Our reference: BIOC4915 P-authorquery-v8 AUTHOR QUERY FORM ^*^7#%N Journal: BIOC Article Number: 4915 Please e-mail or fax your responses and any corrections to: E-mail: corrections.esch@elsevier.sps.co.in 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 article Query / Remark: click on the 0 link to go 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 1 August 2011 ARTICLE IN PRESS Highlights No. of Pages 1, Model 5G ? 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 1 August 2011 ARTICLE IN PRESS No. of Pages 10, Model 5G Biological Conservation xxx (2011) xxx-xxx ELSEVIER Contents lists available at ScienceDirect Biological Conservation 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: 12 Received 12 January 2011 13 Received in revised form 13 July 2011 14 Accepted 19 July 2011 15 Available online xxxx 16 Keywords: 17 Conservation priorities 18 Ecosystem services 19 Extinction 20 Information shortfalls 21 Science funding 22 Species diversity 23 Despite their high diversity and importance for humankind, invertebrates are often neglected in biodiver- sity conservation policies. We identify seven impediments to their effective protection: (1) invertebrates and their ecological services are mostly unknown to the general public (the public dilemma): (2) policy- makers and stakeholders are mostly unaware of invertebrate conservation problems (the political dilemma): (3) basic science on invertebrates is scarce and underfunded (the scientific dilemma): (4) most species are undescribed (the Linnean shortfall): (5) the distribution of described species is mostly unknown (the Wallacean shortfall): (6) the abundance of species and their changes in space and time are unknown (the Prestonian shortfall): (7) species ways of life and sensitivities to habitat change are lar- gely unknown (the Hutchinsonian shortfall). Numerous recent developments in taxonomy, inventorying, monitoring, data compilation, statistical analysis and science communication facilitate overcoming these impediments in both policy and prac- tice. We suggest as possible solutions for the public dilemma: better public information and marketing. For the political dilemma: red-listing, legal priority listing and inclusion in environmental impact assess- ment studies. For the scientific dilemma: parataxonomy, citizen science programs and biodiversity infor- matics. For the Linnean shortfall: biodiversity surrogacy, increased support for taxonomy and advances in taxonomic publications. For the Wallacean shortfall: funding of inventories, compilation of data in public repositories and species distribution modeling. For the Prestonian shortfall: standardized protocols for inventorying and monitoring, widespread use of analogous protocols and increased support for natural history collections. For the Hutchinsonian shortfall: identifying good indicator taxa and studying extinc- tion rates by indirect evidence. ? 2011 Published by Elsevier Ltd. 47 48 1. The importance of invertebrates 49 Invertebrates dominate among multicellular organisms in 50 terms of richness, abundance and often biomass; for example, 51 more than 100,000 species of terrestrial arthropods occupy a single 52 hectare of rain forest in the western Amazon (Erwin et al? 2004) 53 and there is more ant biomass in the soils of the Serengeti Plains 54 than there is of surface mammals (Holldobler and Wilson, 1990). 55 About 80% of all described species are invertebrates. Beetles alone 56 comprise at least 10 times the number of species of all vertebrates 57 together and over 25% of all described species. Invertebrates may 58 be as small as 30-40 p,m (male Cycliophorans, which have fewer 59 than 60 cells on average (Neves et al? 2009)) or as large as 14 m 60 (the colossal squid Mesonychoteuthis hamiltoni). They may be 61 saprophagous, phytophagous, symbionts, parasites, endo and ecto- * Corresponding author at: Azorean Biodiversity Group (CITA-A), Universidade dos Acores, Rua Capitao Joao d'Avila, 9700-042 Angra do Heroismo, Portugal. Tel.: +351 295 402 200: fax: +351 295 402 205. E-mail address: pcardoso@ennor.org (P. Cardoso). 0006-3207/$ - see front matter ? 2011 Published by Elsevier Ltd. doi:10.1016/j.biocon.2011.07.024 parasitoids, even hyper-parasitoids, or the top predators of a long chain. They may be cosmopolitan, or present in extremely re- stricted distributions of a few hectares (e.g. some cave adapted species). They live on land, in fresh water, and in all the oceans of the world. With such richness of species and roles in all ecosys- tems, preserving the diversity of invertebrates, as of all other organisms, is a true life insurance for humankind. As eloquently noted by Wilson (1987), "If human beings were to disappear tomorrow, the world would go on with little change. (...) But if invertebrates were to disappear, I doubt that the human species could last more than a few months". The ways human beings benefit from the conservation of inver- tebrates are hard to quantify and the general public is often una- ware of them. A study by Costanza et al. (2007) calculated that global ecosystem services are valued at US$33 trillion per year, a large part of it directly or indirectly related with invertebrates. By 2050, biodiversity loss will be valued at 7% of the World's GDP (see: http://ec.europa.eu/environment/nature/biodiversity/ economics/teeb_en.htm). In the United States alone, and with a conservative and partial estimate, ecological services provided by 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 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 1 August 2011 ARTICLE IN PRESS No. of Pages 10, Model 5G P. Cardoso et al./Biological Conservation xxx (2011) xxx-xxx 82 insects annually were valued at US$57 billion (Losey and Vaughan, 83 2006). 84 In order to reiterate the importance of ecosystems and their 85 constituent species to humankind, ecosystem services have been 86 divided in four broad categories by the Millennium Ecosystem 87 Assessment (2003, 2005): provisioning, regulating, cultural, and 88 supporting services. 89 1.1. Provisioning services 90 These are related with the goods that humans can use and 91 trade. Besides being or providing food (e.g. molluscs, bees), inver- 92 tebrates yield many new pharmaceuticals and compounds or pro- 93 cesses useful for technological and industrial purposes (see: http:// 94 www.wwf.org.au/publications/wwf-2010-and-beyond/), or may 95 even be a target for mining activities (e.g. coral reefs). 96 1.2. Regulating services 97 These are related to the benefits of regulation of ecosystem pro- 98 cesses provided by the different species. These services include 99 pollination (e.g. of crop cultures), trophic regulation (e.g. pest con- 100 trol), or water purification (e.g. of ground waters by cave-obligate 101 aquatic species). 102 1.3. Cultural services These are non-material benefits. Invertebrates may serve as touristic attractions (e.g. coral reefs, butterflies), and many species are also essential model organisms for the study of biology, for example, the genetics of Drosophila and the many studies on increasing life-span performed with nematodes. In addition, many invertebrates are regularly used for environmental monitoring purposes (e.g. aquatic insects), as indicators of changes in the eco- systems that may not be felt as promptly in other taxonomic groups. Existence values are related with the willingness to pay for the conservation of species and communities (Martin-Lopez et al., 2007). These are often prominent in flagship species, such as butterflies, dragonflies and corals, with which people may feel affinity or sympathy. 1.4. Supporting services These are necessary for the production of all other ecosystem services and only indirectly impact on people's lives. Supporting services provided by invertebrates include nutrient cycling (e.g. dung burial, nitrogen volatilization), soil and ecosystem formation (e.g. aeration by tunneling, coral reefs) or as food source to other species (e.g. to commercial fisheries or game vertebrates). 2. The neglect of invertebrates One of the major crises Earth's ecological stability faces today is the ever-growing and accelerating mass extinction of species due to human activities (Erwin, 1991a; Lawton and May, 1995; Purvis and Hector, 2000; Smith et al., 1993). Our knowledge of global bio- diversity and its rate of extinction is very limited, but of the 3-100 million species believed to exist, conservative estimates point to about 3000 being lost each year, that is, eight species per day (Wil- son, 2003a; Gonzalez-Oreja, 2008). The vast majority belongs to understudied taxa such as certain groups of invertebrates, "the lit- tle things that run the world" (Evans, 1993; Wilson, 1987). They are subject to the same extinction processes as larger and more familiar organisms, plus a few additional ones, such as co-extinc- tion and extinction of narrow habitat specialists (Dunn, 2005; Dunn et al., 2009). When corrected for knowledge bias, data from 137 invertebrates show even higher extinction rates and proportions 138 of threatened species than those of well-known taxa such as birds 139 and mammals (MacKinney, 1999; Moir et al., 2010; Stork and Lyal, 140 1993; Thomas and Morris, 1994). Nevertheless, only 70 species 141 have been officially reported extinct for the last 600 years (Dunn, 142 2005), all others having vanished before discovery or description, 143 the so-called Centinelan (Wilson, 1992) or Linnean extinctions 144 (Cardoso et al., 2010; Ladle and Jepson, 2008; Regnier et al., 145 2009; Triantis et al., 2010). 146 The loss of species often implies the loss of functional diversity 147 and the provision of ecosystem services, with consequences to hu- 148 man well-being (Section 1; see a review in Balvanera et al., 2006). 149 The loss of pollinators may cause the loss of productivity in many 150 crops (Kremen et al., 2002; Kremen and Ostfeld, 2005); the loss of 151 predators and parasitoids in agricultural fields may cause the loss 152 of ecosystem capacity to control pest outbreaks and the conse- 153 quent loss in productivity (Landis et al., 2000; Symondson et al., 154 2002); the loss of groundwater fauna may cause the disruption 155 of purification and bioremediation processes and consequent pol- 156 lution problems (Boulton et al., 2008); the loss of coral reefs may 157 cause diminishing returns from tourism (Moberg and Folke, 158 1999); among many other examples. 159 Despite their high diversity and importance for humankind, 160 invertebrates have largely been neglected in conservation studies 161 and policies worldwide (Cardoso et al., in press; Kremen et al., 162 1993; New, 1999; Zamin et al., 2010). Reflecting this neglect, the 163 World Conservation Union's (IUCN) Red List of Threatened Species 164 (IUCN, 2010) lists less than 0.5% of all described arthropods and 4% 165 of all described molluscs worldwide (Fig. 1), when most verte- 166 brates have already been assessed. Of all the species evaluated, 167 the endangered categories occupy similar if not higher proportions 168 than comparable numbers for vertebrates (Fig. 1). Even if such pro- 169 portions are inflated by the evaluation of species thought a priori to 170 be endangered, the increases are countered by the vast numbers of 171 undescribed species that mostly have restricted distributions and 172 have not yet been collected or diagnosed (Gaston, 1994). National 173 red lists follow the same trend, with invertebrates being among the 174 taxa with the least comprehensive coverage in countries world- 175 wide (Zamin et al., 2010). 176 Even in areas such as Europe where invertebrate species are rel- 177 atively well known (Fig. 2a; Schuldt and Assmann, 2010), the sup- 178 port given to their conservation is markedly inappropriate 179 considering their role in ecological processes upon which a healthy 180 planet and human welfare depend (Leather, 2009). The largest 181 funding program for the conservation of species and habitats in 182 Europe is the LIFE-Nature program. Justification for funding is lar- 183 gely based on the priority lists of the Habitats and Birds Directives. 184 Because such lists are markedly biased towards some well-known 185 taxa, funding is equally biased (Fig. 2b; see also Cardoso, in press). 186 On average, each arthropod species received 1000 times less fund- 187 ing for its conservation than each mammal species (Fig. 2c). 188 Contradicting the low level of conservation support given to 189 invertebrates, when evaluated in equal stance to vertebrates, they 190 rank high in conservation priority lists. In a recent resource alloca- 191 tion exercise for the Macaronesian archipelagos (Martin et al., 192 2010), using unbiased criteria to rank almost every insular taxon, 193 invertebrates constituted more than twice the number of verte- 194 brates among the highest ranking species. This was in a rank 195 largely dominated by plants, which are also remarkably under- 196 represented in most conservation efforts (Figs. 1 and 2). In the 197 Azores, where invertebrates have been thoroughly studied (Borges 198 et al., 2005; Cardoso et al., 2007; Caspar et al., 2008, in press; 199 Triantis et al., 2010), more so than in the other archipelagos and 200 most other regions worldwide, they constituted more than half 201 of all priority species (Martin et al., 2010). 202 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 BIOC 4915 1 August 2011 ARTICLE IN PRESS No. of Pages 10, Model 5G P. Cardoso et al. /Biological Conservation xxx (2011) xxx-xxx (a) 100% 90% 80% 70% 60% 50% 40% 30% 20% 10% 0% (b) 100% 90% 80% 70% 60% 50% 40% 30% 20% 10% 0% i Evaluated NT/LR/LC VU ? EN ? CR ? EX/EW * ** / <$ # / f ^ // Scientific I Political Linnean => Hutchinsonian d II Wallacean .=> Prestonian Scientific shortfalls Fig. 3. The seven impediments in invertebrate conservation and respective relations. to understand the concepts (Jacobson et al., 2007; Labao et al., 2008). Initiatives as simple as using common names for species may radically change the public perception regarding invertebrates (New, 2008, 2010; Samways, 2005). Even imaginative scientific names may easily capture public attention, including naming spe- cies after celebrities, such as Kate Winslett and Arnold Schwarze- negger (Erwin, 2002). As often heard in lectures given by Daniel Janzen about species and ecosystems, "if you don't know it, you can't love it, if you don't love it, you won't save it." 3.2. Policymakers and stakeholders are mostly unaware of 251 invertebrate conservation problems (the political dilemma) 252 Policymakers and stakeholders usually assume that protected 253 large animals will serve as "umbrella" species, protecting all other 254 species occupying the same habitats (Simberloff, 1998). This view 255 is however largely unsupported and untested. In the vast majority 256 of cases it is simply assumed (Cabeza et al., 2008; Mufioz, 2007; 257 Prendergast et al., 1993; Roth and Weber, 2008; Simberloff, 258 1998). When tested, the concept often fails (Martin et al., 2010; 259 Schuldt and Assmann, 2010). Indeed, our lack of knowledge may 260 preclude investigation of any such relationships for most inverte- 261 brate groups, because the questions cannot be framed. Misconcep- 262 tions regarding the effectiveness of umbrella species have been 263 detrimental to possible invertebrate conservation, by limiting the 264 amount of available funding. 265 As with the general public, information regarding the impor- 266 tance of invertebrates in ecosystem functioning may be very effec- 267 tive in explaining the value of less charismatic species to 268 policymakers and stakeholders. Without legal value but with polit- 269 ical significance, mechanisms such as the IUCN Red List are power- 270 ful tools for lobbying and this use should increase (Mace et al., 271 2008; Rodrigues et al., 2006). Many invertebrate taxa have recently 272 been assessed, especially molluscs, butterflies, dragonflies, fresh- 273 water crabs, and corals (Clausnitzer et al., 2009; Cumberlidge 274 et al., 2009; IUCN, 2010; Lewis and Senior, 2011). There are also 275 many regional studies already published (e.g. butterflies and drag- 276 onflies in Europe) (Kalkman et al., 2010; Van Swaay et al., 2010, 277 2011). After red-listing, it may be easier to include a species in con- 278 servation priority lists with legal support. Legally binding lists 279 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 BIOC 4915 1 August 2011 ARTICLE IN PRESS No. of Pages 10, Model 5G P. Cardoso et al./Biological Conservation xxx (2011) xxx-xxx 280 should include more species, chosen according to objective param- 281 eters applicable to all organisms (Martin et al., 2010). Finally, envi- 282 ronmental impact assessment studies should not be limited to 283 abundant, non-threatened organisms, which are often widespread. 284 These three measures (red-listing, legal priority listing and inclu- 285 sion in environmental impact assessment studies) would force 286 stakeholders to include invertebrates in their plans and the knowl- 287 edge regarding each putatively threatened invertebrate species 288 could rapidly increase without public expenditure. 289 3.3. Basic science on invertebrates is scarce and underfunded (the 290 scientific dilemma) 291 Traditional taxonomy is on the verge of extinction, facing ever 292 scarcer resources, and mostly regarded as "counting for the sake 293 of counting", with "modern" sciences occupying taxonomy's for- 294 mer space (Boero, 2001, 2010; Leather and Quicke, 2009; Wheeler, 295 2007). Taxonomists are moving towards other fields and many of 296 those remaining, besides approaching retirement, are based in 297 countries where most species are already known (Gaston and 298 May, 1992; Kim, 1993). Natural history and ecological studies, 299 based on broad sampling programs that allow knowing the species 300 distributions and abundances, how such parameters change in 301 space and time and how these changes relate with ecological 302 change are also largely neglected (Cotterill and Foissner, 2010; 303 Kim, 1993). 304 A number of partial solutions are in effect to counter the lack of 305 experienced taxonomists, even if modern taxonomy is more con- 306 cerned with resolving high-level phytogenies using molecular 307 techniques that require specialized skills and equipment, than with 308 basic species descriptions and diagnoses. Especially in the tropics, 309 parataxonomists with training that allows them to recognize and < 310 sort morphospecies are often used with success (Basset et al., 311 2004; Janzen, 2004; Pearson et al., 2011). Amateurs are frequently 312 the most proficient descriptors of species in many taxa (Pearson 313 et al., 2011) and, often integrated in citizen science programs, also 314 provide extremely useful data on the distribution and abundance 315 of species (Braschler, 2009; Cohn, 2008; Silverton, 2009). Given 316 the high costs of obtaining comparative taxonomic and ecological 317 information, cybertaxonomy (Table 2; Wheeler, 2004, 2007; 318 Wheeler et al., 2004), and the field of biodiversity informatics in 319 general allow the efficient and universal access to species lists, dis- 320 tribution databases and ecological data. Biodiversity informatics 321 facilitates species identification and access to a wealth of informa- 322 tion (Borges et al., 2010; Wilson, 2000, 2003b). 323 3.4. Most species are undescribed (the Linnean shortfall) 324 Most living species are still to be described (Erwin et al., 2004; 325 May, 1999). This problem is especially prevalent in invertebrates, 326 with researchers still far from agreeing on the possible number 327 of species, estimated to be anywhere between 3 and 50 million, 328 with the most probable estimates between 5 and 30 million (Erwin et al., 2004; Wilson, 2000; but see Novotny et al., 2002). When more than one order of magnitude separates different global richness estimates, the size of this so-called "Linnean shortfall" be- comes obvious (Brown and Lomolino, 1998). In fact, the number of new species described every year is not approaching an asymptote. About 15,000 new species and sub-species of invertebrates are recorded by Zoological Record each year (see: http://www.organ ismnames.com). This represents one new taxon (mostly species) described every 35 min. And yet, at the present rate of description, and even by the most conservative estimates claiming that half the species have already been described, it could take close to 100 years to reach the end of the process. Hundreds of thousands of species may become extinct before description (Gonzalez-Oreja, 2008). Surrogacy, either by higher taxa (Gaston and Williams, 1993) or by indicator taxa (Pearson and Cassola, 1992), can be an efficient way of obtaining useful information for conservation without the need to identify every single species. This strategy allows the retention of broad biological information enabling the understand- ing of distribution patterns and efficiency in the definition of con- servation priority areas. Its use is, however, necessarily limited and for most conservation questions it is in fact important to know the species identity. The resolution of this impediment ultimately depends on the resolution of others, predominantly, the lack of taxonomists and the wider recognition by policymakers that to conserve biodiversity it may be important to know what biodiver- sity is present. Knowledge allows wise decisions and should guide priorities for best use of very restricted resources available for practical conservation. Importantly, new projects have appeared funded by the US National Science Foundation, such as the Partner- ships to Enhance Expertise in Taxonomy (PEET), Assembling the Tree of Life (AToL), and the Planetary Biodiversity Inventory (PBI) and the Smithsonian Institution, such as the currently developing Global Genome Project. In Europe, the EDIT project is a good example of taxonomy enhancement. In addition, new advances in taxonomic publication processes are designed to speed species information automatically to diverse users (Penev et al., 2008, 2011). 3.5. The distribution of described species is mostly unknown (the Wallacean shortfall) Most species remain undescribed and unknown. Recognizing and describing them is, however, just the beginning of a process. For most of the species already described, we probably know little more than some morphological characteristics and a few, if not a single, locality (as a spot distribution within an unknown range). This shortfall was named by Lomolino (2004) as the "Wallacean shortfall". Compiling good distributional data is the first stage of any systematic conservation planning exercise (Margules and Pressey, 2000). Without reasonable information of where species live, it is impossible to know which are endangered and where to concentrate efforts to preserve them. Table 2 Examples of cybertaxonomy projects. Name Target taxa Geographical extent URL DELTA Several World EUTAXA Several Europe Ground beetles of Ireland Carabidae Ireland National Barkfly Recording Scheme Psocoptera United Kingdom NatureGate Several Finland Spinnen Mittclcuropa% Araneae Central Europe UK Butterflies Lepidoptera United Kingdom UK Moths Lepidoptera United Kingdom Universal Chalcidoidea Database Hymenoptera World http://delta-intkey.com/www/data.htm http://www.eutaxa.com/ http://www.habitas.org.uk/groundbeetles/index.html http://www.brc.ac.uk/schemes/barkfly/homepage.htm http://www.luontoportti.com/suomi/en/ http://www.araneae.unibe.ch/ http://www.ukbutterflies.co.uk/ http://www.ukmoths.org.uk/ http://www.nhm.ac.uk/research-curation/research/projects/chalcidoids/keysl_14.html 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 1 August 2011 ARTICLE IN PRESS No. of Pages 10, Model 5G P. Cardoso et al./Biological Conservation xxx (2011) xxx-xxx Qi Table 3 Examples of large-scale sampling initiatives. Name Target taxa Geographical extent URL or reference Arthropod Initiative of the Smithsonian Several Tropics Center for Tropical Forest Science BALA Arthropods Azores COBRA Spiders Worldwide ALL Ants Tropics TEAM Several Tropics RAP Several Worldwide Pollard and Yates Butterflies Worldwide http://www.ctfs.si.edu/group/arthropodmonitoring Borges et al. (2005), Cardoso et al. (2007), and Caspar et al. (2008, 3844<) Cardoso (2009) and Cardoso et al. (in preparation) Agosti and Alonso (2000) http://www.teamnetwork.org/en/ https://learning.conservation.org/biosurvey/RAP/Pages/default.aspx Pollard and Yates (1993) A suggestion for overcoming the Wallacean shortfall implies the recognition that there is need to enhance the funding of traditional local and regional inventories, if possible using adequate standard- ized and optimized protocols (see below). Nonetheless, such data need to be readily available. Different initiatives compile distribu- tion data of diverse taxa from local to global levels, most remark- ably, the GBIF - Global Biodiversity Information Facility (http:// www.gbif.org). It intends to compile in a single platform all data, especially primary data, stored in thousands of museums world- wide. But even compiling all available information this will be scat- tered and probably biased for most taxa (Mortal et al., 2007), with documented distribution tending to be that of interested special- ists and where they have collected. Several species distribution modeling techniques have therefore been proposed to fill the gaps in information (Elith et al., 2006; Hernandez et al., 2006; Phillips et al., 2006). These allow mapping the probabilities of occurrence for species for which only some records are available by evaluating what climatic, land-use or other variables are suitable for the occurrence of the species. Such probabilities of occurrence can be used in conservation planning (Cabeza et al., 2010; Williams and Araujo, 2000) together with a number of other variables, such as management costs and prevalence of threats. Although such distribution models may present several problems, often not tak- ing into account the way of life and history of taxa, species interac- tions or the possibly biased geographical sampling (Soberon and Nakamura, 2009), they can be seen as a way of reducing the unavoidable bias of using data from only a few scattered places for conservation planning (Diniz-Filho et al., 2010). 3.6. The abundance of species and their changes in space and time are unknown (the Prestonian shortfall) Absolute abundances of invertebrates are usually impossible to obtain and too variable to measure. Hence, we have to trust on rel- ative abundance. This can be compared in space (through invento- rying) and time (through monitoring), both processes presuming we can recognize and categorize the entities we measure. Studying such variables requires standardized and optimized sampling protocols (Cardoso, 2009; Duelli, 1997; Duelli et al., 1999; Erwin, 1991b; Jones and Eggleton, 2000; Regnier et al., 2009; Stork et al., 1996). Researchers involved in invertebrate sampling, how- ever, usually do not immediately extract all information possible to obtain from the specimens collected. Those data vanish in time, with specimens being forgotten or even lost in privately-run col- lections, even in universities. The collected material is therefore not usable to its full potential. Given the work by Frank W. Preston on the commonness and rarity of species and their changes in space and time (Preston, 1948, i960) we refer to this impediment as the "Prestonian shortfall". Improvement of sampling and analytical methods for biodiver- sity assessment and monitoring has been identified as an important priority in insect conservation and diversity research (Didham et al., 2010; Kim, 1993). Standard protocols have been proposed for large-scale or even global comparative inventories 431 (Table 3) of different taxa such as ants (Agosti and Alonso, 2000) 432 and butterflies (Pollard and Yates, 1993). Based on a semi- 433 quantitative sampling strategy first proposed by Coddington 434 et al. (1991), Cardoso (2009) proposed guidelines and statistical 435 methods to improve the standardization and optimization of 436 arthropod inventories, and demonstrated that it is possible to sam- 437 pie in a standardized, yet optimized, way. The use of standardized 438 and optimized protocols, well-supported by extensive data, may 439 contribute to the more rapid accumulation of knowledge in ways 440 that allow using all the information to its full potential, for a num- 441 ber of different studies (Diniz-Filho et al., 2010; Kremen et al., 442 1993). There is also a need for long term ecological studies to mon- 443 itor ecosystem change through time and such studies also require 444 standardized and optimized protocols for good indicator inverte- 445 brate taxa. The new NSF-funded program NEON is beginning to 446 piece together the protocols for exactly this strategy. Preserving 447 all possible information for future studies, often impossible to 448 predict, is possible only if specimens are maintained as long-term, 449 secure, archive collections with full documentation. This preserva- 450 tion is best accomplished through the support of natural history 451 collections, namely in museums, which constitute rich sources of 452 long-term datasets (Cotterill and Foissner, 2010; Lister et al., 2011). 453 3.7. Species ways of life and sensitivities to habitat change are largely 454 unknown (the Hutchinsonian shortfall) 455 In addition to grossly inadequate taxonomic, distributional and 456 abundance knowledge, the very diverse ways of life (autecological 457 aspects) and the ecosystem services associated with the different 458 species are usually unknown. This impediment was named by 459 Mokany and Ferrier (2011) as the "Hutchinsonian shortfall". Not 460 knowing what species contribute to what ecosystem services 461 means that the full consequences of species extinctions are extre- 462 mely hard to predict. Complementary information, such as sensi- 463 tivity to ecological change driven by anthropogenic causes, is 464 known only for a limited number of species (Kozlowski, 2008). 465 Even in the best-documented faunas the threats to most individual 466 species can be suggested in only general terms, often drawing on 467 knowledge of biologically different but related species elsewhere. 468 Our knowledge is however steadily growing. Many invertebrate 469 species are now known to be sensitive to ecological change (e.g. 470 Basset et al., 2008; Cardoso et al., 2007) and when sufficient data 471 is available it is even possible to infer on the past (Cardoso et al., 472 2010) or future (Fonseca, 2009; Triantis et al., 2010) man-caused 473 extinctions of numerous species. Moreover, many invertebrates 474 are susceptible to extinction causes that mostly do not occur in 475 better-known taxa, such as extreme habitat specificity and co- 476 extinctions along with hosts (Dunn, 2005; Dunn et al., 2009). In- 477 deed, coextinction may be the most common form of extinction 478 (Dunn et al., 2009; Moir et al., 2010). Although the ecology and 479 sensitivity to habitat change of most species is unknown, many 480 studies indicate that invertebrates can be as sensitive as any other 481 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 BIOC 4915 1 August 2011 ARTICLE IN PRESS No. of Pages 10, Model 5G P. Cardoso et al./Biological Conservation xxx (2011) xxx-xxx 482 taxa (MacKinney, 1999). Given their variety of species, sizes and 483 functional roles, with short generation times, rapid evolutionary 484 rates and often marked habitat fidelity, many invertebrate taxa 485 are indeed ideal indicators of habitat change caused by human 486 activity, more so than vertebrates, providing datasets with higher 487 temporal and spatial resolution for conservation (Diniz-Filho 488 et al., 2010; Caspar et al., in press; Kremen et al., 1993). 489 4. Conclusions 490 We have outlined seven topics that we regard as impediments 491 that hamper progress in the conservation of invertebrate species 492 at a global level. These impediments represent only one of the sev- 493 eral possible ways of dividing the problems related to invertebrate 494 conservation. Nevertheless, we think that the present division is 495 constructive. It is the public and politicians who ultimately decide 496 which science is worth supporting at each moment. The Linnean 497 shortfall is the obvious basis for the other scientific shortfalls 498 (Fig. 3). The Wallacean, Prestonian and Hutchinsonian shortfalls 499 have parallels with the three basic forms of rarity, by respectively 500 relating with distribution, abundance and habitat (Gaston, 1994; 501 Rabinowitz, 1981). 502 We also list possible ways of overcoming such impediments 503 and they are therefore not intractable. In fact, we mention a num- 504 ber of initiatives, not in any way comprehensively, that indicate 505 progress. At least in developed countries it should be easy to incor- 506 porate effective invertebrate conservation in environmental poli- 507 cies in full parallel to other taxa. In underdeveloped countries, 508 where most invertebrate diversity resides, all these problems are 509 far greater. Funding and appropriate environmental policies are 510 lacking even for charismatic taxa. Nevertheless, all the tools devel- 511 oped for countries where the problem seems easier to resolve are ' 512 or will certainly be useful at a global level and, if mastered, will 513 be available in the future. 514 Finally, it must be highlighted that invertebrate conservation, as 515 well as of all biodiversity, is only possible with the preservation of 516 ecosystems and their structure, function and processes (Kim, 1993; 517 Samways, 1993). Describing and understanding the roles and eco- 518 system services provided by different species could help linking 519 invertebrate conservation with human well-being. This link is crit- 520 ical for increasing the public, political and even scientific support 521 for invertebrate conservation. Single-species management is useful 522 in a limited sense only, as all species are interconnected in ways we 523 are just beginning to understand. 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