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ESSAY
Year : 2012  |  Volume : 10  |  Issue : 3  |  Page : 285-303

The Butterfly House Industry: Conservation Risks and Education Opportunities


1 Albert-Ludwigs-Universität, Forstzoologisches Institut, Freiburg, Germany
2 Department of Entomology, The Natural History Museum, London; Durrell Institute of Conservation and Ecology (DICE), School of Anthropology and Conservation, University of Kent, Canterbury, United Kingdom

Correspondence Address:
Michael Boppré
Albert-Ludwigs-Universität, Forstzoologisches Institut, Freiburg
Germany
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0972-4923.101831

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Date of Web Publication29-Sep-2012
 

   Abstract 

This paper addresses the mass supply and use of butterflies for live exhibits, discusses the risks to biodiversity which this creates, and the educational opportunities it presents. Over the past 30 years a new type of insect zoo has become popular worldwide: the butterfly house. This has given rise to the global Butterfly House Industry (BHI) based on the mass production of butterfly pupae as a cash crop. Production is largely carried out by privately-owned butterfly farms in tropical countries, notably Central America and Southeast Asia. Most pupae are exported to North America and Europe, although the number of butterfly houses in tropical countries is growing. The BHI is described with respect to its stakeholders, their diverse interests, and its extent. It is estimated that the global turnover of the BHI is in the order of USD 100 million. From a conservation perspective, there is a tension between risks and benefits. The risks to biodiversity are primarily unsustainable production, potential bastardisation of local faunas and floras, and genetic mixing within and even between butterfly species. This paper discusses general ways of managing these risks. Ethical concerns range from fair trade issues to animal husbandry and the use of wildlife for entertainment. For the risks to biodiversity and unresolved ethical issues to be tolerable, the BHI needs to make a significant contribution to conservation, primarily through effective education about butterfly biology as a means to raise public awareness of basic ecological processes, and conservation and environmental issues. It should also engage with local conservation initiatives. Currently the BHI's great potential for public good in these respects is rarely realised. The paper concludes by looking at the special nature of the BHI, and its need for effective self-regulation if it is to continue to escape from public scrutiny and the introduction of restrictive regulations. The BHI needs to engage in active cooperation between its various stakeholders regarding a raft of critical issues if it is to survive and fulfil a beneficial role in society. The BHI also needs to forge active partnerships with conservation NGOs, educationalists, and scientists-communities that also need to recognise their own responsibilities towards the industry. We also discuss the need for an effective umbrella organisation for the BHI, as well as a "Code for trading and exhibiting live butterflies".

Keywords: insect trading, edutainment, ecoliteracy, ethical standards, insect conservation, environmental risks, alien species, genetic mixing


How to cite this article:
Boppré M, Vane-Wright R I. The Butterfly House Industry: Conservation Risks and Education Opportunities. Conservat Soc 2012;10:285-303

How to cite this URL:
Boppré M, Vane-Wright R I. The Butterfly House Industry: Conservation Risks and Education Opportunities. Conservat Soc [serial online] 2012 [cited 2017 Aug 22];10:285-303. Available from: http://www.conservationandsociety.org/text.asp?2012/10/3/285/101831


   What is the butterfly house industry? Top


The emergence over the past three decades of live butterfly exhibits as fashionable leisure attractions has created a new global phenomenon: the Butterfly House Industry (BHI). The key innovation was the "butterfly house": a walk-through vivarium in which curious people and beautiful insects share the same space. Its success has been made possible by means of electronic communication, rapid transportation, and mass production of butterfly livestock.

Unlike traditional invertebrate terrariums included by some zoos, with ants, grasshoppers, spiders, and scorpions in glass-fronted cases and occasional hands-on demonstrations of stick-insects and cockroaches, the butterfly house visitor is free to roam the whole space, typically planted and landscaped like a tropical garden, and interact with all the creatures on display. For a child to have a spectacular butterfly flutter just in front of her, or land spontaneously on his head, can be a highly affective experience [Figure 1]. Butterflies are very popular-for many the only 'good' insects-but, until the advent of the butterfly house, there was little opportunity to see them up close and on demand.
Figure 1 Expressions of joy experienced in a butterfly house as seen by artist Erica Sturla (www.ericasturla.com). Polymer clay and acrylic.

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The BHI was established during a period of changing attitudes to conservation in general, and insects in particular (Morris 1987; Morris et al. 1991). In addressing both the environmental risks and conservation opportunities created by the BHI, we seek answers to three fundamental questions: To what extent is the industry a threat to biodiversity? To what extent is it a benefit to conservation and environmental education? And, how can it be managed and regulated to minimise the former and maximise the latter?

There are some difficulties in producing an overview of the current situation, mainly due to the lack of robust data, but also the different interests and attitudes of the various stakeholders, their varied and often limited biological knowledge, and the inconsistent regulatory and recording procedures that affect all aspects of this global industry. Despite this, we believe that the major issues are clear and need to be addressed now to ensure the BHI is 'fit for the future'. In particular, we discuss the complexity of factors, both positive and negative, affecting the environmental risks and ethical issues involved, as well as the unfulfilled educational opportunities the BHI has created. To address these issues, various actions need to be taken, not only by the industry itself, but also by the NGO and science communities.

Due to a lack of systematic studies on the many aspects of the BHI, and their complex interrelationships, we have largely had to rely on soft 'data' derived from visits, talks, websites, leaflets, and newsletters, for most of which we cannot give citations. We are therefore unable to provide robust references for various important statements. However, this neither invalidates the problems we highlight, nor eliminates the need for new empirical data on the BHI. At the same time, we largely refrain from naming individuals or specific enterprises. Because a complete overview is not available, in this paper we do not wish to accuse or praise individuals or enterprises, or advertise particular activities of any kind.


   Insect Trading: Past and Present Top


Insect trading has a long and complex history. Trade in butterflies goes back to post-Renaissance, Enlightenment Europe, when "cabinets of curiosity" became fashionable among the rich. Four historical innovations underpin the BHI: development in late nineteenth century Europe of commercial butterfly 'farming' to produce livestock of native and exotic species (largely for amateur entomologists); development in mid-twentieth century of the concept of butterfly gardening to encourage native species for pleasure and conservation; foundation of the Insect Farming and Trading Agency (IFTA) in Papua New Guinea in 1978, with the express mission to ranch exceptionally desirable and supposedly endangered butterflies for collectors (e.g., birdwings, Ornithoptera) to promote species and habitat conservation in a sustainable manner through local economic benefit (Hutton 1985; Parsons 1992; Orsak 1993; New 1994; Black et al. 2001); and the emergence from about 1980 of the live butterfly house as a public entertainment, notably Clive Farrell's London Butterfly House (LBH).

Farrell wanted to share his passion for butterflies with the public at large, especially children-to create not only enthusiasm for butterflies and other invertebrates, but also contribute to education. The main innovation, first introduced by David Lowe in Guernsey in 1976, was presentation of exotic butterflies within a simulated tropical environment, in the form of a plant-filled, hot and humid 'walk through' greenhouse in which young and old were free to explore. Farrell's successful LBH enterprise also stimulated the next key step: establishment of commercial butterfly farms in the tropics needed to stock the exhibits, such as the large scale facilities created in Costa Rica in 1983 and Malaysia in 1986 (Goh 2007).

The LBH became a prototype for the modern temperate-region live tropical butterfly exhibition-a particular type of insect zoo (Saul-Gershenz 2009) often termed a butterfly zoo, butterfly garden, butterfly centre, or butterfly park. However, for consistency we use butterfly house throughout to refer to the LBH type of exhibition, restricting butterfly garden to open-air developments where only native butterflies are encouraged to visit and, if possible, breed naturally. Butterfly gardens have a different history that can be traced back, at least, to the Drum Manor Butterfly Garden, opened in 1970 with the objectives of serving the needs of butterfly conservation, providing a visitor attraction, and educating the public about conservation "in a familiar context, that of gardening" (Heal 1973). Only native species were to be included-mostly those already present or thought likely to establish 'naturally' at its location near Cookstown, Northern Ireland (Heal 1973).


   New Dimensions: Internet Communication and Courier Shipping Top


Rapid communication (internet, cell phones) and fast, small-volume courier services made ordering and shipping pupae and the display of live butterflies much easier and, together with the pioneer initiatives of the late 1970s, led to the establishment of a booming industry involving several groups of stakeholders [Figure 2]: breeders and farmers (producers), suppliers (dealers), and exhibitors along with visitors (the 'consumers' in this economic system), all with different interests, knowledge, responsibilities, and needs. The basis of the industry is that live butterfly pupae (chrysalids) are mass-produced for the regular re-stocking required due to the relatively short adult lifespan of butterflies.
Figure 2 Sketch of the complex network of stakeholders of the Butterfly House Industry and principal / major trade lines of pupae. I. Pupae are produced either by "individual breeders" (individuals / families producing more or less many pupae), "breeding cooperatives" (associations of individual breeders sharing facilities) and "butterfly farms" (privately owned with employed staff for breeding), some having their own exhibit. II. "Single-country-based suppliers" collect pupae for export to international suppliers and/or to live exhibits usually from a mix of sources in their vicinity/country, and often have their own farm and/or exhibit. "Global suppliers" trade with pupae from different countries and provide exhibits with a wide range of species, again often acting as exhibitors, too. III. Butterfly houses vary greatly in size, and they often purchase pupae from international suppliers, supported by material from national suppliers, rarely directly from breeders. Some exhibits or chains of exhibits have their own breeding facilities abroad or have exclusive bilateral contracts with farms, and are thus not involved in the main network. IV. The butterfly "art and souvenir" and V the butterfly "release" industries operate largely independently of the BHI, although there are some or sporadic connections. * = potential environmental risks occur at a number of points within the network.

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   Current Extent and Philosophy of The Butterfly House Industry Top


As already indicated, there are no comprehensive statistics on the magnitude of the BHI-in part due to the enormous variation in size, scope, management, and impact of individual enterprises, at every level [Figure 2], but also the widespread lack of regulations and of a co-ordinating organisation. Despite this, it is possible to give some idea of the current levels of activity.

Breeders

Breeders (often called farmers) can be single people or families operating a 'cottage industry' to produce pupae. Small breeders are sometimes organised in cooperatives. At the other extreme, large butterfly farms can have many employees. We cannot assess the number of breeders, but many hundreds are involved, notably in tropical countries (including Colombia, Costa Rica, Ecuador, El Salvador, Indonesia, Kenya, Malaysia, Suriname, Philippines, Tanzania, and Thailand). Dickinson (2004) reported that 250 farmers were contributing to the Amani Butterfly Project (Morgan-Brown 2007). Being engaged in such a process can have social, economic, and environmental benefits: "Butterfly farming allows the local community to diversify their income generating activities and to work at home around childcare and domestic duties. It also raises awareness among residents and decision makers of the benefits of conservation." (Zanzibar Butterfly Centre 2011; see also Morgan-Brown 2007).

Suppliers

Suppliers are also diverse, from local businesses handling hundreds of pupae per week to those operating internationally and dealing with thousands. Some suppliers also produce pupae, while others never do so [Figure 2]. An important distinction exists between single-country-based suppliers (sending pupae from one country to many others) and global suppliers (who obtain pupae from many countries and supply many countries). Again, we have little idea of numbers, but many people are involved. 1

Exhibits

Great diversity is characteristic of butterfly houses too, ranging from family enterprises added to garden centres attracting a few hundred visitors per year, to major, high-profile institutional butterfly houses attracting hundreds of thousands. Butterfly houses operate in large cities, in tourist areas and theme parks, attached to zoos, botanical gardens, museums, shopping malls, garden centres, stately homes, airports, hotels, resorts, and butterfly farms, and as temporary attractions at fairs and festivals. Some houses operate seasonally while others are open year-round; some offer educational information but others don't; some have guided tours, and some have butterfly gardens too. Almost all have shops and cafés, and many exhibit other insects and/or other animals as well.

By searching internet sites, it is demonstrable that butterfly houses and gardens have been established in more than 50 countries worldwide, not only in developed but also developing nations-unfortunately, in many cases, not for the benefit of local people, but foreign tourists only. The total number runs to several hundred. 2 Just as there is great variation in the exhibits, the same applies to regulations affecting how and by whom such exhibitions are presented and managed.

Species involved

Lists produced by major suppliers show that pupae of about 300 species have been offered to butterfly houses over the last decade, maintaining a number already established by the mid-1980s (Collins 1987; Morris et al. 1991). For many, availability is seasonal or only occasional. The trade is sustained by less than 50 common species mostly belonging to the Nymphalidae (notably Danaus, Idea, Morpho, Caligo, Cethosia, Heliconius, Hypolimnas, Parthenos), Papilionidae (Papilio), with a smaller number of Pieridae (e.g., Hebomoia) (cf. [Table 1])-representing between them 0.25 per cent of global butterfly species diversity. There is practically no live trade in the other four families of butterflies, which together include more than half the ca. 20,000 known species. This reflects an emphasis on colourful and fairly large species that can be mass reared, shipped, and reliably 'flown' in house conditions, rather than the specialised and supposedly endangered taxa that accounted for IFTA's early success with collectors (Hutton 1985). Indeed, some of the most popular species, such as the swallowtail Papilio demoleus and the owl butterfly Caligo eurilochus, have pest populations in their countries of origin (e.g., Malo and Willis 1961). Curiously, even to science, many morphological and life history details of several of these butterflies remain undocumented-including the courtship of Morpho species.

Numbers of pupae involved

About 2 million pupae per year are imported into the European Union (Calvert pers. comm. 2010). Since 2000, the average value of pupae exported from Costa Rica exceeded USD 700,000 per year (Rios 2002; Montero 2007). This equates to about 350,000 pupae per year from Costa Rica alone (price per pupa from CR averages about USD 2). 3 However, prices charged vary at least five-fold, from about USD 0.7 to USD 4.

Worldwide, the number runs to several million per annum, with a dollar value to suppliers approximately twice that number. Speculating on a total sale of 5-10 million pupae per annum worldwide, this would represent an annual market value of livestock in the range USD 10-20 million. The value of deadstock for collectors and production of butterfly artefacts and decorative objects is likely to be of the same order (Morris et al. 1991).

The number of pupae that an exhibit uses per unit display area depends not only on how extensively an exhibition is stocked but also on butterfly welfare (see below and [Figure 3]); there are enormous differences in butterfly life spans in different exhibits due to conditions. A medium-sized exhibit may use about 30,000 pupae per year.
Figure 3 Fruit-eating butterflies like and need really rotten fruit-but this supposedly upsets the aesthetic sense of visitors to live butterfly exhibits. Thus, 'fresh' fruit is often offered instead of rotten, while visitors could easily be enlightened with respect to the real needs of the butterflies. Spraying artificial flowers with sugar water is another example of poor husbandry-due to evaporation the concentration increases rapidly, and the solution becomes too viscous to imbibe.

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Visitors

How many people visit butterfly houses? Collins (1987) reported annual numbers in excess of 4 million in the UK. Currently, several exhibits in Europe attract over one million per year. A temporary UK exhibit recently attracted on average more than 20,000 visitors per month for three consecutive summer seasons. At the opposite end of the scale, some live exhibits attached to tropical breeding facilities may only attract a few hundred people per year. Globally, we conservatively estimate 40 million people visit butterfly houses and butterfly gardens per year (26 million in USA alone: Rios 2002).

Philosophy

Diversity within the BHI does not just rest in numbers of species, visitors, exhibition sizes, etc. There is also much variation in the underlying motivations and goals pursued in creating and running an exhibit. A personal quest to share a wonder in butterflies and educate people about them is one, others engage in edutainment, and yet others focus on entertainment or are 'decorations' in a shopping mall or hotel. As already noted, there is great diversity in the 'offer' in terms of facilities and information. Exhibitions have to cater for a wide range of customers, diverse with respect to culture, age, income, interests, and background knowledge.

Organisation

There is no single governing body or any formal requirement to belong to an association, and many entrepreneurs within the BHI operate largely or even entirely independently of each other. The International Association of Butterfly Exhibitors and Suppliers (IABES) currently represents some 80 BHI stakeholders only, and has a limited Mission Statement: "Advancing the international butterfly exhibition industry through representation, communication, education, and marketing" (IABES 2011a). They have a newsletter ["International Flutterings" (IABES 2002-2011)], and a document proposing Ethical Guidelines (IABES 2011b), which offers a useful start but is incomplete and hardly implemented or implementable.

The Sonoran Arthropod Studies Institute (SASI) presented a series of conferences on Invertebrates in captivity and is now running Invertebrates in education and conservation. SASI (2011; see also Prchal 1991) offers a useful forum for exchange among BHI stakeholders and others concerned with captive invertebrates in relation to conservation and education. SASI's activities are, however, far from comprehensive, and this USA-based group has limited global outreach.


   Consequences of The Butterfly House Industry: A New Era Of Butterfly 'Uses' and Conservation Risks Top


Risks are apparent at four levels and involve breeders through suppliers to exhibitors: unsustainable production; potential introduction of aliens through translocation; inter- and intra-specific genetic mixing; and trafficking of diseases.

Risks due to changes in breeding methods

The IFTA ranching model, based on a conservation ethic, although still pursued and even encouraged for deadstock (UNEP-WCMC 2007), is not suited to the current needs of the BHI. Large-scale commercial breeding of tropical butterflies has shifted from 'small volume with high unit value' to 'large volume with small unit value'. However, although the prime IFTA conservation philosophy has largely been dropped, the idea of producing a cash crop beneficial to local people has survived (see below).

Butterfly farming: breeding, ranching or rearing? 4

Mass production can only be achieved reliably by breeding. Starting with a small number of founder individuals from the wild, butterflies can be bred, generation after generation, in confinement. This requires facilities that provide adequate food, good physical conditions (e.g., temperature, humidity), and protection from antagonists (predators, parasitoids, pathogens), to ensure high survival rates for cropping healthy pupae. Good conditions for mating and egg laying are also needed. The main practical problems involve build up of antagonists, which can destroy an entire culture (Rivers 1991).

Assuming the ideal that founder butterflies are obtained locally, to act sustainably, a significant number of adults from each cohort should be released to bolster the source population in a semi-natural way. This should be done regularly because, after several generations of inbreeding, there is risk of genetic deterioration (e.g., Lewis and Thomas 2001; Woodworth et al. 2002; Joron and Brakefield 2003). Simultaneously, to avoid inbreeding depression, fresh local individuals should be added regularly. We consider this a reasonable model for butterfly breeding systems that can be cropped heavily yet remain sustainable without harming local populations.

Ranching, introduced by IFTA, refers to an open system, where hostplants are increased by horticultural methods within a more or less wild area, egg laying is by wild females, and protection is provided by "sleeving". However, although such a system is well suited to production of small volumes of high value adult deadstock, it cannot continuously deliver predictable numbers of live pupae necessary for the BHI.

Rearing describes any situation where each and every generation is founded by a wild-caught female and all her progeny are cropped at the pupal stage (without captive multiplication), or the collecting of larvae and pupae in the field. Although this is the simplest way for local people to contribute to the industry, such uncontrolled extractive use of natural resources is unsustainable and must be discouraged.

Risks of mass production: the breeding imperative

Using non-timber forest products (which BHI pupae are) requires sustainable means of production and should not be extractive. To be both sustainable and continuously available, mass production needs to be achieved by breeding, not through ranching or rearing. Small individual breeders, either as members of cooperatives or working alone, are likely to operate less sustainably than major farms ([Figure 2]: I) because they have less opportunity for continuous culture due to lack of facilities (e.g., large flight areas for mating). Some breeding projects may be socio-economically beneficial but not necessarily ecologically sustainable. 5

Risks of livestock translocation: alien species

The release of translocated livestock, accidentally or intentionally, is a major threat to biodiversity (e.g., Lovei 1997; Wilson 2003; Kenis et al. 2009), risking bastardisation of faunas and floras (also called "biopollution").

The dynamics of most ecosystems can be disturbed by introduced species, generally in unpredictable ways. Butterflies are often perceived as benign-but this is by no means always so. In accordance with the precautionary principle, care and vigilance should be given to avoid release of any exotic butterfly and its associated organisms, including hostplants, where they have any chance of establishment. It should also be appreciated that translocated species typically first establish at low, seemingly insignificant levels but can undergo explosive increase many years later (e.g., Boggs et al. 2006).

The biological basis of the threat is due to the fact that all butterflies, like the vast majority of organisms, have more or less restricted natural ranges caused by the interaction of history (phylogenesis) and ecology. If released from their historically limited ranges by translocation, they can find suitable climatic conditions and hostplants to become established. For example, 97 per cent of the 4,000 species of butterflies now known from the Afrotropics do not occur naturally elsewhere (Ackery et al. 1995). However, the South African geranium bronze (Cacyreus marshalli) has become established in southern Europe as a result of horticultural trade and is now a potential threat to native Geraniaceae-feeding Lycaenidae (Quacchia et al. 2008). None of the approximately 400 species of butterflies native to western Europe occurs among the 6,000 species of butterflies native to the Andes, but European whites (Pieris spp.) are now established on most continents including South America, with economic impacts; moreover, at least one study has demonstrated an indirect ecological impact on a native Pieris species through parasitoids (Tanaka et al. 2007). Due to the geological history of North America and Eurasia, many North American and European butterflies are closely related and have similar ecological needs-but few belong to the same species. These sorts of differences apply everywhere, at all scales, from global to local.

The activities of the BHI result in translocation of butterflies between countries and continents, including those with similar environmental conditions and habitats. 6 However, this only becomes a potential or real problem if the butterflies are not contained en route and at final destinations. The occasional escape of tropical butterflies in northern Europe is not expected to cause problems (although this is not so with their parasitoids-see below). In southern Europe and southern USA, however, the climatic conditions, coupled with widespread introduction of exotic plants for horticulture, can provide suitable conditions for subtropical species, such as certain Danaus butterflies (e.g., Haeger et al. 2011).

Introduction of banana-feeding Caligo, native to South America, into butterfly exhibitions in tropical Africa or Asia is fraught with likely economic and ecological danger. Were they to escape, Caligo might easily become a pan-tropical pest of cultivated banana. In some areas, similar considerations apply to Papilio demoleus, frequently used in butterfly houses but a significant citrus pest in its native Southeast Asia, and now established in the Gulf region of North America (Smith and Vane-Wright 2008: 194; Garraway et al. 2009).

The recent establishment of the American heliconian Dryas iulia in Thailand, now spread south to Malaysia (Küppers 2007; Khew 2009), is almost certainly the result of translocation to, and escape from, a butterfly house. The consequences for native heliconiines that are likewise specialist feeders on Passifloraceae are unknown. Plausibly this common butterfly, especially if released from its natural control agents, could extirpate populations of native species by competitive displacement (Reitz and Trumble 2002), especially in the increasingly anthropogenic landscapes of Southeast Asia. The list of potential risks includes even the most popular and charismatic Morpho peleides, which has a wide hostplant range within the Fabaceae family and can easily be reared even in Europe (in summer only); if it were released in Kenya or the Malay Archipelago, what might be the result? Translocation risks also affect other steps in the supply chain [Figure 2].

Spreading of parasitoids and pathogens

Translocation also brings the risk of spreading species of parasitoid flies and wasps as well as diseases associated with butterflies [entomopathogens, including viruses, bacteria, protozoans, fungi, and microsporidians (Altizer and de Roode 2010)].

Every butterfly species supports its own guild of parasitoids, not all of which will be specific (but see findings of, e.g., Smith et al. 2007). The presence of parasitoids within a butterfly house is not in itself a problem, but their local escape is a serious conservation risk-in extreme cases possibly comparable to the impact of certain generalist parasitoids released as biocontrol agents [e.g., the tachinid fly Compsilura concinnata in North America (Elkinton and Boettner 2004)]. In the US, parasitisation rates of imported pupae fluctuate greatly but can be as high as 5 per cent (Wehling pers. comm. 2011). 7 Due to lack of knowledge about the very large number of insect parasitoids that exist [many of which have not even been named: e.g., Smith et al. (2008)], and the great practical difficulties of sampling and identifying such small and highly unapparent insects, introductions of many parasitoids could easily go undetected, with unknown consequences for local faunas.

Concern has been raised about possible risks associated with wedding releases of monarch butterflies (Danaus plexippus; see below) potentially carrying the neogregarine parasite Ophryocystis elektroscirrha. Although low levels of this parasite have been reported to have relatively minor effects (e.g., Altizer and Oberhauser 1999), more recent work has shown impacts on flight speed and endurance (Bradley and Altizer 2005) and reduced body size and life span (e.g., de Roode et al. 2008a, b). We have little idea how this organism affects healthy butterflies in natural populations. The impact of many pathogens is more acute for insects bred or flown in crowded conditions, or otherwise under stress (Rivers 1991). With respect to butterfly pathogens and diseases in general, our knowledge remains rudimentary. 8 We lack reliable knowledge of the natural ranges of even those butterfly pathogens that have been identified, and we have no idea of their possible phylogeographic differentiation. Emergence of the BHI makes the study of butterfly diseases an applied science. Davis and Lawrence (2006) have taken a first step, providing information about prevention and management of diseases affecting laboratory- and greenhouse-reared insects.

Genetic mixing

In addition to worries about bastardisation of faunas by spread of butterfly species and their antagonists, mixing genes within and between species is another key issue. Aardema et al. (2011) discuss local adaptations of butterflies as a conservation issue.

Almost all Lepidoptera investigated exhibit high levels of genetic diversity, revealed by intraspecific variations in chromosome number, electrophoretic studies of protein polymorphisms, and molecular sequencing (e.g., Descimon and Mallet 2009 and references therein). In almost all cases, this genetic diversity has a strong geographical component 9 , traditionally and indirectly recognised by division into subspecies; in some of these so-called polytypic species (e.g., [Figure 4]) literally dozens have been named. Although certain subspecies are clearly diagnosable by discrete differences in pattern and colour, many are not, being accepted more as a matter of subjective opinion (Kitching and Cadiou 2000). Almost all named subspecies of butterflies are based on differences in colouration and, although in most cases this will prove to have some genetic basis, these conventional subspecies may or may not correspond to ecologically relevant differences between the populations so defined.
Figure 4 Distribution map of the natural range of the butterfly Idea leuconoe in SE Asia (pecked line), showing its division into numerous named subspecies. This spectacular butterfly, the paper kite, or large tree nymph, is flown in many butterfly houses but is sourced from several different islands, bringing with it the risk of genetic mixing if livestock is exchanged between breeders or traded within the butterfly's distributional range. If it is bred in captivity in Southeast Asia outside its natural range, then there is also the risk of bastardisation of the local fauna.

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Where geographical intraspecific genetic differences have been demonstrated, either as discontinuous or clinal patterns of variation, these are not always accompanied or marked by changes in visible characters, such as colouration. Such invisible genetic differences can, however, relate to ecologically significant shifts, including hostplant preferences (e.g., Singer and Thomas 1996; Janz 2003; Mercader and Scriber 2007) and other phenotypically plastic traits. While there is every reason to believe that such hidden differences are almost universal, their scientific documentation is rare because of intrinsic difficulties in this type of research. 10

In general, molecular studies reveal that traditional taxonomic divisions frequently underestimate local differentiation (e.g., Kozak et al. 2006). The challenge now is to recognise and address "evolutionary significant units" (ESUs) for conservation (Crandall et al. 2000; Fraser and Bernatchez 2001), rather than just 'species' as conventionally labelled by Linnaean binomina. In most cases, we lack information regarding the degree and significance of genetic differentiation between the hundreds of potential source populations being used by the BHI. All we can be reasonably sure of is that, in almost all cases, there will be some degree of genetic difference. Of the 50 most common BHI species, all but Vanessa cardui and Hypolimnas bolina are divided into two or more named subspecies. For example, Papilio dardanus from Africa has over 10, the South American Heliconius melpomene more than 12, and Parthenos sylvia as well as Idea leuconoe [Figure 4] from Southeast Asia over 20. There is an urgent need to study the species used by the BHI in the context of ESUs.

The term genetic mixing (sometimes referred to as "genetic pollution") can be used to describe the situation where genetically (geographically) differentiated populations of a species are brought into contact and hybridise. In crosses between different subspecies, this can be referred to as intra-specific hybridisation, but genetic mixing is more general and, applying the precautionary principle, reminds us of the possibility of undesirable consequences from bringing together any geographically differentiated stocks, even when there are no visible markers to alert us. Concern about genetic mixing is not generally expressed because many breeders, suppliers, and even exhibitors seem largely unaware of different concepts of species and populations and risks revealed by population genetics. In our experience, butterflies given the same species name tend to be treated as undifferentiated entities in which all individuals are essentially equivalent. In reality, this is rarely if ever the case.

Concern over genetic mixing is not confined to hybridisation at the level of subspecies or ESUs. Descimon and Mallet (2009) have documented that ca. 16 per cent out of a total of 440 European butterfly species hybridise in the wild, and that about half of these hybrids are fertile, with evidence of backcrossing. From this we see that a further risk of genetic mixing can arise in continuous culture facilities from hybridisation between species that normally never encounter each other. If such individuals escape or are released and then mate with members of their parental species in the wild, the consequences are unpredictable. With respect to hybridisation, rearing closely related butterflies in an artificial, closed environment represents an uncontrolled experiment.

There are specific examples where the BHI may be causing genetic mixing. Papilio machaon occurs widely across the north temperate, from North America to eastern Asia and western Europe, and is polytypic (Eller 1936). Sperling and Harrison (1994) carried out molecular analyses using mtDNA from P. machaon representing several, but by no means all, of its many subspecies. While their findings did not in all cases reveal differences between races with respect to the mitochondrial genes investigated, they confirmed that P. machaon does exhibit extensive geographical genetic differentiation. Release of a subspecies of Papilio machaon endemic to China, pupae of which have been marketed in Europe for years, from a butterfly house in France or Germany, could thus have a significant impact on one of the most spectacular butterflies found in Europe, P. machaon machaon. 11

There is considerable risk of genetic mixing among those butterflies bred for ceremonial releases (see below), of which the monarch butterfly is a prime example. Monarchs are also used frequently in butterfly houses. It is not widely appreciated that this species is divisible into several subspecies (Brower et al. 2007). Most houses use stock of the North American migratory monarch, which forms a major subpopulation of the nominate subspecies, Danaus plexippus plexippus. South of Mexico, monarch populations are not known to exhibit long-distance migratory behaviour, and most are considered to belong to various distinct subspecies. Accidental release, for example, of Costa Rican monarchs supplied to a butterfly house in eastern Canada could have unknown consequences were they to hybridise with the local migratory population. Recent research has demonstrated that the migratory ability of this butterfly is fine-tuned by a system under direct genetic control (Reppert et al. 2010).

In Costa Rica, the Pacific and Atlantic coast populations of several Morpho species will almost certainly become mixed, due to butterfly farmers who mass-rear M. peleides at a rate of many hundreds per week. The threat this represents is unknown, but it seems likely that mixing has already occurred through exchange of breeding stock. 12

In Asia, butterflies from a breeder's stock of Papilio memnon produced by intraspecific hybridisation (genetic mixing) of two Malaysian subspecies of this highly polytypic butterfly recently escaped in Ambon, Indonesia. This apparently invasive hybrid is now spreading through the Moluccas (Peggie et al. 2005), and could have a negative impact on specialised native swallowtails that are increasingly dependent on cultivated citrus. It is potentially an acute threat to any of the poorly-known native races of P. memnon that occur in this region, which could be lost through overwhelming hybridisation even before they have been properly documented.

Heliconius are widely used by the BHI. Laboratory hybrids between Heliconius species are routinely created by researchers investigating evolution and development (e.g., Gilbert 2003), and spontaneous species hybrids of Heliconius are known to occur widely in butterfly farms and houses (Mallet 2005). Were such hybrids to escape almost anywhere in Latin America and interbreed with wild populations, a huge investment of scientific research into the evolution of these butterflies (Beltrán et al. 2011 and references therein) would appear to be at risk. There is growing evidence that a number have already escaped (Mallet pers. comm. 2011).


   Environmental and Conservation Opportunities of the Butterfly House Industry Top


Around 40 million visitors per year, worldwide and ever increasing, attending entertainment venues devoted to insects represents a huge opportunity for creating ecological, environmental, and conservation awareness. Live butterfly exhibits stimulate strong and positive responses among people of all cultures and age groups. Butterflies are flagships for all the small organisms essential to any functional ecosystem. The special 'hook' is thus the emotional appeal of butterflies as ambassadors for the invertebrate world. Even though butterfly houses can contribute little to conservation directly (but see below), because of the possibility that they will improve public understanding, from autecology to earth system science, the charisma of butterflies offers a starting point for increasing conservation awareness.

Biological knowledge and conservation awareness

Any biological principle can be taught with butterflies; they offer ideal subjects to introduce sexual reproduction and life-cycles (with the added 'spice' of their remarkable metamorphosis), dependence on critical resources (e.g., specific hostplants), existence of specific antagonists (e.g., parasitoids) as well as general predators (and thus food webs), and the need of different food for energy and growth. To understand many conservation issues, it is necessary to appreciate that the vast majority of organisms only occur naturally in particular parts of the world, and require specific habitats. Butterflies are ideal subjects for creating such awareness. Given accurate information about the species on display, where they occur, their life cycles and basic habitat requirements, the ground is prepared for the next step in conservation awareness.

The need for habitat conservation can be directly connected to butterfly exhibits by awareness that the butterflies on display only occur naturally in particular geographical areas where they are dependent on specific resources, and that many of these places are threatened by human activity. But there is also opportunity to highlight conservation needs in areas local to the butterfly house, or where the majority of visitors come from. An exhibit can link to local as well as global conservation concerns and initiatives, in part focused on butterflies and plants, but also addressing the need to promote ecosystem conservation.

Ecological and environmental literacy

Combining basic biological knowledge with the need for conservation provides an opportunity to introduce an understanding about ecosystems and how they work: energy flows, nutrient cycles, food webs, nested systems, feedback loops, self-organisation, and so on. These ideas underpin the need for sustainability, including food security (Stone and Barlow 2005). Butterfly houses have two special opportunities to get this message across: they can demonstrate how the butterflies on display have been bred in a sustainable way, and the butterfly house itself can provide an example of a sustainable enterprise by practising, for example, efficient energy use by employing only renewable or durable materials, offering organic food, and adopting and promoting fair trade principles.

Live butterfly exhibits thus have an enormous potential to educate visitors about nature, ecology, ecosystems, conservation, the environment, and even social responsibility-a far greater educational potential than anticipated when the industry began. They can take advantage of the emotional response to butterflies to get visitors' attention, and then convey not only facts about butterflies, but also a more rational understanding of insects and their ecological roles, including many benefits to humans. There must be explicit attention to the goals of a better understanding of nature, increased engagement with invertebrates, and with ecological, conservation and environmental issues, and appreciation of the need for environmental policies and actions. We do not suggest that these educational opportunities outweigh the environmental risks. Instead, we propose cooperation between stakeholders (see below) to minimise the risks while maximising the education.


   Some Novel Social and Ethical Considerations Top


In addition to the ethical issue of risks to biodiversity, the industry also gives rise to novel ethical concerns about human socio-economics, and of animal care.

The BHI has suddenly propelled butterfly pupae into the global economy, as a cash crop. The need for continuous supplies from tropical and subtropical countries provides an opportunity for a steady income to breeders and farm workers. As users of potentially sustainable non-timber forest products, the BHI can directly contribute to economic welfare of people in developing countries, at the same time indirectly fostering habitat conservation. However, for this to be sustainable, not only with respect to the butterflies and their habitats but also the producers, it is economically as well as ethically essential that fair trade principles are rigorously applied. Any desire of suppliers and end-users (exhibitors and visitors) to drive down prices for pupae through market practices needs to be moderated in light of this; price competition with respect to the primary product on which the whole industry depends is potentially destructive. Healthy competition within the industry needs to focus on quality of value-added components delivered at the point of use (e.g., butterfly houses renowned for their good presentation, educational offer, and restaurant facilities).

The availability of spectacular live butterflies has also created demand for their use where fun or momentary amusement is the only rationale. Release of butterflies during a private party, or as part of a nightclub event (Anonymous 2011), is unacceptable. That this happens in countries where mistreating a dog or cat can be a punishable offence is partly a measure of our collective distaste for insects in general (Morris 1987). It also reflects the distance to go in extending ethical concern, first to all humans and then, slowly, to a wider and wider circle of sentient creatures (Singer 1981). Respect for the lives of insects has yet to be widely accepted, but it is an ethical issue nonetheless. Closely linked is the problem of seeing wildlife, including butterflies, as only material objects that can be used without regard to their intrinsic value, as mere commodities. This is not the place to enter the huge debate that surrounds this issue, but the existence of the BHI requires that, ultimately, it is addressed: in what circumstances is it ethically acceptable to confine butterflies within an artificial space for our entertainment? Similar issues affect some public opinions regarding commercial aquaria. The existence of souvenir and decorative industries based on butterfly deadstock raises further issues in relation to the BHI (cf. Morris et al. 1991: 335).


   Actions Needed to Reduce Risks and Increase Opportunities Top


Managing the conservation risks

Three key requirements are identified to combat the major conservation risks: sustainable breeding as the sole means of mass production for livestock; preventing introduction (accidental or intentional) of alien species of butterflies, their hostplants, parasitoids, and pathogens; and avoiding genetic mixing, both at breeding facilities or through short- or long-range translocations. These can be translated into a fourth, overarching action: educating all industry stakeholders to understand why it is important to avoid these risks-and why they should voluntarily engage in reciprocal monitoring and control to ensure a high degree of compliance. Only by managing the risks and ensuring that staff are aware can the BHI demonstrate environmental and ethical responsibility.

Sustainable breeding

The need to adopt sustainable breeding throughout, rather than employ rearing, is fundamental. However, this is not a simple issue and it has consequences. A key implication is that farmers should invest in breeding only a small range of industry-suitable, common species native to their own area of operation, with appropriate technical expertise. They should resist the temptation (normally satisfied, we believe, by rearing) to make other, typically rarer species available to the supply chain on an opportunistic basis. Rare species are not necessary for education, and they are rarely if ever more valued than common butterflies by the vast majority of visitors.

In our view, the industry should not continue to extend its species range by including rarer butterflies as 'specials'-on the contrary, less common species already on the market should be omitted. Common species that can be supplied with low risk to agreed countries worldwide (see below) provide sufficient diversity to satisfy all the needs of butterfly houses and their public. 13

Discouraged translocations

Not only is it undesirable to trade species from one region to another where they could establish (tropical to tropical location, or temperate to temperate region, north to south, or vice versa), but it is also quite unnecessary, as all regions offer a wide range of suitable local species for display, or are 'safe' recipients of numerous exotics very unlikely to become established were they to escape. Sensible self-regulation of these matters by house-managers could be turned to advantage with respect to local conservation and sustainability issues. 14 A general rule should be that exhibits in the tropics only use local species. 15

Parasitoids and diseases


With respect to parasitoids and diseases, it is in the breeders' own economic interests to have healthy livestock. Consequently, one might expect that the export of infected pupae would be rare. However, if breeders and suppliers depend on or include pupae accumulated from opportunistic rearers, then infestation is likely to be higher. In addition, although breeders will be well aware of egg and larval parasitoids, they are likely far less aware of parasitoids that only emerge from pupae (so-called larval-pupal parasitoids), as by that stage most of their stock has normally been sold. Good communication between exhibitors and producers is necessary to alert breeders that they are sending out unhealthy stock. The presence of such parasitoids within a butterfly house is rarely a problem for exhibitors, since they are not rearing all life stages-but it can be for the environment if they escape! Containment of small flies and wasps is far more difficult than butterflies and there is little direct reward for preventing their release.

In general, the precautionary principle suggests that breeders and suppliers need to be more aware of the risks, undertake better management of diseases in their breeding facilities, and take as many precautions as practical to avoid passing on parasitised or 'sick' pupae. This is no more than good animal husbandry, of the sort now widely practised by modern zoos. To achieve this, however, there is a need for new research, and this could only be undertaken by willing cooperation between BHI stakeholders and the scientific community.

Even without further research, thorough education and effective monitoring of breeders should be taken seriously. In general, larger, well-organised and well-equipped breeding facilities seem preferable to small or individual production enterprises. The development of well-managed cooperatives might overcome this potentially unfortunate socio-economic limitation.

Genetic mixing

It is unwise and unnecessary to use alien stock of any species that occurs locally or even regionally in the area where a butterfly house is located. The same principle applies to breeding-farmers should not mix stock, nor should they source stock from elsewhere of species that occur naturally in their area of operation. If hybrids become established in a breeding facility, they should be terminated immediately. These problems can largely be avoided if breeders resist the temptation to exchange livestock, even within the same country. Dependence on nearby source populations will also encourage breeders to be more forthright about local conservation issues.

Responsibility for combating these risks lies at all stages in the supply chain. This includes the need to develop effective livestock screening procedures (for short-lived creatures quarantine procedures are not practical). Further, it is not only a matter of individual butterflies accidentally escaping or hitchhiking on visitors-members of the public quite often steal live butterflies, for fun, as a joke, or in some misplaced 'act of mercy' to give the insects their freedom. Without inadvertently encouraging the idea, exhibitors need to make their public aware that such actions carry a real risk of ecological damage and that, moreover, it is rarely 'merciful' for the butterflies to be released into what is, for them, an alien environment.

Conservation opportunities

Although some believe the industry can make a direct input to conservation (e.g., Hughes and Bennett 1991; van der Heyden 1992; Gordon and Ayiemba 2003; Goh 2007; Saul-Gershenz 2009; Sambhu and van der Heyden 2010), unlike modern zoo programmes for threatened vertebrates, butterfly houses should not endeavour to breed and display endangered butterflies. The survival of myriad endangered invertebrates is almost entirely dependent on habitat conservation, coupled with mitigation of impacts such as pollution and climate change.

The industry can make a direct contribution to conservation when and if the economic return from breeding facilities is sufficient to persuade people to protect specific natural or semi-natural habitats for biodiversity. Examples include the Kenyan Kipepeo Project, intended to conserve the Arabuko-Sokoke Forest (Gordon and Ayiemba 2003; Saul-Gershenz 2009), and similar projects in Tanzania (Morgan-Brown 2007), Malaysia (Goh 2007), Peru (Canseco 2007), Guyana (Sambhu and van der Heyden 2010) and elsewhere. Some farms are using their profit to buy land for biodiversity conservation (EBN 2011). The International Tropical Conservation Foundation, in part funded by a Swiss butterfly house, owns and manages Shipstern Nature Reserve in Belize (Bijleveld and McField 2006).

Where appropriate and economically feasible, butterfly houses can also help raise awareness and promote habitat conservation projects for particular endangered taxa. 16 Such initiatives should never disguise lack of attention to basic biological education and local conservation. House managers should ensure that sustainable practices and habitat conservation are promoted by all their breeders, and a demonstration of this should always be part of the exhibition. Wherever possible, a butterfly garden should be added as an outdoor attraction to encourage native species, offer additional opportunities for education about butterfly ecology and the natural environment in general (Mathew and Anto 2007), and feature the work of and cooperate with local conservation projects-which need not and indeed should not only relate to butterflies. More generally, butterfly houses serving local people need to be encouraged in developing countries.

The educational imperative

For butterfly houses to justify the environmental risks they present, we believe they must engage in effective environmental education (including use of edutainment methods wherever helpful). "Zoos must recognize that our greatest contributions to conservation will not be by the breeding of animals and their ultimate re-introduction to the wild, it is through the proper education of our millions of visitors that we can have the greatest impact in protecting species and their habitats" (Toone 1990: 65). Or, as succinctly formulated by Robinson (1991: 3): "We cannot afford to simply fascinate; we must educate." The BHI has created a potent opportunity to reach millions of people about environmental issues. The chance to educate children about natural systems is particularly important.

Exhibitors should provide educational material and, wherever possible, other opportunities (e.g., films, guided tours, talks, demonstrations, bookshops, further reading suggestions, web sites, etc.) for visitors to learn about the biology of butterflies and their place in nature. This must include information about the natural systems in which they occur, and transmit the idea that habitat conservation is essential for long-term survival. This understanding should, if possible, reach the level of basic systems thinking, to appreciate the other organisms that are part of the living communities on which butterflies depend, and of which they are a part. Ideally, this would demonstrate the principles of ecological literacy ['ecoliteracy' (Stone and Barlow 2005; see also Center for Ecoliteracy 2011)] within a general environmental literacy framework (Orr 2004; Reynolds et al. 2010). Wherever possible, this information should be linked to school initiatives based on such principles (e.g., Stone and Center for Ecoliteracy 2009)-or, failing this, to international NGO programmes accessible via the internet (e.g., FEE 2010).

Although there are rare examples of good educational practice, the educational offers presented by most butterfly houses are insufficient, misleading, incorrect, or even lacking altogether, particularly in private for-profit exhibits. At present, most visitors seem happy just to experience (and photograph) free-flying butterflies, and make little demand for educational information-other than to inquire about the names of butterflies on display. But people cannot demand what they do not know about, and there is thus little or no pressure on exhibitors to provide a good educational experience as well as a 'butterfly experience'. Such investments need to be made. However, because exhibitors sense little demand and start-up costs are likely to be considerable, few butterfly houses seem willing to sustain suitable educational programmes.

We suggest that another reason for lack of appropriate and accurate biological and conservation messages is a lack of profound knowledge about butterflies and natural systems on the part of the three groups of primary stakeholders. These stakeholders also need to recognise that they will do better in all respects if they cooperate rather than compete. Cooperation will be essential for successful self-regulation if they are to avoid increasing legal restriction.

Many people engaged in the BHI are involved because they have a love of nature. We suggest that, in addition to what E.O. Wilson termed biophilia (Kellert and Wilson 1993; Kellert 1997, 2009), many have 'butterfly-philia', and by adding a more rational understanding of butterflies and their ecological requirements to this emotional enthusiasm will allow them to run a knowledge-based operation. In a similar way, the majority of butterfly house visitors have an emotional affection for butterflies. While nurturing and encouraging this, they must also be helped to understand the place of butterflies in the natural world, and get a better idea of how our world works. Only in this way can visitors add rational understanding to emotion to get full value from their butterfly house experience. This will only be possible if those running the industry have that knowledge themselves, and thereby become confident, able, and keen to communicate it.

Although the needs and opportunities for effective education at different venues are very varied, even the best-run houses have considerable room for improvement, at least with respect to the wider issues of environmental awareness and sustainability. For most exhibitors the immediate challenge must be to increase their educational offer considerably. Given the generally low standard, rapid improvement to some minimum level should be a realistic target, assuming the industry can get assistance from competent educators and scientists to help prepare suitable pedagogical material.

The ethical imperative

Managing the conservation risks and ensuring staff are aware of the issues involved are ethical responsibilities of the BHI. Public education and good animal husbandry are equally important ethical imperatives if the industry is to survive increased scrutiny and future regulation.

With respect to good husbandry, it is essential that suitable temperature, light, and humidity conditions are maintained within exhibitions, and that particular attention is paid to access to water and suitable food [Figure 3]. The sight of a dehydrated zoo animal without access to water is likely to invoke public outrage. How long before the public become aware that dehydrated butterflies are equally unacceptable (and unnecessary), or that morpho and owl butterflies denied access to suitable fruit are also being badly treated?

Good husbandry has practical benefits for the exhibitor: healthy butterflies provided with appropriate resources will behave in more interesting ways. This also raises an apparent conflict of interest between stakeholders, breeders and suppliers on one side, and exhibitors on the other. Good husbandry by exhibitors is likely to reduce their need for pupae, as the butterflies will live longer. Short term, this will be an economic advantage to exhibitors, at least offsetting the increased costs of good husbandry, but an economic loss to the breeders and suppliers. However, we believe this apparent conflict is illusory: the normal dynamics of supply and demand will rapidly come into play. Moreover, security of the entire supply chain is predicated on the success of the exhibitors and, crucially, their public patronage. Just as modern zoos can no longer afford to display emaciated and disturbed animals in tiny cages, an increasingly sophisticated public will begin to demand that butterflies in a butterfly house are demonstrably well cared for. With respect to buyers who purchase pupae simply as material for fun events with no educational potential, such indoor releases are ethically unacceptable, send a poor message, and have the potential to bring the entire BHI into disrepute-suppliers should restrict their sales to serious exhibitors.


   Some Other Consequences of Electronic Communication And Rapid Courier Services for Trade In Butterflies Top


The principal risks exemplified for the BHI also apply to national and international exchange of insect livestock by 'amateur' entomologists, hobbyists, and insect lovers, and the new fashion for outdoor ceremonial butterfly releases. As these uses for live butterflies offer no opportunities for public education about environmental and conservation issues, we mention them only briefly here.

Livestock 'trading' for and by amateurs

In the past, amateur exchanges of livestock and commercial insect trading were rather small scale activities, largely carried out by relatively well-informed enthusiasts and a few, mostly well-known traders. Even so, Morris et al. (1991: 332) considered that global turnover of deadstock "certainly runs into tens of millions of dollars." Nowadays, traditional print media offering livestock are substituted by internet-based interactive platforms (e.g., Actias 2011; ELG 2011). The World Wide Web and courier services now make shipping of livestock an activity in which anyone can join and which in effect has no limits. Many different kinds of live insects (not just butterflies) are sold and exchanged worldwide within days or even hours. What recipients do with their livestock is uncontrolled. As with the BHI, legislation is missing-but even if it existed, it is very doubtful it could be implemented. Thus, only good environmental education can address these risks. Most amateurs are even more biophilic than stakeholders in the BHI and, even if they have limited general biological understanding, many are real specialists and often extremely knowledgeable about the particular species in which they are interested. However, there are potentially high translocation and genetic risks attached to amateur livestock trading and exchange, and this remains largely unrecognised; Buschinger (2004) seems to be an exception.

Ceremonial butterfly releases

The spiritual issues associated with butterflies (e.g., Manos-Jones 2000) makes one wonder why they have been so little used in ceremonial activities until recently. Modern means of communication and transport in combination with the new ability to mass-produce butterflies has now given rise to the phenomenon of 'ceremonial releases', typically involving flights of monarchs and several other species released at weddings, funerals, birthdays, and comparable occasions. Pyle et al. (2010) report 11 million individual butterflies released per year in North America alone. In contrast to live exhibits, such acts rarely have education value but raise similar conservation issues as the BHI. The release industry is largely served by a different set of entrepreneurs well organised through the International Butterfly Breeders Association (IBBA), currently with 150 members-many more than IABES. Notably, they are breeders and suppliers at the same time. A considerable controversy concerning the conservation risks and ethical issues has developed, to which the interested reader is referred [for overview see Federman 2008; IBBA 2011; see also, e.g., Brower et al. 1995, 1996; Keiper 1996; Glassberg et al. 1998 (see also reply by Moreau 1999); New 2008; Pyle 2010; Pyle et al. 2010; Wagner et al. 2011].

School kits

Another development has seen major growth in the supply of school "butterfly kits", with larvae or fertilised eggs and artificial diet to feed the caterpillars. Once children have witnessed the fascination of metamorphosis, the temptation to give the lovely butterflies their freedom is often irresistible. While this schoolroom use of live butterflies undeniably has educational potential (Wagner et al. 2011), it is beyond the scope of this paper. However, a treatment of butterfly kits similar to this discussion on the BHI is certainly warranted.


   The Special Nature of The Butterfly House Industry Requires Special Attitudes-and Assistance Top


Within the BHI, which has 'exploded' opportunistically, most stakeholders apparently act independently. To meet the many issues discussed above, networking will be essential. Legislation might also appear important, but can only be effective locally because the general factors involved are too complex, with worldwide dimensions and dynamics, and cannot be policed. Instead, intensive networking and self-regulation will be required. The industry needs to be convinced that it should act neither on the basis of 'what is not illegal is OK' nor 'what generates money must be done'. If the BHI does not do everything possible to work sustainably, deliver good education, and adopt ethical principles with respect to both people and insects, then it is as much at risk from negative public opinion as it is from local legislation.

To be responsible, the BHI has to be mindful of an exceptional number of ethical, environmental, and social requirements: all exhibition material should be sourced from sustainably managed cultures; only suitable, relatively common species should be bred; breeders must be vigilant to avoid genetic mixing, either within their cultures, or on release back into the wild; pupae should not be shipped to locations where escape would carry any risk of bastardisation of local fauna, including genetic mixing; suppliers need to give accurate proper names to the species as well as declare their origin; and breeders and suppliers should sell only to exhibitors who use butterflies for educational purposes, and should refuse any temptation to provide pupae or butterflies for ceremonial releases or other momentary amusements.

Attempts to maximise income without regard to ethical issues may lead to a loss of respect by breeders, suppliers, and exhibitors for the living organisms on which they depend, reducing the living animals to mere commodities. Driving down the cost of pupae specifically runs the risk of undermining the economic benefits to the primary producers; if producers are not fairly rewarded, they will likely adopt poor or unsustainable practices. In general, temptations to 'cut corners' to maximise profits add to the problems caused by widespread unfamiliarity of many of those engaged in the industry regarding the biological needs of butterflies.

As Orr (2004: 205) commented, "there is a growing potential for disaster caused by someone who is merely incompetent rather than malign." 17 Given the special nature and responsibility of the BHI, to become fully competent it needs to formulate a meaningful common mission statement and create a co-ordinating and self-regulatory umbrella organisation. A meaningful mission statement for a butterfly house, or the BHI as a whole, would need to include the following elements:

To promote the worldwide conservation of living organisms and their habitats exemplified by butterflies and their ecological requirements and roles, to be achieved by fair trade with farmers who practice sustainable production of suitable butterfly pupae. Aware of the overarching environmental, social, and ethical issues, every effort must be made to: avoid the risk of faunal bastardisation and genetic mixing; establish and sustain high quality educational programmes concerning ecology and environmental issues in general; operate all facilities in as sustainable a manner as possible; co-operate with local organisations to help and promote conservation; and practice good husbandry and encourage respect for living organisms throughout the industry.

To achieve these goals, close cooperative (not competitive) networking will be necessary between all stakeholders, and open communication with the scientific and pedagogical communities essential and of mutual benefit. Within the industry, training seminars and materials should disseminate 'best practices' for stock maintenance and rearing, and trading practices that take into account impacts of the industry on ecological and economic sustainability in the butterfly source areas, and ecological sustainability where they are displayed. For visitor services, model educational programmes, curricula, and materials addressing visitors of different age groups are needed, as is information for breeders. 18

Eventually, the umbrella organisation should introduce certification for sustainable production and operation, responsible sales, fair trade, good husbandry, and educational quality. A star rating reflecting success in achieving high standards could be introduced.

Possibly, it will be too difficult to found a new umbrella organisation or to extend the membership, goals, and activities of the International Association of Butterfly Exhibitors and Suppliers (IABES 2011a). To meet the requirements, establishing a Code of Trading and Exhibiting Live Butterflies might be an alternative which could also offer certification. The Code of Insect Collecting and the Code of Insect Re-introductions by Invertebrate Link (JCCBI 2011) could offer useful models. The North American Pollinator Protection Campaign (NAPPC 2011) might also be an appropriate guide for the necessary organisation.

The role of science

To achieve all that is required, it is clear that the scientific community has a responsibility to support the BHI, in particular by doing research on, for example, sustainability of harvesting wild butterflies, on pathogens and parasitoids, and ESUs. The species used by the BHI need to be studied in detail 19 , so they can be used authoritatively to illustrate specific and general principles in educational material. Scientists should also cooperate in preparing exhibits and programmes about local butterflies, assist in education, and help develop optimal husbandry. 20

Some breeders and exhibitors carry out their own research on butterflies. There is, in fact, a considerable amount of knowledge available from the experiences of breeders and exhibition guides-but, unfortunately, this is rarely or ineffectively communicated within the industry, or to the scientific community.

The role of funding agencies

Funding agencies supporting butterfly farming projects should not just provide money but also insist on contextual education and training. Economic benefits that come without increasing environmental awareness will undermine efforts to make the BHI sustainable. There is an imperative to educate all those involved in such initiatives, and funding agencies should ensure that programmes and training costs are included.

The management of butterfly houses

Although butterfly houses have similarities to zoos, there are fundamental differences in their needs for successful management and the effective roles they can play in society, including conservation. The direct conservation role of modern zoos cannot be matched by the BHI (cf. Crone et al. 2007), and regular stocking with new individual butterflies will always be necessary. However, with respect to organisation and cooperation there is much to be learnt from the recent changes in zoo philosophy-notably the establishment of effective self-regulating mechanisms through excellent international organisation [e.g., World Association of Zoos and Aquariums (WAZA 2011) and their member institutions], regular sharing of information, improving husbandry, etc. It is notable that zoos have had to change in many ways to be tolerated by modern society, a major aim now being education (e.g., Robinson 1991; Andersen 2007).

In some countries, no permits are necessary to run a butterfly exhibit. Often, no standards are imposed or even expected. Even if exhibitors do not think only of generating income, they often make insufficient educational efforts, and sometimes reveal poor husbandry. But if a mission related to ecology and education is omitted, and there is no conservation benefit, is there any ethical justification for displaying live organisms at all?


   Perspectives Top


We anticipate that the intentional translocation of insects for the purposes of entertainment will continue to increase, a scenario in which the BHI will play a leading role. Moreover, this activity will become ever more global, with insects being moved not only from the tropics to temperate regions, but also from country to country within the tropics. The issues discussed in this paper will thus become ever more relevant and even more pressing than now.

We have referred to the bastardisation (some call it "MacDonaldisation") of fauna and flora with the more or less tacit assumption that this is a bad thing. There are biological reasons to expect that increasing homogenisation will lead to numerous extinctions. In reality, however, with respect to plants at least, the genie is well and truly out of the bottle. Ever since humans adopted agriculture and ceased to be hunter-gatherers, intentional hybridisation, genetic mixing (now including GMOs), and translocation of plants have followed at an ever accelerating rate. Not only plants for food, but also those we grow in our back yards simply for pleasure, come from all over the world and are thrown together with little reason or thought. Although plant translocation creates numerous environmental problems (e.g., Brasier 2008), little is done to stop it.

If so, what does it matter if a few of the world's most beautiful butterflies become feral on other continents, or have their genomes muddled up?-after all, they evolved in natural systems that almost everywhere are now more or less disrupted by human activity, including the presence of numerous non-indigenous plants. In the great scheme of things, do butterflies matter? Why should we worry about them? All we can say in response is that, in agreement with Wilson (2003) and numerous other commentators, we believe that all species and natural ecosystems are valuable, and we should do all that we reasonably can to protect them. Moreover, we do not intend to 'defend' this belief by resorting to economic or other utilitarian arguments-not least because it will always be possible to make a case that more money, or some other supposed good, can be realised by transforming any given component of the natural system without regard for its relationship to the whole.

The BHI presents a wonderful opportunity for spreading environmental awareness. However, the extent to which this promise can be made real will depend very much on the industry rising to the challenge to engage effectively in education, research, and conservation, and self-regulate to minimise the environmental risks involved.


   Acknowledgements Top


We wish to acknowledge Mark Collins' seminal paper on butterfly houses in Britain (Collins 1987). Although we have not cited his work widely, Mark anticipated a number of the arguments and recommendations presented here, and it is regrettable that his excellent report is so difficult to access. If his early recommendations had been adopted at the outset, several problems still perceived might have been avoided or solved already.

We are very grateful to Lincoln Brower, Clive Farrell, Ottmar Fischer, Neil Gale, Nathan Morehouse, Michael Morris, Karen Oberhauser, Werner Schröder, Mark Scriber, Felix Sperling, Wayne Wehling, and Klaus Wenzel for reading an initial draft of this paper, and suggesting numerous improvements. Dr Oberhauser, in particular, went 'beyond the call of duty' in not only highlighting several important problems, but also proposing numerous editorial improvements; Dr Wehling most kindly provided us with unpublished statistical data from United States Department of Agriculture; and Dr Morris suggested the creation of a Code. However, while we have gratefully adopted several of our colleagues' suggestions, the views expressed here remain entirely the responsibility of the authors. We are also indebted to four anonymous reviewers for their constructive criticisms.[121]

Notes

  1. It appears as though some form of centralisation of global suppliers has now occurred, with the implication that small new enterprises may find it difficult to join the world market without co-operation with one or more global suppliers.
  2. In the USA alone there are 79 exhibits with tropical Lepidoptera, 44 of which run all year, and 200 butterfly gardens (Wehling pers. comm. 2011).
  3. In 2010, Costa Rica exported 350,000 pupae to the USA alone (Wehling pers. comm. 2011), thus the real number of pupae exported from this county must be much higher.
  4. In the context of endangered species, the Convention on International Trade in Endangered Species (CITES) uses the terms farming and ranching in a slightly different way (cf. Black et al. 2001).
  5. There is a suspicion that small, individual farmers extractively gather gravid females opportunistically from the wild, rear the progeny to the pupal stage, and then pass the pupae directly to the supplier. Suppliers often advertise small numbers of pupae of certain species on an occasional basis (or include them in 'species mixes'), suggestive of such practice.
  6. Official statistics state that during 2000-2005, Costa Rica exported large numbers of pupae to the former Netherlands Antilles, Argentina, Mexico, and Nicaragua, and even Philippines, South Africa, and Singapore (Montero 2007). Tropical destinations of pupae originating from Southeast Asia are unavailable to us.
  7. The recent establishment of the first sturmiine tachinid fly in Great Britain might be accidental, due to climate change, or a result of BHI activity bringing Sturmia bella-infected pupae into the country. The Sturmiini are a tribe of mainly tropical and subtropical flies, many of which specialise on butterflies belonging to the Nymphalidae; Sturmia bella is known from continental Europe, Israel, and Japan and its establishment in the UK, by whatever means, may at least be partially responsible for the current decline of the formerly common nymphalid Aglais urticae in southern England (Allen 2005). However, flies currently identified as S. bella may represent more than one species.
  8. Ophryocystis elektroscirrha was discovered in the monarch, a particularly common and well-studied butterfly, only 45 years ago (McLaughlin and Myers 1970). It is highly probable that in addition to the few known nuclear polyhedrosis viruses, bacteria, and microsporidian species, many more as yet totally unknown butterfly pathogens exist.
  9. Hebert et al. (2010) reported very low levels of genetic variation in the DNA 'barcode' sequence of 1,300 species of North American Lepidoptera, with minor geographical variation in samples collected as much as 2,800 km apart. At first sight, this appears to contradict the assertions that high levels of genetic variability exist within most Lepidoptera, and in most species this variation exhibits a strong geographical component. However, the 'barcode' comes from CO1, a fragment of cytochrome c oxidase 1 gene of the mitochondria, a particular region chosen explicitly for its property of showing great variation between species but little within, so that it can be used as a marker for species identification. The point of Hebert et al. (2010) is to demonstrate that the barcode region does behave as claimed, even when tested across as many as 1,300 species sampled from an entire continent. Their study says nothing about variability in the nuclear genes that exhibit polymorphism and geographical variation in most sexually reproducing organisms.
  10. Molecular studies readily reveal intraspecific differences-but these are not necessarily ecologically significant or interpretable (Forister et al. 2008). Although a recent molecular investigation into the long-tailed blue (Lampides boeticus; one of the few widespread butterflies not divided into subspecies) demonstrated relatively low divergence in mitochondrial sequence data across much of its range, haplotype variation revealed a complex history of colonisation events in Australia (Lohman et al. 2008). Australian L. boeticus are, however, phenotypically indistinguishable from other long-tailed blues, and the ecological relevance of these findings is as yet unknown.
  11. A similar and possibly more acute risk occurs in the UK, where the narrowly distributed subspecies P. machaon britannicus, despite being almost indistinguishable by colour pattern from P. machaon machaon, is a clear example of an ESU-in this case involving changes in behaviour and hostplant preference (Dempster et al. 1976).
  12. Singapore has a rare native subspecies of Idea, I. leuconoe chersonesia, but at the local zoo, they breed and exhibit I. leuconoe clara from Taiwan (Khew 2009). How long before 'escapees' mix with the native population, and what are the trade-routes for the many locally occurring subspecies of I. leuconoe (cf. [Figure 4])?
  13. None of these species should be listed under CITES regulations or appear on any Red List-although in Australia, a butterfly house exhibits the CITES-listed Cairns birdwing, Ornithoptera euphorion-but it is locally bred, used in the exhibit, and not traded.
  14. The possibility of increased breeding in developing countries faces the problem that the main international markets (e.g., USA, Europe) are already saturated. However, breeding for local butterfly houses for education of local people and tourists offers potential.
  15. A butterfly house in Mexico is happy to state on posters that they obtain their pupae from 'sustainable' farms in Costa Rica. Given the broad overlap of the Mexican and Costa Rican neotropical faunas, but their almost certain geographical differentiation, the risks of genetic mixing are obvious to us, but seem totally unappreciated by those responsible-and the valuable educational message about the differentiation of populations is also lost.
  16. "Save Homerus", an initiative to save Papilio homerus, the largest New World swallowtail butterfly from extinction, involves a number of butterfly exhibitors (IABES 2011c).
  17. The authors are aware of a real case that involves breeding for the BHI a butterfly endemic to a particular tropical island on an island nearby where the genus, let alone the species, does not naturally occur. There is mounting evidence that, due to inadequate containment, the butterfly is now established and spreading. No harm was intended-but that does not make it better. Ignorance and incompetence are parents of many a disaster.
  18. Unfortunately, manuals for breeders (see for e.g., Canseco 2007; Montero 2007) rarely address potential risks, and do not mention the need to act sustainably and avoid risky translocations.
  19. Brewster and Otis (2009) quantified differences in suitability, in terms of behavioural traits and longevity, of a number of different butterfly species used within the BHI. From their data, together with a knowledge of the prices charged per species, they derived a cost-effectiveness index, or "relative suitability score". This index varied over 200-fold across the species studied. The authors noted that "exhibitors can maximize adult butterfly life span by ensuring that diet requirements are met" (Brewster and Otis 2009: 113). Despite this, no attempt appears to have been made to control for these or other animal husbandry variables (light levels, humidity, temperature, etc.) affecting the particular butterflies and butterfly house on which their observations were based. Even so, this work offers a step towards a more quantitative approach to assessing the suitability of different species. Additional research is needed to establish the environmental optima of a wide range of those species regularly used by the industry, which will not only offer a basis for improving animal husbandry, but also provide a more rigorous basis on which to make performance comparisons.
  20. A concrete issue, at first sight minor but now emerging as an acute problem, is the often provisional and seemingly endless change of scientific names applied to species. Even the flagship of the BHI, the Morpho species widely known as M. peleides, has recently suffered a name change in some scientific literature (notably, Lamas 2004), a change which is now causing confusion not only for import and export regulations, but also the preparation of educational materials, dealers lists, and access to information in books. As science progresses, revision of particular names from time to time becomes essential, but the present free-for-all of the distributed taxonomic system (Vane-Wright 2003) is increasingly irresponsible in our 'information age' (Scoble 2004). Self-regulating groups are beginning to emerge willing to challenge this problem in a constructive way. For example, the names committee system developed by NABA for North American butterflies (Cassie et al. 2001.) could act as a model-and this would necessarily involve cooperation with butterfly taxonomists and other scientists. Similarly, a group is required to establish protocols for 'safe' trading destinations for reciprocal use by suppliers and exhibitors.


 
   References Top

1.Aardema, M.L., J.M. Scriber and J.J. Hellman. 2011. Considering local adaptation in issues of lepidopteran conservation-a review and recommendations. American Midland Naturalist 165: 294-303.  Back to cited text no. 1
    
2.Ackery, P.R., C.R. Smith and R.I. Vane-Wright (eds.). 1995. Carcasson's African butterflies: An annotated catalogue of the Papilionoidea and Hesperioidea of the Afrotropical region. East Melbourne: CSIRO.  Back to cited text no. 2
    
3.Actias. Forum und Internetbörse für Insekten und Spinnen. 2011. http://www.actias.de. Accessed on April 3, 2011.  Back to cited text no. 3
    
4.Allen, A.A. 2005. The recent occurrence of Sturmia bella (Meigen) (Diptera: Tachinidae) in south-west England, including rearings from two host species of Nymphalidae. British Journal of Entomology and Natural History 18: 269-270.  Back to cited text no. 4
    
5.Altizer, S.M. and K.S. Oberhauser. 1999. Effects of the protozoan parasite Ophryocystis elektroscirrha on the fitness of monarch butterflies (Danaus plexippus). Journal of Invertebrate Pathology 74: 76-88.  Back to cited text no. 5
    
6.Altizer, S. and J. de Roode. 2010. When butterflies get bugs: the ABCs of lepidopteran disease. American Butterflies (Summer): 16-26.  Back to cited text no. 6
    
7.Andersen, L.L. 2007. Zoo education: from formal school programmes to exhibit design and interpretation. International Zoo Yearbook 38: 78-81.  Back to cited text no. 7
    
8.Anonymous. 2011. http://www.butterflies.lv. Accessed on April 3, 2011.  Back to cited text no. 8
    
9.Beltrán, M., A.V.Z. Brower and C. Jiggins. 2011. Heliconius. Longwings or passion-flower butterflies. http://tolweb.org/Heliconius/72231/2010.07.21. Accessed on April 3, 2011.  Back to cited text no. 9
    
10.Bijleveld, C. and M. McField. 2006. Report on 10 years activities in Belize (Central America). Belize City: International Tropical Conservation Foundation and Shipstern Nature Reserve. http://www.shipstern.org/CMS/default.asp?ID=139. Accessed on April 3, 2011.  Back to cited text no. 10
    
11.Black, S.H., M. Shepard and M.M. Allen. 2001. Endangered invertebrates: the case for greater attention to invertebrate conservation. Endangered Species Update 18: 42-50.  Back to cited text no. 11
    
12.Boggs, C.L., C.E. Holdren, I.G. Kulahci, T.C. Bonebrake, B.D. Inouye, J.P. Fay, J.P. McMillan, et al. 2006. Delayed population explosion of an introduced butterfly. Journal of Animal Ecology 75: 466-475.  Back to cited text no. 12
    
13.Bradley, C.A. and S. Altizer. 2005. Parasites hinder monarch butterfly flight: implications for disease spread in migratory hosts. Ecology Letters 8: 290-300.  Back to cited text no. 13
    
14.Brasier, C.M. 2008. The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathology 57: 792-808.  Back to cited text no. 14
    
15.Brewster, A.L.E. and G.W. Otis. 2009. A protocol for evaluating cost-effectiveness of butterflies in live exhibits. Journal of Economic Entomology 102: 105-114.  Back to cited text no. 15
    
16.Brower, L.P., L.S. Fink, A.V.Z. Brower, K. Leong, K. Oberhauser, S. Altizer, O. Taylor, et al. 1995. On the dangers of interpopulational transfers of monarch butterflies. BioScience 45: 540-544.  Back to cited text no. 16
    
17.Brower, L.P., L.S. Fink, A.V.Z. Brower, K. Leong, K. Oberhauser, S. Altizer, O. Taylor, et al. 1996. Reply to Keiper. BioScience 46: 563-564.  Back to cited text no. 17
    
18.Brower, L.P., K.S. Oberhauser, M. Boppré, A.V.Z. Brower and R.I. Vane-Wright. 2007. Monarch sex: ancient rites, or recent wrongs? Antenna 31: 12-18.  Back to cited text no. 18
    
19.Buschinger, A. 2004. International pet ant trade: increasing risk and danger in Europe (Hymenoptera, Formicidae). Aliens Newsletter 19/20: 24-26.  Back to cited text no. 19
    
20.Canseco, A.J.M.D. 2007. Mariposas. Guía Para el Manejo Sustentable de las Mariposas del Perú. http://www.iiap.org.pe/Publicaciones/PublicacionesMostrar.aspx?PublicacionesId=329&TabId=5. Accessed on April 3, 2011.  Back to cited text no. 20
    
21.Cassie, B., J. Glassberg, A. Swengel and G. Tudor. 2001. North American Butterfly Association (NABA). Checklist and English names of North American butterflies. 2 nd edition. Morristown, NJ: North American Butterfly Association.  Back to cited text no. 21
    
22.Center for Ecoliteracy. 2011. www.ecoliteracy.org. Accessed on April 3, 2011.  Back to cited text no. 22
    
23.Collins, N.M. 1987. Butterfly houses in Britain: the conservation implications. Report to the Nature Conservancy Council, Department of the Environment and World Wildlife Fund (UK). Cambridge: IUCN.  Back to cited text no. 23
    
24.Crandall, K.A., O.R.P. Bininda-Emonds, G.M. Mace and R.K. Wayne. 2000. Considering evolutionary processes in conservation biology. Trends in Ecology & Evolution 15: 290-295.  Back to cited text no. 24
    
25.Crone, E.E., D. Pickering and C.B. Schultz. 2007. Can captive rearing promote recovery of endangered butterflies? An assessment in the face of uncertainty. Biological Conservation 139: 103-112.  Back to cited text no. 25
    
26.Davis, F.M. and A. Lawrence. 2006. Prevention and management of microbial diseases of insects being reared under laboratory environments. http:// butterflybreeders.com/public/health/disease_prevention_and_management.html. Accessed April 3, 2011.  Back to cited text no. 26
    
27.Dempster, J.P., M.L. King and K.H. Lakhani.1976. The status of the swallowtail butterfly in Britain. Ecological Entomology 1: 71-84.  Back to cited text no. 27
    
28.de Roode, J.C., A.B. Pedersen, M.D. Hunter and S. Altizer. 2008a. Host plant species affects virulence in monarch butterfly parasites. Journal of Animal Ecology 77: 120-126.  Back to cited text no. 28
    
29.de Roode, J.C., A.J. Yates and S. Altizer. 2008b. Virulence-transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite. Proceedings of the National Academy of Sciences 105: 7489-7494.  Back to cited text no. 29
    
30.Descimon, H. and J. Mallet. 2009. Bad species. In: Ecology of butterflies in Europe (eds. Settele J., T. Shreeve, M. Konvika and H. Van Dyck). Pp. 219-249. Cambridge: Cambridge University Press.  Back to cited text no. 30
    
31.Dickinson, D. 2004. Butterfly farming proves worth a flutter. BBC News: http://news.bbc.co.uk/1/hi/business/3569164.stm. Accessed on April 3, 2011.  Back to cited text no. 31
    
32.EBN (El Bosque Nuevo) 2011. Welcome to El Bosque Nuevo - Butterfly pupae from Costa Rica. http://www.elbosquenuevo.org/. Accessed on April 3, 2011.  Back to cited text no. 32
    
33.Elkinton, J.S. and G.H. Boettner. 2004. The effects of Compsilura concinnata, an introduced generalist tachinid, on non-target species in North America: a cautionary tale. In: Assessing host ranges for parasitoids and predators used for classical biological control: A guide to best practice (eds. Van Driesche, R.G., T. Murray and R. Reardon). Pp. 4-14. Morgantown, WV: United States Department of Agriculture Forest Health Technology Enterprise Team. FHTET-2004-03. http:// www.fs.fed.us/foresthealth/technology/pub_titles.shtml. Accessed on April 3, 2011.  Back to cited text no. 33
    
34.Eller, K. 1936. Die Rassen von Papilio machaon L. Abhandlungen der Bayerischen Akademie der Wissenschaften Mathematisch-naturwissenschaftliche Abteilung. Neue Folge 36: 96 pp., 16 pls.   Back to cited text no. 34
    
35.ELG (Entomological Livestock Group). 2011. http://www.pwbelg.clara.net. Accessed on April 3, 2011.  Back to cited text no. 35
    
36.Federman, A. 2008. All aflutter. The flap over the mail order butterfly industry. http://www.earthisland.org/journal/index.php/eij/article/all_aflutter/. Accessed on April 3, 2011.  Back to cited text no. 36
    
37.Forister, M.L., C.C. Nice, J.A. Fordyce, Z. Gompert and A.M. Shapiro. 2008. Considering evolutionary processes in the use of single-locus genetic data for conservation, with examples from the Lepidoptera. Journal of Insect Conservation 12: 37-51.  Back to cited text no. 37
    
38.FEE (Foundation for Environmental Education). 2010. http://www.fee-international.org/en. Accessed on April 3, 2011.  Back to cited text no. 38
    
39.Fraser, D.J. and L. Bernatchez. 2001. Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Molecular Ecology 10: 2741-2752.  Back to cited text no. 39
    
40.Garraway, E., C.P. Murphy and G.A. Allen. 2009. Papilio demoleus (the lime swallowtail) in Jamaica, a potential pest of citrus, expanding its range in the Caribbean. Tropical Lepidoptera 19: 58-59.   Back to cited text no. 40
    
41.Gilbert, L. 2003. Adaptive novelty through introgression in Heliconius wing patterns: evidence for a shared genetic "toolbox" from synthetic hybrid zones and a theory of diversification. In: Butterflies: Ecology and evolution taking flight (eds. Boggs, C.L., W.B. Watt and P.R. Ehrlich). Pp. 281-318, 6 pls. Chicago, IL: University of Chicago Press.  Back to cited text no. 41
    
42.Glassberg, J., P. Opler, R.M. Pyle, R. Robbins and J. Tuttle. 1998. There's no need to release butterflies - they're already free. http://www.naba.org/weddings.html. Accessed on April 3, 2011.  Back to cited text no. 42
    
43.Goh, D. 2007. Roles of butterfly farms and breeding for conservation of Lepidoptera. In: Proceedings of the First South East Asian Lepidoptera Conservation Symposium, Hong Kong 2006 (ed. Kendrick, R.C.). Pp. 101-107. Hong Kong: Kadoorie Farm & Botanic Garden. http://hkmoths.webs.com/SEALCS_2006_proceedings.pdf. Accessed on April 3, 2011.   Back to cited text no. 43
    
44.Gordon, I. and W. Ayiemba. 2003. Harnessing butterfly biodiversity for improving livelihoods and forest conservation: the Kipepeo Project. Journal of Environment and Development 12: 82-98.  Back to cited text no. 44
    
45.Haeger, J.F., D. Jordano and M.L. Meléndez. 2011. Status and conservation of Asclepiadaceae and Danaus in southern Spain. Journal of Insect Conservation 15: 361-365.  Back to cited text no. 45
    
46.Heal, H.G. 1973. An experiment in conservation education: the Drum Manor butterfly garden. International Journal of Environmental Studies 4: 223-229.  Back to cited text no. 46
    
47.Hebert, P.D.N., J.R. deWaard and J.F. Landry. 2010. DNA barcodes for 1/1000 of the animal kingdom. Biology Letters 6: 359-362.  Back to cited text no. 47
    
48.Hughes, D.G. and P.M. Bennett. 1991. Captive breeding and the conservation of invertebrates. International Zoo Yearbook 30: 45-51.  Back to cited text no. 48
    
49.Hutton, A.F. 1985. Butterfly farming in Papua New Guinea. Oryx 19: 158-162.  Back to cited text no. 49
    
50.IABES (International Association of Butterfly Exhibitors and Suppliers). 2002-2011. IABES Newsletter International Flutterings. http://iabes.org/newsletters.htm. Accessed on April 3, 2011.  Back to cited text no. 50
    
51.IABES (International Association of Butterfly Exhibitors and Suppliers). 2011a. http://www.iabes.org. Accessed on April 3, 2011.  Back to cited text no. 51
    
52.IABES (International Association of Butterfly Exhibitors and Suppliers). 2011b. http://www.iabes.org/bylaws.htm. Accessed on April 3, 2011.  Back to cited text no. 52
    
53.IABES (International Association of Butterfly Exhibitors and Suppliers). 2011c. http://iabes.org/IABES-conservation.htm. Accessed on April 3, 2011.  Back to cited text no. 53
    
54.IBBA (International Butterfly Breeders Association). 2011. http://butterflybreeders.org. Accessed on April 3, 2011.  Back to cited text no. 54
    
55.Janz, N. 2003. Sex-linkage of host plant use in butterflies. In: Butterflies: Ecology and evolution taking flight (eds. Boggs, C.L., P.R. Ehrlich and W.B. Watt). Pp. 229-239. Chicago, IL: University of Chicago Press.  Back to cited text no. 55
    
56.JCCBI (Invertebrate Link). 2011. http:/www.royensoc.co.uk/InvLink/Index.html. Accessed on April 3, 2011.  Back to cited text no. 56
    
57.Joron, M. and P.M. Brakefield. 2003. Captivity masks inbreeding effects on male mating success in butterflies. Nature 424: 191-194.  Back to cited text no. 57
    
58.Keiper, J.B. 1996. Monarch transfer: a real concern? BioScience 46: 562.  Back to cited text no. 58
    
59.Kellert, S. 1997. Kinship to mastery. Biophilia in human evolution and development. Washington, DC: Island Press.  Back to cited text no. 59
    
60.Kellert, S. 2009. A biocultural basis for an environmental ethic. In: The coming transformation. Values to sustain human and natural communities (eds. Kellert, S.R. and J.G. Speth). Pp. 21-38. New Haven, CT: Yale School of Forestry & Environmental Studies.  Back to cited text no. 60
    
61.Kellert, S. and E.O. Wilson. 1993. The Biophilia hypothesis. Washington, DC: Island Press.  Back to cited text no. 61
    
62.Kenis, M., M.A. Auger-Rozenberg, A. Roques, L. Timms, C. Péré, M.J.W. Cock, J. Settele, et al. 2009. Ecological effects of invasive alien insects. Biological Invasions 11: 21-45.  Back to cited text no. 62
    
63.Khew, S.K. 2009. New taxon for Malaysia. Discovery of a new butterfly species on Pulau Langkawi - Dryas iulia. Butterflies of Singapore. http://butterflycircle.blogspot.com/2009/09/new-taxon-for-malaysia.html. Accessed on April 3, 2011.  Back to cited text no. 63
    
64.Kitching, I.J. and J.M. Cadiou. 2000. Hawkmoths of the world. An annotated and illustrated revisionary checklist (Lepidoptera: Sphingidae). Ithaca, NY: Cornell University Press.  Back to cited text no. 64
    
65.Kozak, K.H., A.B. Russell and A. Larson. 2006. Gene lineages and eastern North American paleodrainage basins: phylogeography and speciation in salamanders of the Eurycea bislineata species complex. Molecular Ecology 15: 191-207.  Back to cited text no. 65
    
66.Küppers, P.V. 2007. Ist Dryas iulia (Fabricius, 1775) mittlerweile ein fester Bestandteil der thailändischen Lepidopterenfauna? (Lepidoptera, Nymphalidae). Atalanta 38: 325-328.  Back to cited text no. 66
    
67.Lamas, G. 2004. Atlas of Neotropical Lepidoptera: Checklist 4a: Hesperoidea-Papilionoidea. Gainesville, CA: Scientific Publishers.  Back to cited text no. 67
    
68.Lewis, O.T. and C.D. Thomas. 2001. Adaptations to captivity in the butterfly Pieris brassicae (L.) and the implications for ex situ conservation. Journal of Insect Conservation 5: 55-63.  Back to cited text no. 68
    
69.Lohman, D.J., D. Peggie, N.E. Pierce and R. Meier. 2008. Phylogeography and genetic diversity of a widespread Old World butterfly, Lampides boeticus (Lepidoptera: Lycaenidae). BMC Evolutionary Biology 8: 301.  Back to cited text no. 69
    
70.Lovei, G.L. 1997. Global change through invasion. Nature 388: 627-628.  Back to cited text no. 70
    
71.Mallet, J. 2005. Artificially produced hybrids between species and races of Heliconius butterflies. http://www.ucl.ac.uk/taxome/hyb/artif/artifhyb.html. Accessed on April 3, 2011.  Back to cited text no. 71
    
72.Malo, F. and E.R. Willis. 1961. Life history and biological control of Caligo eurilochus, a pest of banana. Journal of Economic Entomology 54: 530-536.  Back to cited text no. 72
    
73.Manos-Jones, M. 2000. The spirit of butterflies. Myth, magic, and art. New York, NY: Abrams.  Back to cited text no. 73
    
74.Mathew G. and M. Anto. 2007. In situ conservation of butterflies through establishment of butterfly gardens: a case study at Peechi, Kerala, India. Current Science 93: 337-347.  Back to cited text no. 74
    
75.McLaughlin, R.E. and J. Myers. 1970. Ophryocystis elektroscirrha sp. n., a neogregarine pathogen of the Monarch butterfly Danaus plexippus (L.) and the Florida Queen butterfly D. gilippus berenice Cramer. Journal of Protozoology 17: 300-305.  Back to cited text no. 75
    
76.Mercader, R.J. and J.M. Scriber. 2007. Diversification of host use in two polyphagous butterflies: differences in oviposition specificity or host rank hierarchy? Entomologia Experimentalis et Applicata 125: 89-101.  Back to cited text no. 76
    
77.Montero, J.R. 2007. Manual Para el Manejo de Mariposarios. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad (INBio).  Back to cited text no. 77
    
78.Moreau, S. 1999. Butterfly releases unjustly maligned. http://butterflywebsite.com/farming/smrebuttal.htm. Accessed on April 3, 2011.  Back to cited text no. 78
    
79.Morgan-Brown, T. 2007. Butterfly farming and conservation behavior in the East Usambara Mountains of Tanzania. M.Sc. thesis. University of Florida, Gainesville, USA. http://www.equatorinitiative.org/images/stories/2006winner/Amani_Butterfly/butterfly_farming_amani.pdf. Accessed on April 3, 2011.  Back to cited text no. 79
    
80.Morishita, K. 1985. Part II: Danaidae. In: Butterflies of the South-East Asian islands (ed. Tsukada, E.). Volume II. Pp. 439-598, pls 85-162. Tokyo: Plapac.  Back to cited text no. 80
    
81.Morris, M.G. 1987. Changing attitudes to nature conservation: the entomological perspective. Biological Journal of the Linnean Society 32: 213-223.  Back to cited text no. 81
    
82.Morris, M.G., N.M. Collins, R.I. Vane-Wright and J. Waage. 1991. The utilization and value of non-domesticated insects. In: The conservation of insects and their habitats (eds. Collins, M.R. and J.A. Thomas). Pp. 319-347. London: Academic Press.  Back to cited text no. 82
    
83.New, T.R. 1994. Butterfly ranching: sustainable use of insects and sustainable benefit to habitats. Oryx 28: 169-172.   Back to cited text no. 83
    
84.New, T.R. 2008. Are butterfly releases at weddings a conservation concern or opportunity? Journal of Insect Conservation 12: 93-95.  Back to cited text no. 84
    
85.NAPPC (North American Pollinator Protection Campaign). 2011. http://www.pollinator.org. Accessed on April 3, 2011.  Back to cited text no. 85
    
86.Orr, D.W. 2004. Earth in mind. On education, environment, and the human prospect. 10 th anniversary edition. Washington, DC: Island Press.  Back to cited text no. 86
    
87.Orsak, L. 1993. Killing butterflies to save butterflies: a tool for tropical forest conservation in Papua New Guinea. News of the Lepidopterists' Society 3/1993: 71-80.  Back to cited text no. 87
    
88.Parsons, M. 1992. Butterfly farming and conservation in the Indo-Australian region. Tropical Lepidoptera 3(Suppl. 1): 1-31.  Back to cited text no. 88
    
89.Peggie, D., A. Rawlins and R.I. Vane-Wright. 2005. An illustrated checklist of the papilionid butterflies (Lepidoptera: Papilionidae) of northern and central Maluku, Indonesia. Nachrichten des entomologischen Vereins Apollo, N.F. 26(1/2): 41-60.  Back to cited text no. 89
    
90.Prchal, S.J. 1991. Sonoran Arthropod Studies, Inc: a new concept in environmental education. International Zoo Yearbook 30: 40-45.  Back to cited text no. 90
    
91.Pyle, M. 2010. Under their own steam: the biogeographic case against butterfly releases. News of the Lepidopterists' Society 52: 54-57.  Back to cited text no. 91
    
92.Pyle, M., S.J. Jepsen, S.H. Black and M. Monroe. 2010. Xerces Society policy on butterfly releases. http://www.xerces.org/wp-content/uploads/2010/01/xerces-butterfly-release-policy.pdf. Accessed on April 3, 2011.  Back to cited text no. 92
    
93.Quacchia, A., C. Ferracini, S. Bonelli, E. Balletto and A. Alma. 2008. Can the geranium bronze, Cycyreus marshalli, become a threat for European biodiversity? Biodiversity and Conservation 17: 1429-1437.  Back to cited text no. 93
    
94.Reitz, S.R. and J.T. Trumble. 2002. Competitive displacement among insects and arachnids. Annual Review of Entomology 47: 435-465.  Back to cited text no. 94
    
95.Reppert, S.M., R.J. Gegear and C. Merlin. 2010. Navigational mechanisms of migrating monarch butterflies. Trends in Neuroscience 33: 399-406.  Back to cited text no. 95
    
96.Reynolds, H.L., E.S. Brondizio and J.M. Robinson. 2010. Teaching environmental literacy. Bloomington, IN: Indiana University Press.  Back to cited text no. 96
    
97.Rios, A.A. 2002. Flying North: potential roles of North American butterfly houses in promoting sustainable economic activities and conservation. M.Sc. thesis. University of Florida, Gainesville, USA.   Back to cited text no. 97
    
98.Rivers, C.F. 1991. The control of diseases in insect cultures. International Zoo Yearbook 30: 131-137.   Back to cited text no. 98
    
99.Robinson, M.H. 1991. Invertebrates: exhibiting the silent majority. International Zoo Yearbook 30: 1-7.  Back to cited text no. 99
    
100.Sambhu, H. and T. van der Heyden. 2010. Sustainable butterfly farming in tropical developing countries as an opportunity for man and nature-the "Kawê Amazonica Butterfly Farm" project in Guyana as an example (Insecta: Lepidoptera). SHILAP Revista de Lepidopterología 38: 451-456.  Back to cited text no. 100
    
101.SASI (Sonoran Arthropod Studies Institute). 2011. http:www.sasionline.org. Accessed on April 3, 2011.  Back to cited text no. 101
    
102.Saul-Gershenz, L. 2009. Insect zoos. In: Encyclopedia of insects (eds. Resh, W. and R. Cardé). Pp. 516-523. Amsterdam: Academic Press.  Back to cited text no. 102
    
103.Scoble, M.J. 2004. Unitary or unified taxonomy? Philosophical Transactions of the Royal Society London B 359: 699-710.  Back to cited text no. 103
    
104.Singer, P. 1981. The expanding circle: Ethics and sociobiology. New York, NY: Farrar, Straus & Giroux.  Back to cited text no. 104
    
105.Singer, M.C. and C.D. Thomas. 1996. Evolutionary responses of a butterfly metapopulation to human and climate-caused environmental variation. American Naturalist 148: S9-S39.   Back to cited text no. 105
    
106.Smith, M.A., J.J. Rodriguez, J.B. Whitfield, A.R. Deans, D.H. Janzen, W. Hallwachs and P.D.N. Hebert. 2008. Extreme diversity of tropical parasitoid wasps exposed by interative integration of natural history, DNA barcoding, morphology, and collections. Proceedings of the National Academy of Sciences 105: 12359-12364.  Back to cited text no. 106
    
107.Smith, C.R. and R.I. Vane-Wright. 2008. Classification, nomenclature and identification of lime swallowtail butterflies: a post-cladistic analysis (Lepidoptera: Papilionidae). Systematics and Biodiversity 6: 175-203.  Back to cited text no. 107
    
108.Smith, M.A., D.M. Wood, D.H. Janzen, W. Hallwachs and P.D.N. Hebert. 2007. DNA barcodes affirm that 16 species of apparently generalist tropical parasitoid flies (Diptera, Tachinidae) are not all generalists. Proceedings of the National Academy of Sciences 104: 4967-4972.  Back to cited text no. 108
    
109.Sperling, F.A.H. and R.G. Harrison. 1994. Mitochondrial DNA variation within and between species of the Papilio machaon group of swallowtail butterflies. Evolution 48: 408-422.  Back to cited text no. 109
    
110.Stone, M.K. and Z. Barlow (eds.). 2005. Ecological literacy. Educating our children for a sustainable world. San Francisco, CA: Sierra Club Books.   Back to cited text no. 110
    
111.Stone, M.K. and Center for Ecoliteracy. 2009. Smart by nature. Schooling for sustainability. Healdsburg, CA: Watershed Media.  Back to cited text no. 111
    
112.Tanaka, S., T. Nishida and N. Ohsaki. 2007. Sequential rapid adaptation of indigenous parasitoid wasps to the invasive butterfly Pieris brassicae. Evolution 61: 1791-1802.  Back to cited text no. 112
    
113.Toone, W.D. 1990. Butterfly exhibitry. International Zoo Yearbook 29: 61-65.  Back to cited text no. 113
    
114.UNEP-WCMC (United Nations Environment Programme - World Conservation Monitoring Centre). 2007. Review of trade in ranched birdwing butterflies. http://www.ec.europa.eu/environment/cites/pdf/review_butterflies.pdf. Accessed on April 3, 2011.  Back to cited text no. 114
    
115.van der Heyden, T. 1992. "Butterfly houses" - a chance for the conservation of European butterflies, education and research. In: Future of butterflies in Europe: Strategies for survival (eds. Pavlicek-van Beek, T., A.H. Ovaa and J.G. van der Made). Pp. 315-318. Wageningen: Department of Nature Conservation, Agricultural University.  Back to cited text no. 115
    
116.Vane-Wright, R.I. 2003. Indifferent philosophy versus almighty authority: on consistency, consensus and unitary taxonomy. Systematics and Biodiversity 1: 3-11.  Back to cited text no. 116
    
117.Wagner, D., F. Sperling and B. Walsh. 2011. More on butterfly releases. News of the Lepidopterists' Society 52: 87-88.   Back to cited text no. 117
    
118.Wilson, E.O. 2003. The future of life. New York, NY: Random House.  Back to cited text no. 118
    
119.Woodworth, L.M., M.E. Montgomery, D.A. Briscoe and R. Frankham. 2002. Rapid genetic deterioration in captive populations: causes and conservation implications. Conservation Genetics 3: 277-288.  Back to cited text no. 119
    
120.WAZA (World Association of Zoos and Aquariums). 2011. http://www.waza.com. Accessed on April 3, 2011.  Back to cited text no. 120
    
121.Zanzibar Butterfly Centre. 2011. http://www.zanzibarbutterflies.com/zanzibarbutterfa.html. Accessed on April 3, 2011.  Back to cited text no. 121
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
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