wild roses in Canada. In G. Csóka, W. J. Mattson, G. N. Stone, & P. W. Price (Eds.). The biology of gall-inducing arthropods. US Department of Agriculture Forest Service. Technical Report NC-199, St.Paul, pp. 61–81Google Scholar
  79. Skuhravá M, Skuhravý V (2009) Species richness of gall midges (Diptera:Cecidomyiidae) in Europe (West Palaearctic): biogeography and coevolution with host plants. Acta Soc Zool Bohem 73:87–156Google Scholar
  80. Skuhravá M, Skuhravy V, Pujade-Villar J (1996) Gall midges (Díptera:Cecidomyiidae) of the Iberian Península. Boletin Asociación Española de Entomología 20:41–61Google Scholar
  81. Skuhravá M, Skuhravý V, Blasco-Zumeta J, Pujade-Villar J (2006) Gall midges (Diptera:Cecidomyiidae) of the Iberian Peninsula 2. Zoogeographical analysis of the gall midge fauna. Boletín Asociacion Española de Entomologia 30:93–159Google Scholar
  82. Skuhravý V, Hrubík P, Skuhravá M, Pozgaj J (1998) Occurrence of insects associated with nine Quercus species (Fagaceae) in cultured plantations in southern Slovakia during 1987–1992. J Appl Entomol 122:149–155CrossRefGoogle Scholar
  83. Stone GN, Cook JM (1998) The structure of cynipid oak galls: patterns in the evolution of an extended phenotype. Proc R Soc B 265: 979–988CrossRefGoogle Scholar
  84. Stone GN, Schönrogge K, Rachel J et al (2002) The population biology of oak gall wasps (Hymenoptera:Cynipidae). Annu Rev Entomol 47:633–668CrossRefGoogle Scholar
  85. Tavares JS (1900) As zoocecidias portuguezas. Ann Sci Nat 8:15–108Google Scholar
  86. Tavares JS (1902) As zoocecidias portuguezas. Addenda. Com a descripção de quinze especies cecidogenicas novas. Broteria 1:3–49Google Scholar
  87. Tavares JS (1905) Synopse das zoocecidias portuguezas. Broteria 4:4–122Google Scholar
  88. Tavares JS (1907) Primeiro appendice á Synopse das zoocecidias portuguezas. Broteria 6:109–134Google Scholar
  89. Veldtman R, McGeoch MA (2003) Gall-forming insect species richness along a non-scleromorphic vegetation rainfall gradient in South Africa: the importance of plant community composition. Austral Ecol 28:1–13CrossRefGoogle Scholar
  90. Veldtman R, Lado TF, Botes A, Procheş Ş, Timm AE, Geertsema H, Chown SL (2011) Creating novel food webs on introduced Australian acacias: indirect effects of galling biological control agents. Divers Distrib 17:958–967CrossRefGoogle Scholar
  91. Whittaker RH (1965) Dominance and diversity in land plant communities. Science 147:250–260CrossRefGoogle Scholar
  92. Wilson EO (1987) The little things that run the World (the importance and conservation of invertebrates). Conserv Biol 1:344–346CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Centre for Functional Ecology, Department of Life SciencesUniversity of CoimbraCoimbraPortugal
  2. 2.Escola Superior AgráriaInstituto Politécnico de Coimbra. BencantaCoimbraPortugal

Personalised recommendations