Drivers of diversity in Macaronesian spiders and the role of species extinctions
Corresponding Author
Pedro Cardoso
Azorean Biodiversity Group (CITA-A), Departamento de Ciências Agrárias, Universidade dos Açores, Terra-Chã, 9701-851 Angra do Heroísmo, Portugal
Smithsonian Institution, National Museum of Natural History, 10th & Constitution NW, MRC 105, Room E-509, Washington, DC 20560-0105, USA
Correspondence: Pedro Cardoso, Smithsonian Institution, National Museum of Natural History, PO Box 37012, MRC 105, Room E-509, Washington, DC 20013-7012, USA.E-mail: [email protected]Search for more papers by this authorMiquel A. Arnedo
Biodiversity Research Institute & Department of Animal Biology, Universitat de Barcelona, Av. Diagonal 645, 08028 Barcelona, Spain
Search for more papers by this authorKostas A. Triantis
Azorean Biodiversity Group (CITA-A), Departamento de Ciências Agrárias, Universidade dos Açores, Terra-Chã, 9701-851 Angra do Heroísmo, Portugal
Biodiversity Research Group, Oxford University Centre for the Environment, South Parks Road, Oxford OX1 3QY, UK
Search for more papers by this authorPaulo A. V. Borges
Azorean Biodiversity Group (CITA-A), Departamento de Ciências Agrárias, Universidade dos Açores, Terra-Chã, 9701-851 Angra do Heroísmo, Portugal
Search for more papers by this authorCorresponding Author
Pedro Cardoso
Azorean Biodiversity Group (CITA-A), Departamento de Ciências Agrárias, Universidade dos Açores, Terra-Chã, 9701-851 Angra do Heroísmo, Portugal
Smithsonian Institution, National Museum of Natural History, 10th & Constitution NW, MRC 105, Room E-509, Washington, DC 20560-0105, USA
Correspondence: Pedro Cardoso, Smithsonian Institution, National Museum of Natural History, PO Box 37012, MRC 105, Room E-509, Washington, DC 20013-7012, USA.E-mail: [email protected]Search for more papers by this authorMiquel A. Arnedo
Biodiversity Research Institute & Department of Animal Biology, Universitat de Barcelona, Av. Diagonal 645, 08028 Barcelona, Spain
Search for more papers by this authorKostas A. Triantis
Azorean Biodiversity Group (CITA-A), Departamento de Ciências Agrárias, Universidade dos Açores, Terra-Chã, 9701-851 Angra do Heroísmo, Portugal
Biodiversity Research Group, Oxford University Centre for the Environment, South Parks Road, Oxford OX1 3QY, UK
Search for more papers by this authorPaulo A. V. Borges
Azorean Biodiversity Group (CITA-A), Departamento de Ciências Agrárias, Universidade dos Açores, Terra-Chã, 9701-851 Angra do Heroísmo, Portugal
Search for more papers by this authorAbstract
Aim To identify the biogeographical factors underlying spider species richness in the Macaronesian region and assess the importance of species extinctions in shaping the current diversity.
Location The European archipelagos of Macaronesia with an emphasis on the Azores and Canary Islands.
Methods Seven variables were tested as predictors of single-island endemics (SIE), archipelago endemics and indigenous spider species richness in the Azores, Canary Islands and Macaronesia as a whole: island area; geological age; maximum elevation; distance from mainland; distance from the closest island; distance from an older island; and natural forest area remaining per island – a measure of deforestation (the latter only in the Azores). Different mathematical formulations of the general dynamic model of oceanic island biogeography (GDM) were also tested.
Results Island area and the proportion of remaining natural forest were the best predictors of species richness in the Azores. In the Canary Islands, area alone did not explain the richness of spiders. However, a hump-shaped relationship between richness and time was apparent in these islands. The island richness in Macaronesia was correlated with island area, geological age, maximum elevation and distance to mainland.
Main conclusions In Macaronesia as a whole, area, island age, the large distance that separates the Azores from the mainland, and the recent disappearance of native habitats with subsequent unrecorded extinctions seem to be the most probable explanations for the current observed richness. In the Canary Islands, the GDM model is strongly supported by many genera that radiated early, reached a peak at intermediate island ages, and have gone extinct on older, eroded islands. In the Azores, the unrecorded extinctions of many species in the oldest, most disturbed islands seem to be one of the main drivers of the current richness patterns. Spiders, the most important terrestrial predators on these islands, may be acting as early indicators for the future disappearance of other insular taxa.
References
- Arnedo, M.A. & Ribera, C. (1997) Radiation of the genus Dysdera (Araneae, Haplogynae, Dysderidae) in the Canary Islands: the island of Gran Canaria. Zoologica Scripta, 26, 205–243.
- Arnedo, M.A. & Ribera, C. (1999) Radiation of the genus Dysdera (Araneae, Dysderidae) in the Canary Islands: the island of Tenerife. Journal of Arachnology, 27, 604–662.
- Arnedo, M.A., Oromí, P. & Ribera, C. (1996) Radiation of the genus Dysdera (Araneae, Haplogynae, Dysderidae) in the Canary Islands: the Western islands. Zoologica Scripta, 25, 241–274.
- Arnedo, M.A., Oromí, P. & Ribera, C. (2000) Systematics of the genus Dysdera (Araneae, Dysderidae) in the Eastern Canaries. Journal of Arachnology, 28, 261–292.
- Arnedo, M.A., Oromí, P. & Ribera, C. (2001) Radiation of the spider genus Dysdera (Araneae, Dysderidae) in the Canary Islands: cladistic assessment based on multiple data sets. Cladistics, 17, 313–353.
- Borges, P.A.V. & Brown, V.K. (1999) Effect of island geological age on the arthropod species richness of Azorean pastures. Biological Journal of the Linnean Society, 66, 373–410.
- Borges, P.A.V. & Brown, V.K. (2004) Arthropod community structure in pastures of an island archipelago (Azores): looking for local–regional species richness patterns at small-scales. Bulletin of Entomological Research, 94, 111–121.
- Borges, P.A.V. & Hortal, J. (2009) Time, area and isolation: factors driving the diversification of Azorean arthropods. Journal of Biogeography, 36, 178–191.
- Borges, P.A.V. & Wunderlich, J. (2005) Araneae. A list of the terrestrial fauna (Mollusca and Arthropoda) and flora (Bryophyta, Pteridophyta and Spermatophyta) from the Azores (ed. by P.A.V. Borges, R. Cunha, R. Gabriel, A.M.F. Martins, L. Silva and V. Vieira), pp. 178–180. Direcção Regional de Ambiente and Universidade dos Açores, Horta, Angra do Heroísmo and Ponta Delgada.
- Borges, P.A.V. & Wunderlich, J. (2008) Spider biodiversity patterns and their conservation in the Azorean archipelago, with description of new taxa. Systematics and Biodiversity, 6, 249–282.
- Borges, P.A.V., Cunha, R., Gabriel, R., Martins, A.M.F., Silva, L., Vieira, V., Dinis, F., Lourenço, P. & Pinto, N. (2005) Description of the terrestrial Azorean biodiversity. A list of the terrestrial fauna (Mollusca and Arthropoda) and flora (Bryophyta, Pteridophyta and Spermatophyta) from the Azores (ed. by P.A.V. Borges, R. Cunha, R. Gabriel, A.M.F. Martins, L. Silva and V. Vieira), pp. 21–68. Direcção Regional de Ambiente and Universidade dos Açores, Horta, Angra do Heroísmo and Ponta Delgada.
- Cardoso, P. & Crespo, L. (2008) Araneae. A list of the terrestrial fungi, flora and fauna of Madeira and Selvagens archipelagos (ed. by P.A.V. Borges, C. Abreu, A.M.F. Aguiar, P. Carvalho, R. Jardim, I. Melo, P. Oliveira, C. Sérgio, A.R.M. Serrano and P. Vieira), pp. 283–286. Direcção Regional do Ambiente da Madeira and Universidade dos Açores, Funchal and Angra do Heroísmo.
- Cardoso, P., Borges, P.A.V. & Gaspar, C. (2007) Biotic integrity of the arthropod communities in the natural forests of Azores. Biodiversity and Conservation, 16, 2883–2901.
- Cardoso, P., Borges, P.A.V. & Macías-Hernández, N. (2008a) Dysdera crocata C.L. Koch, 1838. Invasive terrestrial flora and fauna of Macaronesia. Top 100 in Azores, Madeira and Canaries (ed. by L. Silva, E.L. Ojeda and J.L. Rodriguez-Luengo), pp. 415–417. ARENA, Ponta Delgada.
- Cardoso, P., Gaspar, C., Pereira, L.C., Silva, I., Henriques, S.S., Silva, R.R. & Sousa, P. (2008b) Assessing spider species richness and composition in Mediterranean cork oak forests. Acta Oecologica, 33, 114–127.
- Cardoso, P., Scharff, N., Gaspar, C., Henriques, S.S., Carvalho, R., Castro, P.H., Schmidt, J.B., Silva, I., Szüts, T., Castro, A. & Crespo, L.C. (2008c) Rapid biodiversity assessment of spiders (Araneae) using semi-quantitative sampling: a case study in a Mediterranean forest. Insect Conservation and Diversity, 1, 71–84.
- Cardoso, P., Aranda, S.C., Lobo, J.M., Dinis, F., Gaspar, C. & Borges, P.A.V. (2009) A spatial scale assessment of habitat effects on arthropod communities of an oceanic island. Acta Oecologica, 35, 590–597.
- Carine, M.A. & Schaefer, H. (2010) The Azores diversity enigma: why are there so few Azorean endemic flowering plants and why are they so widespread? Journal of Biogeography, 37, 77–89.
- Carracedo, J.C., Singer, B., Jicha, B., Guillou, H., Rodríguez, E., Badiola, E.R., Meco, J., Pérez Torrado, F.J., Gimeno, D., Socorro, S. & Láinez, A. (2003) La erupción y el tubo volcánico del Volcán Corona (Lanzarote, Islas Canarias). Estudios Geológicos, 59, 277–302.
- Crespo, L.C., Cardoso, P., Silva, I. & Menezes, D. (2009a) Spiders (Arachnida: Araneae) from the Selvagens Islands (Portugal): additions to the current knowledge. Boletín de la Sociedad Entomologica Aragonesa, 45, 343–348.
- Crespo, L.C., Cardoso, P., Henriques, S.S & Gaspar, C. (2009b) Spiders (Araneae) from Porto Santo (Portugal, Madeira): additions to the current knowledge. Boletín de la Sociedad Entomologica Aragonesa, 45, 471–475.
- Davies, K.F., Margules, C.R. & Lawrence, J.F. (2000) Which traits of species predict population declines in experimental forest fragments? Ecology, 81, 1450–1461.
- Didham, R.K., Lawton, J.H., Hammond, P.M. & Eggleton, P. (1998) Trophic structure stability and extinction dynamics of beetles (Coleoptera) in tropical forest fragments. Philosophical Transactions of the Royal Society B: Biological Sciences, 353, 437–451.
- Dimitrov, D. & Ribera, C. (2006) Three new species of Pholcus (Araneae, Pholcidae) from the Canary Islands with notes on the genus Pholcus in the archipelago. Journal of Arachnology, 34, 126–134.
- Dimitrov, D. & Ribera, C. (2007) The genus Pholcus (Araneae, Pholcidae) in the Canary Islands. Zoological Journal of the Linnean Society, 151, 59–114.
- Dimitrov, D., Arnedo, M.A. & Ribera, C. (2008) Colonization and diversification of the spider genus Pholcus Walckenaer, 1805 (Araneae, Pholcidae) in the Macaronesian archipelagos: evidence for long-term occupancy yet rapid recent speciation. Molecular Phylogenetics and Evolution, 48, 596–614.
- Emerson, B.C. & Gillespie, R.G. (2008) Phylogenetic analysis of community assembly and structure over space and time. Trends in Ecology and Evolution, 23, 619–630.
- Fattorini, S. (2009) On the general dynamic model of oceanic island biogeography. Journal of Biogeography, 36, 1100–1110.
- Fernández-Palacios, J.M., Arévalo, J.R., Delgado, J.D. & Otto, R. (2004) Canarias: ecología, medio ambiente y desarrollo. Centro de la Cultura Popular de Canarias, La Laguna.
-
Funk, V.A. &
Wagner, W.L. (1995) Biogeographic patterns in the Hawaiian Islands.
Hawaiian biogeography: evolution on a hot spot archipelago (ed. by
W.L. Wagner and
V.L. Funk), pp. 379–419. Smithsonian Institution, Washington, DC.
10.5962/bhl.title.129909 Google Scholar
- García, L.V. (2004) Escaping the Bonferroni iron claw in ecological studies. Oikos, 105, 657–663.
- Gaspar, C., Borges, P.A.V. & Gaston, K.J. (2008) Diversity and distribution of arthropods in natural forests of the Azores archipelago. Arquipélago. Life and Marine Sciences, 25, 1–30.
- Geldmacher, J., Hoernle, K., van den Bogaard, P., Zankl, G. & Garbe-Schonberg, D. (2001) Earlier history of the ≥70-Ma-old Canary hotspot based on the temporal and geochemical evolution of the Selvagen Archipelago and neighboring seamounts in the eastern North Atlantic. Journal of Volcanology and Geothermal Research, 111, 55–87.
- Geldmacher, J., Hoernle, K., Bogaard, P.V.D., Duggen, S. & Werner, R. (2005) New 40Ar/39Ar age and geochemical data from seamounts in the Canary and Madeira volcanic province: support for the mantle plume hypothesis. Earth and Planetary Science Letters, 237, 85–101.
- Gilbert, F., Gonzalez, A. & Evans-Freke, I. (1997) Corridors maintain species richness in the fragmented landscapes of a microecosystem. Philosophical Transactions of the Royal Society B: Biological Sciences, 265, 577–582.
- Gillespie, R.G. (2004) Community assembly through adaptive radiation in Hawaiian spiders. Science, 303, 356–359.
- Gillespie, R.G. & Roderick, G.K. (2002) Arthropods on islands: colonization, speciation, and conservation. Annual Review of Entomology, 47, 595–632.
- Hormiga, G., Arnedo, M.A. & Gillespie, R.G. (2003) Speciation on a conveyor belt: sequential colonization of the Hawaiian Islands by Orsonwelles spiders (Araneae: Linyphiidae). Systematic Biology, 52, 70–88.
- Juan, C., Emerson, B.C., Oromí, P. & Hewitt, G.M. (2000) Colonization and diversification: towards a phylogeographic synthesis for the Canary Islands. Trends in Ecology and Evolution, 15, 104–109.
- Kalmar, A. & Currie, D.J. (2006) A global model of island biogeography. Global Ecology and Biogeography, 15, 72–81.
-
Kimberling, D.N.,
Karr, J.R. &
Fore, L.S. (2001) Measuring human disturbance using terrestrial invertebrates in the shrub-steppe of eastern Washington (USA).
Ecological Indicators, 1, 63–81.
10.1016/S1470-160X(01)00009-7 Google Scholar
- Kreft, H., Jetz, W., Mutke, J., Kier, G. & Barthlott, W. (2008) Global diversity of island floras from a macroecological perspective. Ecology Letters, 11, 116–127.
- López-Mercader, N. (2005) Evolutionary processes of the genus Spermophorides (Araneae, Pholcidae) in the Canary Islands. Departamento de Biología Animal, Universitat de Barcelona, Barcelona.
- Losos, J.B. & Ricklefs, R.E. (2009) Adaptation and diversification on islands. Nature, 457, 830–836.
- MacArthur, R.H. & Wilson, E.O. (1963) An equilibrium theory of insular zoogeography. Evolution, 17, 373–387.
-
MacArthur, R.H. &
Wilson, E.O. (1967) The theory of island biogeography. Princeton University Press, Princeton, NJ.
10.1111/j.1463-6409.2007.00280.x Google Scholar
- Macías-Hernández, N., Oromí, P. & Arnedo, M.A. (2008) Patterns of diversification on old volcanic islands as revealed by the woodlouse-hunter spider genus Dysdera (Araneae, Dysderidae) in the eastern Canary Islands. Biological Journal of the Linnean Society, 94, 589–615.
- Martins, A.M.F. (1993) The Azores – westernmost Europe: where evolution can be caught red-handed. Boletim do Museu Municipal do Funchal, S2, 181–198.
-
Martins, A.M.F. (2005) The shaping of a species: the Azorian Drouetia Gude (Pulmonata: Zonitidae: Oxychilus) as a model.
Records of the Western Australian Museum, Supplement, 668, 143–157.
10.18195/issn.0313-122x.68.2005.143-157 Google Scholar
- Moran, M.D. (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos, 100, 403–405.
- Myers, N., Mittermeier, R.A., Mittermeier, C.G., Fonseca, G.A.B. & Kent, J. (2000) Biodiversity hotspots for conservation priorities. Nature, 403, 853–858.
- Nunes, J.C. (1999) A actividade vulcânica na ilha do Pico do Plistocénico Superior ao Holocénico: mecanismo eruptivo e hazard vulcânico. PhD Thesis, Universidade dos Açores, Ponta Delgada.
- Oromí, P., García, A. & Macías, N.E. (2004) Araneae. Lista de especies silvestres de Canarias (hongos, plantas y animales terrestres) (ed. by I. Izquierdo, J.L. Martín, N. Zurita and M. Arechavaleta), pp. 164–172. Consejería de Medio Ambiente y Ordenación Territorial, Gobierno de Canarias, Tenerife.
- Parent, C.E. & Crespi, B.J. (2006) Sequential colonization and diversification of Galapagos endemic land snail genus Bulimulus (Gastropoda, Stylommatophora). Evolution, 60, 2311–2328.
- Paris, R., Guillou, H., Carracedo, J.C. & Perez Torrado, F.J. (2005) Volcanic and morphological evolution of La Gomera (Canary Islands), based on new K–Ar ages and magnetic stratigraphy: implications for oceanic island evolution. Journal of the Geological Society, 162, 501–512.
- Peck, S.B. & Kukalova-Peck, J. (1990) Origin and biogeography of the beetles (Coleoptera) of the Galápagos Archipelago, Ecuador. Canadian Journal of Zoology, 68, 1617–1638.
- Peck, S.B., Wigfull, P. & Nishida, G. (1999) Physical correlates of insular species diversity: the insects of the Hawaiian Islands. Annals of the Entomological Society of America, 92, 529–536.
- Platnick, N.I. (2009) The world spider catalog, version 9.5. American Museum of Natural History, New York. Available at: http://research.amnh.org/entomology/spiders/catalog/index.html (accessed 20 May 2009).
- Price, J.P. & Clague, D.A. (2002) How old is the Hawaiian biota? Geology and phylogeny suggest recent divergence. Proceedings of the Royal Society B: Biological Sciences, 269, 2429–2435.
-
Rosenzweig, M.L. (1995) Species diversity in space and time. Cambridge University Press, Cambridge.
10.1111/j.2006.0906-7590.04272.x Google Scholar
- Silva, L., Ojeda, E.L. & Rodríguez-Luengo, J.L. (eds) (2008) Invasive terrestrial flora and fauna of Macaronesia. Top 100 in Azores, Madeira and Canaries. ARENA, Ponta Delgada.
- Silveira, L.M.A. (2007) Learning with history: interaction with nature during the human colonization in Terceira Island. MSc Thesis, University of Azores, Angra do Heroísmo.
- Steadman, D.W. (2006) Extinction and biogeography of tropical Pacific birds. University of Chicago Press, Chicago.
- Triantis, K.A., Mylonas, M. & Whittaker, R.J. (2008a) Evolutionary species–area curves as revealed by single-island endemics: insights for the inter-provincial species–area relationship. Ecography, 31, 401–407.
- Triantis, K.A., Nogués-Bravo, D., Hortal, J., Borges, P.A.V., Adsersen, H., Fernández-Palacios, M., Araújo, M.B. & Whittaker, R.J. (2008b) Measurements of area and the (island) species–area relationship: new directions for an old pattern. Oikos, 117, 1555–1559.
- Whittaker, R.J. (2006) Island species–energy theory. Journal of Biogeography, 33, 11–12.
- Whittaker, R.J. & Fernández-Palacios, J.M. (2007) Island biogeography: ecology, evolution, and conservation, 2nd edn. Oxford University Press, Oxford.
- Whittaker, R.J., Triantis, K.A. & Ladle, R.J. (2008) A general dynamic theory of oceanic island biogeography. Journal of Biogeography, 35, 977–994.
- Whittaker, R.J., Triantis, K.A. & Ladle, R.J. (2010) A general dynamic theory of oceanic island biogeography: extending the MacArthur–Wilson theory to accommodate the rise and fall of volcanic islands. The theory of island biogeography revisited (ed. by J.B. Losos and R.E. Ricklefs), pp. 88–115. Princeton University Press, Princeton, NJ.
- Wilson, E.O. (1969) The species equilibrium. Brookhaven Symposium of Biology, 22, 38–47.
- Wright, D.H. (1983) Species–energy theory: an extension of species–area theory. Oikos, 41, 496–506.