, Volume 18, Issue 1, pp 71–83 | Cite as

Larval development and growth ratios of Odonata of the Azores

  • Lucas Lamelas-LópezEmail author
  • Margarita Florencio
  • Paulo A. V. Borges
  • Adolfo Cordero-Rivera
Research paper


To fully understand odonate life cycles, it is vital to analyse the patterns of larval growth, which are tightly associated with variations in environmental factors. However, the identification of larval instars is often difficult, especially for early development stages. We hypothesise that pond hydroperiod influences odonate larval growth, and test this idea with novel information about the environmental characteristics of 12 study ponds in Terceira Island (Azores). This study, which represents the first analysis of larval development of Odonata in the Azores, involved determining the instars of development and growth ratios. We measured the morphological characteristics of 898 Odonata larvae, and found that they significantly differed between temporary and permanent ponds. To estimate the larval instars, we used two methods: frequency distribution methods and correlation diagrams between body characteristics. The first method was the most effective, allowing the estimation of 17 instars for Anax imperator, 13 for Sympetrum fonscolombii and 10 for Ischnura hastata, as well as growth ratios between instars for head width, total length, abdomen length, wings and antenna length. Our results also suggest that a combination of the two methods is the most appropriate strategy for estimating the number of instars and growth ratios during larval development.


Odonata Oceanic islands Larval development Growth ratio Aquatic ecosystems 



We are grateful to Olalla Lorenzo-Carballa for the taxonomical identification of larvae in the laboratory and for her support and comments, and to Laura Serrano for the analyses of the total phosphorus concentration in the water column. We are also grateful to Jose Sarangollo, Ana Gómez, David Rodilla, María Olivo, Herlander Lima, Rui Carvalho, Lucía Lamelas, Luis Ansias, Paco Gutiérrez and Raquel Daza for their assistance with the fieldwork. This research was partially funded by the project CGL2011-22629, the Spanish Ministry of Economy and Competitiveness (including FEDER funds), and by the Fundación Barrié (for the academic fellowship awarded to LLL). MF’s current grant was funded by the Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq (401045/2014-5), program Ciência sem Fronteiras.

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  1. Aoki T (1999) Larval development, emergence and seasonal regulation in Asiagomphus pryeri (Selys) (Odonata: Gomphidae). Hydrobiologia 394:179–192. doi: 10.1023/A:1003626011117
  2. Askew RR (1988) The dragonflies of Europe. Harley, EssexGoogle Scholar
  3. Bick GH (1951) The early nymphal stages of Tramea lacerata Hagen (Odonata: libellulidae). Entomol News 52:293–303Google Scholar
  4. Cazado LE, Van Nieuwenhove GA, O’brien CW, Gastaminza GA, Murúa MG (2014) Determination of number of instars of Rhyssomatus subtilis (Coleoptera: curculionidae) based on head capsule widths. Fla Entomol 97(2):639–643. doi: 10.1653/024.097.0241 CrossRefGoogle Scholar
  5. Cham S (2007) Field guide to the larvae and exuviae of British dragonflies. British Dragonfly Society, WhittleseyGoogle Scholar
  6. Cheriak L (1993) Etude de la reproduction et du développement des odonates du Lac Bleu. Magister thesis. Université de Constantine, ConstantineGoogle Scholar
  7. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. primer-E, PlymouthGoogle Scholar
  8. Corbet PS (1955) The immature stages of the emperor dragonfly, Anax imperator Leach (Odonata: Aeshnidae). Entomol Gaz 6:189–204Google Scholar
  9. Corbet PS (1957) The life-history of the emperor dragonfly Anax imperator Leach (Odonata: Aeshnidae). J Anim Ecol. doi: 10.2307/1781
  10. Corbet PS (1999) Dragonflies: behaviour and ecology of Odonata. Harley, Colchester Google Scholar
  11. Corbet PS (2002) Stadia and growth ratios of Odonata: a review. Int J Odonatol 5(1):45–73. doi: 10.1080/13887890.2002.9748176 CrossRefGoogle Scholar
  12. Corbet PS, Suhling F, Soendgerath D (2006) Voltinism of Odonata: a review. Int J Odonatol 9(1):1–44. doi: 10.1080/13887890.2006.9748261 CrossRefGoogle Scholar
  13. Cordero Rivera A (1987) Estructura de población en Ischnura graellsii Rambur, 1842 (Zygop. Coenagrionidae). Bol Asoc Esp Entomol 11:269–286Google Scholar
  14. Cordero-Rivera A, Lorenzo-Carballa MO, Utzeri C, Vieira V (2005) Parthenogenetic Ischnura hastata (say), widespread in the Azores (Zygoptera: coenagrionidae). Odonatologica 34(1):11–26Google Scholar
  15. Córdoba-Aguilar A (2008) Dragonflies and damselflies: model organisms for ecological and evolutionary research. Oxford University Press, Oxford. doi: 10.1653/024.094.0350 CrossRefGoogle Scholar
  16. Daly HV (1985) Insect morphometrics. Annu Rev Entomol 30(1):415–438. doi: 10.1146/annurev.en.30.010185.002215 CrossRefGoogle Scholar
  17. Delbac L, Lecharpentier P, Thiery D (2010) Larval instars determination for the European grapevine moth (Lepidoptera: tortricidae) based on the frequency distribution of head-capsule widths. Crop Protect 29(6):623–630. doi: 10.1016/j.cropro.2010.01.009 CrossRefGoogle Scholar
  18. Di Giovanni MV, Goretti E, La Porta G, Ceccagnoli D (2000) Larval development of Libellula depressa (Odonata, Libellulidae) from pools in central Italy. Ital J Zool 67(4):343–348. doi: 10.1080/11250000009356337 CrossRefGoogle Scholar
  19. Dyar HG (1890) The number of molts of lepidopterous larvae. Psyche J Entomol 5(175–176):420–422. doi: 10.1155/1890/23871 CrossRefGoogle Scholar
  20. Ecole CC, Dos Anjos N, Michereff-Filho M, Picanço MC (2008) Determinação do número de ínstares larvais em Plutella xylostella (L.) (Lepidoptera: yponomeutidae). Acta Scientiarum Biol Sci 21:331–335. doi: 10.4025/actascibiolsci.v21i0.4447 Google Scholar
  21. Ferreras-Romero M (1997) The life history of Boyeria irene (Fonscolombe, 1838)(Odonata: aeshnidae) in the Sierra Morena mountains (southern Spain). Hydrobiologia 345(2–3):109–116. doi: 10.1023/A:1002967220090 CrossRefGoogle Scholar
  22. Fink TJ (1984) Errors in instar determination of mayflies (Ephemeroptera) and stoneflies (Plecoptera) using the simple frequency, Janetschek, Cassie and Dyar’s law methods. Freshw Biol 14(4):347–365. doi: 10.1111/j.1365-2427.1984.tb00159.x CrossRefGoogle Scholar
  23. Fleck G, Brenk M, Misof B (2006) DNA taxonomy and the identification of immature insect stages: the true larva of Tauriphila argo (Hagen 1869) (Odonata: Anisoptera: Libellulidae). Ann Soc Entomol Fr 42:91–98. doi: 10.1080/00379271.2006.10697453
  24. Gardner AE (1951) The life-history of Sympetrum fonscolombii Selys Odonata-Libellulidae. Entomol Gaz 2:56–66Google Scholar
  25. Gerlach J, Samways MJ, Hochkirch A, Seddon M, Cardoso P, Clausnitzer V, Cumberlidge N, Daniel BA, Black SH, Ott J, Williams PH (2015) Prioritizing non-marine invertebrate taxa for red listing. J Insect Conserv 18:573–586. doi: 10.1007/s10841-014-9660-6 CrossRefGoogle Scholar
  26. Golterman HL (2004) The chemistry of phosphate and nitrogen compounds in sediments. Kluwer, DordrechtGoogle Scholar
  27. Goretti E, Ceccagnoli D, La Porta G, Di Giovanni MV (2001) Larval development of Aeshna cyanea (Müller, 1764) (Odonata: aeshnidae) in Central Italy. Hydrobiologia 457(1–3):149–154. doi: 10.1023/A:1012227400613 CrossRefGoogle Scholar
  28. Hassal C (2015) Odonata as candidate macroecological barometers for global climate change. Freshw Sci 34:1040–1049. doi: 10.1086/682210 CrossRefGoogle Scholar
  29. Hawking JH, New TR (1996) The development of dragonfly larvae (Odonata: Anisoptera) from two streams in north-eastern Victoria Australia. Hydrobiologia 317(1):13–30. doi: 10.1007/BF00013722
  30. Jacquemin G (1987) Les odonates de la Merja de Sidi Bou Ghaba (Mehdiya, Maroc). Bull Inst Sci 11:175–183Google Scholar
  31. Jödicke R (2003) Mid-winter occurrence of dragonflies in southern Tunisia (Insecta: Odonata). Kaupia 12:119–128Google Scholar
  32. Johansson F (2003) Latitudinal shifts in body size of Enallagma cyathigerum (Odonata). J Biogeogr 30:29–34CrossRefGoogle Scholar
  33. Kalkman VJ, Boudot JP, Bernard R, Conze KJ, Knijf GD, Dyatlova E, Ferreira S, Jović M, Ott J, Riservato E, Sahlén G (2010) European Red List of dragonflies. Publications Office of the European Union, LuxembourgGoogle Scholar
  34. Logan JA, Bentz BJ, Vandygriff JC, Turner DL (1998) General program for determining instar distributions from headcapsule widths: example analysis of mountain pine beetle (Coleoptera: Scolytide) data. Environ Entomol 27(3):555–563. doi: 10.1093/ee/27.3.555
  35. Lorenzo-Carballa MO, Cordero-Rivera A (2014) Odonates. In: Vargas P, Zardoya R (eds) The tree of life. Sinauer, Sunderland, pp 352–363Google Scholar
  36. Lorenzo-Carballa MO, Beatty CD, Utzeri C, Vieira V, Cordero-Rivera A (2009) Parthenogenetic Ischnura hastata revisited: present status and notes on population ecology and behaviour (Odonata: Coenagrionidae). Int J Odonatol 12(2):395–411. doi: 10.1080/13887890.2009.9748353
  37. Lorenzo-Carballa MO, Beatty CD, Haitlinger R, Valdecasas AG, Utzeri C, Vieira V, Cordero-Rivera A (2011) Larval aquatic and terrestrial mites infesting parthenogenetic Ischnura hastata (Odonata: Coenagrionidae) from the Azores islands. Exp Appl Acarol 54(3):225–241. doi: 10.1007/s10493-011-9437-5
  38. Nicolai P, Carchini G (1985) A note on the life cycle features in two perennial pond coenagrionid associations (Zygoptera). Not Odonatol 2:89–93Google Scholar
  39. Panzavolta T (2007) Instar determination for Pissodes castaneus (Coleoptera: Curculionidae) using head capsule widths and lengths. Environ Entomol 36(5):1054–1058. doi:10.1603/0046-225X(2007)36[1054:IDFPCC]2.0.CO;2Google Scholar
  40. Richardi VS, Rebechi D, Aranha JM, Navarro-Silva MA (2013) Determination of larval instars in Chironomus sancticaroli (Diptera: Chironomidae) using novel head capsule structures. Zoologia (Curitiba) 30(2):211–216. doi: 10.1590/S1984-46702013000200011
  41. Robert PA (1958) Les Libellules (Odonates) Delachaux et Niestlé. Neuchâtel, ParisGoogle Scholar
  42. Rowe RJ (1991) Larval development and emergence in Hemianax papuensis (Burmeister) (Odonata: Aeshnidae). Aust J Entomol 30(3):209–215. doi: 10.1111/j.1440-6055.1991.tb00413.x
  43. Schaller FE (1959) Etude du développement post-embryonnaire d’Aeschna cyanea Müll. Doctoral dissertation. Université de Strasbourg, StrasbourgGoogle Scholar
  44. Schnapauff I, Ullmann K, Suhling F (2000) Die Libellen-Lebensgemeinschaft griechischer Reisfelder: auswirkungen von Habitatdauer, Anbaumethode und Vegetationsdichte. Libellula 3:63–80Google Scholar
  45. Schütte C, Schridde P, Suhling F (1998) Life history patterns of Onychogomphus uncatus (Charpentier) (Anisoptera: Gomphidae). Odonatologica 27(1):71–86Google Scholar
  46. Silva DD, Kaminski LA, Dell’Erba R, Moreira GR (2008) Morfologia externa dos estágios imaturos de heliconíneos neotropicais: VII. Dryadula phaetusa (Linnaeus) (Lepidoptera, Nymphalidae, Heliconiinae). Rev Bras Entomol 52(4):500–509. doi: 10.1590/S0085-56262008000400003
  47. Skuhrovec J (2006) Identification of instars of Hypera postica using chaetotaxy. J Econ Entomol 99(6):2216–2218. doi: 10.1603/0022-0493-99.6.2216 CrossRefPubMedGoogle Scholar
  48. Suhling F, Schenk K, Padeffke T, Martens A (2004) A field study of larval development in a dragonfly assemblage in African desert ponds (Odonata). Hydrobiologia 528(1–3):75–85. doi: 10.1007/s10750-004-3047-8 CrossRefGoogle Scholar
  49. Suhling F, Sahlén G, Kasperski J, Gaedecke D (2005) Behavioural and life history traits in temporary and perennial waters: comparisons among three pairs of sibling dragonfly species. Oikos 108(3):609–617. doi: 10.1111/j.0030-1299.2005.13230.x CrossRefGoogle Scholar
  50. Suhling F, Sahlén G, Gorb S, Kalkman VJ, Dijkstra KDB, van Tol J (2015) Order Odonata. In: Thorp J, Rogers DC (eds) Ecology and general biology: Thorp and Covich’s freshwater invertebrates. Academic, London, pp 893–932. doi:  10.1016/B978-0-12-385026-3.00035-8
  51. Velásquez N, Bautista K, Guevara M, Ramirez D, Realpe E, Pérez-Gutiérrez LA (2009) Larval development and growth ratio in Ischnura cruzi De Marmels, with description of last larval instar (Zygoptera: Coenagrionidae). Odonatologica 38(1):29–38Google Scholar
  52. Vieira V, Cordero-Rivera A (2015) First record of Pantala flavescens from the Azores (Odonata: Libellulidae). Odonatologica 44:1–9Google Scholar
  53. Vieira V, Cordero-Rivera A (2016) As Libélulas dos Açores e Madeira. Amigos dos Açores-Associação Ecológica, São Miguel Google Scholar
  54. Williams DD (2006) The biology of temporary waters. Oxford University Press, OxfordGoogle Scholar
  55. Winterbourn MJ, Pohe SR (2013) Life histories of four dragonfly species (Odonata: Anisoptera) in northern New Zealand. N Z Entomol 36(1):8–14. doi: 10.1080/00779962.2012.752225
  56. Winterbourn MJ, Pohe SR, Ball OP (2011) Establishment of larval populations of the dragonfly Tramea loewii Kaup, 1866 (Odonata: Libellulidae) in lakes of northern New Zealand. N Z J Zool 38(2):173–179. doi: 10.1080/03014223.2010.548561

Copyright information

© The Japanese Society of Limnology 2016

Authors and Affiliations

  • Lucas Lamelas-López
    • 1
    • 2
    Email author
  • Margarita Florencio
    • 1
    • 3
  • Paulo A. V. Borges
    • 1
  • Adolfo Cordero-Rivera
    • 2
  1. 1.CE3C, Centre for EcologyEvolution and Environmental Changes/Azorean Biodiversity Group and Universidade dos Açores-Departamento de Ciências e Engenharia do AmbienteAngra do HeroísmoPortugal
  2. 2.ECOEVO Lab, Departamento de Ecoloxía e Bioloxía AnimalUniversidade de Vigo, EUE Forestal, Campus UniversitarioPontevedraSpain
  3. 3.Departamento de EcologiaUniversidade Federal de GoiásGoiâniaBrazil

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