Abstract
Absence of light, typical of the subterranean environment can lead to the loss of synchronizers of physiological and behavioral activities, mainly those related to photoperiods and light perception. Cave-dwelling species present phototactic responses that vary from photonegative to photopositive ones. There are few studies focusing on reaction to light in millipedes and the most studied species are considered photophobic. In this study, we analyzed the phototactic response of cave-dwelling and epigean millipedes of the genus Pseudonannolene (Spirostreptida, Pseudonannolenidae). For this, the chamber choice method was used. We related the phototatic reactions to morphological characters that indicate troglomorphisms (e.g., eyes and melanic pigmentation). The eight-studied operational taxonomic unit (OTU) showed photophobic reaction to all light intensities tested (150, 500 and 1000 lx) and photophobia can be considered a plesiomorphic character in the group. The morphological analysis showed that the light response is negatively correlated to the number of ommatidia and ocular area, that is, the larger the area and the number of ommatidia, the more negative is the light response (photonegative), suggesting that the eyes are the main sensory organs in the perception of light and, apparently, the integument of Pseudonannolene is not related to light sensitivity, opposite to that observed for other millipede species.
Similar content being viewed by others
References
Alvares CA, Stape JL, Sentelhas PC, de Moraes G, Leonardo J, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorol Z 22:711–728. https://doi.org/10.1127/0941-2948/2013/0507
Ayres M (2007) BioEstat 5.0: aplicações estatísticas nas áreas das ciências biológicas e médicas. Sociedade Civil Mamirauá, Belém
Barlow CA (1957) A factorial analysis of distribution in three species of diplopods. Tijdschrift voor Entomologie 100:349–426
Barr TC, Holsinger JR (1985) Speciation in Cave Faunas. Annu Rev Ecol Syst 16:313–337
Bessa E, Trajano E (2001) Light reaction and cryptobiotic habits in armoured catfishes, genus Ancistrus, from caves in Central and Northwest Brazil (Siluriformes: Loricariidae). Mémoires de biospéologie 28:29–37
Bichuette ME (2003) Distribuição, biologia, ecologia populacional e comportamento de peixes subterrâneos, gênero Ituglanis (Siluriformes:Trichomycteridae) e Eigenmannia (Gymnotiformes: Sternopygidae) área cárstica de São Domingos, nordeste de Goiás. Tese (Doutorado em Zoologia). Instituto de Biociências, Universidade de São Paulo, São Paulo
Bichuette M, Trajano E (1999) Light reaction, spontaneous and feeding behaviour in epigean and cave Potamolithus species from upper Ribeira Valley, Southeastern Brazil (Mollusca: Gastropoda: Hydrobiidae). Mémoires de biospéologie 26:1–6
Borowsky B (2011) Responses to light in two eyeless cave dwelling amphipods (Niphargus ictus and Niphargus frasassianus). J Crustacean Biol 31:613–616. https://doi.org/10.1651/10-3450.1
Brasil (2014) Ministério do Meio Ambiente Portaria nº 444 de 17 de Dezembro de 2014. Diário Oficial da União, Seção 1 245:121–126
Causey N (1960) Speciation in North American Cave Millipedes. Am Midl Nat 64:116–122. https://doi.org/10.2307/2422896
Christiansen K (1962) Proposition pour la classification des animaux cavernicoles. Spelunca 2:76–78
Cloudsley-Thompson J (1951) On the responses to environmental stimuli, and the sensory physiology of Millipedes (Diplopoda). In: Proceedings of the Zoological Society of London, vol 2. Wiley Online Library, pp 253–277. https://doi.org/10.1111/j.1096-3642.1951.tb00795.x
Cullingford CHD (1962) Cave fauna and flora. British Caving, an introduction to speleology, 2 edn. Routledge and Kegan Paul, London, pp 347–389
Culver DC (1982) Cave life: evolution and ecology. Harvard University Press, Cambridge
Enghoff H, Golovatch S, Short M, Stoev P, Wesener T (2015) Diplopoda—taxonomic overview. In: Minelli A (ed) The Myriapoda, vol 2. Brill, Netherlands, pp 363–453. https://doi.org/10.1163/9789004188273_017
Fišer Ž, Novak L, Luštrik R, Fišer C (2016) Light triggers habitat choice of eyeless subterranean but not of eyed surface amphipods. Sci Nat 103:1–12. https://doi.org/10.1007/s00114-015-1329-9
Fontanetti CS (2002) Taxonomic Importance of the Prefemoral Process of the first Pair of Legs in Males of the Genus Pseudonannolene (Diplopoda, Siprostreptida). Folia Biol-Krakow 50:199–202
Fuhrmann H (1922) Beiträge zur Kenntnis der Hautsinnesorgane der Tracheaten. I. Die antennalen Sinnesorgane der Myriapoden. Zeitschrift für wissenschaftliche Zoologie 119:1–52
Golovatch SI, Kime RD (2009) Millipede (Diplopoda) distributions: a review. Soil Org 81:565–597
Hopkin SP, Read HJ (1992) The biology of millipedes. Oxford University Press, New York
Iniesta LFM, Ferreira RL (2014) New species of Pseudonannolene Silvestri, 1895 from Brazilian limestone caves with comments on the potential distribution of the genus in South America (Spirostreptida: Pseudonannolenidae). Zootaxa 3846:361–397. https://doi.org/10.11646/zootaxa.3846.3.3
Iniesta LFM, Ferreira RL (2015) Pseudonannolene lundi n. sp., a new troglobitic millipede from a Brazilian limestone cave (Spirostreptida: Pseudonannolenidae). Zootaxa 3949:123–128. https://doi.org/10.11646/zootaxa.3949.1.6
Krell FT (2004) Parataxonomy vs. taxonomy in biodiversity studies—pitfalls and applicability of ‘morphospecies’ sorting. Biodivers conserv 13:795–812. https://doi.org/10.1023/B:BIOC.0000011727.53780.63
Kruskal WH, Wallis WA (1952) Use of ranks in one-criterion variance analysis. J Am Stat Assoc 47(260):583–621
Langecker T (1992) Light sensitivity of cave vertebrates. Behavioral and morphological aspects. In: Camacho AI (ed) The natural history of biospeleology. Museo Nacional de Ciencias Naturales, Madrid, pp 295–326
Makarov SE (2015) Diplopoda—integument. In: Minelli A (ed) The Myriapoda, vol 2. Brill, Netherlands, pp 69–99. https://doi.org/10.1163/9789004188273_004
Mauriès JP (1987) Cambalides nouveaux et peu connus d’Asie, d’Amérique et d’Océanie. II. Pseudonannolenidae, Choctellidae (Myriapoda, Diplopoda). Bull Mus natn Hist nat Paris 9:169–199
McKillup SC (1988) Behaviour of the millipedes Ommatoiulus moreletii. Ophyiulus verruculiger and Oncocladosoma castaneum in response to visible light; an explanation for the invasion of houses by Ommatoiulus moreletii. J Zool 215:35–46. https://doi.org/10.1111/j.1469-7998.1988.tb04883.x
Moracchioli N (1994) Estudo da Biologia de Aegla spp. Cavernícolas do Vale do Alto Rio Ribeira, São Paulo (Crustacea: Anomura: Aeglidae). Dissertação (Mestrado em Zoologia). Instituto de Biociências, Universidade de São Paulo, São Paulo
Müller CH, Sombke A (2015) Diplopoda—sense organs. In: Minelli A (ed) The Myriapoda, vol 2. Brill, Netherlands, pp 181–235. https://doi.org/10.1163/9789004188273_010
Park O, Roberts T, Harris S (1941) Preliminary analysis of activity of the cave crayfish, Cambarus pellucidus. Am Nat 154–171
Parzefall J (1986) Behavioural ecology of cave-dwelling fishes. The behaviour of teleost fishes. Springer, Berlin, pp 433–445. https://doi.org/10.1007/978-1-4684-8261-4_17
Rantin B, Bichuette ME (2013) Phototactic behaviour of subterranean Copionodontinae Pinna, 1992 catfishes (Siluriformes, Trichomycteridae) from Chapada Diamantina, central Bahia, northeastern Brazil. Int J Speleol 42:7. https://doi.org/10.5038/1827-806X.42.1.7
Schubart O (1944) Os Diplopodos de Pirassununga. Acta zool. Lilloana, 2:321–440
Schubart O (1952) Diplopoda de Pirassununga IV. Adenda a fauna regional. Dusenia 3:403–420
Toye S (1966) The reactions of three species of Nigerian millipedes (Spirostreptus assiniensis. Oxydesmus sp., and Habrodesmus falx) to light, humidity and temperature. Entomol Exp Appl 9:468–483. https://doi.org/10.1111/j.1570-7458.1966.tb01007.x
Trajano E (1987) Fauna cavernícola brasileira: composição e caracterização preliminar. Rev Bras Zool 3:533–561. https://doi.org/10.1590/S0101-81751986000400004
Trajano E (1993) A review of biospeleology in Brazil. Bol Soc Venez Espeleol 27:18–23
Trajano E, Cobolli M (2012) Evolution of Lineages. In: White WB, Culver DC (eds) Encyclopedia of caves, 2° edn. Academic, Oxford, pp 295–304
Trajano E, Gerhard P (1997) Light reaction in brazilian cave fishes (Siluriformes: Pimelodidae, Trichomycteridae, Loricaridae). Mémoires de biospéologie 24:127–138
Trajano E, Souza A (1994) The behavior of Ancistrus cryptophthalmus, an armored blind catfish from caves of Central Brazil, with notes on syntopic Trichomycterus sp.(Siluriformes, Loricariidae, Trichomycteridae). Mémoires de Biospéologie 21:151–159
Trajano E, Golovatch S, Geoffroy J, Pinto-da-Rocha R, Fontanetti C (2000) Synopsis of Brazilian cave-dwelling millipedes (Diplopoda). Papéis Avulsos de Zoologia 41:259–287
Trajano E, Bichuette ME, Batalha MA (2012) Estudos ambientais em cavernas: os problemas da coleta, da identificação, da inclusão e dos índices. Espeleo-Tema 23:13–22
Wilkens H (2010) Genes, modules, and the evolution of cave fish. Heredity, Edinburgh 105:413–422. https://doi.org/10.1038/hdy.2009.184
Acknowledgements
We specially thank Jonas E. Gallão, Diego M. von Schimonsky and Camile S. Fernandes for providing part of material studied here and for information on localities, to Ramiro H. dos Santos and Fabiano P. de Jesus for assistance in field; Camile S. Fernandes, Tamires Zepon and Diego M. von Schimonsky for suggestions on the work; to Carmem Fontanetti, Amazonas Chagas-Jr and Marcelo A. Fernandes, for criptics; to Angélica Maria Penteado Martins Dias, coordinator of National Institute of Science and Technology of the Hymenoptera Parasitoids from Brazilian Southeast Region, INCT Hympar Sudeste (in Portuguese)—FAPESP #2008/57949-4 and CNPq # 573802/2008-4, for stereomicroscope use; to Luciana B. R. Fernandes, for images obtained through the stereomicroscope; to Rodrigo V. Mello for editing the images; to Diego M. von Schimonsky for map production; to Bianca Rantin for helping with the English; to International Paper (Rafael Silva and Miguel Magela) for support and access to caves of Altinópolis. We also thank ICMBio (Instituto Chico Mendes de Conservação à Biodiversidade) for collection license (28992-7), to PPG-ERN (Programa de Pós-graduação em Ecologia e Recursos Naturais—UFSCar) for infrastructure to develop this work, to CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for Master scholarship to JSG (132457/2015-6) and partial financing to MEB (303715/2011-1), and to FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo) for partial financing to MEB (2010/08459-4 and 2008/05678-7).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical approval
All experiments conducted in this study were in accordance with Brazilian laws involving invertebrates. The authorisation for keeping these invertebrates alive was part of our scientific collector’s permit granted by ICMBio (Instituto Chico Mendes de Conservação à Biodiversidade) number 28992-7.
Rights and permissions
About this article
Cite this article
Gallo, J.S., Bichuette, M.E. Is there correlation between photophobia and troglomorphism in Neotropical cave millipedes (Spirostreptida, Pseudonannolenidae)?. Zoomorphology 137, 273–289 (2018). https://doi.org/10.1007/s00435-017-0389-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00435-017-0389-0