A novel symbiotic relationship between sociable weaver birds (Philetairus socius) and a new cheliferid pseudoscorpion (Pseudoscorpiones : Cheliferidae) in southern Africa
Mark S. Harvey A B C D H , Patricia C. Lopes E , Gregory R. Goldsmith F , Ali Halajian G , Mia J. Hillyer A and Joel A. Huey A B C
+ Author Affiliations
- Author Affiliations
A Department of Terrestrial Zoology, Western Australian Museum, Locked Bag 49, Welshpool DC, WA 6986, Australia.
B School of Animal Biology, University of Western Australia, Crawley, WA 6009, Australia.
C School of Natural Sciences, Edith Cowan University, Joondalup, WA 6027, Australia.
D Division of Invertebrate Zoology, American Museum of Natural History, 79th Street at Central Park West, New York, NY 10024–5192, USA; Department of Entomology, California Academy of Sciences, Golden Gate Park, San Francisco, CA 94103–3009, USA.
E Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, CH-8057, Zurich, Switzerland.
F Environmental Change Institute, School of Geography and the Environment, South Parks Road, Oxford, OX1 3QY, UK.
G Department of Biodiversity, School of Molecular and Life Sciences, Faculty of Science and Agriculture, University of Limpopo, PO Box X1106, Sovenga 0727, South Africa.
H Corresponding author. Email: mark.harvey@museum.wa.gov.au
Invertebrate Systematics 29(5) 444-456 https://doi.org/10.1071/IS15027
Submitted: 22 June 2015 Accepted: 7 August 2015 Published: 30 October 2015
Abstract
Birds harbour a wide array of other taxa in their nests or in their plumage, which either have an ectoparasitic or commensal relationship with the host. We report on the discovery of a cheliferid pseudoscorpion found in the plumage and nests of the sociable weaver bird (Philetairus socius) in southern Africa. The nests of these communal birds are the largest of any bird, and may contain up to 500 individuals. The pseudoscorpion is likely to have a mutualistic relationship with the birds, most likely preying on other small invertebrates in the nests. Molecular data derived from two populations of the pseudoscorpion found divergence levels of 1.1% in cytochrome oxidase 1 (CO1), and an analysis of CO1 and two rRNA genes (18S and 28S) found a close relationship with Chelifer and Parachelifer in the tribe Cheliferini, which is supported by the morphology of the male genitalia. The molecular analysis also suggests that Beierius may not belong to the Cheliferini. The pseudoscorpion found in association with the sociable weaver represents a new genus and species, Sociochelifer metoecus Harvey, sp. nov.
Additional keywords: taxonomy, morphology, phoresy, South Africa, Namibia.
References
Arabi, J., Judson, M. L., Deharveng, L., Lourenco, W. R., Cruaud, C., and Hassanin, A. (2012). Nucleotide composition of CO1 sequences in Chelicerata (Arthropoda): detecting new mitogenomic rearrangements. Journal of Molecular Evolution 74, 81–95.| Nucleotide composition of CO1 sequences in Chelicerata (Arthropoda): detecting new mitogenomic rearrangements.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xktlaktr0%3D&md5=2a1fc0f94ab8f051fbe765c54ba5918fCAS | 22362465PubMed |
Beier, M. (1932). Pseudoscorpionidea II. Subord. C. Cheliferinea. Das Tierreich 58, i–1–294.
Beier, M. (1940). Die Pseudoscorpionidenfauna der landfernen Inseln. Zoologische Jahrbucher. Abteilung fur Systematik, Ökologie und Geographie der Tiere 74, 161–192.
Beier, M. (1948). Phoresie und Phagophilie bei Pseudoscorpionen. Österreichische Zoologische Zeitschrift 1, 441–497.
Beier, M. (1953). Pseudoscorpionidea von Sumba und Flores. Verhandlungen der Naturforschenden Gesellschaft in Basel 64, 81–88.
Benedict, E. M., and Malcolm, D. R. (1979). Pseudoscorpions of the family Cheliferidae from Oregon (Pseudoscorpionida, Cheliferoidea). The Journal of Arachnology 7, 187–198.
Boissin, L. (1964). Remarques sur la morphologie des adultes et des nymphes d’Hysterochelifer meridianus (L. Koch) (Arachnides, Pseudoscorpions, Cheliferidae). Bulletin de la Société Zoologique de France 89, 650–669.
Brown, R. W. (1956). ‘Composition of Scientific Words.’ Revised edition. (Smithsonian Institution Press: Washington, DC.)
Chamberlin, J. C. (1931). The arachnid order Chelonethida. Stanford University Publications, Biological Sciences 7, 1–284.
Chamberlin, J. C. (1932). A synoptic revision of the generic classification of the chelonethid family Cheliferidae Simon (Arachnida) (continued). Canadian Entomologist 64, 17–35–39.
| A synoptic revision of the generic classification of the chelonethid family Cheliferidae Simon (Arachnida) (continued).Crossref | GoogleScholarGoogle Scholar |
Chamberlin, J. C. (1933). Some false scorpions of the atemnid subfamily Miratemninae (Arachnida – Chelonethida). Annals of the Entomological Society of America 26, 262–269.
| Some false scorpions of the atemnid subfamily Miratemninae (Arachnida – Chelonethida).Crossref | GoogleScholarGoogle Scholar |
Chamberlin, J. C. (1949). New and little-known false scorpions from various parts of the world (Arachnida, Chelonethida), with notes on structural abnormalities in two species. American Museum Novitates 1430, 1–57.
Chamberlin, J. C. (1952). New and little-known false scorpions (Arachnida, Chelonethida) from Monterey County, California. Bulletin of the American Museum of Natural History 99, 259–312.
Clayton, D. H., and Drown, D. M. (2001). Critical evaluation of five methods for quantifying chewing lice (Insecta: Phthiraptera). The Journal of Parasitology 87, 1291–1300.
| Critical evaluation of five methods for quantifying chewing lice (Insecta: Phthiraptera).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2FlsFalug%3D%3D&md5=144c119488e4a538244f87452aa9492bCAS | 11780812PubMed |
Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
| jModelTest 2: more models, new heuristics and parallel computing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFWmsbfP&md5=f0463a1a372a25c49bc206a93dc6de15CAS | 22847109PubMed |
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
| MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisF2ks7w%3D&md5=5e5a51a2851e50039acd3b34601cddcbCAS | 15034147PubMed |
Ellingsen, E. (1913). Note on some pseudoscorpions in the British Museum. Annals & Magazine of Natural History 11, 451–455.
| Note on some pseudoscorpions in the British Museum.Crossref | GoogleScholarGoogle Scholar |
Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. C. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 1:CAS:528:DyaK2MXjt12gtLs%3D&md5=c84f72a2d796a7fee91c4e2e01175599CAS | 7881515PubMed |
Gärdenfors, U., and Wilander, P. (1995). Ecology and phoretic habits of Anthrenochernes stellae (Pseudoscorpionida, Chernetidae). Bulletin of the British Arachnological Society 10, 28–30.
Giribet, G., Carranza, S., Baguñà, J., Riutort, M., and Ribera, C. (1996). First molecular evidence for the existence of a Tardigrada + Arthropoda clade. Molecular Biology and Evolution 13, 76–84.
| First molecular evidence for the existence of a Tardigrada + Arthropoda clade.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhtVylur8%3D&md5=3929e906bf01ea2e7297deed531bbc59CAS | 8583909PubMed |
Harvey, M. S. (1992). The phylogeny and classification of the Pseudoscorpionida (Chelicerata: Arachnida). Invertebrate Taxonomy 6, 1373–1435.
| The phylogeny and classification of the Pseudoscorpionida (Chelicerata: Arachnida).Crossref | GoogleScholarGoogle Scholar |
Harvey, M. S. (Ed.) (2013). ‘Pseudoscorpions of the World, version 3.0.’ Western Australian Museum, Perth. Available at http://museum.wa.gov.au/catalogues-beta/pseudoscorpions. [Accessed 22 June 2015.]
Harvey, M. S. (2014). A review and redescription of the cosmopolitan pseudoscorpion Chelifer cancroides (Pseudoscorpiones: Cheliferidae). The Journal of Arachnology 42, 86–104.
| A review and redescription of the cosmopolitan pseudoscorpion Chelifer cancroides (Pseudoscorpiones: Cheliferidae).Crossref | GoogleScholarGoogle Scholar |
Harvey, M. S., Ratnaweera, P. B., Udagama, P. V., and Wijesinghe, M. R. (2012). A new species of the pseudoscorpion genus Megachernes (Pseudoscorpiones: Chernetidae) associated with a threatened Sri Lankan rainforest rodent, with a review of host associations of Megachernes. Journal of Natural History 46, 2519–2535.
| A new species of the pseudoscorpion genus Megachernes (Pseudoscorpiones: Chernetidae) associated with a threatened Sri Lankan rainforest rodent, with a review of host associations of Megachernes.Crossref | GoogleScholarGoogle Scholar |
Hoff, C. C. (1945). New species and records of cheliferid pseudoscorpions. American Midland Naturalist 34, 511–522.
| New species and records of cheliferid pseudoscorpions.Crossref | GoogleScholarGoogle Scholar |
Hoff, C. C. (1946a). New pseudoscorpions, chiefly Neotropical, of the suborder Monosphyronida. American Museum Novitates 1318, 1–32.
Hoff, C. C. (1946b). The pseudoscorpion tribe Cheliferini. Bulletin of the Chicago Academy of Sciences 7, 485–490.
Hoff, C. C. (1949). The pseudoscorpions of Illinois. Bulletin of the Illinois Natural History Survey 24, 407–498.
Hoff, C. C. (1950). Some North American cheliferid pseudoscorpions. American Museum Novitates 1448, 1–18.
Hoff, C. C. (1956). Pseudoscorpions of the family Cheliferidae from New Mexico. American Museum Novitates 1804, 1–36.
Hoff, C. C. (1964). Atemnid and cheliferid pseudoscorpions, chiefly from Florida. American Museum Novitates 2198, 1–43.
Jiang, W., Chen, S. Y., Wang, H., Li, D. Z., and Wiens, J. J. (2014). Should genes with missing data be excluded from phylogenetic analyses? Molecular Phylogenetics and Evolution 80, 308–318.
| Should genes with missing data be excluded from phylogenetic analyses?Crossref | GoogleScholarGoogle Scholar | 25124098PubMed |
Judson, M. L. I. (2007). A new and endangered species of the pseudoscorpion genus Lagynochthonius from a cave in Vietnam, with notes on chelal morphology and the composition of the Tyrannochthoniini (Arachnida, Chelonethi, Chthoniidae). Zootaxa 1627, 53–68.
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P., and Drummond, A. (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.
| Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data.Crossref | GoogleScholarGoogle Scholar | 22543367PubMed |
Legg, G. (1975). A generalised account of the male genitalia and associated glands of pseudoscorpions (Arachnida). Bulletin of the British Arachnological Society 3, 66–74.
Maclean, G. L. (1973a). The sociable weaver, part 1: description, distribution, dispersion and populations. Ostrich: Journal of African Ornithology 44, 176–190.
| The sociable weaver, part 1: description, distribution, dispersion and populations.Crossref | GoogleScholarGoogle Scholar |
Maclean, G. L. (1973b). The sociable weaver, part 2: nest architecture and social organisation. Ostrich: Journal of African Ornithology 44, 191–218.
| The sociable weaver, part 2: nest architecture and social organisation.Crossref | GoogleScholarGoogle Scholar |
Maclean, G. L. (1973c). The sociable weaver, part 4: predators, parasites and symbionts. Ostrich: Journal of African Ornithology 44, 241–253.
| The sociable weaver, part 4: predators, parasites and symbionts.Crossref | GoogleScholarGoogle Scholar |
Mahnert, V. (1980). Arachnids of Saudi Arabia. Pseudoscorpiones. Fauna of Saudi Arabia 2, 32–48.
Mahnert, V. (1981). Mesochelifer ressli n. sp., eine mit Chelifer cancroides (L.) verwechselte Art aus Mitteleuropa (Pseudoscorpiones, Cheliferidae). Veröffentlichungen des Tiroler Landesmuseums Ferdinandeum 61, 47–53.
Mendelsohn, J. M., and Anderson, M. D. (1997). Sociable weaver Philetairus socius. In ‘The Atlas of Southern African Birds’. (Eds J.A. Harrison, D.G. Allan, L.G. Underhill, M. Herremans, A.J. Tree, V. Parker and C.J. Brown.) pp. 534–535. (BirdLife South Africa: Johannesburg.)
Morikawa, K. (1957). Kashimachelifer cinnamoneus, a new genus and species of cheliferid pseudoscorpions from Japan. Zoological Magazine, Tokyo 66, 399–402.
Muchmore, W. B. (1971). Phoresy by North and Central American pseudoscorpions. Proceedings of the Rochester Academy of Science 12, 79–97.
Muchmore, W. B. (1973). New and little known pseudoscorpions, mainly from caves in Mexico (Arachnida, Pseudoscorpionida). Bulletin of the Association for Mexican Cave Studies 5, 47–62.
Muchmore, W. B. (1998). A new species of Xenochelifer with comments on the genus (Pseudoscorpionida, Cheliferidae). The Journal of Arachnology 26, 447–451.
Murienne, J., Harvey, M. S., and Giribet, G. (2008). First molecular phylogeny of the major clades of Pseudoscorpiones (Arthropoda: Chelicerata). Molecular Phylogenetics and Evolution 49, 170–184.
| First molecular phylogeny of the major clades of Pseudoscorpiones (Arthropoda: Chelicerata).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFOltrzP&md5=5d1b9d559cc3b0dd1f994c3af62ebf24CAS | 18603009PubMed |
Murthy, V. A., and Ananthakrishnan, T. N. (1977). Indian Chelonethi. Oriental Insects Monograph 4, 1–210.
Nunn, G. B., Theisen, B. F., Christensen, B., and Arctander, P. (1996). Simplicity-correlated size growth of the nuclear 28S ribosomal RNA D3 expansion segment in the crustacean order Isopoda. Journal of Molecular Evolution 42, 211–223.
| Simplicity-correlated size growth of the nuclear 28S ribosomal RNA D3 expansion segment in the crustacean order Isopoda.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XitFSku7c%3D&md5=17220c2451a5382f70ddf4602ffa49fdCAS | 8919873PubMed |
Olson, D. M., Dinerstein, E., Wikramanayake, E. D., Burgess, N. D., Powell, G. V. N., Underwood, E. C., D’Amico, J. A., Itoua, I., Strand, H. E., Morrison, J. C., Loucks, C. J., Allnutt, T. F., Ricketts, T. H., Kura, Y., Lamoreux, J. F., Wettengel, W. W., Hedao, P., and Kassem, K. R. (2001). Terrestrial ecoregions of the world: a new map of life on Earth. Bioscience 51, 933–938.
| Terrestrial ecoregions of the world: a new map of life on Earth.Crossref | GoogleScholarGoogle Scholar |
Pfeiler, E., Bitler, B. G., Castrezana, S., Matzkin, L. M., and Markow, T. A. (2009). Genetic diversification and demographic history of the cactophilic pseudoscorpion Dinocheirus arizonensis from the Sonoran Desert. Molecular Phylogenetics and Evolution 52, 133–141.
| Genetic diversification and demographic history of the cactophilic pseudoscorpion Dinocheirus arizonensis from the Sonoran Desert.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvF2ks7g%3D&md5=eb2a157ccf31f6c801cafdfb2b39d68bCAS | 19166949PubMed |
Poinar, G. O., Ćurčić, B. P. M., and Cokendolpher, J. C. (1998). Arthropod phoresy involving pseudoscorpions in the past and present. Acta Arachnologica 47, 79–96.
| Arthropod phoresy involving pseudoscorpions in the past and present.Crossref | GoogleScholarGoogle Scholar |
Princis, K. (1971). Blattariae: Subordo Epilamproidea. Fam.: Ectobiidae. In ‘Orthopterorum Catalogus. Vol. 14’. (Ed. M. Beier.) pp. 1041–1224. (W. Junk: The Hague, Netherlands.)
Proctor, H., and Owens, I. (2000). Mites and birds: diversity, parsitism and coevolution. Trends in Ecology & Evolution 15, 358–364.
| Mites and birds: diversity, parsitism and coevolution.Crossref | GoogleScholarGoogle Scholar |
Redikorzev, V. (1935). Apocheiridium rossicum sp. n. Compte Rendu de l’Académie des Sciences de l’U.R.S.S., n.s. 1, 184–186.
Rehn, J. A. G. (1965). A new genus of symbiotic cockroach from southwest Africa (Orthoptera: Blattaria: Oxyhaloinae). Notulae Naturae of the Academy of Natural Sciences of Philadelphia 374, 1–8.
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
| RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFKlsbfI&md5=df50a1f20f2be0cbcb0dff3c135f1b17CAS | 16928733PubMed |
Turienzo, P., Iorio, O. d., and Mahnert, V. (2010). Global checklist of pseudoscorpions (Arachnida) found in birds’ nests. Revue Suisse de Zoologie 117, 557–598.
Vachon, M. (1938). Recherches anatomiques et biologiques sur la réproduction et le développement des pseudoscorpions. Annales des Sciences Naturelles. Zoologie 1, 1–207.
Vachon, M. (1940). Éléments de la faune portugaise des Pseudoscorpions (Arachnides) avec description de quatre espèces nouvelles. Anais da Faculdade de Ciencias do Porto Academia Polytechnica do Porto 25, 141–164.
Vachon, M. (1947). Nouvelles remarques a propos de la phorésie des pseudoscorpions. Bulletin du Muséum National d’Histoire Naturelle 19, 84–87.
Weygoldt, P. (1969). ‘The Biology of Pseudoscorpions.’ (Harvard University Press: Cambridge, MA.)
White, F. N., Bartholomew, G. A., and Howell, T. R. (1975). The thermal significance of the nest of the sociable weaver Philetairus socius: winter observations. The Ibis 117, 171–179.
| The thermal significance of the nest of the sociable weaver Philetairus socius: winter observations.Crossref | GoogleScholarGoogle Scholar |
Whiting, M. F., Carpenter, J. M., Wheeler, Q. D., and Wheeler, W. C. (1997). The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Systematic Biology 46, 1–68.
| 1:STN:280:DC%2BD383js1yqtQ%3D%3D&md5=d44f1c97028888e070e932607539b111CAS | 11975347PubMed |
Worth, C. B. (1975). Pseudoscorpions on a dark-eyed junco, Junco hyemalis. Bird-banding 46, 76.
| Pseudoscorpions on a dark-eyed junco, Junco hyemalis.Crossref | GoogleScholarGoogle Scholar |
Zeh, D. W., and Zeh, J. A. (1992a). Emergence of a giant fly triggers phoretic dispersal in the neotropical pseudoscorpion, Semeiochernes armiger (Balzan) (Pseudoscorpionida: Chernetidae). Bulletin of the British Arachnological Society 9, 43–46.
Zeh, D. W., and Zeh, J. A. (1992b). Failed predation or transportation? Causes and consequences of phoretic behavior in the pseudoscorpion Dinocheirus arizonensis (Pseudoscorpionida: Chernetidae). Journal of Insect Behavior 5, 37–49.
| Failed predation or transportation? Causes and consequences of phoretic behavior in the pseudoscorpion Dinocheirus arizonensis (Pseudoscorpionida: Chernetidae).Crossref | GoogleScholarGoogle Scholar |
