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Comparing individual raptor species and coarse taxonomic groups as biodiversity surrogates in desert ecosystems

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Abstract

Prioritizing biodiversity conservation strategies is urgently needed. Surrogate species have been used for that purpose as a means to lower costs/effort to assess representation of other species important for conservation planning. Such strategy should include multiple species and habitats within a given landscape or geographic area. The use of surrogates provides an appealing shortcut to monitoring biodiversity as it enables an efficient use of limited resources. As a group, raptors feed on a very wide range of prey sizes and, therefore, on a high diversity of prey species, which should improve their surrogacy complementarity. The aim of this paper is to identify a suitable approach that can be used as an efficient surrogate of regional diversity in desert ecosystems. First, through assemblage concordance analysis we tested two alternative approaches either using: (a) a single raptor species or (b) the entire group of raptor species as surrogates of biodiversity. Second, through correlation analysis we also tested whether the species richness of single target groups (raptors, other birds, reptiles, mammals and plants), or of two-group combinations, was correlated with the pooled species richness of the remaining groups, and then determine each of the taxonomic groups as surrogates of the entire biodiversity at the regional scale. Four single raptor species showed significant concordance with the entire bird community but, overall, most comparisons between single raptor species and other taxonomic groups failed to show any consistent correlation. A remarkable finding from the single species approach was that the strongest significant positive association was that found between caracara C. cheriway and bird species richness. This raptor is a habitat and diet generalist, thus contradicting the hypothesis that specialist species make the best bioindicators. Raptor species were significantly associated with non-raptor birds, vegetation and rodents, but not with the mammal or reptile communities. Plant species richness showed a statistically significant concordance with most of the other groups except for reptiles. Reptiles were the group that showed less concordance with the others. Between-groups comparisons showed that the species richness was strongly correlated between birds and plants, followed by between raptors and birds; correlations between birds and mammals, reptiles and mammals and raptors and plants were weak albeit statistically significant. Species richness of some individual groups, namely other birds, plants and mammals, were significantly correlated with their corresponding remaining richness values. The pooled species richness of two-group combinations were strongly correlated for raptors and other birds, raptors and plants, other birds and mammals, and reptiles and plants, and their corresponding remaining richness. We propose an approach using the combined species richness of two taxonomic groups given the high, statistically significant correlation with their corresponding remaining richness in the Baja California peninsula and possibly in other desert ecosystems too.

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References

  • Agosti D, Majer JD, Alonso LE, Schultz TR (2000) Ants: standard methods for measuring and monitoring biodiversity. Smithsonian Institution Press, Washington, DC, p 280

    Google Scholar 

  • Andrews P, O’Brien EM (2000) Climate, vegetation, and predictable gradients in mammal species richness in southern Africa. J Zool 251:205–231

    Article  Google Scholar 

  • Bednarz J, David J (1988) A study of the ecological basis of cooperative breeding in the Harris’ Hawk. Ecology 69:1176–1187

    Article  Google Scholar 

  • Bini LM, da Silva LC, Velho LF, Bonecker CC, Lansac-Tôha FA (2008) Zooplankton assemblage concordance patterns in Brazilian reservoirs. Hydrobiologia 598:247–255

    Article  Google Scholar 

  • Bird D, Negro JJ (1996) Social behavior of captive fledging American kestrels (Falco sparverius). J Raptor Res 30:240–241

    Google Scholar 

  • Brack V, Cable T, Driscoll D (1985) Food habits of urban American kestrels. Indiana Acad Sci (Zool) 94:607–613

    Google Scholar 

  • Burgas D, Byholm P, Parkkima T (2014) Raptors as surrogates of biodiversity along a landscape gradient. J Appl Ecol 51:786–794

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodal inference: a practical information-theoretic approach. Springer, Nueva York

    Google Scholar 

  • Cabeza M, Arponen A, van Teeffelen A (2008) Top predators: hot or not? A call for systematic assessment of biodiversity surrogates. J Appl Ecol 45:976–980

    Article  Google Scholar 

  • Cardador L, Sardà-Palomera F, Carrete M, Mañosa S (2014) Incorporating spatial constraints in different periods of the annual cycle improves species distribution model performance for a highly mobile bird species. Divers Distrib 20:515–528

    Article  Google Scholar 

  • Caro T (2010) Conservation by proxy. Indicator, umbrella, keystone, flagship, and other surrogate species. Island Press, Washington, DC

    Google Scholar 

  • Castellano S, Balletto E (2002) Is the partial Mantel test inadequate? Evolution 56:1871–1873

    Article  PubMed  Google Scholar 

  • Ceballos G, Ehrlich PR, Dirzo R (2017) Biological annihilation via the ongoing sixth mass extinction signaled by vertebrate population losses and declines. Proc Natl Acad Sc USA 114:E6089–E6096

    Article  CAS  Google Scholar 

  • Conroy S (1999) Lizard assemblage response to a forest ecotone in Northeastern Australia: a synecological approach. J Herpetol 33:409–419

    Article  Google Scholar 

  • Coulson J, Coulson T (1995) Group hunting by Harris’ Hawks in Texas. J Raptor Res 29:265–267

    Google Scholar 

  • Cox J, Kautz R, MacLaughlin M, Gilbert T (1994) Closing the gaps in Florida’s wildlife habitat conservation system. Florida Game and Freshwater Fish Commission, Tallahassee

    Google Scholar 

  • Cueto V, Lopez JC (1999) Determinants of bird species richness: role of climate and vegetation structure at a regional scale. J Biogeogr 26:487–492

    Article  Google Scholar 

  • Danielson B (1991) Communities in a landscape: the influence of habitat heterogeneity on the interactions between species. Am Nat 138:1105–1120

    Article  Google Scholar 

  • 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 13:1030–1040

    PubMed  Google Scholar 

  • Donázar JA, Hiraldo F, Bustamante J (1993) Factors influencing nest site selection, breeding density and breeding success in the Bearded Vulture (Gypaetus barbatus). J Appl Ecol 30:504–514

    Article  Google Scholar 

  • Drever C, Norris K, Martin A (2008) Woodpecker are reliable indicators of bird richness, forest health and harvest. Biol Conserv 141:624–634

    Article  Google Scholar 

  • Eldredge N (1998) Life in the balance. Humanity and the biodiversity crisis. Princeton University Press, Princeton

    Google Scholar 

  • Estrada CG, Rodríguez-Estrella R (2016) In the search of good biodiversity surrogates: are raptors poor indicators in the Baja California Peninsula desert? Anim Conserv 19:360–368

    Article  Google Scholar 

  • Fleishman E, Thomson JR, Mac Nally R, Murphy DD, Fay JP (2005) Using indicator species to predict species richness of multiple taxonomic groups. Conserv Biol 19:1125–1137

    Article  Google Scholar 

  • Gaston KJ (1996) Species richness: measure and measurement. In: Gaston KJ (ed) Biodiversity: a biology of numbers and difference. Blackwell Science, Oxford, pp 77–113

    Google Scholar 

  • Gatto A, Grubb T, Chambers C (2005) Red-tailed hawk dietary overlap with Northern Goshawk on the Kaibab Plateau, Arizona. J Raptor Res 39:439–444

    Google Scholar 

  • George TL (1987) Greater land bird densities on island vs. mainland: relation to nest predation level. Ecology 68:1393–1400

    Article  Google Scholar 

  • Goslee S, Urban D (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19

    Article  Google Scholar 

  • Gregory RD, Strien AV (2010) Wild bird indicators: using composite population trends of birds as measures of environmental health. Ornithol Sci 22:3–22

    Article  Google Scholar 

  • Gregory RD, van Strien A, Vorisek P, Meyling AWG, Noble DG, Foppen RPB, Gibbons DW (2005) Developing indicators for European birds. Philos Trans R Soc B 360:269–288

    Article  Google Scholar 

  • Grelle CE (2002) Is higher-taxon analysis a useful surrogate of species richness in studies of neotropical mammal diversity? Biol Conserv 108:101–106

    Article  Google Scholar 

  • Grenouillet G, Brosse S, Tudeque L, Lek S, Baraille Y, Loot G (2008) Concordance among stream assemblages and spatial autocorrelation along a fragmented gradient. Divers Distrib 14:592–603

    Article  Google Scholar 

  • Grismer L (2002) Amphibians and reptiles of Baja California: 416. In: Grismer L (ed) University of California Press, Los Angeles

  • Guareschi S, Gutiérrez-Cánovas C, Picazo F, Sánchez-Fernández D, Abellán P, Velasco J, Millán A (2012) Aquatic macroinvertebrate biodiversity: patterns and surrogates in mountainous Spanish national parks. Aquat Conserv 22:598–615

    Article  Google Scholar 

  • Guisan A, Zimmerman NE (2000) Predictive habitat distribution models in ecology. Ecol Model 135:147–186

    Article  Google Scholar 

  • Heino J, Paavola R, Virtanen R, Muotka T (2005) Searching for biodiversity indicators in running waters: do bryophytes, macroinvertebrates, and fish show congruent diversity patterns? Biodivers Conserv 14:415–428

    Article  Google Scholar 

  • Heyer WR, Donnelly MA, McDiarmid RW, Hayek LAC, Foster MS (1994) Measuring and monitoring biological diversity: standard methods for amphibians. Smithsonian Institution Press, Washington, DC

    Google Scholar 

  • Hunter ML (2001) Fundamentals in conservation biology. Blackwell Science, Cambridge

    Google Scholar 

  • Instituto Nacional de Estadística, Geografía e Informática (INEGI) (1981) Carta de climas. Escala 1:1,000,000. INEGI, La Paz

  • Instituto Nacional de Estadística, Geografía e Informática (INEGI) (2011) Estados Unidos Mexicanos. XII. Censo General de Población y Vivienda, 2010. Tabulados Básicos y por Entidad Federativa. Bases de Datos y Tabulados de la Muestra Censal. INEGI, La Paz

  • Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P et al (2014) Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346(6215):1320–1331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnsgard P (1990) Hawks, eagles, and falcons of North America. Smithsonian Institution, Washington, DC

    Google Scholar 

  • Jones DT, Eggleton P (2000) Sampling termite assemblages in tropical forests: testing a rapid biodiversity assessment protocol. J Appl Ecol 37:191–203

    Article  Google Scholar 

  • Jones MC, Marron JS, Sheather SJ (1996) A brief survey of bandwidth selection for density estimation. J Am Statist Assoc 91:401–407

    Article  Google Scholar 

  • Juutinen A, Monkkonen M (2004) Testing alternative indicators for biodiversity conservation in old-growth boreal forests: ecology and economics. Ecol Econ 50:35–48

    Article  Google Scholar 

  • Kati V, Devillers P, Dufrêne M, Legakis A, Vokou D, Lebrun P (2004) Testing the value of six taxonomic groups as biodiversity indicators at a local scale. Conserv Biol 18:667–675

    Article  Google Scholar 

  • Kissling W, Field R, Böhning-Gaese K (2008) Spatial patterns of woody plant and bird diversity: functional relationships or environmental effects? Global Ecol Biogeogr 17:327–339

    Article  Google Scholar 

  • Koch AJ, Drever MC, Martin K (2011) The efficacy of common species as indicators: avian responses todisturbance in British Columbia, Canada. Biodivers Conserv 20:3555–3575

    Article  Google Scholar 

  • Lambeck RJ (1997) Focal species: a multi-species umbrella for nature conservation. Conserv Biol 11:849–856

    Article  Google Scholar 

  • Lawton J, May R (1995) Extinction rates. Oxford Press, Oxford

    Google Scholar 

  • Legendre P (1993) Spatial autocorrelation: trouble or new paradigm? Ecology 74:1659–1673

    Article  Google Scholar 

  • Legendre P, Legendre L (1998) Numerical ecology. Developments in environmental modelling, vol 20. Elsevier, Amsterdam

    Google Scholar 

  • Legendre P, Legendre L (2012) Numerical ecology. Elsevier Science BV, Amsterdam

    Google Scholar 

  • Lewandowski AS, Noss RF, Parsons DR (2010) The effectiveness of surrogate taxa for the representation of biodiversity. Conserv Biol 24:1367–1377

    Article  PubMed  Google Scholar 

  • Lindenmayer DB, Barton PS, Lane PW, Westgate MJ, McBurney L, Blair D, Gibbons P, Likens GE (2014) An empirical assessment and comparison of species-based and habitat-based surrogates: a case study of forest vertebrates and large old trees. PLoS ONE 9:e89807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindenmayer DB, Pierson J, Barton PS, Beger M, Branquinho C, Calhoun A, Caro T, Greig H, Gross J, Heino J, Hunter M, Lane P, Longo C, Martin K, McDowell WH, Mellin C, Salo H, Tulloch A, Westgate M (2015) A new framework for selecting environmental surrogates. Sci Total Environ 538:1029–1038

    Article  CAS  Google Scholar 

  • MacArthur R, MacArthur J (1961) On bird species diversity. Ecology 42:594–598

    Article  Google Scholar 

  • Martin K, Ibarra J, Drever M (2015) Avian surrogates in terrestrial ecosystems. In: Lindenmayer D, Barton P, Pierson J (eds) Indicators and surrogates of biodiversity and environmental change. CSIRO Publishing, Clayton South

    Google Scholar 

  • McCallum ML (2007) Amphibian decline or extinction? Current declines dwarf background extinction rate. J Herpetol 41:483–491

    Article  Google Scholar 

  • McCullagh P, Nelder JA (1983) Generalized linear models. Chapman and Hall London, Nueva York

    Book  Google Scholar 

  • Morelli F (2015) Indicator species for avian biodiversity hotspots: combination of specialists and generalists is necessary in less natural environments. J Nat Conserv 27:54–62

    Article  Google Scholar 

  • Morelli F, Mousseau TA, Møller AP (2017) Cuckoos vs. top predators as prime bioindicators of biodiversity in disturbed environments. J Environ Radioactiv 177:158–164

    Article  CAS  Google Scholar 

  • Moreno CE, Pineda E, Escobar F, Sánchez-Rojas G (2007) Shortcuts for biodiversity evaluation: a review of terminology and recommendations for the use of target groups, bioindicators and surrogates. Int J Environ Health 1:71–86

    Article  Google Scholar 

  • Mueller-Dombois M, Ellenberg H (1974) Aims and methods of vegetation ecology. Wiley, New York

    Google Scholar 

  • Mukaka MM (2012) A guide to appropriate use of correlation coefficient in medical research. Malawi Med J 24:69–71

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oksanen J, Blanchet G, Kindt R, Legendre P, Minchin P, O’Hara R, Simpson G, Solymos P, Stevens M, Wagner H (2015) vegan: community ecology package. R package version 2.3-0. http://CRAN.R-project.org/package=vegan

  • Paavola R, Muotka T, Virtanen R, Heino J, Jackson D, Mäki-Petäys A (2006) Spatial scale affects community concordance among fishes, benthic macro- invertebrates, and bryophytes in streams. Ecol Appl 16:368–379

    Article  PubMed  Google Scholar 

  • Padial A, Declerck A, de Meester L, Bonecker C, Lansac-Tôha F, Rodriguez L, Takeda A, Train S, Velho L, Bini L (2012) Evidence against the use of surrogates for biomonitoring of Neotropical floodplains. Freshw Biol 57:2411–2423

    Article  Google Scholar 

  • Partida MAP (2015) Ecología trófica y éxito reproductivo del halcón de Harris en una zona fragmentada del desierto de Baja California Sur, México. Unpubl. M.Sc. thesis. Universidad Autónoma de Tlaxcala. Tlaxcala, México

  • Pearson DL (1994) Selecting indicator taxa for the quantitative assessment of biodiversity. Philos Trans R Soc B 345:75–79

    Article  CAS  Google Scholar 

  • Prendergast J, Eversham B (1997) Species richness covariance in higher taxa: empirical tests of the biodiversity indicator concept. Ecography 20:210–216

    Article  Google Scholar 

  • Preston CR, Beane RD (1993) Red-tailed hawk. The birds of North America. The Academy of Natural Sciences, Philadelphia, PA and The American Ornithologists’ Union, Washington, DC

  • Qian H, Kissling WD (2010) Spatial scale and cross-taxon congruence of terrestrial vertebrate and vascular plant species richness in China. Ecology 91:1172–1183

    Article  PubMed  Google Scholar 

  • Qian H, Kissling WD, Wang X, Andrews P (2009) Effects of woody plant species richness on mammal species richness in southern Africa. J Biogeogr 36:1685–1697

    Article  Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical. R Foundation for Statistical Computing. Vienna. http://www.R-project.org

  • Reynolds RT, Scott JM, Nussbaum RA (1980) A variable circular-plot method for estimating bird numbers. Condor 82:309–313

    Article  Google Scholar 

  • Rivera-Rodriguez L, Rodríguez-Estrella R (1998) Breeding biology of the crested caracara in the Cape region, Baja California, Mexico. J Field Ornithol 69:160–168

    Google Scholar 

  • Rodríguez-Estrella R (1997) Factores que condicionan la distribución y abundancia de las aves terrestres en Baja California Sur, México: El efecto de los cambios al hábitat por actividad humana. Dissertation. Universidad Autónoma de Madrid, Spain

  • Rodríguez-Estrella R (2007) Land use changes affect distributional patterns of desert birds in the Baja California peninsula, Mexico. Divers Distrib 13:877–889

    Article  Google Scholar 

  • Rodríguez-Estrella R, Rivera LBR (1997) Crested Caracara food habits in the Cape region of Baja California, Mexico. J Raptor Res 31:228–233

    Google Scholar 

  • Sætersdala M, Gjerdea I, Bloma HH, Ihlenc PG, Myrsethb EW, Pommerescheb R, Skartveitb J, Solhøyb T, Aas O (2004) Vascular plants as a surrogate species group in complementary site selection for bryophytes, macrolichens, spiders, carabids, staphylinids, snails, and wood living polypore fungi in a northern forest. Biol Conserv 115:21–31

    Article  Google Scholar 

  • Sánchez-Fernández D, Abellán P, Mellado A, Velasco J, Millán A (2006) Are water beetles good indicators of biodiversity in Mediterranean aquatic ecosystems? The case of Segura river basin (SE Spain). Biodivers Conserv 15:4507–4520

    Article  Google Scholar 

  • Santana J, Reino L, Stoate C, Borralho R, Carvalho CR, Schindler S, Moreira F, Bugalho MN, Ribeiro PF, Santos JL, Vaz A, Morgado R, Porto M, Beja P (2013) Mixed effects of long term conservation investment in Natura 2000 farmland. Conserv Lett 7:1–10

    Google Scholar 

  • Seddon PJ, Leech T (2008) Conservation short cut, or long and winding road? A critique of umbrella species criteria. Oryx 42:240–245

    Article  Google Scholar 

  • Sergio F, Newton I, Marchesi L, Pedrini P (2006) Ecologically justified charisma: preservation of top predators delivers biodiversity conservation. J Appl Ecol 43:1049–1055

    Article  Google Scholar 

  • Sergio F, Caro T, Brown D, Clucas B, Hunter J, Ketchum J, McHugh K, Hiraldo F (2008) Top predators as conservation tools: ecological rationale, assumptions, and efficacy. Annu Rev Ecol Evol Syst 391:1–19

    Article  Google Scholar 

  • Shrader-Frechette K, McCoy E (1993) Methods in ecology: strategies for conservation. Cambridge Univ Press, Cambridge

    Book  Google Scholar 

  • Soberón J, Llorente J (1993) The use of species accumulation functions for the prediction of species richness. Conserv Biol 7:480–488

    Article  Google Scholar 

  • Sørensen T (1948) A method of establishing groups of equal amplitude in plant sociology based on similarity of species and its application to analyses of the vegetation on Danish commons. Biol Skr 5:1–34

    Google Scholar 

  • Su JC, Debinski DM, Jakubauskas ME, Kindscher K (2004) Beyond species richness: community similarity as a measure of cross-taxon congruence for coarse-filter conservation. Conserv Biol 18:167–173

    Article  Google Scholar 

  • Taylor R (1990) Interpretation of the correlation coefficient: a basic review. J Diagn Med Sonog 1:35–39

    Article  Google Scholar 

  • The Royal Society (2003) Measuring biodiversity for conservation. The Royal Society, London

    Google Scholar 

  • Tognelli M (2005) Assessing the utility of indicator groups for the conservation of South American terrestrial mammals. Biol Conserv 121:409–417

    Article  Google Scholar 

  • Ward TJ, Vanderklift MA, Nicholls AO, Kenchington RA (1999) Selecting marine reserves using habitats and species assemblages as surrogates for biological diversity. Ecol Appl 9:691–698

    Article  Google Scholar 

  • Wiens JJ, Graham CH (2005) Niche conservatism: integrating evolution, ecology, and conservation biology. Annu Rev Ecol Evol Syst 36:519–539

    Article  Google Scholar 

  • Wiens J, Hayward G, Holthausen R, Wisdom MJ (2008) Using surrogate species and groups for conservation planning and management. Bioscience 58:241–252

    Article  Google Scholar 

  • Williams P, Faith D, Manne L, Sechrestd W, Preston C (2006) Complementarity analysis: mapping the performance of surrogates for biodiversity. Biol Conserv 128:253–264

    Article  Google Scholar 

  • Wilson MJ, Bayley SE (2012) Use of single versus multiple biotic communities as indicators of biological integrity in northern prairie wetlands. Ecol Indic 20:187–195

    Article  Google Scholar 

  • Wilson ED, Cole RF, Nichols JD, Rudran R, Foster MS (1996) Measuring and monitoring biological diversity: standard methods for mammals. Smithsonian Institution Press, Washington, DC

    Google Scholar 

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Acknowledgements

Thanks to G. Ruano, Abelino Cota and F. Cota for field assistance, and to Fabrizio Sergio, C. Gutiérrez-Cánovas and one anonymous reviewer for critical comments and suggestions that improved our drafts. This work was supported by a SEP-CONACYT México Grant (155956) to RRE and by CIBNOR funds. CGE received a Ph.D. scholarship (329819) from CONACYT México. RRE received a CONACyT sabbatical grant during the writing of this manuscript, at the University of Arizona.

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Rodríguez-Estrella, R., Estrada, C.G., Alvarez-Castañeda, S.T. et al. Comparing individual raptor species and coarse taxonomic groups as biodiversity surrogates in desert ecosystems. Biodivers Conserv 28, 1225–1244 (2019). https://doi.org/10.1007/s10531-019-01721-y

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