Abstract
The genus Micaria Westring, 1851 (Araneae, Gnaphosidae) is a group of small (1.85–5 mm) ant-like spiders that can be distinguished from other gnaphosids by their piriform gland spigots that are similar in size to the major ampullate gland spigots. According to the World Spider Catalog, there are 105 species of Micaria in the world, of which only three species are known from the African part of the Afrotropical Region, namely M. chrysis (Simon, 1910), M. tersissima Simon, 1910 and M. beaufortia (Tucker, 1923). The objectives of this study were to revise Micaria in the Afrotropical Region, providing new and updated records for each of the species, evaluating the relationships between them using COI barcoding data, and providing information on their biology, mimetic relationships and feeding ecology. These objectives were met by collecting fresh material from the KwaZulu-Natal, Western Cape, Northern Cape and Free State provinces in South Africa. Fresh material of M. tersissima and M. chrysis were collected from their type localities, Komaggas and Port Nolloth (Northern Cape Province), respectively, for identification and DNA analyses. COI sequences generated, together with those sourced from Barcode of Life Data Systems (BOLD) and GenBank, were aligned using the CulstalW alignment algorithm in the Mega X software, and molecular phylogenetic analyses were performed using MrBayes for Bayesian Inference (BI) and RaxML for maximum likelihood (ML) analyses. Morphological examination of the collected and voucher material yielded 17 new species for the Afrotropical Region, namely M. basaliducta sp. nov. (♀, ♂, South Africa), M. bimaculata sp. nov. (♀, ♂, Mauritania), M. bispicula sp. nov. (♀, ♂, Namibia, South Africa), M. durbana sp. nov. (♀, ♂, South Africa, Zambia), M. felix sp. nov. (♀, ♂, Cameroon, Ethiopia, Malawi, Mozambique, Namibia, South Africa, Zambia, Zimbabwe), M. gagnoa sp. nov. (♀, ♂, Côte d’Ivoire, Mozambique, Mozambique, Tanzania), M. koingnaas sp. nov. (♂, South Africa), M. lata sp. nov. (♂, Namibia, South Africa), M. laxa sp. nov. (♀, South Africa), M. mediospina sp. nov. (♂, South Africa), M. parvotibialis sp. nov. (♀, ♂, Senegal), M. plana sp. nov. (♀, ♂, Ethiopia), M. quadrata sp. nov. (♀, Ethiopia), M. quinquemaculosa sp. nov. (♀, ♂, Namibia, South Africa), M. rivonosy sp. nov. (♀, ♂, Madagascar), M. sanipass sp. nov. (♂, South Africa) and M. scutellata sp. nov. (♂, South Africa). Furthermore, both sexes of M. beaufortia, as well as the male of M. tersissima, are redescribed. Both sexes of M. chrysis are described for the first time, as this species was only known from a juvenile. Of the previously known species, M. beaufortia (Botswana, Ethiopia, Lesotho, Namibia, South Africa, Zimbabwe) and M. chrysis (Côte d’Ivoire, Ethiopia, Lesotho, Namibia, South Africa, Tanzania) are widespread in the Afroptropics, while M. tersissima is only known from South Africa. Both the Bayesian inference and the maximum likelihood analysess recovered Micaria (sensu lato) as monophyletic with the inclusion of the subopaca group. The pulicaria species group was recovered as polyphyletic in both the BI and ML analyses. Four Afrotropical species, as well as the M. rossica Thorell, 1875/M. foxi Gertsch, 1933 group, formed a clade sister to M. formicaria (Sundevall, 1831). Eight of the Afrotropical species now have COI barcoding data uploaded to BOLD.
References
Altekar, G., Dwarkadas, S., Huelsenbeck, J.P. & Ronquist, F. (2004) Parallel Metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics, 20 (3), 407–415.
https://doi.org/10.1093/bioinformatics/btg427
Álverez-Padilla, F. & Hormiga, G. (2008) A protocol for digesting internal soft tissues and mounting spiders for scanning electron microscopy. Journal of Arachnology, 35 (3), 538–542.
https://doi.org/10.1636/Sh06-55.1
Azevedo, G.H.F., Griswold, C.E. & Santos, A.J. (2018) Systematics and evolution of ground spiders revisited (Araneae, Dionycha, Gnaphosidae). Cladistics, 34 (6), 579–626.
https://doi.org/10.1111/cla.12226
Bercovici, A., Hadley, A. & Villanueva-Amadoz, U. (2009) Improving depth of field resolution for palynological photomicrography. Paleontologica Electronica, 12 (2), 1–12.
Blackwall, J. (1858) Descriptions of six newly discovered species and characters of a new genus of Araneida. Annals and Magazine of Natural History, Series 3, 1 (6), 426–434.
https://doi.org/10.1080/00222935808696953
Bosmans, R. & Blick, T. (2000) Contribution to the knowledge of the genus Micaria in the West-palaearctic region, with description of the new genus Arboricaria and three new species (Araneae Gnaphosidae). Memorie della Società entomologica Italiana, 78 (2), 443–476.
Bosselaers, J. & Jocqué, R. (2000) Studies in Corinnidae: transfer of four genera and description of the female of Lessertina mutica Lawrence 1942. Tropical Zoology, 13, 305–325.
https://doi.org/10.1080/03946975.2000.10531138
Breitling, R. (2017) Public DNA barcoding data resolve the status of the genus Arboricaria (Araneae: Gnaphosidae). Arachnology Letters, 54, 24–27.
https://doi.org/10.5431/aramit5405
Caporiacco, L. (1936) Aracnidi fezzanesi raccolti dal prof. G. Scortecci nel 1934—XII. (Missione della R. Societa geografica). Atti de la Societa Italiana di Scienze Naturali, 75, 67–93.
Chyzer, C. & Kulczyński, W. (1897) Araneae Hungariae. Tomus II. Academia Scientarum, Hungary, Budapest, 366 pp.
Cushing, P.E. (1997) Myrmecomorphy and myrmecophily in spiders. Florida Entomologist, 80 (2), 165–192.
https://doi.org/10.2307/3495552
Cushing, P.E. (2012) Spider-ant associations: an updated review of myrmecomorphy, myrmecophily, and myrmecophagy in spiders. Psyche, 2012, 1–23.
https://doi.org/10.1155/2012/151989
Dippenaar-Schoeman, A.S. (1990) A revision of the spider genus Seothyra Purcell (Araneae: Eresidae). Cimbebasia, 12, 135–160.
Elgar, M.A. & Allan, R.A. (2006) Chemical mimicry of the ant Oecophylla smaragdina by the myrmecophilous spider Cosmophasis bitaeniata: Is it colony-specific? Journal of Ethology, 24 (3), 239–246.
https://doi.org/10.1007/s10164-005-0188-9
Foord, S.H., Dippenaar-Schoeman, A.S., Haddad, C.R., Lyle, R., Lotz, L.N., Sethusa, T. & Raimondo, D. (2020) The South African National Red List of spiders: patterns, threats, and conservation. Journal of Arachnology, 48, 110–118.
https://doi.org/10.1636/0161-8202-48.2.110
Haddad, C.R. (2004) A revision of the spider genus Graptartia Simon, 1896 (Araneae: Corinnidae) in the Afrotropical Region. African Entomology, 12 (1), 71–81.
Haddad, C.R. & Bosmans, R. (2013) Synonymy of the North African spider genus Castanilla Caporiacco, 1936 with Micaria Westring, 1851 (Araneae: Gnaphosidae). Zootaxa, 3734 (3), 397–399.
https://doi.org/10.11646/zootaxa.3734.3.10
Haddad, C.R. & Marusik, Y.M. (2019) Clarifying the taxonomic status and distributions of the spider species collected during the Leonhard Schultze expeditions in western and central southern Africa (Arachnida: Araneae). Zootaxa, 4608 (3), 451–483.
https://doi.org/10.11646/zootaxa.4608.3.3
Jocqué, R. & Dippenaar-Schoeman, A.S. (2006) Spider families of the world. Royal Museum for Central Africa, Tervuren, 336 pp.
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35 (6), 1547–1549.
https://doi.org/10.1093/molbev/msy096
Lanfear, R., Frandsen, P.B., Wright, A.M., Senfield, T. & Calcott, B. (2016) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34 (3), 772–773.
https://doi.org/10.1093/molbev/msw260
Locket, G.H. & Millidge, A.F. (1951) British Spiders. Vol. 1. Ray Society, London, 316 pp.
Logunov, D.V. & Obenauer, S.M. (2019) A new species of Uroballus Simon, 1902 (Araneae: Salticidae) from Hong Kong, a jumping spider that appears to mimic lichen moth caterpillars. Israel Journal of Entomology, 49 (1), 1–9.
https://doi.org/10.5281/zenodo.2632730
Magalhaes, I.L.F. (2019) Spreadsheets to expedite taxonomic publications by automatic generation of morphological descriptions and specimen lists. Zootaxa, 4624 (1), 147–150.
https://doi.org/10.11646/zootaxa.4624.1.12
Marusik, Y.M. & Omelko, M.M. (2017) Redescription of Micaria beaufortia (Araneae, Gnaphosidae), with notes on Afrotropical Micaria. Zootaxa, 4294 (4), 462–470.
https://doi.org/10.11646/zootaxa.4294.4.5
Mikhailov, K.G. & Fet, V.Y. (1986) [Contribution to the spider fauna (Aranei) of Turkmenia. I. Families Anyphaenidae, Sparassidae, Zoridae, Clubionidae, Micariidae, Oxyopidae]. Sborník Trudov Zoologicheskogo Muzeya MGU, Moscow State University, 24, 168–186.
Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Miller, M., Proceedings of the Gateway Computing Environment Workshop (GCE). IEEE Press, New Orleans, Louisiana, 8 pp.
https://doi.org/10.1109/GCE.2010.5676129
Miller, J.A., Beentjes, K.K., van Helsdingen, P. & IJLAND, S. (2013) Which specimens from a museum collection will yield DNA barcodes? A time series study of spiders in alcohol. ZooKeys, 365, 245–261.
https://doi.org/10.3897/zookeys.365.5787
Murphy, J.A. (2007) Gnaphosid genera of the world. 1st Edition. British Arachnological Society, St. Neots, 697 pp.
Muster, C. & Michalik, P. (2020) Cryptic diversity in ant‐mimic Micaria spiders (Araneae, Gnaphosidae) and a tribute to early naturalists. Zoologica Scripta, 49 (2), 197–209.
https://doi.org/10.1111/zsc.12404
Myers, N., Mittermeier, R.A., Mittermeier, C.G., Fonseca, G.A.B. da & Kent. J. (2000) Biodiversity hotspots for conservation
priorities. Nature, 403, 853–858.
https://doi.org/10.1038/35002501
Panzer, G.W.F. (1798) Fauna insectorum germanicae initia, oder Deutschlands Insecten. Heft 54. Felssecker, Nürnberg, 24 pp.
Paul, J., Sankaran, P.M., Sebastian, P.A. & Joseph, M.M. (2018) A review of the wasp mimicking spider genus Coenoptychus Simon, 1885 (Araneae: Corinnidae: Castianeirinae). Zootaxa, 4413 (1), 163–172.
https://doi.org/10.11646/zootaxa.4413.1.6
Pekár, S. & Jarab, M. (2011a) Assessment of colour and behavioural resemblance to models by inaccurate myrmecomorphic spiders (Araneae). Invertebrate Biology, 130 (1), 83–90.
https://doi.org/10.1111/j.1744-7410.2010.00217.x
Pekár, S. & Jarab, M. (2011b) Life-history constraints in inaccurate Batesian myrmecomorphic spiders (Araneae: Corinnidae, Gnaphosidae). European Journal of Entomology, 108 (2), 225–260.
https://doi.org/10.14411/eje.2011.034
Pekár, S., Jarab, M., Fromhage, L. & Herberstein, M.E. (2011) Is the evolution of inaccurate mimicry a result of selection by a suite of predators? A case study using myrmecomorphic spiders. The American Naturalist, 178 (1), 124–134.
https://doi.org/10.1086/660287
Pekár, S. & Král, J. (2002) Mimicry complex in two central European zodariid spiders (Araneae: Zodariidae): how Zodarion deceives ants. Biological Journal of the Linnean Society, 75 (4), 517–532.
https://doi.org/10.1046/j.1095-8312.2002.00043.x
Pekár, S., Král, J. & Lubin, Y. (2005) Natural history and karyotype of some ant-eating zodariid spiders (Araneae, Zodariidae) from Israel. Journal of Arachnology, 33 (1), 50–62.
Platnick, N.I. & Shadab, M.U. (1988) A revision of the American spiders of the genus Micaria (Araneae, Gnaphosidae). American Museum Novitates, 2916, 1–64.
Purcell, W. F. (1907) New South African spiders of the family Drassidae in the collection of the South African Museum. Annals and Magazine of Natural History, Series 7, 20 (118), 297–336.
https://doi.org/10.1080/00222930709487339
Rambaut, A. (2014) FigTree. Version 1.4.4. Available from: http://tree.bio.ed.ac.uk/software/figtree/ (accessed 25 November 2019)
Raška, J. & Pekár, S. (2019) Do ladybird spiders really mimic ladybird beetles? Biological Journal of the Linnean Society, 126 (1), 168–177.
https://doi.org/10.1093/biolinnean/bly152
Reiskind, J. (1969) The spider subfamily Castianeirinae of North and Central America (Araneae, Clubionidae). Bulletin of the Museum of Comparative Zoology, 138 (5), 1–84.
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19 (12), 1572–1574.
https://doi.org/10.1093/bioinformatics/btg180
Rubio, G.D., Arbino, M.O. & Cushing, P.E. (2013) Ant mimicry in the spider Myrmecotypus iguazu (Araneae: Corinnidae), with notes about myrmecomorphy in spiders. The Journal of Arachnology, 41 (3), 395–399.
https://doi.org/10.1636/J13-35.1
Simon, E. (1879) [Replacement names for Gaetulia and Chrysothrix]. Annales de la Société Entomologique de France, 9 (5), 160–161.
Simon, E. (1910) Arachnoidea. Araneae (II). In: Schultze, L. (Ed.), Zoologische und anthropologische Ergebnisse einer Forschungsreise im westlichen und zentralen Südafrika. Denkschriften der Medizinisch-Naturwissenschaftlichen Gesellschaft zu Jena, 16, pp. 175–218.
Shorthouse, D.P. (2010) SimpleMappr. An online tool to produce publication-quality point maps. Available from: https://www.simplemappr.net (accessed 8 May 2020)
Smith, F. (1858) Catalogue of Hymenopterous insects in the collection of the British Museum. Part VI. Formicidae. British Museum, London, 216 pp.
Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30 (9), 1312–1313.
https://doi.org/10.1093/bioinformatics/btu033
Tucker, R.W.E. (1923) The Drassidae of South Africa. Annals of the South African Museum, 19, 251–437.
Vaidya, G., Loham, D.J. & Meier, R. (2011) SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics, 27 (2), 171–180.
https://doi.org/10.1111/j.1096-0031.2010.00329.x
Veira, C., Ramires, E.N., Vasconcellos-Neto, J., Poppi, R.J. & Romero, G.Q. (2017) Crab spider lures prey in flowerless neighborhoods. Scientific Reports, 7, 1–7.
https://doi.org/10.1038/s41598-017-09456-y
Walckenaer, C.A. (1802) s.n. In: Faune parisienne. Insectes. ou Histoire abrégée des insectes de environs de Paris. Vol. 2. Dentu, Paris, pp. 187–250.
Westring, N. (1851). Förteckning öfver de till närvarande tid Kände, i Sverige förekommande Spindlarter, utgörande ett antal af 253, deraf 132 äro nya för svenska Faunan. Göteborgs Kungliga Vetenskaps och Vitterhets Samhälles Handlingar, 2, 25–62.
https://doi.org/10.5962/bhl.title.66044
Westring, N. (1861) Araneae svecicae. Göteborgs Kungliga Vetenskaps och Vitterhets Samhälles Handlingar, 7, 1–615.
Wheeler, W.C., Coddington, J.A., Crowley, L.M., Dimitrov, D., GolobofF, D.A., Griswold, C.E., Horminga, G., Prendini, L., Ramírez, M.J., Sierwald, P., Almeida-Silva, L., Alvarez-Padilla, F., Arnedo, M.A., Bernavides Silva, L.R., Benjamin, S.P., Bond, J.E., Grismado, C.J., Hasan, E., Hedin, M., Izquierdo, M.A., Labarque, F.M., Ledford, J., Lopardo, L., Maddison, W.P., Miller, J.A., Piacentini, L.N., Platnick, N.I., Polowtow, D., Silva-Dávila, Scharff, N., Szuts, T., Ubick, D., Vink, C.J., Wood, H.M. & Zhang, J. (2017) The spider tree of life: phylogeny of Araneae based on target-gene analyses from an extensive taxon sampling. Cladistics, 33 (6), 574–616.
https://doi.org/10.1111/cla.12182
Wunderlich, V.J. (1980) Revision der europäischen Arten der Gattung Micaria Westring 1851, mit Anmerkungen zu den übrigen paläarktischen Arten (Arachnida: Araneida: Gnaphosidae). Zoologische Beiträge, 25, 233–341.
Wunderlich, J. (2017) Descriptions, notes and synonyms of some mainly Mediterranean and Macaronesian spiders (Araneae) of various families. Beiträge zur Araneologie, 10, 298–326, 354.
World Spider Catalog (2020) World Spider Catalog, Version 21.0. Available from: Natural History Museum, Bern. Available from: https://wsc.nmbe.ch/ (accessed 11 May 2020)