Our reference: BIOC4915 P-authorquery-v8 AUTHOR QUERY FORM Journal: BIOC Please e-mail or fax your responses and any corrections to: E-mail: [email protected] ^*^7#%N Article Number: 4915 Fax: +31 2048 52799 ELSEVIER Dear Author, Please check your proof carefully and mark all corrections at the appropriate place in the proof (e.g., by using on-screen annotation in the PDF file) or compile them in a separate list. To ensure fast publication of your paper please return your corrections within 48 hours. For correction or revision of any artwork, please consult http://www.elsevier.com/artworkinstructions. Any queries or remarks that have arisen during the processing of your manuscript are listed below and highlighted by flags in the proof. Click on the 'CT link to go to the location in the proof. Location in Query / Remark: click on the 0 link to go article Please insert your reply or correction at the corresponding line in the proof Qi References Cardoso et al. (in preparation) and Caspar et al. (2011) is cited in the text but not listed. Kindly check. Thank you for your assistance. BIOC 4915 No. of Pages 1, Model 5G ARTICLE IN PRESS 1 August 2011 Highlights ► We identify seven impediments to invertebrate conservation. ► Three dilemmas: public, political and scientific. ► Four shortfalls: Linnean, Wallacean, Prestonian and Hutchinsonian. ► We present possible solutions for each impediment. BIOC 4915 No. of Pages 10, Model 5G ARTICLE IN PRESS 1 August 2011 Biological Conservation xxx (2011) xxx-xxx Contents lists available at ScienceDirect Biological Conservation ELSEVIER journal homepage: www.elsevier.com/locate/biocon The seven impediments in invertebrate conservation and how to overcome them Pedro Cardoso a'b'*, Terry L Erwina, Paulo A.V. Borgesb, Tim R. Newc 3 Smithsonian Institution, National Museum of Natural History, 10th & Constitution NW, Washington, DC 20560, USA bAzorean Biodiversity Group (CITA-A), Departamento de Ciencias Agrdrias, Universidade dos Acores, 9700-042 Angra do Heroismo, Portugal cDepartment of Zoology, La Trobe University, Bundoora, Victoria 3086, Australia ARTICLE INFO ABSTRACT }i 11 Article history: Despite their high diversity and importance for humankind, invertebrates are often neglected in biodiver- 25 12 Received 12 January 2011 sity conservation policies. We identify seven impediments to their effective protection: (1) invertebrates 26 13 Received in revised form 13 July 2011 and their ecological services are mostly unknown to the general public (the public dilemma): (2) policy- 27 14 Accepted 19 July 2011 makers and stakeholders are mostly unaware of invertebrate conservation problems (the political 28 15 Available online xxxx dilemma): (3) basic science on invertebrates is scarce and underfunded (the scientific dilemma): (4) most 29 species are undescribed (the Linnean shortfall): (5) the distribution of described species is mostly 30 16 Keywords: unknown (the Wallacean shortfall): (6) the abundance of species and their changes in space and time 31 17 Conservation priorities 32 18 Ecosystem services are unknown (the Prestonian shortfall): (7) species ways of life and sensitivities to habitat change are lar- 33 19 Extinction gely unknown (the Hutchinsonian shortfall). 20 Information shortfalls Numerous recent developments in taxonomy, inventorying, monitoring, data compilation, statistical 34 21 Science funding analysis and science communication facilitate overcoming these impediments in both policy and prac- 35 22 Species diversity tice. We suggest as possible solutions for the public dilemma: better public information and marketing. 36 23 For the political dilemma: red-listing, legal priority listing and inclusion in environmental impact assess- 37 ment studies. For the scientific dilemma: parataxonomy, citizen science programs and biodiversity infor- 38 matics. For the Linnean shortfall: biodiversity surrogacy, increased support for taxonomy and advances in 39 taxonomic publications. For the Wallacean shortfall: funding of inventories, compilation of data in public 40 repositories and species distribution modeling. For the Prestonian shortfall: standardized protocols for 41 inventorying and monitoring, widespread use of analogous protocols and increased support for natural 42 history collections. For the Hutchinsonian shortfall: identifying good indicator taxa and studying extinc- 43 tion rates by indirect evidence. 44 © 2011 Published by Elsevier Ltd. 45 46 47 48 1. The importance of invertebrates parasitoids, even hyper-parasitoids, or the top predators of a long 62 chain. They may be cosmopolitan, or present in extremely re- 63 49 Invertebrates dominate among multicellular organisms in stricted distributions of a few hectares (e.g. some cave adapted 64 50 terms of richness, abundance and often biomass; for example, species). They live on land, in fresh water, and in all the oceans 65 51 more than 100,000 species of terrestrial arthropods occupy a single of the world. With such richness of species and roles in all ecosys- 66 52 hectare of rain forest in the western Amazon (Erwin et al„ 2004) tems, preserving the diversity of invertebrates, as of all other 67 53 and there is more ant biomass in the soils of the Serengeti Plains organisms, is a true life insurance for humankind. As eloquently 68 54 than there is of surface mammals (Holldobler and Wilson, 1990). noted by Wilson (1987), "If human beings were to disappear 69 55 About 80% of all described species are invertebrates. Beetles alone tomorrow, the world would go on with little change. (...) But if 70 56 comprise at least 10 times the number of species of all vertebrates invertebrates were to disappear, I doubt that the human species 71 57 together and over 25% of all described species. Invertebrates may could last more than a few months". 72 58 be as small as 30-40 p,m (male Cycliophorans, which have fewer The ways human beings benefit from the conservation of inver- 73 59 than 60 cells on average (Neves et al„ 2009)) or as large as 14 m tebrates are hard to quantify and the general public is often una- 74 60 (the colossal squid Mesonychoteuthis hamiltoni). They may be ware of them. A study by Costanza et al. (2007) calculated that 75 61 saprophagous, phytophagous, symbionts, parasites, endo and ecto- global ecosystem services are valued at US$33 trillion per year, a 76 large part of it directly or indirectly related with invertebrates. 77 By 2050, biodiversity loss will be valued at 7% of the World's 78 * Corresponding author at: Azorean Biodiversity Group (CITA-A), Universidade dos Acores, Rua Capitao Joao d'Avila, 9700-042 Angra do Heroismo, Portugal. Tel.: GDP (see: http://ec.europa.eu/environment/nature/biodiversity/ 79 +351 295 402 200: fax: +351 295 402 205. economics/teeb_en.htm). In the United States alone, and with a 80 E-mail address: [email protected] (P. Cardoso). conservative and partial estimate, ecological services provided by 81 0006-3207/$ - see front matter © 2011 Published by Elsevier Ltd. doi:10.1016/j.biocon.2011.07.024 Please cite this article in press as: Cardoso, P., et al. The seven impediments in invertebrate conservation and how to overcome them. Biol. Conserv. (2011), doi: 10.1016/j.biocon.2011.07.024 BIOC4915 No. of Pages 10, Model 5G ARTICLE IN PRESS 1 August 2011 P. Cardoso et al./Biological Conservation xxx (2011) xxx-xxx 82 insects annually were valued at US$57 billion (Losey and Vaughan, Dunn et al., 2009). When corrected for knowledge bias, data from 137 83 2006). invertebrates show even higher extinction rates and proportions 138 84 In order to reiterate the importance of ecosystems and their of threatened species than those of well-known taxa such as birds 139 85 constituent species to humankind, ecosystem services have been and mammals (MacKinney, 1999; Moir et al., 2010; Stork and Lyal, 140 86 divided in four broad categories by the Millennium Ecosystem 1993; Thomas and Morris, 1994). Nevertheless, only 70 species 141 87 Assessment (2003, 2005): provisioning, regulating, cultural, and have been officially reported extinct for the last 600 years (Dunn, 142 88 supporting services. 2005), all others having vanished before discovery or description, 143 the so-called Centinelan (Wilson, 1992) or Linnean extinctions 144 89 1.1. Provisioning services (Cardoso et al., 2010; Ladle and Jepson, 2008; Regnier et al., 145 2009; Triantis et al., 2010). 146 90 These are related with the goods that humans can use and The loss of species often implies the loss of functional diversity 147 91 trade. Besides being or providing food (e.g. molluscs, bees), inver- and the provision of ecosystem services, with consequences to hu- 148 92 tebrates yield many new pharmaceuticals and compounds or pro- man well-being (Section 1; see a review in Balvanera et al., 2006). 149 93 cesses useful for technological and industrial purposes (see: http:// The loss of pollinators may cause the loss of productivity in many 150 94 www.wwf.org.au/publications/wwf-2010-and-beyond/), or may crops (Kremen et al., 2002; Kremen and Ostfeld, 2005); the loss of 151 95 even be a target for mining activities (e.g. coral reefs). predators and parasitoids in agricultural fields may cause the loss 152 of ecosystem capacity to control pest outbreaks and the conse- 153 96 1.2. Regulating services quent loss in productivity (Landis et al., 2000; Symondson et al., 154 2002); the loss of groundwater fauna may cause the disruption 155 97 These are related to the benefits of regulation of ecosystem pro- of purification and bioremediation processes and consequent pol- 156 98 cesses provided by the different species. These services include lution problems (Boulton et al., 2008); the loss of coral reefs may 157 99 pollination (e.g. of crop cultures), trophic regulation (e.g. pest con- cause diminishing returns from tourism (Moberg and Folke, 158 100 trol), or water purification (e.g. of ground waters by cave-obligate 1999); among many other examples.