Biodiversity and Conservation

, Volume 24, Issue 5, pp 1131–1146 | Cite as

Conservation along a hotspot rim: spiders in Brazilian coastal restingas

  • Thiago Gonçalves-Souza
  • Adalberto J. Santos
  • Gustavo Q. Romero
  • Thomas M. Lewinsohn
Original Paper


Protected areas are essential for the maintenance of biodiversity, but defining criteria for prioritizing areas to conserve is not an easy task. In general, selection has been based on species richness and endemism of plants and vertebrates; however, these do not necessarily match invertebrate data, hence the need of using other groups in conservation prioritization. Moreover, species richness represents one of several biodiversity facets and does not subsume other facets such as functional and phylogenetic diversity. Restingas are coastal ecosystems within the Atlantic Forest biome, one of the World’s biodiversity hotspots. We investigated whether there is congruence between three different spider biodiversity facets: functional (FD, the variety of functional traits of species), phylogenetic (PD, the evolutionary distinctness of species), and taxonomic (TD, the number and the relative abundance of species), and whether currently protected restingas are effective in protecting these facets. We studied vegetation-living spider communities in 11 restingas along 2,000 km of the Brazilian coast. We found that no value of any biodiversity facet was higher in protected restingas compared with unprotected ones. We demonstrated low congruence between the three biodiversity facets, so that the use of TD as a surrogate of other facets is unwarranted. Whilst some protected restingas hold high values of spider TD, other still unprotected areas present high PD or FD. This result suggests that conservation efforts should be extended to every remaining restinga because they are unique sites to at least one spider biodiversity facet. In particular, we recommend three unprotected restingas as high priorities in future conservation plans based on spider diversity, which corroborate findings for plants and vertebrates in the same sites.


Biodiversity facets Conservation prioritization Hotspots Coastal ecosystems 



We thank Rob Colwell, Mário Almeida-Neto, and José Hidasi-Neto for stimulating ideas during the preparation of the manuscript, and Vincent Devictor and Fabio Scarano for their comments and suggestions. The jackknife procedure was performed with help of J. Hidasi-Neto. This study was supported by FAPESP doctoral and post-doctoral Grants to TG-S. AJS was financially supported by CNPq (Grants 308072/2012-0 and 475179/2012-9), FAPEMIG (PPM-00335-13) and INCT de Hymenoptera Parasitóides da Região Sudeste Brasileira ( TML and GQR received support from FAPESP Grants and CNPq research fellowships.

Supplementary material

10531_2014_846_MOESM1_ESM.docx (17 kb)
Supplementary material 1 (DOCX 17 kb)
10531_2014_846_MOESM2_ESM.pdf (10 kb)
Supplementary material 2 (PDF 9 kb)
10531_2014_846_MOESM3_ESM.docx (17 kb)
Supplementary material 3 (DOCX 16 kb)


  1. Agnarsson I (2004) Morphological phylogeny of cobweb spiders and their relatives (Araneae, Araneoidea, Theridiidae). Zool J Linn Soc 141:447–626CrossRefGoogle Scholar
  2. Agnarsson I, Gregorič M, Blackledge TA, Kuntner M (2013) The phylogenetic placement of Psechridae within Entelegynae and the convergent origin of orb-like spider webs. J Zool Syst Evol Res 51:100–106CrossRefGoogle Scholar
  3. Álvarez-Padilla F, Dimitrov D, Giribet G, Hormiga G (2009) Phylogenetic relationships of the spider family Tetragnathidae (Araneae, Araneoidea) based on morphological and DNA sequence data. Cladistics 25:109–146CrossRefGoogle Scholar
  4. Arnedo MA, Hormiga G, Scharff N (2009) Higher-level phylogenetics of linyphiid spiders (Araneae, Linyphiidae) based on morphological and molecular evidence. Cladistics 25:231–262CrossRefGoogle Scholar
  5. Assis AMDE, Pereira OJ, Thomaz LD (2004) Fitossociologia de uma floresta de restinga no Parque Estadual Paulo César Vinha, Setiba, município de Guarapari (ES). Rev Bras Bot 27:349–361CrossRefGoogle Scholar
  6. Bayer S, Schönhofer AL (2013) Phylogenetic relationships of the spider family Psechridae inferred from molecular data, with comments on the Lycosoidea (Arachnida: Araneae). Invertebr Syst 27:53–80CrossRefGoogle Scholar
  7. Bodner MR, Maddison WP (2012) The biogeography and age of salticid spider radiations (Araneae: Salticidae). Mol Phylogenet Evol 65:213–240CrossRefPubMedGoogle Scholar
  8. Câmara IG (2003) Brief history of conservation in the Atlantic Forest. In: Galindo-Leal C, Câmara IG (eds) The Atlantic Forest of South America: biodiversity status, threats, and outlook. Island Press, Washington, pp 31–42Google Scholar
  9. Clarke KR, Warwick RM (1998) A taxonomic distinctness index and its statistical properties. J Appl Ecol 35:523–531CrossRefGoogle Scholar
  10. Clarke KR, Warwick RM (2001a) A further biodiversity index applicable to species lists: variation in taxonomic distinctness. Mar Ecol Prog Ser 216:265–278CrossRefGoogle Scholar
  11. Clarke KR, Warwick RM (2001b) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E, PlymouthGoogle Scholar
  12. Coddington JA, Levi HW (1991) Systematics and evolution of spiders (Araneae). Annu Rev Ecol Syst 22:565–592CrossRefGoogle Scholar
  13. Colwell RK (2009) Biodiversity: concepts, patterns, and measurement. In: Levin S (ed) The Princeton guide to ecology. Princeton University Press, PrincetonGoogle Scholar
  14. D’Amen M, Bombi P, Campanaro A, Zapponi L, Bologna MA, Mason F (2013) Protected areas and insect conservation: questioning the effectiveness of Nature 2000 network for saproxylic beetles in Italy. Anim Conserv 16:370–378CrossRefGoogle Scholar
  15. De Bello F, Lavergne S, Meynard CN, Lepš J, Thuiller W (2010) The partitioning of diversity: showing Theseus a way out of the labyrinth. J Veg Sci 21:992–1000CrossRefGoogle Scholar
  16. Dean W (1995) With broadax and firebrand: the destruction of the Brazilian Atlantic Forest. University of California Press, BerkeleyGoogle Scholar
  17. Devictor V, Mouillot D, Meynard C, Jiguet F, Thuiller W, Mouquet N (2010) Spatial mismatch and congruence between taxonomic, phylogenetic and functional diversity: the need for integrative conservation strategies in a changing world. Ecol Lett 13:1030–1040PubMedGoogle Scholar
  18. Dimitrov D, Lopardo L, Giribet G, Arnedo MA, Álvarez-Padilla F, Hormiga G (2012) Tangled in a sparse spider web: single origino f orb weavers and their spinning work unravelled by denser taxonomic sampling. Proc R Soc B 279:1341–1350CrossRefPubMedCentralPubMedGoogle Scholar
  19. Döbel HG, Denno RF, Coddington JA (1990) Spider (Araneae) community structure in an intertidal salt marsh: effects of vegetation structure and tidal flooding. Environ Entomol 19:1356–1370CrossRefGoogle Scholar
  20. Entling W, Schmidt MH, Bacher S, Brandl R, Nentwig W (2007) Niche properties of Central European spiders: shading, moisture and the evolution of the habitat niche. Glob Ecol Biogeogr 16:440–448CrossRefGoogle Scholar
  21. Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10CrossRefGoogle Scholar
  22. Foelix RF (2011) Biology of spiders, 3rd edn. Oxford University Press, New YorkGoogle Scholar
  23. Forest F et al (2007) Preserving the evolutionary potential of floras in biodiversity hotspots. Nature 445:757–760CrossRefPubMedGoogle Scholar
  24. Gavish-Regev E, Lubin Y, Coll M (2008) Migration patterns and functional groups of spiders in a desert agroecosystem. Ecol Entomol 33:202–212CrossRefGoogle Scholar
  25. Gibb H, Hochuli DF (2002) Habitat fragmentation in an urban environment: large and small fragments support different arthropod assemblages. Biol Conserv 106:91–100CrossRefGoogle Scholar
  26. Gonçalves-Souza T. (2012) Decifrando a função de processos ecológicos e evolutivos na distribuição local e regional de artrópodes em plantas. PhD thesis. Universidade Estadual Paulista/UNESPGoogle Scholar
  27. Gonçalves-Souza T, Brescovit AD, Rossa-Feres DC, Romero GQ (2010) Bromeliads as biodiversity amplifiers and habitat segregation of spider communities in a Neotropical rainforest. J Arachnol 38:270–279CrossRefGoogle Scholar
  28. Gonçalves-Souza T, Diniz-Filho JAF, Romero GQ (2014) Disentangling the phylogenetic and ecological components of spider phenotypic variation. PLoS ONE 9(2):e89314CrossRefPubMedCentralPubMedGoogle Scholar
  29. Greenstone MH (1984) Determinants of web spider species diversity: vegetation structural diversity vs. prey availability. Oecologia 62:299–304CrossRefGoogle Scholar
  30. Griswold CE, Coddington JA, Hormiga G, Scharff N (1998) Phylogeny of the orb-web building spiders (Araneae, Orbiculariae: Deinopoidea, Araneiodea). Zool J Linn Soc 123:1–99CrossRefGoogle Scholar
  31. Hedin MC, Maddison WP (2001) A combined molecular approach to phylogeny of the jumping spider subfamily Dendryphantinae (Araneae: Salticidae). Mol Phylogenet Evol 18:386–403CrossRefPubMedGoogle Scholar
  32. Heino J, Mykrä H, Kotanen J (2008) Weak relationships between landscape characteristics and multiple facets of stream macroinvertebrate biodiversity in a boreal drainage basin. Landscape Ecol 23:417–426CrossRefGoogle Scholar
  33. Hidasi-Neto J, Loyola RD, Cianciaruso MV (2013) Conservation actions based on red lists do not capture the functional and phylogenetic diversity of birds in Brazil. PLoS One 8:e73431CrossRefPubMedCentralPubMedGoogle Scholar
  34. Hoffmann M et al (2010) The impact of conservation on the status of the world’s vertebrates. Science 330:1503–1509CrossRefPubMedGoogle Scholar
  35. Hormiga G (1994) Cladistics and the comparative morphology of linyphiid spiders and their relatives (Araneae, Araneoidea, Linyphiidae). Zool J Linn Soc 111:1–71CrossRefGoogle Scholar
  36. Huang S, Stephens PR, Gittleman JL (2012) Traits, trees and taxa: global dimensions of biodiversity in mammals. Proc R Soc B 279:4997–5003CrossRefPubMedCentralPubMedGoogle Scholar
  37. Isaac NJB, Turvey ST, Collen B, Waterman C, Baillie JEM (2007) Mammals on the EDGE: conservation priorities based on threat and phylogeny. PLoS One 2:e296CrossRefPubMedCentralPubMedGoogle Scholar
  38. Kendall MG, Babington Smith B (1939) The problem of m rankings. Ann Math Stat 10:275–287CrossRefGoogle Scholar
  39. Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305CrossRefPubMedGoogle Scholar
  40. Legendre P, Legendre L (2012) Numerical ecology. Elsevier, AmsterdamGoogle Scholar
  41. Lewinsohn TM, Freitas AVL, Prado PI (2005) Conservation of terrestrial invertebrates and their habitats in Brazil. Conserv Biol 19:640–645CrossRefGoogle Scholar
  42. Lewis RJ, Marrs RH, Pakeman RJ (2014) Inferring temporal shifts in landuse intensity from functional response traits and functional diversity patterns: a study of Scotland’s machair grassland. Oikos 123:334–344CrossRefGoogle Scholar
  43. Maddison WP, Bodner MR, Needham KM (2008) Salticid spider phylogeny revisited, with the discovery of a large Australasian clade (Araneae: Salticidae). Zootaxa 64:49–64Google Scholar
  44. Manicom C, Schwarzkopf L, Alford RA, Schoener TW (2008) Self-made shelters protect spiders from predation. Proc Natl Acad Sci USA 105:14903–14907CrossRefPubMedCentralPubMedGoogle Scholar
  45. Margules CR, Pressey RL (2000) Systematic conservation planning. Nature 405:243–253CrossRefPubMedGoogle Scholar
  46. Marques MCM, Swaine MD, Liebsch D (2011) Diversity distribution and floristic differentiation of the coastal lowland vegetation: implications for the conservation of the Brazilian Atlantic Forest. Biodivers Conserv 20:153–168CrossRefGoogle Scholar
  47. Mazel F et al (2014) Multifaceted diversity–area relationships reveal global hotspots of mammalian species, trait and lineage diversity. Glob Ecol Biogeogr 23:836–847CrossRefPubMedCentralPubMedGoogle Scholar
  48. Ministério do Meio Ambiente, Brasil(MMA) (2000) SNUC (Sistema Nacional de Unidades de Conservação). Document in portuguese.
  49. Ministério do Meio Ambiente, Brasil(MMA) (2004) Priority areas for the conservation, sustainable use and benefit sharing of Brazilian Biological Diversity.
  50. Mouchet MA, Villéger S, Mason NWH, Mouillot D (2010) Functional diversity measures: an overview of their redundancy and their ability to discriminate community assembly rules. Funct Ecol 24:867–876CrossRefGoogle Scholar
  51. Mouillot D et al (2011) Protected and threatened components of fish biodiversity in the Mediterran Sea. Curr Biol 21:1–7CrossRefGoogle Scholar
  52. Mouquet N et al (2012) Ecophylogenetics: advances and perspectives. Biol Rev 87:769–785CrossRefPubMedGoogle Scholar
  53. Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858CrossRefPubMedGoogle Scholar
  54. Nentwig W, Wissel C (1986) A comparison of prey lengths among spiders. Oecologia 68:595–600CrossRefGoogle Scholar
  55. Neuhofer D, Machan R, Schmid A (2009) Visual perception of motion in a hunting spider. J Exp Biol 212:2819–2823CrossRefPubMedGoogle Scholar
  56. New TR (1999) Untangling the web: spiders and the challenges of invertebrate conservation. J Insect Conserv 3:251–256CrossRefGoogle Scholar
  57. Niederegger S (2013) Functional aspects of spider scopulae. In: Nentwig W (ed) Spider Ecophysiology. Springer, Heidelberg, pp 57–66CrossRefGoogle Scholar
  58. Oksanen J et al (2013) vegan: Community Ecology PackageGoogle Scholar
  59. Orme CDL et al (2005) Global hotspots of species richness are not congruent with endemism or threat. Nature 436:1016–1019CrossRefPubMedGoogle Scholar
  60. Pavoine S, Vallet J, Dufour A-B, Gachet S, Daniel H (2009) On the challenge of treating various types of variables: application for improving the measurement of functional diversity. Oikos 118:391–402CrossRefGoogle Scholar
  61. Preisser EL, Orrock JL, Schmitz OJ (2007) Predator hunting mode and habitat domain alter nonconsumptive effects in predator-prey interactions. Ecology 88:2744–2751CrossRefPubMedGoogle Scholar
  62. Quinn R, Keough M (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  63. R Development Core Team (2013) R: A language and environment for statistical computingGoogle Scholar
  64. Redding DW, Mooers AØ (2006) Incorporating evolutionary measures into conservation prioritization. Conserv Biol 20:1670–1678CrossRefPubMedGoogle Scholar
  65. Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153CrossRefGoogle Scholar
  66. Riechert SE (1999) The hows and whys of successful pest suppression by spiders: insights from case studies. J Arachnol 27:387–396Google Scholar
  67. Rocha CFD, Van Sluys M, Bergallo HG, Alves MAS (2005) Endemic and threatened tetrapods in the restingas of the biodiversity corridors of Serra do Mar and of the Central da Mata Atlântica in eastern Brazil. Braz J Biol 65:159–168CrossRefPubMedGoogle Scholar
  68. Rocha CFD, Bergallo HG, Van Sluys M, Alves MAS, Jamel CE (2007) The remnants of restinga habitats in the brazilian Atlantic Forest of Rio de Janeiro state, Brazil: habitat loss and risk of disappearance. Braz J Biol 67:263–273CrossRefPubMedGoogle Scholar
  69. Rocha CFD, Hatano FH, Vrcibradic D, Van Sluys M (2008) Frog species richness, composition and beta-diversity in coastal Brazilian restinga habitats. Braz J Biol 68:101–107CrossRefPubMedGoogle Scholar
  70. Rodrigues ASL et al (2004) Global gap analysis: priority regions for expanding the global protected-area network. Bioscience 54:1092–1100CrossRefGoogle Scholar
  71. Scarano FR (2002) Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic Rainforest. Ann Bot 90:517–524CrossRefPubMedCentralPubMedGoogle Scholar
  72. Scarano FR (2009) Plant communities at the periphery of the Atlantic rain forest: rare-species bias and its risks for conservation. Biol Conserv 142:1201–1208CrossRefGoogle Scholar
  73. Scarano FR et al (2001) Four sites with contrasting environmental stress in southeastern Brazil: relations of species, life form diversity, and geographic distribution to ecophysiological parameters. Bot J Linn Soc 136:345–364CrossRefGoogle Scholar
  74. Scharff NJ, Coddington JA (1997) A phylogenetic analysis of the orbweaving spider family Araneidae (Arachnida, Araneae). Zool J Linn Soc 120:355–424CrossRefGoogle Scholar
  75. Schleuter D, Daufresne M, Massol F, Argillier C (2010) A user’s guide to functional diversity indices. Ecol Monogr 80:469–484CrossRefGoogle Scholar
  76. Schweiger O et al (2005) Quantifying the impact of environmental factors on arthropod communities in agricultural landscapes across organizational levels and spatial scales. J Appl Ecol 42:1129–1139CrossRefGoogle Scholar
  77. Schweiger O, Klotz S, Durka W, Kühn I (2008) A comparative test of phylogenetic diversity indices. Oecologia 157:485–495CrossRefPubMedGoogle Scholar
  78. Soares-Filho B, Rajão R, Macedo M, Carneiro A, Costa W, Coe M, Rodrigues H, Alencar A (2014) Cracking Brazil’s forest code. Science 344:363–364CrossRefPubMedGoogle Scholar
  79. Srivastava DS, Cadotte MW, MacDonald AAM, Marushia RG, Mirotchnick N (2012) Phylogenetic diversity and the functioning of ecosystems. Ecol Lett 15:637–648CrossRefPubMedGoogle Scholar
  80. Tucker CM, Cadotte MW, Davies TJ, Rebelo TG (2012) Incorporating geographical and evolutionary rarity into conservation prioritization. Conserv Biol 26:593–601CrossRefPubMedGoogle Scholar
  81. Uehara-Prado M et al (2009) Selecting terrestrial arthropods as indicators of small-scale disturbance: a first approach in the Brazilian Atlantic Forest. Biol Conserv 142:1220–1228CrossRefGoogle Scholar
  82. Villéger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301CrossRefPubMedGoogle Scholar
  83. Violle C, Navas M-L, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional! Oikos 116:882–892CrossRefGoogle Scholar
  84. Waldorf E (1976) Spider size, microhabitat selection, and use of food. Am Midl Nat 96:76–87CrossRefGoogle Scholar
  85. Walpole M et al (2009) Tracking progress toward the 2010 biodiversity target and beyond. Science 325:1503–1504CrossRefPubMedGoogle Scholar
  86. Winter M, Devictor V, Schweiger O (2013) Phylogenetic diversity and nature conservation: where are we? Trends Ecol Evol 28:199–204CrossRefPubMedGoogle Scholar
  87. Wolff JO, Nentwig W, Gorb SN (2013) The great silk alternative: multiple co-evolution of web loss and sticky hairs in spiders. PLoS One 8:e62682CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Thiago Gonçalves-Souza
    • 1
    • 3
  • Adalberto J. Santos
    • 2
  • Gustavo Q. Romero
    • 1
  • Thomas M. Lewinsohn
    • 1
  1. 1.Departamento de Biologia Animal, Instituto de BiologiaUniversidade Estadual de Campinas (UNICAMP)CampinasBrazil
  2. 2.Departamento de Zoologia, Instituto de Ciências BiológicasUniversidade Federal de Minas Gerais (UFMG)Belo HorizonteBrazil
  3. 3.Departamento de Biologia, Área de EcologiaUniversidade Federal Rural de Pernambuco (UFRPE)RecifeBrazil

Personalised recommendations