A Global Perspective on Conserving Butterflies and Moths and Their Habitats

14 A global perspective on conserving butterflies and moths and their habitats

Thomas Merckx1, Blanca Huertas2, Yves Basset3 and Jeremy Thomas4

1Wildlife Conservation Research Unit, Department of Zoology, Recanati-Kaplan Centre, University of Oxford, Oxford, UK 2Life Sciences Department, The Natural History Museum, Cromwell Road, London, UK 3Smithsonian Tropical Research Institute, Apartado, 0843-03092, Balboa, Ancon, Peru 4Department of Zoology, University of Oxford, Oxford, UK

Just living is not enough, said the butterfly, one must have sunshine, freedom and a little flower. — Hans Christian Andersen

Introduction The order represents a mega-diverse radiation of almost exclusively phytophagous insects, probably correlated with the great diversification of Lepidoptera are one of the four major insect flowering plants since the Cretaceous (Menken orders, and one of the best studied invertebrate et al. 2010). They provide many vital and eco- groups, containing over 160,000 described species nomically important services within terrestrial and an estimated equal number of undescribed ecosystems (e.g. nutrient recycling, soil forma- species, arranged in 124 families (Kristensen et al. tion, food resources and pollination). The scale 2007). Lepidoptera occupy all except the very of these contributions is illustrated by the coldest terrestrial regions, but the Neotropics and estimate that blue tit (Parus caeruleus) chicks Indoaustralian region have five times more consume at least 35 billion caterpillars each year species per unit area than the Palaearctic and in the UK alone (Fox et al. 2006). Lepidoptera Nearctic, and three times more than the also have considerable human significance, both Afrotropical region (Heppner 1991). They are economic and scientific. A growing industry scale-winged insects, traditionally divided into farms pupae for supply to butterfly houses across three major assemblages: micro-moths, butter- the world. One moth species has been domesti- flies and macro-moths (Kristensen et al. 2007). cated in order to provide silk (i.e. Bombyx mori

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from the wild B. mandarina). For scientists, changed dramatically since the 1850s. Some the group offers a model system valuable to species have increased their range but most studies of biodiversity conservation, ecology, have declined, and 7% of British species are ethology, genetics, (co)evolution and systemat- extinct. The mean decline in butterflies has been ics (Samways 1995; Boggs et al. 2003). an order of magnitude greater than that of birds Human appreciation of the beauty and or vascular plants (or, where monitored, mam- vulnerability of (especially) butterflies has grown mals), whether measured at the scale of single exponentially in recent decades, particularly in sites, regions or the entire nation (Thomas et al. developed nations. For example, among the 40 2004). Moreover, until the recent application of national biodiversity mapping schemes extant in ecological principles to conservation described the UK, more than 2.5 million records were sub- below, local extinction rates on nature reserves mitted for Lepidoptera thanks to the work of the often exceeded those on commercially managed Centre for Ecology and Hydrology, Rothamsted land, in sharp contrast to the stability achieved Research and Butterfly Conservation (BC) UK, for vertebrates and plants (Thomas 1991). with key input from amateur enthusiasts The four methods of assessment available in (butterflies 2.2 m; macro-moths 384 k) prior to the UK (Red Data Books (RDBs), species sur- 2000, roughly double the number received for veys, mapping and population monitoring all other invertebrates combined, or indeed for schemes) are of shorter antiquity elsewhere but birds (1.2 m) (Thomas 2005). Despite a bur- it is clear that UK declines are typical of other geoning interest in UK moths that has seen 12.4 developed nations, and are exceeded by some million records amassed by over 5000 volunteer (Maes & Van Dyck 2001). In The Netherlands, recorders in recent years (BC’s Moths Count ini- for example, 24% of 71 butterfly species tiative) (see Chapter 8), butterflies are currently became extinct during the 20th century while (and regrettably) probably the only taxon of ter- the number of breeding birds increased by 20% restrial invertebrates across much of the world (Thomas 1995). for which it is realistic to assess the scale and There is some debate as to whether butterflies rates of change in species’ ranges or populations are indicators of change in other insects: Hambler (Lewis & Senior 2011). For the same reason, & Speight (2004) argued that butterflies have butterflies have been successfully used as char- suffered higher extinction rates than other ismatic flagships and umbrella species (see invertebrates according to UK RDBs; Thomas & Box 14.1) in insect conservation programmes Clarke (2004) attributed this discrepancy to an (New 1997; Thomas & Settele 2004; Fleishman artefactual underestimate of decline inherent in et al. 2005; Guiney & Oberhauser 2009). comparing poor with well-sampled taxa, and showed that butterflies experienced similar extinction rates to other groups when sampling Long-term change in populations intensity is factored in. Moreover, observed of Lepidoptera extinction rates in dragonflies, bumblebees and macro-moths have unequivocally been slightly higher than those of UK butterflies (Thomas Rates and causes 2005; Conrad et al. 2006). Whilst clearly unrep- resentative of certain species and functional Before discussing practical conservation of types, because of their popularity, ease of study Lepidoptera, it is necessary to consider their (e.g. conspicuous, day-active, often identifiable known rates and causes of change, and whether in the field) and patterns of species richness and these are representative of other insect species endemism that mirror those of many other (Thomas & Clarke 2004; Fleishman et al. 2005). insects, butterflies are increasingly used as indi- In the UK, which has the longest history of rig- cators of change in other taxa in Europe and to a orous recording, butterfly populations have lesser extent elsewhere.

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Butterflies may be useful indicators of habitat able to remove more than a small proportion of change (Ricketts et al. 1999). We distinguish the effective breeding population of adult two types of indicator (Thomas et al. 2005): Lepidoptera per generation, because in most (i) the ’miners’ canary’ whose decline heralds studied species the majority of eggs are laid future losses for less sensitive species; and within 2–5 days of each female’s emergence, (ii) taxa which mirror change or predict the and for species with discrete generations, the presence (Fleishman et al. 2005) of poorly short-lived individuals emerge over a period of monitored organisms. Across Europe (Erhardt & 4–8 weeks. Thomas 1991; Thomas 2005), butterflies in Habitat loss, undoubtedly the prime culprit general are early warning systems for future (Stewart et al. 2007), can broadly be divided change in vertebrate (apart from mega-fauna) into two processes (Thomas 1991): (i) the and vascular plant populations. One family of destruction of primary and species-rich second- butterflies, the Lycaenidae, provides ultra- ary ecosystems by intensive modern agriculture, sensitive indicators of coming change in other exotic-species forestry, mining, armed conflict families, because many of them need two and illicit crops (Dávalos et al. 2011) and, to a specialized larval resources (foodplants, ants) lesser extent, urbanization; (ii) the reduced size, to co-occur (Thomas et al. 2005). We there- increased isolation and degradation in quality of fore advocate the application of standardized those fragments of potentially inhabitable bio- mapping and population monitoring schemes topes that survive. The first process effectively in nations where such schemes are absent, and eliminates all populations apart from pests of the monitoring of other arthropod taxa. crops and exploiters of ruderal plants. The second is less clear-cut but equally harmful, especially in developed regions (see below). Drivers of change Another driver of population reductions is climate change. Its observed impacts on Of the main drivers of global biodiversity loss, Lepidoptera are relatively minor so far but it is the spread of exotic pest species and direct over- predicted to rival habitat change (with which it exploitation by humans have had negligible interacts) in future decades (van Swaay et al. detectable impacts on populations of 2010a). Already in the Holarctic, non-migra- Lepidoptera (e.g. Collins & Morris 1985). So the tory species have shown southern or lowland banning of trade and collecting – the main contractions that exceed their northward or measure applied in many nations today and for altitudinal shifts in ranges (e.g. Parmesan et al. the first century of conservation practice in the 1999), whilst similar altitudinal shifts are UK – is inappropriate (unless coupled with detectable in moth communities in Borneo habitat conservation), because it fails to account (Chen et al. 2009). The net impacts on for the very different population dynamics and Lepidoptera of future climate and land use life-history traits of insects compared with changes are rightly a research priority. vertebrates and many plants (Thomas 1995). This resilience arises because Lepidoptera populations typically have high intrinsic rates of Single-species conservation increase wherever the quality of habitat is high, with individual females laying many eggs which subsequently experience high density- Compared with tropical regions, species rich- dependent mortalities (in unperturbed popula- ness within temperate biomes is generally much tions), especially in the later larval stages, lower, both in ecosystems as a whole and allowing numbers to recover quickly if the among the taxa they support. Lower diversity previous generation of adults was depleted by has undoubtedly made it easier to name and collectors. Furthermore, collectors are seldom understand a large proportion of temperate

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Box 14.1 From single-species to community and landscape conservation: Maculinea arion in the UK

(a) Mortality (a) M. arion is a globally threatened flagship butterfly with specialized on Thymus larvae that briefly eat Thymus flowers before inhabiting Myrmica ant Oviposition (SF) nests, where they prey on ant brood. A 6-year study identified and (V ) w modelled the parameters driving its population dynamics (see Thomas et al. 2009 for symbols). The key discovery was its host specificity to one ant, Myrmica sabuleti, rather than to any Myrmica species.

Host specificity (Pi)

Myrmica Myrmica scabrinodis sabuleti

Drought Density-dependent mortality(Qw) mortality(Dt )

at+1 = atSF (Psab (t) + cPsab (t)) Dt Qw Vw where Dt = a – b log(Lt /Rt) 1/21/2013 3:38:56 PM Box 14.1 From single-species to community and landscape conservation: Maculinea arion in the UK 0001738427.INDD 243

(b) (b) Different Myrmica ants occupy different niches within grassland; M. sabuleti dominates in warm short swards under UK climates. Land use changes resulted in the abandonment of most sites causing M. sabuleti to disappear or be displaced by unsuitable congeners, causing M. arion’s extinction in the UK in 1979. Targeted conservation management Parasitoid shifted the sward structure (indicated by the position of sleeves along the +– habitat gradient in the diagram) back to the optimum for M. sabuleti, Maculinea arion – + – – which quickly returned to dominate the turf. M. arion was then + Thymus + reintroduced from Sweden and increased rapidly, closely matching – model predictions on 21 tested sites (Thomas et al. 2009, 2011). Not Myrmica sabuleti – Other Myrmicaspp only did M. arion’s immediate community of interacting rarities benefit, + or – + or – Short hot dry Tall cool damp but the restoration of a disappearing type of habitat caused other grassland grassland Gradient of underlying habitat structure Biodiversity Action Plan organisms belonging to the same guild to Thymus/Oreganum recover, including threatened plants, insects and birds. Schencki Sabuleti Scabrinodis RuginodisMyrmica rubra niches ild Wi gu der me co f sa mmu pp o nity: myrmecophiles + s

(c)

(c) The collateral benefits from M. arion restorations justified conservationists in applying similar targeted management across the landscape, including the restoration of calcareous grassland and the creation of new 1 km habitat on railway constructions. M. arion has spread to 25 sites (dark patches), forming a meta-population of loosely connected colonies, as have other priority species. Mid-grey indicates woodland plantations form which most sites were restored. (d)

(d) Today, similar programmes are being initiated in the other UK landscapes formerly inhabited by M. arion. In all regions, some sites are deliberately managed to create heterogeneous and suboptimal (but suitable) swards for M. arion, to buffer the new communities from extreme weather and to prepare for future climate change.

Part (a) adapted with permission from Thomas et al. (2009) 1/21/2013 3:39:00 PM 244 T. MERCKX, B. HUERTAS, Y. BASSET AND J. THOMAS

biodiversity, a process that began with the rise failed (simpler) approaches such as the regula- of ‘natural history’ in Europe during the 1700s. tion of collecting and the establishment of bio- Hence, there is much more knowledge on topes as nature reserves without recourse to distribution, ecology and life-history of managing their internal structures or succes- Lepidoptera, and of many more species, in sional dynamics (Thomas 1991). In the UK, it is temperate regions than in the intrinsically more arguable that five butterfly species (Satyrium diverse tropical regions, where a significant pruni, Polyommatus bellargus, Hesperia comma, percentage of taxa remains undescribed. Today, Melitaea athalia, Papilio machaon) have been many temperate countries have valid Red List saved from national extinction by science-based assessments of nearly all butterfly species, and management since the 1970s–90s, whilst three in Europe there is even a continental Red List nationally extinct, globally threatened Maculinea (van Swaay et al. 2010b) whereas tropical species have been re-established on specifically countries do not, or rather, only of subsamples managed sites in the UK or The Netherlands (see below). However, only Norway and (Thomas et al. 2011; Wynhoff et al. 2011). Finland have national Red Lists for moths, The single-species approach has therefore although other developed countries are consid- had several benefits. First and foremost, it has ering them. succeeded for several declining butterflies, By contrast, tropical birds and mammals have whereas biotope protection per se historically received considerable attention, both because failed to maintain them, for population extinc- they are more popular and because their tion rates on nature reserves up to 1980 typi- combined global species richness is only 5% of cally exceeded those on neighbouring land that estimated for Lepidoptera. The relatively (Thomas 1991). Importantly, success breeds small numbers of species-specific conservation success in conservation, and the demonstrable actions in the tropics mainly focus on these recovery of (alas rather few) declining iconic popular taxa, whereas most species-specific species in Europe has greatly increased public conservation research is done within temperate and political interest in Lepidoptera, and has regions. The lack of the ecological knowledge hugely increased the flow of funding, leading to necessary for species-specific actions for tropi- wider gains. Among these are multi-million cal Lepidoptera, combined with financial con- euro projects to protect pristine ecosystems and straints, may explain the contrast between to restore and recreate degraded ones, which, conservation efforts for them (mainly as eco- although targeted for one species, inevitably system protection) and in the west (mainly support diverse communities of other threat- as species action plans) (New 2009; Bonebrake ened taxa (Bickmore & Thomas 2000; Thomas et al. 2010). 2001; Settele & Kühn 2009). The current and welcome increase in species- Species-specific research and actions, e.g. the specific research and action plans mainly focuses UK Biodiversity Action Plan, now increasingly on regionally threatened habitat specialists, include specialist moths among their priority confined to rare biotopes within generally small species. The problem is that, given the increased nature reserves. The prospects for the insects pressures on the natural environment, it seems targeted are improved by specific management impossible to follow such an ‘intensive care’ measures applying evidence-based science. approach for the majority of species in trouble Although now well established, the introduc- (Merckx et al. 2010a). Worst off are generalists, tion of ecological research to practical manage- many of which are also experiencing severe ment marked a paradigm shift in Lepidoptera declines (Van Dyck et al. 2009), less popular taxa conservation (Hanski 1999). It resulted in the such as moths (Conrad et al. 2006), and species first successful recovery programmes of endan- within the diverse communities of the tropics. gered species, following a >100-year period of The expensive, time-consuming and dedicated

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approach is obviously desirable to rescue highly meta-population of populations to persist in a threatened iconic species in desperate situations, landscape. In practice, the two concepts are such as the monarch roosts of central Mexico, inextricably entwined, both in their causes and and the Queen Alexandra’s birdwing (the world’s in their consequences for population dynamics. largest and perhaps most endangered butterfly) The same socio-economic changes that lead to in Papua New Guinea (Thomas & Settele 2004). ecosystem destruction and fragmentation typi- There is an argument that such care should be cally alter both successional dynamics and the temporary and eventually relaxed as threat development of plagioclimaxes within the levels decrease. Perhaps the strongest arguments surviving habitat islands (Thomas et al. 2001). for its current continuation are: (i) beneficial Apart from special cases, such as monarch umbrella impacts on other species, and (ii) the butterfly overwintering sites, reduced habitat gaining of the knowledge required for designing quality primarily affects fitness of Lepidoptera efficient biotope-specific management. in the larval stage (Thomas 1991). In a degraded We therefore believe there is currently still biotope, the larval foodplant typically remains a need for both species-specific and biotope- abundant (in some cases increases) but grows specific approaches in temperate and (sub)trop- in less suitable forms or with altered nutritional ical regions. The focus on biotopes should value in response to pollution, changed water gradually be increased in temperate regions, levels or other attributes such as microclimate including on land outside nature reserves (Thomas et al. 2011). For most butterflies stud- managed for agriculture, silviculture and ied, the mean density of adults on isolated sites urban-industrial purposes such as road and rail- containing optimum larval habitat was around way constructions. At the same time, the 100 times greater (spatially or temporally) than species-specific conservation effort for highly on those containing the lowest-quality source endangered iconic tropical species should be habitat that had supported a population for at considerably increased, especially those with least 10 consecutive generations. In contrast, severely restricted ranges. Indeed, a conse- fluctuations caused by weather and variation in quence of the lack of population studies in the adult resources (e.g. nectar, mating sites), were tropics is the minimal knowledge of foodplants 10 to 100 times smaller. And only in one stud- for larvae, and spatial structure and dispersal ied species (Celastrina argiolus) were interactions capabilities of most populations of tropical with an enemy (a specific parasitoid) sufficient Lepidoptera (Bonebrake et al. 2010, but see to overrule the population variation due to Marini-Filho & Martins 2010). habitat quality (Thomas et al. 2011). In contrast, isolation of habitat patches affects mainly the adult stage, which is unexpectedly From single sites to meta-populations: sedentary in most studied species of Lepidoptera, ecological conservation at especially in habitat specialists. Increased isola- landscape scales tion causes meta-populations to disappear from landscapes as populations die out, having failed either to track the generation of new habitat The development of the modern ecological patches or resources across modern landscapes approach to Lepidoptera conservation included or to replenish those that go extinct (Hanski two paradigm shifts: first, the concept that sur- 1999). On the spectrum between classic ‘blink- viving patches of habitat were declining in ing light’ meta-populations or mainland-island quality and had reduced (or no) capacity to ones, the positions of most populations of ‘colo- support a valued species; and later, that irre- nial’ species of Lepidoptera have been a matter spective of their quality, the surviving islands of of some debate. The former structure probably habitat were too few, small and isolated for a approaches the norm for several Melitaenini

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and related fritillaries (Schtickzelle & Baguette many plants and vertebrates (see Box 14.1). 2009), but in other species may be a transient Still, there are key questions to be addressed by phase following habitat fragmentation, presag- future research both at patch and landscape ing the breakdown of the whole system scales. To what extent are subsets of species (Harrison 1994). regionally adapted to different biotic interac- At the applied level, there was an unwelcome tions or environmental conditions (e.g. local dichotomy during the 1980s–90s in Europe climate)? How responsive are local phenotypes between (i) spending scarce resources solely on to rapid environmental change, for example in improving the (degenerating) internal habitat selection for more dispersive forms or types quality of existing conservation sites for endan- physiologically adapted to a warmer climate or gered guilds or species of Lepidoptera, rather capable of switching foodplants or hosts? than adding to the suite of reserves, and (ii) the Although larval habitat quality and adult disper- exact opposite approach. Today an evidence- sal are the two overriding factors so far found to based consensus recognizes that it is equally regulate populations and meta-populations in important to address both processes. This most studied Lepidoptera (Thomas et al. 2001), resulted from a series of field studies from do other factors (e.g. adult resources) play a key Thomas et al. (2001) onwards, which found role for populations elsewhere (Dennis 2010) or that, whilst the density of individuals within a under tropical climates? How important is the site reflects the quality of habitat within each matrix separating patches of breeding habitat in occupied patch rather than its isolation or size, providing resources for adults or facilitating/ the chance of a patch being occupied in the first obstructing their spread (Dennis 2010)? place was correlated strongly, independently and almost equally with both its isolation from neighbours and (again) the quality of the patch. Advancing towards multi-species Surprisingly, very few single-species studies (as conservation opposed to whole communities of species) have shown patch size to be a significant predictor of occupancy once account is taken of habitat As we argue elsewhere, with only half of the quality (Thomas et al. 2011). There are three world’s estimated Lepidoptera described and a explanations for the contribution of patch qual- minute proportion well studied, it is impossible ity to meta-population stability in Lepidoptera: to provide targeted conservation programmes (i) for a given patch size, optimum habitat sup- for more than a small number of highly valued ports populations that are up to 100-fold larger, species, at least outside nations where diversity and hence more likely to persist, than those of is exceedingly low (e.g. the UK). Moreover, low (but just suitable) source habitat; (ii) the very few nature reserves are managed primar- former release more emigrants into the matrix ily for Lepidoptera, although typically the to seek new sites, disproportionally so since plants, ants and (often more endangered) spe- individual butterflies hatching into high-density cific parasitoids with which each interacts ben- populations are more likely to leave their natal efit directly (e.g. Anton et al. 2007). patch (Hovestadt et al. 2010); (iii) new sites We have seen that declines in Lepidoptera containing high-quality habitat are more likely are driven primarily by factors that affect all to be colonized successfully by an immigrant species, rather than by targeted overcollecting female, since the vulnerable period of low (see above). In addition, we have suggested numbers is short (Thomas et al. 2011). that butterflies can be sensitive predictors of the By applying the above principles, European impacts of environmental change on other conservationists concerned with Lepidoptera organisms, as well as useful representatives of are (at last) matching the successes achieved for less conspicuous terrestrial insects (Thomas

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2005). In theory, therefore, the restoration of ca. 100-fold increase on three sites of Viola and optimum conditions for a rapidly declining a 10–15-fold increase (and new populations) of butterfly will require restoring a type of habitat three fritillary butterflies whose larvae eat Viola, within existing biotopes, or a network of sites including Argynnis adippe and Boloria euphrosyne, to landscapes, that should benefit the two of the UK’s most endangered insect species community characteristic of that configuration (Randle et al. 2005). In this respect the target of habitat patches. butterfly, M. arion, acted as an indicator for a In practice, there are few examples of keystone species of ant, M. sabuleti, which observed umbrella benefits resulting from dominates its habitat at its scale. Since most single-species conservation of insects, which Lycaenidae (nearly a third of butterfly species) has caused its efficacy to be doubted (Stewart interact with ants as larvae or pupae, we suspect et al. 2007) despite abundant evidence in sup- that they will prove to be an especially useful port from biotope manipulation for other taxa umbrella taxon for other groups. (e.g. Dunk et al. 2006). This is an inevitable con Encouraging as these results may be, there is sequence of a lack of resources to monitor col- clearly a pressing need for future research and lateral changes in most Lepidoptera conservation conservation practice to understand the ecologi- projects. In the USA, Launer & Murphy (1994) cal requirements of a spectrum of endangered found that protection of all those serpentine Lepidoptera with enough precision to ensure the soil-based grasslands in central California continuity of sufficient habitat for each compo- occupied by the federally protected butterfly nent within a single heterogeneous ecosystem, Euphydryas editha bayensis would also conserve for example as co-existing successional stages 98% of native spring-flowering plant species within woodland, heath and grassland. Equally (although the percentage fell sharply if only the clearly, this is more likely to succeed in multi- largest butterfly sites were targeted). In the UK sited landscape-scale projects which, in our view (Thomas et al. 2011), the restoration of scrub rightly, have been the trend in recent years. habitats designed to increase Satyrium pruni, of chalk grassland for Polyommatus coridon, and of limestone and acid grasslands for Maculinea Two multi-species approaches arion (see Box 14.1) produced rapid and diverse gains across a suite of declining insects, plants and (where studied) birds. In the case of M. Landscape restoration arion, the beneficiaries included 33% of the declining butterfly species listed in the UK’s The successful landscape-scale conservation of Biodiversity Action Plan, as well as RDB-listed multi-species assemblages basically boils down to species of ants, beetles, flies, cockroaches, plants either conserving/protecting ‘pristine’ landscapes and birds. Most species increased because they or restoring human-altered landscapes. Although were adapted to the warm early-successional adequate protection of the world’s remaining grassland structures created for M. arion in the ‘wilderness’ areas is both more important and UK. Several also increased due to a direct or also more effective, such areas are dwindling indirect relationship with ants. For example, worldwide. Human-altered landscapes keep alongside another Viola species, the UK-RDB V. extending ever larger, so conservation efforts lactea has myrmecochorous seeds that are par- within them are becoming relatively more sig- ticularly attractive to Myrmica ants, which after nificant. Overall, landscape-scale restoration eating the eliasomes eject the seeds into sparsely approaches within such areas should minimize vegetated soil around their nests. The conse- the fragmentation of specific habitat resources. quences of up to a thousand-fold increase of We believe it is useful to make a distinction Maculinea arion’s host-ant Myrmica sabuleti was a between areas that (i) have a short history of

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human alteration, e.g. deforested in recent mid-successional natural seral stages or plagio- decades, (ii) have a long history, e.g. farmed for climaxes, prevented from reverting towards several centuries, and (iii) are ‘pristine’. We forest. Only scattered fragments of ancient argue that, above the general ecological conser- woodland remain, and these have suffered vation principles applying to all, successful con- continuous disturbance as human needs for servation of the extant biodiversity in each woodland products changed. For example, up needs a different approach. to a century ago most European woodland was The massive recent and ongoing deforestation/ maintained as coppice or very open coppice- degradation of tropical forests (in several West with-standards, to provide fuel and fencing African countries, forest cover loss exceeds 90%; materials, whereas today much woodland has a Safian et al. 2011) has dramatic consequences more uniformly closed shady canopy than is for the highly diverse Lepidoptera fauna adapted found in ancient forests with no history of to these climax ecosystems. Agri- and silvicul- disturbance. And since very old trees were no tural mosaics where the percentage of converted more valuable to humans than middle-aged original forest exceeds 30%, including selective ones, the rarest type of arboreal habitats in logging of three or more large trees per hectare, developed countries today are those associated show species compositional shifts with loss of with rotting wood on ancient trees: yet these many components of the butterfly community saproxylic habitats support numerous endan- (Brown 1997). Hence, the only way to repair gered invertebrate specialists, especially some of the damage is the combination of thor- Coleoptera and Diptera, and some moths (e.g. ough protection of remaining patches of primary Parascotia fuliginaria). Although many species forests, successful regeneration of secondary were undoubtedly lost over the centuries dur- forests, and targeted reforestation projects ing this transition, others have managed to within agro-forestry systems and clear-cut areas adapt successfully as specialists in these semi- (Schulze et al. 2004; Safian et al. 2011). Species natural biotopes (e.g. heaths, grasslands, hay recolonization rates depend primarily on life- meadows, marshes and coppiced woodland). history characteristics, patch size and biological The intensification of agriculture and forestry structure, distance to source patches and perme- and of urbanization since the 1950s, and more ability of the intervening matrix. Still, the often recently abandonment in response to socio-eco- substantial dispersal/recolonization potential of nomic imperatives, has severely decreased these tropical butterfly and moth communities allows semi-natural biotopes in quantity and quality, them to regenerate several decades after clear- and with them their specialist fauna and ance (Hilt & Fiedler 2005; Safian et al. 2011). Lepidoptera. The Red List considers agricultural Obviously, recent conversion by agriculture intensification and abandonment a major threat in areas originally not fully forested need pro- for almost 30% of European butterfly species tection and restoration of the original set of (van Swaay et al. 2010b). As a result, most ‘con- biotopes (e.g. Afromontane mosaic landscapes; servationists’ seek to sustain or restore semi- Tropek & Konvicka 2010). natural biotopes, and do so by maintaining very The situation is more complex in countries, specific disturbance regimes (often simply by such as most of Europe, with a long history of copying traditional agricultural practices, since human alteration. Here, ultimate conservation most large wild herbivores were excluded goals are the subject of much, but not enough, centuries ago) (New 2009). Nevertheless, popu- debate. The natural climax forests and sparsely lar management operations to influence vegeta- forested pastures kept open by mega-herbi- tion structure, such as burning and grazing/ vores have been fully replaced, often millennia mowing, need careful planning (mainly to ago, by so-called semi-natural biotopes, which ensure refugia) as they may destroy much of are essentially different versions of early- to the existing invertebrate fauna if applied too

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intensively, too infrequently, on too large a scale of Special Scientific Interest) and High Nature or at unsuitable times of year (New 2009). Value farmland, together with what will be Hence, although wrongly applied conservation politically and financially achievable through management may have unintended negative the soon to be revised Common Agricultural consequences, management is seen as a good Policy, will all be instrumental in producing a thing overall, whereas abandonment of human road-map, with substantially increased funds disturbance is often perceived as a threat. and mechanisms for semi-natural biotope resto- The situation should not be black and white. ration, which will clearly delineate sites/areas Abandonment undoubtedly poses a threat to best managed under each approach. many specialist species that have become adapted In addition, restoration of areas usually to certain semi-natural biotopes, and is a threat regarded as ‘the matrix’ in between (semi-) to specialists that have nowhere else to go natural patches, such as intensive farmland, because natural succession dynamics are cur- brownfields and even urbanized areas, is of rently too disturbed and suitable natural patches value too. These areas are currently often rather are too small and/or isolated. On the other hand, ‘simple’ and ‘homogeneous’ in terms of habitat abandonment will most certainly benefit some resources, so restoration may make a relatively endangered specialist faunal groups too (e.g. large difference to their conservation value closed-woodland Lepidoptera, saproxylic (Tscharntke et al. 2005), as well as increasing groups), and may also provide ‘rewilding’ oppor- the value of neighbouring (semi-)natural tunities in biotopes evolving towards mosaics patches (Dennis 2010). Brownfield sites pro- including mature climax vegetation or natural vide many opportunities for restoration of successional stages such as coastal and river successional biotopes otherwise not strongly areas, wood gaps and high-altitude areas, represented locally, and restoration plans although even here, open habitats may be much should be tailored to focal species and/or gener- rarer than in prehuman landscapes, owing to the ally improve biotopes by assuring a sufficient absence of most former natural herbivores, e.g. quantity, quality and spatiotemporal diversity bison, aurochs, wild sheep and horses (and, of resources (New 2009; Dennis 2010). more locally, beaver) in Europe (see Chapter 23). Restoration of intensive agricultural areas may We believe there should be room for both be globally important given their huge and active management (i.e. restoration of semi- growing footprint. Here, the aim should be to natural biotopes) and passive abandonment (i.e. reconcile intensive agricultural practices with rewilding), even at small spatial scales (Merckx wider societal benefits, including biodiversity. et al. 2012a). They are complementary, and now The question is how to decide which landscape is the time to designate areas to one or the other, elements to restore, how, and at what spatial on a European-wide scale. Such allocations scale in order to make farmland less hostile to a should be done carefully, and for as many taxa broad range of declining ‘wider countryside’ as possible, taking into account many variables, and rare, localized species (Merckx et al. 2010a). such as historic and recent distributional data, Agri-environment schemes (AES) can reverse international threat status and life-history traits, negative biodiversity trends by increasing and they should have clear, quantifiable conser- resource heterogeneity and improving dispersal vation goals. The information on butterflies (i.e. success (Shreeve & Dennis 2011). However, European Red List: van Swaay et al. 2010b; they must be made more efficient and cost- Prime Butterfly Areas in Europe: van Swaay & effective, so that they actually achieve their Warren 2003) will be a valuable input to such a goals (Kleijn et al. 2006; Settele et al. 2009). One multi-taxa exercise. The current and possible way to achieve this is by implementing specific future distribution and intrinsic properties of measures for high-priority species within AES nature reserves (e.g. Natura 2000 sites, UK Sites targeted at landscapes where such species occur,

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as this approach has been shown to benefit Log-counts specialist butterfly species (Brereton et al. 2011). However, we argue that this species-specific approach must be complemented by a multi- species approach in order to more fully address 2.3 the steep declines in farmland biodiversity. General AES that are focused on the restoration and implementation of vital landscape elements are key to this multi-species approach. Even 2.2 simple AES management prescriptions applied to relatively small areas can benefit Lepidoptera populations. For example, the restoration and management of arable field margins has been shown to benefit a range of butterfly species, 2.1 both on conventionally managed (Feber & Smith 1995; Feber et al. 1996) and organically managed (Feber et al. 2007) farmland. Hedgerow management can have a positive effect on No tree Tree declining species such as the brown hairstreak Treatment Thecla betulae butterfly (Merckx & Berwaerts Figure 14.1 Fortnightly individual moth counts 2010). In addition, we have recently discovered (log N + 1) (with SE) contrasting the effects of pres- that the protection of existing hedgerow trees, ence/absence of a hedgerow tree on moth abun- and the provision of new ones, is likely to be a dance within areas where farmers had (•) and had highly beneficial conservation tool for popula- not been () targeted to apply for agri-environment tions of moths, and probably many other flying schemes. Reprinted from Merckx et al. (2009a), with insects too, as hedgerow trees provide a shel- permission from Elsevier. tered microclimate and other key habitat resources (Merckx et al. 2009a, 2010b, 2012b). species and biotopes (Bruner et al. 2001). The Nevertheless, hedgerow tree and field margin number of national park declarations, mainly AES options are likely to obtain best results for for biodiversity conservation purposes, has moth populations where farmers are targeted to increased in recent years. Resources for these join these schemes across the landscape, proba- national parks are finite, and must be directed bly because this results in a landscape-scale join- to the most important sites. GIS-based prioriti- ing up of habitat resources, which especially zation exercises with a multitude of data layers, benefits the large proportion of moth species of including forest structure change and sound intermediate mobility that use the agricultural distributional and modelled occupancy data of biotope and move through it on a scale larger threatened species, are a prerequisite. than the field scale (Merckx et al. 2009a,b, The first threatened species assessments were 2010b) (Figure 14.1). published for mammals and birds in the mid- 1960s. So far, out of the entire planet’s biodiversity, only ca. 45,000 species have been Landscape conservation assessed against IUCN criteria, mostly vascular plants and vertebrates, plus <1500 insects Sites with ‘no’ or little human disturbance, and including ca. 300 Lepidoptera (Vié et al. 2008). with high biodiversity and/or threat levels, are The IUCN is now conducting assessments, using candidates for landscape conservation, a very the Sampled Red List Index (SRLI) methodol- effective strategy for protecting endangered ogy, of the threat status of samples of 1500

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species of the lesser known groups without comprehensive for the group as a whole. Wells complete Red Lists, such as many invertebrates. et al. (1983) produced the first IUCN inverte- Recent initiatives include IUCN assessments of brate RDB including some butterflies. The first butterflies in Europe (van Swaay et al. 2010b) national assessment for invertebrates was and the rest of the world (Afrotropics: Lewis & produced for England by Shirt (1987) and Senior 2011; Neotropics: Willmott et al. 2011). assessments of threatened butterflies for Europe Some site-based assessment methods have by Heath (1981). been developed with particular reference to Only one family of butterflies, the Papilionidae butterflies. For example, Ackery & Vane-Wright (i.e. ‘swallowtails’), has been assessed on a (1984) proposed the concept of critical fauna global scale (Collins & Morris 1985). This family analysis, whereby regions that contain certain has a pan-global distribution and includes both local faunas are identified by their endemic spe- widespread and habitat-restricted species, cies, and if these regions were protected, all making them well suited for conservation stud- species of a particular group would be too. Only ies. They include some of the largest and most a few analyses of ‘critical faunas’ have been spectacular butterfly species, attracting the conducted in tropical areas (e.g. Collins & attention of amateurs and specialists alike, so Morris 1985; Hall 1999; Vane-Wright & de Jong their taxonomy and distribution are relatively 2003; Willmott 2003). Data are assessed to well known. The assessments were made under identify optimally efficient, single-site sequences earlier versions of IUCN criteria and were of near-equal priority areas for a group using mostly qualitative; 170 papilionids were con- the complementarity principle (Vane-Wright sidered threatened or near-threatened in this et al. 1991; Williams 2001) and incorporating study (Collins & Morris 1985). Later, New & other criteria (Margules & Pressey 2000; Araújo Collins (1991) showed that nearly 14% of et al. 2002). This method is also useful in assess- papilionid taxa are believed to be threatened or ing habitats on a broader geographic scale, declining, plus 17% with no information to be where it is possible to detect areas of unusually assessed. The Lycaenidae is another major but- high significance in understanding evolution- terfly group that has been subject to some ary processes (New 1997). detailed conservation studies (e.g. New 1993; Van Swaay & Warren (2003) proposed a Thomas et al. 2005). This family is difficult to selection of Prime Butterfly Areas (PBAs) for study due to its high diversity (almost 40% threatened species in Europe. PBAs are defined of all described butterfly species) and complex as a preliminary selection of areas supporting and poorly known taxonomy in many regions. species meeting three criteria. The other major butterfly families (Pieridae, Nymphalidae, Hesperiidae and Riodinidae) •• Biogeography: European range-restricted have not had a global assessment. species Van Swaay & Warren (1999) provided the •• Conservation: threatened species defined by first comprehensive regional review of the sta- IUCN criteria tus of butterflies for Europe (except Turkey and •• Legislation: species listed in Appendix II of the Cyprus). Out of 576 butterfly species assessed, Bern Convention and/or the EU Habitats 71 (12% of the total) were categorized as and Species Directive. threatened, of which 19 were globally threatened species and 52 regionally threatened. In This initiative identified 431 PBAs (covering the tropical regions, hardly any such regional 1.8% of Europe). However, not enough is assessments have yet been done, though vari- known of threatened species in tropical regions ous assessments have been carried out at a to apply this method there. Threat assessments national level, some of which use modified for butterflies are available but are not yet IUCN criteria or subjective assessments for

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butterflies and a few moth species (e.g. of KBAs for the Neotropics based on the pres- Colombia: Amat-García et al. 2007; Venezuela: ence of threatened butterfly species studied in Rodríguez & Rojas-Suárez 2008; Brazil: MMA the IUCN SRLI (Box 14.2) (Willmott et al. 2011). 2008). However, those assessments do not The lack of threat assessments for Lepidoptera cover the entire butterfly fauna of each coun- and other invertebrates in the tropics has seri try, and variation in the criteria used introduces ous consequences. Research and conservation discrepancies. For example, the high-elevation resources may not be adequately targeted or butterfly Lymanopoda paramera was separately may rely upon passive conservation of other, assessed twice as it lives in the border region of better known, taxa. The lack of threat assess- Colombia and Venezuela. It was assessed as ments may bias funding towards better known Vulnerable in Venezuela, but as Critically groups. Some grant research programmes Endangered in Colombia, perhaps because dif- require supported projects to concentrate on ferent methodologies were used during the species rated as threatened. Consequently, one assessments, and/or the difference in extent of way of obtaining funding for Lepidoptera each national range. In addition, there are some research has been to conduct surveys within ad hoc assessments of certain recently described multi-taxa studies involving other faunistic species of Andean butterflies (e.g. Hall 1999; groups (e.g. Huertas & Donegan 2006). The Willmott 2003; Huertas et al. 2009; Huertas NGO ProAves (www.proaves.org) has estab- 2011). However, less than 10% of the lished various nature reserves and helped in the Neotropical butterfly fauna (ca. 45% of the declaration of a national park in Colombia for world) has been assessed so far (Willmott et al. threatened bird and butterfly species based on 2011). some of the latter studies. Various site-based conservation assessment initiatives are based mainly on birds. The Important Bird Areas (IBAs) of Grimmett & Conclusion Jones (1989) was later applied to plants as Important Plant Areas (IPAs) (PlantLife 2004), and then to all groups as Key Biodiversity Areas Because of the now global dimension of rapid (KBA) (Langhammer et al. 2007). In order to be biodiversity decline, and its detrimental impact listed as a KBA, a site must support at least one on humanity, we need to manage unsustaina- globally threatened species, range-restricted ble land use and massive conversion and deg- species, biome-restricted species or congregation radation of natural habitats. It is our duty to of species. Notably, in the context of inverte- preserve and restore natural areas, not only brates, the designation of KBAs does not require because of their intrinsic value but also, from a the identity of all threatened or range-restricted utilitarian point of view, to avoid the functional species, just that there is a threatened species at breakdown of the ecosystems on which we the locality. The KBA programme is less useful depend. The worldwide ubiquity, abundance, in tropical regions, where almost all habitats sheer diversity, indicator capacity and both include some threatened species. As a result, a historic and current appeal to scientists and further important initiative is the Alliance for amateur naturalists make the Lepidoptera an Zero Extinction (AZE) (Ricketts et al. 2005). excellent group to monitor conservation efforts AZE sites are defined much more restrictively worldwide, and they complement conserva- (using three specific criteria) as the most impor- tion narrowly focused on birds and mammals tant locality for an Endangered or Critically alone (not least because butterflies decline Endangered species. The Tropical Andean faster than birds and plants: Thomas et al. Butterfly Diversity Project (TABDP; www.ande- 2004). Here, while we have commented on anbutterflies.org) is currently developing a list how approaches to Lepidoptera conservation

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Box 14.2 A case study: the Tropical Andean Butterfly Diversity Project (TABDP) This project (www.andeanbutterflies.org) is a major initiative involving international collaboration among scientists, institutions and students working to establish a foundation for future research on the butterflies of the Andean region, a global biodiversity hotspot. The project was inspired by the BioMap Project (www.biomap.net) and started in 2005 as an international collaboration among institutions based in five Andean countries (Colombia, Peru, Bolivia, Venezuela and Ecuador), the UK and the USA. Threatened species and site assessments require baseline distributional data. This project sought to collect and collate these data, based largely on the resources and information available in museum collections. The TABDP started from scratch in the capture of the data on the distribution of Neotropical butterfly species. A tailored database was designed to capture data on the locality, identification and other details of specimens in museums. Also, a manual for the use of databases (Willmott & Huertas 2006) and another for butterfly photo graphy (Huertas & Willmott 2006), in both Spanish and English, were published. A database of ca. 200,000 records and photographs of the types of Andean species is now freely available online. Building the capacity of host countries to conduct research on tropical Andean butterflies and train a new generation of researchers was a primary goal of this project. Around 300 students and professionals from various collections were trained in eight courses in five countries and a first Andean butterfly network, now with ca. 600 members, has been established. Threatened species assessments have been produced for 350 Neotropical butterfly species, in collaboration with the IUCN, using the SRLI methodology. Based on these assessments, the first KBAs based on butterflies have been proposed for South America (Willmott et al. 2011). The TABDP data capture methods and threat assessment methods can be replicated for any insect group and applied in other conservation initiatives, for example using more species or at national or local levels. Projects and institutions should not spare any effort in improving data sources and providing accessibility. Research programmes and targeted surveys are key sources of data, which should be considered (and funded) as part of the conservation process. Locality information necessary to produce threat assessments can be gathered only with an army of naturalists or parataxonomists (Basset et al. 2004), trained in collating and analysing data effectively. However, as taxonomic expertise is crucial when doing the assessments, more people need to be trained and more resources be facilitated for core taxonomy.

differ between regions and land use types, we poorly known areas and species concerning stress the importance of adopting a landscape distribution, habitat requirements, population scale allied to a resource-based view, both for changes and taxonomy, which would also single-species and for biotope/community benefit such areas by increasing local aware- conservation. ness and by the production of field guides. Rapid land use change, especially in recent Such an increased effort will not be in vain, as decades, has caused serious declines in butter- there is compelling evidence, for vertebrates flies and moths worldwide, despite the recent at least, that conservation efforts can halt and designation of many new nature reserves (e.g. even reverse biodiversity loss, provided there van Swaay et al. 2010b). It is hence clear that are sufficient resources and the collective will we need to go a lot further, with far greater to protect critical habitat resources (Hoffmann long-term resources. Society should now start et al. 2010). The efforts need to be monitored to invest massively on five fronts: (i) protect- too. Lepidoptera are uniquely easy to survey ing and buffering natural areas (i.e. more, bet- for a better understanding of biodiversity ter managed and larger reserves), (ii) restoring change, and as recent experiences in Europe and managing robust networks of semi- suggest that the challenge could be met, we natural biotopes, (iii) rewilding areas where call for projects to make rigorous population this is appropriate, (iv) improving typical trend estimates in undermonitored regions ‘matrix’ areas, and (v) gathering data for (see also Pereira et al. 2010). Such projects

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