Insects as fl agship conservation species

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TAR
Terrestrial Arthropod Reviews 1 (2008) 111–123
www.brill.nl/tar
Insects as flagship conservation species
Margaret S. Guiney1 and Karen S. Oberhauser 2
1
Conservation Biology Program, University of Minnesota, St. Paul MN 55108
sava0080@umn.edu
2
Department of Fisheries, Wildlife and Conservation Biology, University of Minnesota
St. Paul MN 55108
oberh001@umn.edu
Received: 14 October 2008; accepted 9 November 2008
Summary
Insect conservation has generally received less public attention than vertebrate conservation. Less is known
about threats to invertebrates, and invertebrates generally have less public charisma than vertebrates and
thus engender less concern. We argue that an additional reason is that invertebrates are rarely used as flagship conservation species, and that increased focus on invertebrate conservation in public campaigns
would benefit this important group of species and conservation efforts in general. We describe conservation efforts focused on three groups: charismatic insects, endangered insects, and insects that provide
important ecological services. In each of these cases, we provide a case study that illustrates ways in which
these efforts have wide-reaching conservation and education impacts. Our goals are to expand insect conservation efforts and to motivate entomologists and conservationists in general to utilize appropriate insect
species to garner support for conservation efforts.
Keywords
Insect conservation; flagship species; monarch butterfly; Danaus plexippus; Karner blue butterfly; Lycaeides
melissa samuelis; ecological services; pollinators
Introduction
A common strategy for minimizing current and future biodiversity losses is to focus on
one or a small number of species that help identify or improve conservation problems
(Thomas, 1972; Wilcox, 1984; Jarvinen, 1985). These species, often called surrogate
species, can serve several different purposes (Caro and O’Doherty, 1999). Indicator
species are used to assess environmental conditions (Landres et al., 1988); for example,
the presence of specific aquatic invertebrates helps indicate water quality. Umbrella
species help define a habitat or community of species to protect (Wilcox, 1984); the
range of the migratory wildebeest (Connochaetes taurinus) helped define boundaries for
a conservation area in Tanzania (Grzimek and Grzimek, 1959). Finally, flagship species
are used to generate public support and funding for conservation goals beyond the
© Koninklijke Brill NV, Leiden, 2008
DOI 10.1163/187498308X414733
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needs of the specific species (Dietz et al., 1994). Some flagship species, like the giant
panda (Ailuropoda melanoleuca), a symbol of the World Wildlife Fund, are used to
generate support for nature globally (Caro and O’Doherty, 1999), while others, like
the Komodo dragon (Varanus komodoensis) that inhabits a few Indonesia islands, are
used to attract tourists and generate conservation funds in a specific area (Walpole and
Leader-Williams, 2002). While historically most flagship species have been large mammals, some much smaller species, for example butterflies, have been successful flagship
species (New, 1997).
More focus on insect flagship species could serve two important goals. From a
broader perspective, utilizing this large and ubiquitous group in conservation efforts
can effectively draw attention to conservation needs in general. Additionally, it is
important to draw more attention to insect conservation needs per se. The scarcity of
insect flagship species means that few people think about their importance and conservation needs. While extinctions of and threats to land vertebrates are reasonably welldocumented (e.g. Pimm and Raven, 2000; Baillie et al., 2004), extinction rates of
other organisms, which comprise about 99% of the world’s species, are rough guesses,
at best (e.g. Dunn, 2005; Berenbaum, 2008). There is some question about whether
the forces that threaten vertebrates threaten insects with similar levels of intensity.
Some features of insect biology, such as their requirements for smaller habitat areas to
support relatively large populations (Blackburn and Gaston, 1997) and high rates of
reproduction and dispersal, may make insects less prone to extinction. However, some
characteristics may make them prone to factors that are unlikely to affect vertebrates,
such as narrow habitat specialization and requirements for specific hosts that may
themselves be threatened. The protection afforded to insects under the United States
Endangered Species Act is less generous than that afforded to vertebrates; distinct populations of invertebrates cannot be protected, nor can any group that has the potential
to be an agricultural pest during any life stage (Black, 2008). Because citizens can play
a key role in securing protection for species through legislation and habitat protection,
increasing the public’s knowledge of and concern for insects can be an important strategy in securing more equal protection for this group (e.g. Berenbaum, 2008).
Our focus is on conservation efforts that have targeted insect flagship species. We
describe conservation efforts focused on three groups: charismatic insects, endangered
insects, and insects that provide important ecological services. In each of these cases,
we provide a case study that illustrates ways in which these efforts have wide-reaching
conservation and education impacts. Our goals are to expand insect conservation
efforts and to motivate entomologists and conservationists in general to utilize appropriate insect species to garner support for conservation efforts.
Charismatic species
Insects are generally not perceived in a positive light, but rather as crop pests, carriers
of disease, poisonous, or simply pesky (e.g. Berenbaum, 2008). They might thus
seem unlikely charisma candidates. However, butterflies provide an exception to the
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unfavorable view of insects (e.g. Vane-Wright, 2008), and are thus appropriate flagship
species. Butterflies are often beautifully colored, easy to observe as they fly and nectar
from flowers, and do not bite or sting. They are familiar to many people because they
are fairly common across a variety of habitat types, and this familiarity can be an
important conservation tool.
The monarch butterfly (Danaus plexippus L.) provides one of our best examples of
the conservation impacts of a non-threatened species (see Figure 1). In fact, it is likely
that no other non-pest insect has attracted as much attention (Oberhauser and Solensky,
2004). Monarch adults and larvae are both recognized by many people. They are widespread and fairly common, and have unique and well-known attributes, such as their
long distance migration, involvement in a fascinating mimicry complex, and relationship with milkweed. The monarch is the state insect, butterfly or emblem of seven
states in the United States, one Canadian province, and one Mexican state. Children
study monarchs in school, conservationists are concerned about impacts of human
activities on monarchs, and citizens, government agencies and conservation organizations are engaged in a variety of programs designed to alleviate these impacts. Citizen
scientist volunteers throughout North American track their migration and breeding,1
and their involvement in these research efforts not only provides data that are relevant
to conservation decisions, but also helps to develop a corps of citizens that educate and
advocate on behalf of the organisms they study (Oberhauser and Prysby, 2008). These
efforts benefit other organisms through conservation education; habitat protection,
restoration or creation; and alleviation of human activities that degrade habitats, such
as pesticide applications.
The long distance migration of monarchs, from summer breeding grounds in temperate regions of the United States and Canada to wintering habitat in central Mexico
and coastal California (e.g. Brower, 1995), requires a series of habitat types that are
regularly occupied over the course of a year. In the summer, these habitats range from
pristine prairies in the Upper Midwestern United States and Canada to small gardens,
roadside ditches, field edges, and fallow agricultural fields. In the fall, monarchs require
access to nectar sources and nighttime resting spots, and their wintering locations must
provide specific microclimatic conditions that are found in wooded groves near the
Pacific Ocean, and forested mountain-tops in the Transvolcanic Range of central
Mexico. Protection and creation of these habitats will benefit many organisms besides
monarchs. For example, of the 423 vascular plants that are found in the Monarch
Butterfly Biosphere Reserve (MBBR) in Mexico, 32% are Mexican endemics, and
Cornejo-Tenorio et al. (2003) argue that this is a center of diversification for several
groups. Preservation and augmentation of nectar resources along the migratory flyways
will also benefit other pollinators.
1)
Many monarch citizen science programs exist in North America, including the Monarch Larva
Monitoring Project (www.mlmp.org), Monarch Watch (www.monarchwatch.org), and Project Monarch
Health (www.monarchparasties,org). Others have broader foci that include monarchs, such as the North
American Butterfly Association (www.naba.org), Journey North (www.learner.org/jnorth) and several
Butterfly Monitoring Networks.
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Figure 1. Monarch butterfly (Danaus plexippus) © Kurt Adolfson, www.bluedotimages.com
Figure 2. Karner blue butterfly (Lycaeides melissa samuelis) © Kurt Adolfson, www.bluedotimages.com
M.S. Guiney and K.S. Oberhauser / Terrestrial Arthropod Reviews 1 (2008) 111–123
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The attention to monarchs has resulted in conservation efforts at global, continental,
national, state and local scales, despite the fact that the species is not threatened. At a
global scale, the UNESCO (United Nations Educational, Scientific and Cultural
Organization) Convention concerning the Protection of the World Cultural and
Natural Heritage named the Monarch Butterfly Biosphere Reserve in Mexico as a
World Heritage Site in 2008. This Reserve joins a list of 878 sites whose cultural and
natural heritage is deemed to have outstanding universal value. While this recognition
conveys no official protection, it clearly indicates a value recognized on an international level.
On a North American scale, The Commission on Environmental Cooperation
(CEC), a trilateral commission that complements the environmental provisions of the
North American Free Trade Agreement (NAFTA), has supported the development of
the North American Monarch Conservation Plan (Oberhauser et al., 2008), with the
aim of maintaining healthy monarch populations and habitats throughout the migration flyway. Officials from the United States Fish and Wildlife Service, the United
States National Park Service, the Canadian Wildlife Service, the Canadian Parks
Agency and the National Commission of Natural Protected Areas in Mexico have supported this plan, and have designated 13 wildlife preserves (four in Mexico, five in the
US, and two in Canada) as protected areas that comprise a “Trilateral Monarch
Butterfly Sister Protected Area Network” to support international preservation and
restoration of breeding, migration and winter habitat for monarchs. The endorsement
of the Monarch Conservation Plan by agencies within all three North American governments illustrates their embrace of monarch habitat protection. Additionally, state
and local government bodies, as well as private and non-governmental enterprises,
have access to a coherent set of recommended actions that will benefit monarchs and
the myriad of organisms with which they share habitats.
At a national scale, the monarch is listed as a species of special concern under the
Canadian Species at Risk Act (SARA), and the government of Mexico has protected
56,259 hectares of land in the area in which monarchs overwinter. In addition to these
specific protections, a variety of government and non-government agencies and organizations directly and indirectly support monarch conservation in all three North
American countries.
Endangered species
Many successful flagship species exhibit decreasing population numbers or endangered
status (Dietz et al., 1994) due to habitat degradation or loss. They often require a
unique habitat or microhabitat, and are sensitive to ecological disturbances. Official
status, such as being listed as endangered or threatened, often increases funding
resources for research and habitat management, but because insects are less likely to
receive these official designations, few insects have become flagship species as a result
of their endangered status.
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The Karner blue butterfly (Lycaeides melissa samuelis N.) is one example of an endangered flagship insect (see Figure 2). This butterfly has successfully engendered public
support for conservation due to its aesthetic appeal and connection to an imperiled
ecosystem. The Karner blue is a small, attractive butterfly that historically lived in oakpine savanna or pine barren habitats from the northeastern United States to southeastern Minnesota (U.S. Fish and Wildlife Service, 2003). Oak savannas and pine barrens
are unique ecosystems; in the Midwestern United States they are generally part of a
transition zone between western prairie and eastern deciduous forest. Oak or pine trees
predominate in their canopy cover of 10 to 80%, a shrub layer may or may not be
present, and the understory consists of grasses and forbs. These ecosystems require
disturbances, such as fires or drought, which prevent development of closed canopy
woodland or shrub land (Nuzzo, 1986). A common understory plant in these savannas
and barrens is wild lupine (Lupinus perennis L.) the host plant of the Karner blue.
While wild lupine can grow under closed tree canopies, it is unable to flower in these
conditions (Boyonoski, 1992) and is thus dependant on disturbances that maintain an
open or semi-open tree canopy. Oak savannas are one of the most threatened United
States ecosystems, with only 0.02% of their pre-settlement area remaining (Nuzzo,
1986). As its habitat has been destroyed and degraded over the last few decades, a corresponding dramatic decline of Karner blue butterfly populations has occurred, and it
was listed as a federally endangered species in 1992. Conservation efforts to save Karner
blues have focused on maintaining or improving native ecosystems (Andow et al.,
1994; U.S. Fish and Wildlife Service, 2003), an approach that will benefit many other
species in oak savanna and pine barren habitats.
Recovery efforts for the Karner blue butterfly have involved many organizations
working alone and in partnership. For example, through the Wisconsin Statewide
Habitat Conservation Plan, the Wisconsin Department of Natural Resources has led a
grassroots approach to develop a large scale conservation plan, organizing traditional
conservation groups, working in conjunction with non-traditional conservation
groups, such as the Department of Transportation and paper and power companies.
A total of 26 partners are working to apply this plan to over 250,000 acres of Karner
blue habitat (Watermolen et al., 2000; U.S. Fish and Wildlife Service, 2003). In Ohio,
the local Karner blue butterfly population was extirpated in the late 1980’s or early
1990’s (Andow et al., 1994). In 1988, the Toledo Zoo and The Nature Conservancy
joined resources to reintroduce Karner blues to Ohio. The Zoo captively rears the butterflies and releases them on 250 acres of oak savanna habitat owned and restored by
The Nature Conservancy. It has released over 2000 butterflies with positive population
effects, as well as benefits to many other species dependant on the same habitat. The
Ohio Nature Conservancy has noted that the oak savanna restoration has also helped
increase populations of badgers, red-headed woodpeckers, lark sparrows, and the state
endangered frosted elfin and persius duskywing butterflies (The Nature Conservancy,
2008).
Conservationists have utilized the story of the Karner blue butterfly to increase conservation education efforts. For the 25 year anniversary of the Endangered Species Act,
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the National Wildlife Federation (NWF) initiated the “Keep the Wild Alive” campaign,
choosing 25 endangered species to profile, including the Karner blue. The campaign
emphasizes education and local conservation initiatives, including the NWF species
recovery fund which provides financial support for local conservation efforts to support conservation of imperiled species. Additionally, several local and state efforts officially recognize and celebrate the Karner blue butterfly’s presence. The small town of
Black River Falls, Wisconsin is adjacent to Karner blue habitat and hosts an annual
summer festival celebrating this butterfly with activities such as habitat tours and a
butterfly learning center. In 1992, New Hampshire named the Karner blue butterfly as
its state butterfly, and it became the official butterfly of the town of Queensbury, New
York in 2001 (Mlot, 2007) . Such actions draw attention to the conservation needs of
the Karner blue butterfly and other organisms, particularly insects.
Insects that provide ecological services
There is a growing recognition of the value of the services derived from their ecological
functions that insects provide to human well-being (Kremen and Chaplin-Kramer,
2005; Losey and Vaughan, 2006, 2008). These wide-ranging services include pollination, protection from pests, decomposition, food for wildlife, and recreation through
activities such as insect observation. Losey and Vaughan (2006, 2008) have calculated
values for many of these services, and provide an informative comparison of conservation efforts that focus on ecological services with those that focus on endangered status
(Losey and Vaughan, 2008). They argue that the commonness and positive economic
impact of insects that provide ecological services make them excellent candidates for
flagship species. Commonness may make insects more familiar and less threatening,
and thus better able to overcome the “charisma-challenges” (Berenbaum, 2008) that
generally characterize insects. Additionally, if landowners are aware of the benefits provided by insects, they may conduct land management activities that benefit insects,
provided that they are aware of strategies that will accomplish conservation.
Here, we focus on conservation efforts directed toward pollinators (see Figures 3-5).
Pollinators have clear economic and even survival importance to humans. Threequarters of all flowering plants, including most species of food crops, rely on pollinators for fertilization, and decreases in wild pollinator populations could have severe
impacts on natural and managed ecosystems. Pollinators are estimated to provide over
$57 billion worth of services in the United States (Losey and Vaughan, 2006), and
$217 billion worldwide (Gallai et al., 2008). Many organizations are promoting pollinator conservation in a variety of ways that could have broad conservation effects.
The Xerces Society, dedicated to invertebrate conservation (Xerces Society, 2008), and
state extension agencies (e.g. Krichik, 1998; Riedl et al., 2006) have published a variety
of information sheets for the public that describe simple strategies for supporting
pollinators. These range from strategies for avoiding mortality through pest management; supporting pollinators with appropriate plantings in rural, suburban and urban
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Figure 3. Bumblebee (upper row, left, Bombus spp.); Figure 4. Sweat Bee (upper row, right, Family
Halictidae, Subfamily Halictinae); Figure 5. Sweat Bee [lower row, Agapostemon virescens (Fabricius)]. All
figures: © Kurt Adolfson, www.bluedotimages.com
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yards; and providing shelter. The North American Pollinator Protection Campaign
(NAPPC) is an alliance of pollinator researchers, conservation and environmental
groups, private industry, and state and federal agencies in Canada, Mexico and the
United States (The Pollinator Partnership, 2008). NAPPC organizes local, national,
and international projects involving pollinator research, education and awareness, conservation and restoration, special partnership initiatives, and policies.
In late 2006, the United States National Research Council, at the request of NAPPC,
published a report that recognized the downward long-term population trends
for many North American pollinators and called for increased efforts to monitor
pollinators and improve understanding of their basic ecology (NRC, 2006). While
much of the current data on pollinator decline focuses on the non-native honeybee
(Apis mellifera), the report also notes declining numbers for several wild bee species,
especially bumblebees, as well as some butterflies, bats, and hummingbirds. The report
recommends support for research aimed at the sustainable management of these
populations, as well as actions that encourage landowners to make habitats more “pollinator friendly” by growing native plants and limiting pesticide use that could affect
pollinators.
The efforts of NAPPC and other groups focused on pollinator conservation have
recently paid off at the national level. The US Farm Bill passed in 2008 includes measures that will help shape USDA programs to protect and enhance the habitat of native
and managed pollinators. These include recommendations for pollinator friendly
plantings in field borders, hedgerows and shelterbelts; corridors to connect pollinator
habitat patches; and grants for research that will address the impacts of pesticides on
pollinators.
The efforts of organizations addressing pollinator conservation have also included a
variety of public outreach efforts, ranging from pollinator postage stamps to school
curricula. Through these efforts, increasing numbers of people are aware of the importance of pollinators to our survival. This awareness of the absolute necessity of a natural
ecological process carried out, in the main part, by insects, can only benefit natural
system conservation.
Capturing the imagination of public and harnessing resources toward habitat
conservation
There are many ways to increase public interest in insect conservation, and thus habitat
conservation in general. Insects have the distinct advantage of being familiar, common
and almost everywhere that humans live. While a lack of understanding about the
importance and vulnerability of insects means that they are rarely used as flagship conservation species, increased involvement of the public with insects could make these
organisms important in many more conservation efforts.
One way to increase public interest in insects is to expose people to their beauty
through photographs. Insects are small, and thus some of their incredible beauty may
be difficult to discern easily. The current availability of excellent and relatively inexpensive cameras with macro capabilities addresses this problem. Photographic exhibits,
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portrayal of insects in popular and educational media, and classes focused on insect
photography could increase the public’s awareness of the beauty of insects.
Whenever possible, scientists should communicate the relevance of their research
and ways in which individuals can promote insect conservation. There are many excellent examples of such communication focused on K-12 teachers and students. Three
large North American programs (Monarchs in the Classroom, Monarch Watch and
Journey North) as well as many smaller ones promote monarch conservation and study
in classrooms (MonarchLab, 2008; Monarch Watch, 2008; Journey North, 2008). The
Monarch Waystation program run by Monarch Watch (2008) explicitly promotes
monarch and pollinator-friendly habitat gardens in schools. Other excellent examples
include the NAPPC pollinator curriculum (The Pollinator Partnership, 2008) and
the Entomological Association of America President’s prizes for outstanding achievement by elementary and secondary teachers who use insects as educational tools
(Entomological Association of America, 2008). Partnerships with media groups, nonprofit organizations and government agencies can also help spread the word about the
importance of insects, their vulnerability to the same factors that threaten vertebrates,
and their interesting life histories.
One way to engage the public in natural phenomena is to involve them in research.
A growing number of citizen science projects, many of which focus on insects, do this,
and spreading the word about these projects and their findings to as broad an audience
as possible will be important. The conservation efforts on the part of volunteers in
citizen science projects focused on monarchs provide one example (Oberhauser and
Prysby, 2008). Project Butterfly Wings (Florida Museum of Natural History, 2008)
volunteers, who include members of 4H groups in Florida, document butterfly species
observed in their gardens and other local areas; volunteers in the Lost Ladybug Project
(Cornell University, 2008) search for native coccinelid beetles; and cooperators in
national parks and other protected areas North and Central America are using malaise
traps to count insects (Insect Diversity Project, 2008). Whenever possible, entomologists should try to engage the public in their research. Through their engagement with
citizen science and other research programs, citizens can make positive contributions
to research, and in the process, are likely to become strong conservation advocates.
Conclusion
Even though most flagship species have historically been large mammals, an increasing
amount of attention has been directed to smaller species, including insects.
Entomologists and conservationists need to encourage the use of insect flagship species
in order to drawn attention to the importance of this group and their conservation
needs. The descriptions and case studies of charismatic and endangered insects, and
those that provide ecological services, illustrate how the use of a flagship species can
have wide-reaching conservation and education impacts. We encourage entomologists
and conservationists to interact with the public and campaigns that garner support for
insect conservation efforts.
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Acknowledgements
We are grateful to photographer, Kurt Adolfson, for sharing his images in this article.
We also thank two anonymous reviewers for their constructive comments on the manuscript, and the University of Minnesota Extension for financial support.
References
Andow, D. A., R. J. Baker and C. P Lane (eds). 1994. Karner blue butterfly: A symbol of a vanishing
landscape. Minnesota Agricultural Experiment Station (Miscellaneous Publication Series) St. Paul,
Minnesota, USA. 222 pp.
Baillie, J. E., C. Hilton Taylor, and S. N. Stuart. 2004. 2004 IUCN red list of threatened species: A global
assessment. IUCN. Gland, Switzerland.
Berenbaum, M. 2008. Insect conservation and the Entomological Society of America. American
Entomologist 54:117–120.
Black, S. H. 2008. How the ESA (Entomological Society of America) can work with the ESA (Endangered
Species Act) to conserve insects. American Entomologist 54:111–113.
Blackburn, T. M. and K. J. Gaston. 1997. A critical assessment of the form of the interspecific relationship
between abundance and body size in animals. Journal of Animal Ecology 66:233–249.
Boyonoski, A. 1992. Factors affecting the establishment and maintenance of Lupinus perennis (wild
lupine). Masters thesis. University of Guelph, Guelph, Canada.
Brower, L. P. 1995. Understanding and misunderstanding the migration of the monarch butterfly
(Nymphalidae) in North America: 1857-1995. Journal of the Lepidopterists’ Society 49:304–85.
Caro, T. M. and G. O’Doherty. 1999. On the use of surrogate species in conservation biology. Conservation
Biology 13 (4):805–814.
Cornejo-Tenorio, G. A., F. B. Casas and J. L. Villaseñor. 2003. Flora y vegetación de las zonas núcleo de
la Reserva de la Biosfera de la Mariposa Monarca, México. Boletín de la Sociedad Botánica de México
73:43–62.
Cornell University. 2008. The lost ladybug project. http://hosts.cce.cornell.edu/ladybeetles/. Accessed 26
September 2008.
Dietz, J. M, A. L. Dietz, and E. Y. Nagagata. 1994. The effective use of flagship species for conservation
of biodiversity: the example of lion tamarins in Brazil. In: P. J. S. Olney, G. M. Mace and A. T. C.
Feistner (eds) Creative conservation: interactive management of wild and captive animals,
pp. 32–49. Chapman and Hall, London.
Dunn, R. R. 2005. Modern insect extinctions, the neglected majority. Conservation Biology 19
(4):1030–1036.
Entomological Society of American. 2008. President’s prizes for outstanding achievement in primary and
secondary education. http://www.entsoc.org/awards/professional/educational.htm. Accessed 18
November 2008.
Florida Museum of National History. 2008. Project Butterfly Wings. http://www.flmnh.ufl.edu/
education/cise/wings.htm. Accessed 26 September 2008.
Gallai, N., J. M. Salles, J. Settele and B. E. Vaissière. 2009. Economic valuation of the vulnerability
of world agriculture confronted with pollinator decline. Ecological Economics 68: 810–821.
Grzimek, B. and M. Grzimek. 1959. Serengeti shall not die. Ullstein, A.G., Berlin, Germany. 344 pp.
Insect Diversity Project. 2008. http://www.discoverlife.org/pa/or/idp/. Accessed 24 September 2008.
Jarvinen, O. 1985. Conservation indices in land use planning: Dim prospects for a panacea. Ornis Fennica
62:101–106.
Kremin, C. and R. Chaplin-Kramer. 2005. Insects as providers of ecosystem services: Crop pollination
and pest control. In: J. A. Stewart, T. New, and O. T. Lewis (eds). Insect conservation biology,
pp. 349–382. CABI, Wallingford, UK.
122
M.S. Guiney and K.S. Oberhauser / Terrestrial Arthropod Reviews 1 (2008) 111–123
Krishik, V. 1998. Butterfly gardening. University of Minnesota Extension. St. Paul, Minnesota, USA.
21 pp.
Journey North. 2008. Monarch butterfly. http://www.learner.org/jnorth/monarch/index.html. Accessed
18 November 2008.
Landres, P. B., J. Verner, and T. W. Thomas. 1988. Ecological use of vertebrate indicator species: a critique.
Conservation Biology 2:316–327.
Losey, J. E. and M. Vaughan. 2006. The economic value of ecological services provided by insects.
Bioscience 6 (4): 311–323.
Losey, J. E. and M. Vaughan. 2008. Conserving the ecological services provided by insects. American
Entomologist 54:113–115.
Mlot, C. 2007. Rhapsody in blue. Nature Conservancy Magazine: Spring 2007. Available at http://www
.nature.org/magazine/spring2007/features/art20021.html. Accessed 24 September 2008.
Monarch Watch. 2008. http://www.monarchwatch.org/. Accessed 18 November 2008.
MonarchLab. 2008. http://www.monarchlab.org/. Accessed 18 November 2008.
National Research Council. 2006. The status of pollinators in North America. The National Academies
Press. Washington DC. 312 pp.
The Nature Conservancy. 2008. The return of the Karner blue butterfly. Available at http://www
.nature.org/wherewework/northamerica/states/ohio/science/art20046.html. Accessed 24 September
2008.
New, T. R. 1997. Are Lepidoptera an effective ‘umbrella group’ for biodiversity conservation? Journal of
Insect Conservation 1:5–12.
Nuzzo, V.A. 1986. Extent and status of Midwest oak savanna: Presettlement and 1985. Natural Areas
Journal, 6:6–36.
Oberhauser, K. S., L. P. Brower, D. Cotter, D. Davis, R. Décarie, A. E. Behnumea, C. Galino-Leal,
M. P. Gallina Tessaro, E. Howard, J. Lauriault, W. Maczieski, S. Malcolm, F. Martínez, J. M. González,
M. McRae, D. Nernberg, I. Pisanty Baruch, I. Ramírez, J. J. Reyes and A. Wilson. 2008. North
American monarch conservation plan. Commission on Environmental Cooperation. Montreal,
Canada. 51 pp.
Oberhauser, K. S. and M. D. Prysby. 2008. Citizen science: Creating a research army for conservation.
American Entomologist 54:97–99.
Oberhauser, K. S. and M. J. Solensky. (eds). 2004. The monarch butterfly: Biology and conservation.
Cornell University Press. Ithaca New York, U.S.A. 248 pp.
Pimm, S. L. and P. Raven. 2000. Biodiversity – extinction by the numbers. Nature 403:843–845.
The Pollinator Partnership. 2008. http://www.pollinator.org/. Accessed 26 September 2008.
Riedl, H. E., E. Johansen, L. Brewer and J. Barbour. 2006. How to reduce bee poisoning from pesticides.
Publication PNW591. Oregon State University, Corvalis. http://extension.oregonstate.edu/catalog/
pdf/pnw/pnw591.pdf. Accessed 26 September 2008.
Thomas, W. A. 1972. Indicators of environmental quality. Plenus Press, New York. 275 pp.
U. S. Fish and Wildlife Service. 2003. Final recovery plan for the Karner blue butterfly (Lycaeides melissa
samuelis). U. S. Fish and Wildlife Service. Fort Snelling, Minnesota, U.S.A. 273 pp.
Vane-Wright, R. I. 2008. Butterflies, worldviews, biodiversity, general systems theory, and taxonomy. In:
O. Yata, (ed.), Report on Insect Inventory Project in Tropical Asia (TAIIV), pp. 1–20. Kyushu
University, Fukuoka, Japan.
Walpole, M.J. and N. Leader-Williams, 2002. Tourism and flagship species in conservation. Biodiversity
and Conservation 11:543–547.
Watermolen, D. J., C. Bleser, D. Zastrow, J. Christenson, D. R. Lentz, D. Wood, G. Albright, K. Kirk,
N. Merryfield, G. Birch, U. Petersen, M. Luedeke, T. C. Hunt, F. Souba, Jr., D. Hartman, N. Bozek,
G. Janecek, P. Rasmussen, C. Hart, N. Braker, C. Carnes, L. Mandell, J. Smith, E. Gustafson
M.S. Guiney and K.S. Oberhauser / Terrestrial Arthropod Reviews 1 (2008) 111–123
123
and G. Wood. 2000. Wisconsin statewide Karner blue butterfly habitat conservation plan and
environmental impact statement [PUB-SS-947-00]. Wisconsin Dept. Natural Resources, Madison.
386 pp. + 8 appendices. Available at http://dnr.wi.gov/forestry/karner/hcptext/. Accessed June 5,
2008.
Wilcox, B. A. 1984. In situ conservation of genetic resources: determinants of minimum area requirements. In J. A. McNeely and K. R. Miller (eds) National parks: conservation and development,
pp. 639–647. Smithsonian Institution Press, Washington, D.C.
The Xerces Society. 2008. http://xerces.org/. Accessed 26 September 2008.
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