Testing species delimitation with larval morphology: scanning electron microscopy analysis of protonymphon larvae of two closely related sea spiders, Pallenopsis patagonica (Hoek) and Pallenopsis yepayekae Weis*
Jeremy Hübner A B , Philipp Wagner A B , Tobias Lehmann A B and Roland R. Melzer A B C D
+ Author Affiliations
- Author Affiliations
A Zoologische Staatssammlung, Münchhausenstraße 21, 81247 München, Germany.
B Ludwig-Maximilians-Universität München, Biocenter, Department Biologie II, Großhaderner Straße 2, 82152 Planegg-Martinsried, Germany.
C GeoBioCenterLMU, Richard-Wagner-Straße 10, 80333 München, Germany.
D Corresponding author. Email: melzer@zsm.mwn.de
Invertebrate Systematics 31(4) 363-374 https://doi.org/10.1071/IS16050
Submitted: 20 July 2016 Accepted: 6 February 2017 Published: 31 May 2017
Abstract
We used scanning electron microscopy (SEM) to establish species-specific sets of characters for protonymphon larvae of two representatives of the ‘patagonica’ species group of Pallenopsis, P. patagonica and P. yepayekae. The larvae of both species are ‘typical’ protonymphon larvae sensu Bain (2003). Despite the close relationship of the two species, we observed numerous features that allow for differential diagnosis, e.g. general habitus, the number, arrangement and branching type of setules, the armature of the movable and immovable chelifore fingers, and the shape of the dactylus and setules of appendages II and III. SEM is particularly suitable for visualising these features. Our results further support the idea that protonymphon larvae can be identified to species level when adequate imaging techniques are used, as is also the case for larvae of other arthropods. Moreover, the status of the two studied species of Pallenopsis is fully supported by protonymphon larval morphology.
Additional keywords: development, Pantopoda, Pycnogonida.
References
Arango, C. P., Soler-Membrives, A., and Miller, K. J. (2011). Genetic differentiation in the circum-Antarctic sea spider Nymphon australe (Pycnogonida: Nymphonidae). Deep-sea Research. Part II, Topical Studies in Oceanography 58, 212–219.| Genetic differentiation in the circum-Antarctic sea spider Nymphon australe (Pycnogonida: Nymphonidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvFWmu7Y%3D&md5=3efd3a3aab032841f680cd6b030178deCAS |
Bain, B. A. (2003). Larval types and a summary of postembryonic development within the pycnogonids. Invertebrate Reproduction & Development 43, 193–222.
| Larval types and a summary of postembryonic development within the pycnogonids.Crossref | GoogleScholarGoogle Scholar |
Bamber, R. N. (2007). A holistic re-interpretation of the phylogeny of the Pycnogonida Latreille, 1810 (Arthropoda). Zootaxa 1668, 295–312.
Behrens, W. (1984). Larvenentwicklung und Metamorphose von Pycnogonum litorale (Chelicerata, Pantopoda). Zoomorphology 104, 266–279.
| Larvenentwicklung und Metamorphose von Pycnogonum litorale (Chelicerata, Pantopoda).Crossref | GoogleScholarGoogle Scholar |
Bogomolova, E. V. (2007). Larvae of three sea spider species of the genus Nymphon (Arthropoda: Pycnogonida) from the White Sea. Russian Journal of Marine Biology 33, 145–160.
| Larvae of three sea spider species of the genus Nymphon (Arthropoda: Pycnogonida) from the White Sea.Crossref | GoogleScholarGoogle Scholar |
Bogomolova, E. V., and Malakhov, V. V. (2003). Larvae of sea spiders (Arthropoda, Pycnogonida) of the White Sea. Zoologičeskij Zurnal 82, 1–17.
Bogomolova, E. V., and Malakhov, V. V. (2004). Fine morphology of sea spider larvae (Arthropoda, Pycnogonida) of the White Sea. Zoologicheskii Bespozvonochnykh 1, 3–28.
Bogomolova, E. V., and Malakhov, V. V. (2006). Lecithotrophic protonymphon is a special type of postembryonic development of sea spiders (Arthropoda, Pycnogonida). Doklady Biological Sciences 409, 328–331.
| Lecithotrophic protonymphon is a special type of postembryonic development of sea spiders (Arthropoda, Pycnogonida).Crossref | GoogleScholarGoogle Scholar |
Bolte, K. B. (1996). Techniques for obtaining scanning electron micrographs of minute arthropods. Proceedings of the Entomological Society of Ontario 127, 67–87.
Brenneis, G., Arango, C. P., and Scholtz, G. (2011). Morphogenesis of Pseudopallene sp. (Pycnogonida, Callipallenidae) II: postembryonic development. Development Genes and Evolution 221, 329–350.
| Morphogenesis of Pseudopallene sp. (Pycnogonida, Callipallenidae) II: postembryonic development.Crossref | GoogleScholarGoogle Scholar |
Brenneis, G., Bogomolova, E. V., Arango, C. P., and Krapp, F. (2017). From egg to “no-body”: an overview and revision of developmental pathways in the ancient arthropod lineage Pycnogonida. Frontiers in Zoology 14, 6.
Burris, Z. P. (2011). Larval morphologies and potential developmental modes of eight sea spider species (Arthropoda: Pycnogonida) from the southern Oregon coast. Journal of the Marine Biological Association of the United Kingdom 91, 845–855.
| Larval morphologies and potential developmental modes of eight sea spider species (Arthropoda: Pycnogonida) from the southern Oregon coast.Crossref | GoogleScholarGoogle Scholar |
Cano Sánchez, E., and López-González, P. J. (2009). Novel mode of postembryonic development in Ammothea genus (Pycnogonida: Ammotheidae) from Antarctic waters. Scientia Marina 73, 541–550.
| Novel mode of postembryonic development in Ammothea genus (Pycnogonida: Ammotheidae) from Antarctic waters.Crossref | GoogleScholarGoogle Scholar |
Cano Sánchez, E. C., and López-González, P. J. (2010). Postembryonic development of Nymphon unguiculatum Hodgson 1915 (Pycnogonida, Nymphonidae) from the South Shetland Islands (Antarctica). Polar Biology 33, 1205–1214.
| Postembryonic development of Nymphon unguiculatum Hodgson 1915 (Pycnogonida, Nymphonidae) from the South Shetland Islands (Antarctica).Crossref | GoogleScholarGoogle Scholar |
Cano Sánchez, E., and López-González, P. J. (2013). New data concerning postembryonic development in Antarctic Ammothea species (Pycnogonida: Ammotheidae). Polar Biology 36, 1175–1193.
| New data concerning postembryonic development in Antarctic Ammothea species (Pycnogonida: Ammotheidae).Crossref | GoogleScholarGoogle Scholar |
Carpenter, G. H. (1907). No VII – Pycnogonida. Reports of the Percy Sladen Trust Expedition to the Indian Ocean in 1905. Transactions of the Linnean Society of London 12, 95–101.
| No VII – Pycnogonida. Reports of the Percy Sladen Trust Expedition to the Indian Ocean in 1905.Crossref | GoogleScholarGoogle Scholar |
Child, C. A. (1995). ‘Antarctic and Subantarctic Pycnogonida. III. The Family Nymphonidae. Antarctic and Subantarctic Pycnogonida IV. Nymphonidae, Colossendeidae, Rhynchothoraxidae, Pycnogonidae, Endeidae, and Callipallenidae. Biology of the Antarctic Seas XXIV.’ Antarctic research series volume 69. (American Geophysical Union: Washington, DC.)
Dietz, L., Mayer, C., Arango, C. P., and Leese, F. (2011). The mitochondrial genome of Colossendeis megalonyx supports a basal position of Colossendeidae within the Pycnogonida. Molecular Phylogenetics and Evolution 58, 553–558.
| The mitochondrial genome of Colossendeis megalonyx supports a basal position of Colossendeidae within the Pycnogonida.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisFGksLc%3D&md5=1d8114076cd9e666da6e8b7390fe407eCAS |
Dietz, L., Krapp, F., Hendrickx, M. E., Arango, C. P., Krabbe, K., Spaak, J. M., and Leese, F. (2013). Evidence from morphological and genetic data confirms that Colossendeis tenera Hilton, 1943 (Arthropoda: Pycnogonida), does not belong to the Colossendeis megalonyx Hoek, 1881 complex. Organisms, Diversity & Evolution 13, 151–162.
| Evidence from morphological and genetic data confirms that Colossendeis tenera Hilton, 1943 (Arthropoda: Pycnogonida), does not belong to the Colossendeis megalonyx Hoek, 1881 complex.Crossref | GoogleScholarGoogle Scholar |
Dietz, L., Arango, C. P., Dömel, J. S., Halanych, K. M., Harder, A. M., Held, C., Mahon, A. R., Mayer, C., Melzer, R. R., Rouse, G., Weis, A., Wilson, N., and Leese, F. (2015). Regional differentiation and extensive hybridisation between mitochondrial clades of the Southern Ocean giant sea spider Colossendeis megalonyx. Royal Society Open Science 2, 140424.
| Regional differentiation and extensive hybridisation between mitochondrial clades of the Southern Ocean giant sea spider Colossendeis megalonyx.Crossref | GoogleScholarGoogle Scholar |
Dömel, J. S., Convey, P., and Leese, F. (2015). Genetic data support independent glacial refugia and open ocean barriers to dispersal for the Southern Ocean sea spider Austropallene cornigera (Möbius, 1902). Journal of Crustacean Biology 35, 480–490.
| Genetic data support independent glacial refugia and open ocean barriers to dispersal for the Southern Ocean sea spider Austropallene cornigera (Möbius, 1902).Crossref | GoogleScholarGoogle Scholar |
Dömel, J. S., Melzer, R. R., Harder, A., Mahon, A., and Leese, F. (2017). Nuclear and mitochondrial gene data support recent radiation within the sea spider species complex Pallenopsis patagonica (Hoek, 1881). Frontiers in Ecology and Evolution 4, 139.
| Nuclear and mitochondrial gene data support recent radiation within the sea spider species complex Pallenopsis patagonica (Hoek, 1881).Crossref | GoogleScholarGoogle Scholar |
Fornshell, J. A. (2014). Larvae of pycnogonids Ammothea striata (Möbius, 1902) and Ammothea carolinensis Leach, 1814 described from archived specimens. Invertebrate Zoology 11, 325–334.
Fornshell, J. A. (2017). Larval stages Nymphon charcoti Bouvier 1911. Arthropods 6, 1–7.
Gillespie, J. M., and Bain, B. A. (2006). Postembryonic development of Tanystylum bealensis (Pycnogonida, Ammotheidae) from Barkley Sound, British Columbia, Canada. Journal of Morphology 267, 308–317.
| Postembryonic development of Tanystylum bealensis (Pycnogonida, Ammotheidae) from Barkley Sound, British Columbia, Canada.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28%2Fpt1Ontw%3D%3D&md5=802c19f67f754898b07028b54cd60e18CAS |
Gordon, I. (1944). Pycnogonida. Report B.A.N.Z. Antarctic Research Expedition 1929–1931 Reports Series B 5, 1–72.
Harder, A. M., Halanych, K. M., and Mahon, A. R. (2016). Diversity and distribution within the sea spider genus Pallenopsis (Chelicerata: Pycnogonida) in the Western Antarctic as revealed by mitochondrial DNA. Polar Biology 39, 677–688.
| Diversity and distribution within the sea spider genus Pallenopsis (Chelicerata: Pycnogonida) in the Western Antarctic as revealed by mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar |
Hoek, P. P. C. (1881). Report on the Pycnogonida dredged by HMS Challenger 1873–76. Reports of the Scientific Results of the Exploring Voyage of HMS Challenger 3, 1–167.
Krabbe, K., Leese, F., Mayer, C., Tollrian, R., and Held, C. (2010). Cryptic mitochondrial lineages in the widespread pycnogonid Colossendeis megalonyx Hoek, 1881 from Antarctic and Subantarctic waters. Polar Biology 33, 281–292.
| Cryptic mitochondrial lineages in the widespread pycnogonid Colossendeis megalonyx Hoek, 1881 from Antarctic and Subantarctic waters.Crossref | GoogleScholarGoogle Scholar |
Lehmann, T., Weinzierl, C., and Melzer, R. R. (2011). SEM description of the first larval instar of Achelia assimilis (Pycnogonida: Ammotheidae). Journal of the Marine Biological Association of the United Kingdom 91, 1081–1087.
| SEM description of the first larval instar of Achelia assimilis (Pycnogonida: Ammotheidae).Crossref | GoogleScholarGoogle Scholar |
Lovely, E. C. (2005). The life history of Phoxichilidium tubulariae (Pycnogonida: Phoxichilidiidae). Northeastern Naturalist 12, 77–92.
Mahon, A. R., Arango, C. P., and Halanych, K. M. (2008). Genetic diversity of Nymphon (Arthropoda: Pycnogonida: Nymphonidae) along the Antarctic Peninsula with a focus on Nymphon australe Hodgson 1902. Marine Biology 155, 315–323.
| Genetic diversity of Nymphon (Arthropoda: Pycnogonida: Nymphonidae) along the Antarctic Peninsula with a focus on Nymphon australe Hodgson 1902.Crossref | GoogleScholarGoogle Scholar |
Malakhov, V. V., and Bogomolova, E. V. (2001). The first finding of a sea spider (Pantopoda) planktonic larva. Doklady Biological Sciences 376, 91–92.
| The first finding of a sea spider (Pantopoda) planktonic larva.Crossref | GoogleScholarGoogle Scholar |
Meinert, F. (1899). Pycnogonida. The Danish Ingolf-Expedition 3, 1–71.
Melzer, R. R., Heß, M., Ludwig, P., Dunkel, C., and Smola, U. (1996). Fine structure of the “slit organs” of the pycnogonid, Anoplodactylus petiolatus (Anoplodactylidae). Acta Zoologica 77, 167–171.
| Fine structure of the “slit organs” of the pycnogonid, Anoplodactylus petiolatus (Anoplodactylidae).Crossref | GoogleScholarGoogle Scholar |
Nakamura, K. (1981). Post-embryonic development of a pycnogonid, Propallene longiceps. Journal of Natural History 15, 49–62.
| Post-embryonic development of a pycnogonid, Propallene longiceps.Crossref | GoogleScholarGoogle Scholar |
Pagès, F., Corbera, J., and Lindsay, D. (2007). Piggybacking pycnogonids and parasitic narcomedusae on Pandea rubra (Anthomedusae, Pandeidae). Plankton & Benthos Research 2, 83–90.
| Piggybacking pycnogonids and parasitic narcomedusae on Pandea rubra (Anthomedusae, Pandeidae).Crossref | GoogleScholarGoogle Scholar |
Pushkin, A. F. (1975). Revision of the pycnogonids (Pantopoda) of the Pallenopsis patagonica group from Antarctica and adjacent waters. Byulleten Sovietskoi Antarkticheskoi Ekspeditsii 90, 72–83.
Pushkin A.F. (1993). The pycnogonid fauna of the South Ocean: biological results of the Soviet Antarctic expeditions. Russian Academy of Sciences. Exploration of the Fauna of the Seas, part 8. St Petersburg, Portorosa, Sizilien.
Tomaschko, K.-H., Wilhelm, E., and Bückmann, D. (1997). Growth and reproduction of Pycnogonum litorale (Pycnogonida) under laboratory conditions. Marine Biology 129, 595–600.
| Growth and reproduction of Pycnogonum litorale (Pycnogonida) under laboratory conditions.Crossref | GoogleScholarGoogle Scholar |
Vilpoux, K., and Waloszek, D. (2003). Larval development and morphogenesis of the sea spider Pycnogonum litorale (Stroem, 1762) and the tagmosis of the body of Pantopoda. Arthropod Structure & Development 32, 349–383.
| Larval development and morphogenesis of the sea spider Pycnogonum litorale (Stroem, 1762) and the tagmosis of the body of Pantopoda.Crossref | GoogleScholarGoogle Scholar |
Weis, A., and Melzer, R. R. (2012). How did sea spiders recolonize the Chilean fjords after glaciation? DNA barcoding of Pycnogonida, with remarks on phylogeography of Achelia assimilis (Haswell, 1885). Systematics and Biodiversity 10, 361–374.
| How did sea spiders recolonize the Chilean fjords after glaciation? DNA barcoding of Pycnogonida, with remarks on phylogeography of Achelia assimilis (Haswell, 1885).Crossref | GoogleScholarGoogle Scholar |
Weis, A., Friedrich, S., and Melzer, R. R. (2011). Antarctic Pycnogonida housed at the Bavarian State Collection of Zoology. Zoosystematics and Evolution 87, 297–317.
| Antarctic Pycnogonida housed at the Bavarian State Collection of Zoology.Crossref | GoogleScholarGoogle Scholar |
Weis, A., Meyer, R., Dömel, J. S., Dietz, L., Leese, F., and Melzer, R. R. (2014). Pallenopsis patagonica – a species complex revealed by morphology and CoI sequences. Zoological Journal of the Linnean Society 170, 110–131.
| Pallenopsis patagonica – a species complex revealed by morphology and CoI sequences.Crossref | GoogleScholarGoogle Scholar |
Wilhelm, E., Bückmann, D., and Tomaschko, K. H. (1997). Life cycle and population dynamics of Pycnogonum litorale (Pycnogonida) in a natural habitat. Marine Biology 129, 601–606.
| Life cycle and population dynamics of Pycnogonum litorale (Pycnogonida) in a natural habitat.Crossref | GoogleScholarGoogle Scholar |
