Biological Conservation 143 (2010) 18311841

Contents lists available at ScienceDirect

Biological Conservation
journal homepage: www.elsevier.com/locate/biocon

Review

More than just indicators: A review of tropical buttery ecology and conservation
Timothy C. Bonebrake *, Lauren C. Ponisio, Carol L. Boggs, Paul R. Ehrlich
Department of Biology, Stanford University, Stanford, CA 94305-5020, United States

a r t i c l e i n f o a b s t r a c t

Article history: Roughly 90% of buttery species live in the tropics. Despite this, we know very little about tropical but-
Received 17 March 2010 tery ecology particularly when compared to temperate buttery systems. The relative scarcity of data on
Received in revised form 21 April 2010 tropical buttery populations hampers our ability to effectively conserve them. In this review we sum-
Accepted 26 April 2010
marize recurring themes from ecological research on tropical butteries to serve as a framework for
Available online 18 May 2010
understanding their conservation. Key themes include: (1) the tropics represent the evolutionary origins
of buttery diversity, (2) while some tropical butteries exhibit relatively stable population dynamics,
Keywords:
longer-lived adult stages, and more continuous age-specic reproduction compared to temperate zone
Buttery
Lepidoptera
species, the generality of these patterns is debatable, and (3) complex species interactions (e.g. mimicry,
Conservation parasitism and predation) can have signicantly greater inuences on ecological and evolutionary pro-
Tropical cesses in tropical butteries than in temperate ones. This state of ecological knowledge, combined with
Ecology scarce resources, has traditionally constrained tropical buttery conservation efforts to habitat level
approaches, unlike the species- and population-specic approaches familiar in North America and Eur-
ope. Consequently, much conservation research on butteries in the tropics has focused on the relation-
ship between habitat quality (e.g. forest fragmentation) and buttery diversity, though predictive
patterns even in this regard remain elusive. We argue that with the increasing threats of habitat destruc-
tion, fragmentation and climate change, it is necessary to move beyond this diversity and habitat rela-
tionship if we are to improve predictive capabilities when evaluating anthropogenic impacts on
tropical buttery communities. Tropical butteries are more than just useful indicator species. They rep-
resent some of the most spectacular and visually appealing organisms in the world and play many vital
roles in tropical ecosystems. We hope that this synthesis will lay the groundwork for future ecological
studies of tropical buttery populations, species, communities and conservation.
2010 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1832
2. Global distribution and evolutionary origins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1832
3. Demography and life history . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1833
3.1. Survivorship and age-specific reproductive patterns . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1833
3.1.1. Role of adult food sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1833
3.1.2. Diapause, migration and seasonality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1833
3.2. Population dynamics and structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1834
3.2.1. Temporal fluctuation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1834
3.2.2. Spatial structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1834
4. Species interactions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1834
4.1. Predation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1835
4.2. Parasites and parasitoids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1835
4.3. Competition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1835
4.4. Ant association . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1835
4.5. Mate recognition and species boundaries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1835
5. Monitoring . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1835
5.1. Indicator species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1835

* Corresponding author. Tel.: +1 818 642 4093.

E-mail address: tcbone@stanford.edu (T.C. Bonebrake).

0006-3207/$ - see front matter 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biocon.2010.04.044
1832 T.C. Bonebrake et al. / Biological Conservation 143 (2010) 18311841

5.2. Techniques . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1836

6. Threats to tropical butterfly diversity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1836
6.1. Habitat loss . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1836
6.2. Global climate change. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1836
6.3. Invasive species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1837
6.4. Toxins. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1838
6.5. Exploitation and harvest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1838
7. Future research. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1838
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1838
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1838

1. Introduction
The biodiversity crisis is expected to severely impact insect spe-
cies (Pimm and Raven, 2000). Yet, of the approximately 40 000 in-
sect species already estimated to have gone extinct over the past
600 years, only 70 have been documented, half of which were Lep-
idoptera (Dunn, 2005). The likely more serious issue of insect pop-
ulation extinctions is even less well known. Considering that less
than one million insect species have been described out of 510
million believed to exist (Gaston, 1991), all of these observations
indicate that many insect species likely to go extinct as a result
of human impacts have not even yet been named or described
(Samways, 2007) and that these insect populations are disappear-
ing daily in large numbers, unheralded.
If we are to have any chance of effectively conserving insect
populations globally, we must understand their ecologies. This
puts a spotlight on butteries, because of all insects, butteries
are probably the best known taxonomically and ecologically (Tho-
mas, 2005). Indeed, the study of buttery biology has a long history
and has contributed greatly to our understanding generally of ecol-
ogy, evolution, biogeography and conservation (Bates, 1862; Ml-
ler, 1879; Wallace, 1865, 1879; Fisher et al., 1943; Gilbert and
Singer, 1975; Boggs et al., 2003; Mallet, 2004).
However, our knowledge of tropical butteries is decient
when compared to their temperate counterparts. Consider the fol-
lowing rough, but telling, exercise. We conducted a BIOSIS search
for papers from 1990 to 2000 for Lepidoptera and England
and found there were 1287 papers. That same search for Lepidop-
tera and Brazil however only results in 679 papers. Brazil is over
30 times as large as England, has over 50 times as many buttery
species (58 species in England cf. Pollard and Yates, 1993 vs. 3300
in Brazil cf. Brown, 1996), but has half the studies of England.
When you also consider that Brazil is comparatively one of the best
studied tropical regions in the world (Stocks et al., 2008; though to
be fair England is one of the best-studied temperate countries), you
can get a feel for the problem.
The difference in buttery knowledge between tropical and
temperate regions has consequences for their conservation. While
US and UK buttery conservation efforts are mainly species-spe-
cic, in the tropics knowledge and resource limitations dictate
habitat protection approaches with little regard to inclusion of
information or tools from buttery population-level or species-
specic conservation (New et al., 1995; New, 2009). Consequently,
appropriations of recent advances in ecological theory have been
slow for tropical conservation. For example, in a survey of 27 but-
tery biologists, over 80% named metapopulation theory as an
important concept guiding buttery conservation; tellingly, none
of the examples they gave to illustrate the utility of metapopula-
tion or any other ecological theories were tropical (Schultz and
Crone, 2008).
The habitat level conservation approach for butteries practiced
throughout much of the tropics has lead to a proliferation of stud-
ies examining butteries indicator potential for assessing
processes such as habitat degradation and land use (e.g. Daily
and Ehrlich, 1995; Hill, 1995; Brown and Freitas, 2000; Bobo
et al., 2006; Akite, 2008; Bonebrake and Sorto, 2009; Uehara-Prado
and Freitas, 2009). Fleishman and Murphy (2009), among many
others (e.g. Kremen, 1992; Lawton et al., 1998), suggest that only
under limited circumstances may buttery species be reliable indi-
cators of environmental change and that the widespread usage of
the indicator concept in butteries can be and has been problem-
atic. However, the use or misuse of butteries as indicators of envi-
ronmental change in the tropics is not our main concern here.
Instead, we argue that even if butteries are good indicators they
are also much more than that. They play a diversity of ecological
roles, interest lay people in biology and conservation in general
and insects in particular, and should be valued beyond their utility
as indicators.
To that end, we review the literature on tropical buttery ecol-
ogy and conservation in hopes that we might advance beyond
habitat protection as essentially the sole conservation tool in
the tropics. We summarize research on tropical buttery biogeog-
raphy, life history, demography and species interactions to high-
light the differences and similarities between temperate and
tropical buttery ecology. Then, we look at the threats to diversity
in the tropics and end with directions for future research and rec-
ommendations on how to improve our ability to conserve tropical
butteries, and through them tropical biodiversity. Taxonomically
we focus on true butteries (Papilionoidea) but recognize the
role of all Lepidoptera, including in particular large moths (e.g.
Bombycoidea) and skippers (Hesperioidae), to conservation and
ecology. Geographically we focus on the tropics, or buttery popu-
lations that reside between the tropics of Capricorn and Cancer, but
also discuss temperate buttery biology for comparative uses.
2. Global distribution and evolutionary origins
The world contains roughly 18 00020 000 species of butteries
and there is a clear latitudinal gradient in buttery species diver-
sity, with numbers highest in the tropics (Shields, 1989; Larsen,
2005). How many buttery species are tropical? It is difcult to
give a precise estimate given the continual updating of checklists
and splitting and lumping of species worldwide, the difculties
of dening tropical, and the tropical species that extend into
largely temperate zones and the temperate species that are con-
ned to cool montane regions in otherwise tropical areas. But esti-
mates can be made nevertheless. Pelham (2008) lists 800 species
throughout the United States and Canada and Lamas (2004) esti-
mates 7784 species in the neotropics. That suggests that in the
Americas roughly 90% of buttery species have a tropical distribu-
tion. Similarly Tolman and Lewington (2008) list 440 species for
Europe and Britain, compared to the roughly 4000 species found
in the afrotropics (Larsen, 2005) and again we nd roughly 90%
of buttery species in the western half of the Old World are
tropical.
 T.C. Bonebrake et al. / Biological Conservation 143 (2010) 18311841
Evolutionary histories of butteries are difcult to construct
due to the scant fossil record, although recent progress using
genetics has advanced the eld signicantly. This has allowed an
estimate of the diversication of butteries which is believed to
be at around the KT extinction event, about 10060 million years
ago (Wahlberg et al., 2009).
Buttery diversity patterns themselves have traditionally been
explained by large climatic events such as the glacial retreat fol-
lowing the Pleistocene, or refugia effects (e.g. Brown et al.,
1974). However, recent genetic studies have suggested a more
complicated picture of continuing divergence through time and
space over evolutionary history (Knapp and Mallet, 2003; Megens
et al., 2004; Whinnett et al., 2005; Elias et al., 2009). Geologic
events can still have important effects on species assemblages, as
is the case for Lepidoptera in South-East Asia and Wallaces line
(Beck et al., 2006). Though the evolutionary causes for tropical
diversity are likely many, butteries appear to follow an out of
the tropics model (the tropics being both a cradle and a
museum for diversity) for global biodiversity gradients (Jablonski
et al., 2006; Hawkins and DeVries, 2009). Therefore, with both the
current species richness and evolutionary legacy of tropical butter-
ies, the tropics should be a clear priority for buttery
conservation.
3. Demography and life history
While the population biology of butteries has been well stud-
ied in some systems, there has been a comparative dearth of trop-
ical buttery population biology studies (Ehrlich, 1984). Studying
Heliconius ethilla, Ehrlich and Gilbert (1973) conducted the rst
explicitly comparative long-term study between a tropical butter-
y population and temperate populations. The relatively constant
population size, delayed reproduction, and high adult survivorship
of the H. ethilla population led Ehrlich and Gilbert (1973) to con-
clude that the buttery exhibited more K-selected dynamics rel-
ative to more r-selected populations of temperate species
(Pianka, 1970). Here we revisit and update comparative life history
and population biology of tropical butteries.
3.1. Survivorship and age-specic reproductive patterns
The acquisition of resources from heterogeneous sources such
as pollen, fruit and carrion by adult tropical butteries can serve
as a basis for understanding survivorship and age-specic repro-
ductive patterns (Boggs, 2009). In particular, tropical female but-
teries using diverse resources are more likely to have a lower
proportion of mature eggs at emergence and produce eggs
throughout their lives (Boggs, 1986, 1997; Jervis et al., 2005). As
for survivorship, some tropical butteries are known for their
exceptionally long adult lives, sometimes on the order of several
months (Turner, 1971; Molleman et al., 2007). One of the interest-
ing consequences of long-lived adult generations and continuous
reproduction within Heliconius populations is the occurrence of
multiple overlapping generations (Ehrlich and Gilbert, 1973; Turn-
er, 1981).
3.1.1. Role of adult food sources
Adult temperate butteries feed primarily on nectar (Scoble,
1992), supplemented to varying extents by mud, dung or carrion
(reviewed in Boggs and Dau (2004)), while adults in the tropics
also feed on a wide variety of sources including fruit, carrion and
pollen (Gilbert, 1972; DeVries, 1987; DeVries and Walla, 2001; Hall
and Willmott, 2000). This wider resource base likely facilitates the
uniquely long lives of tropical butteries, though how precisely is
1833
not entirely clear (Beck, 2007) except in a few cases (especially pol-
len, e.g. Erhardt and Baker, 1990; OBrien et al., 2003).
Of all non-nectar adult food sources, the consequences of feed-
ing on pollen in the Neotropical genus Heliconius are best under-
stood. Derivation of amino acids and/or other compounds from
pollen allows adults to live longer and also to produce oocytes
throughout adult life (Gilbert, 1972; OBrien et al., 2003). Pollen-
feeding butteries, probably as a result of selection for longer adult
lifespan, also tend to have traits which reduce their susceptibility
to predators (i.e. mimicry and related ight behavior, eyespots,
aposematism) (Chai and Srygley, 1990; Beck and Fiedler, 2009).
The innovation of pollen-feeding within the Heliconius community
has had large inuence on their ecology and evolution (for a review
see Gilbert, 1991).
Fruit-feeding butteries also tend to live longer than solely nec-
tar feeding adult butteries (Beck, 2008) and may derive fertility
benets from fruit diets as well (Molleman et al., 2009). However,
the cause for these patterns is unclear. The quantities of sugar
available and the amounts of carbon allocated to egg production
are comparable between fruit and nectar sources (Fischer et al.,
2004). Nor is there clear evidence that nitrogen content can explain
differences between nectar and fruit feeding buttery life histories
(Fischer et al., 2004; Molleman et al., 2008). The ratios of different
sugars or other compounds within food sources might be impor-
tant (e.g. Boggs, 2009; Molleman et al., 2009) but ultimately the
causes and consequences of fruit feeding life history evolution in
butteries are unknown.
3.1.2. Diapause, migration and seasonality
One of the most fundamental differences between temperate
and tropical ecosystems is the winter temperature drop in temper-
ate regions which freezes (often literally) developmental pro-
cesses. Butteries then must possess strategies to deal with this
inevitable seasonal change. Though tropical butteries generally
do not face the cold and harsh temperate winters, they frequently
face extremely seasonal environments in the form of wet and dry
seasons.
Butteries in the seasonal Australian tropics are among the best
studied with respect to responding to adverse conditions in the
tropical dry season. For example, female adults of some Eurema
species have a reproductive diapause phase coinciding with poor
larval host plant conditions and are triggered to reproduce by
changes in rainfall and/or photoperiod (Jones and Rienks, 1987).
Hypolimnas bolina exhibits a regularly timed adult reproductive
diapause also likely caused by photoperiod changes (Kemp,
2001). Another common dry season strategy is a distribution shift
similar to a migratory strategy, in which butteries retreat to moist
refugia and riparian habitats (Jones and Rienks, 1987; Braby, 1995).
Butteries of the island network in Lago Guri, Venezuela exhibit
a similar wet season habitat expansion-dry season habitat contrac-
tion dynamic (Shahabuddin and Terborgh, 1999; Shahabuddin
et al., 2000). DeVries and Walla (2001) additionally found, at the
onset of wet seasons at La Selva Lodge in Amazonian Ecuador, a
vertical inversion between understory and canopy species rich-
ness within the tropical forest buttery community, suggesting
that there is also a vertical component to seasonal dispersal. Finally
of course, the most famous migratory buttery of the Americas is
the monarch buttery Danaus plexippus. Although the evolutionary
origins of the migratory phenomenon are unclear, populations of
this essentially tropical buttery breed in high latitude North
American habitats but cannot survive the cold winters and there-
fore migrate (over successive generations) to sites in Mexico (or
coastal California, for the western populations) where they over-
winter (Brower, 1995).
The afrotropical satyrine, Bicyclus anynana, exhibits a seasonal
polyphenism, such that increased temperatures in the wet season
1834 T.C. Bonebrake et al. / Biological Conservation 143 (2010) 18311841
trigger eyespot formation in the butteries, while dry season forms
lack conspicuous wing patterning (Brakeeld and Reitsma, 1991;
Brakeeld et al., 2007). Though the mechanism is not clear, rainfall
also appears to determine eyespot formation in some Bicyclus pop-
ulations (Roskam and Brakeeld, 1999). Somewhat like reproduc-
tive diapause in other buttery species (e.g. Kemp, 2001), the
Bicyclus dry season forms have delayed reproduction and larger
but fewer eggs when compared to the wet season phenotypes
(Brakeeld and Reitsma, 1991; Fischer et al., 2003). Thus, a butter-
y species in one season is not necessarily ecologically equivalent
to that buttery species in another season. This phenotypic plastic-
ity (especially with regard to eyespot formation) and the mecha-
nisms behind it have made Bicyclus a model system for
evolutionary developmental biology (Beldade et al., 2005).
Buttery species in India also appear to respond to changing
wet and dry conditions as a function of the monsoon through
migration (Kunte, 2004) and seasonal polyphenism (Tiple et al.,
2009). Interestingly, danaine butteries of southern India exhibit
longitudinal migration patterns and escape the extreme wet and
torrential conditions of the monsoon season by moving to drier
habitats (Kunte, 2004). The population dynamics of Chilades pand-
ava in central India are determined largely by relative humidity
(Tiple et al., 2009). However, seasonal polyphenism also occurs
such that the dry season form of the buttery all but disappears
during the monsoon, though it is unclear why (Tiple et al., 2009).
Each of these seasonal migratory and diapause strategies has
important conservation consequences. For example, if butteries
use different habitats in different seasons, then preserving one area
or habitat where the buttery is found in one season at one time
might not be sufcient for its conservation (Janzen, 1987). Thus
it is an important goal for tropical buttery conservation to deter-
mine how wet/dry seasonality inuences buttery individuals and
populations.
3.2. Population dynamics and structure
3.2.1. Temporal uctuation
Given the predominance of wetdry seasonality in the tropics, it
is unsurprising that many studies have reported seasonal uctua-
tions of tropical insect populations (Bigger, 1976; Wolda, 1978).
Despite this, tropical insects tend to have more stable population
dynamics than temperate populations, particularly in non-seasonal
habitats (Wolda, 1988). The relative absence of buttery popula-
tion dynamic studies in the tropics makes quantitative compari-
sons across latitude difcult (see Fleming et al. (2005) for an
exception within Heliconius). In this section we draw on a few case
studies of tropical butteries to illustrate the diversity in popula-
tion dynamics through time and space.
Several studies of Heliconius population dynamics followed the
initial work of Ehrlich and Gilbert (1973). Brown (1981) reviewed
studies on Heliconius populations and concluded that while some
populations do indeed have constant population sizes, populations
in more seasonal environments do not have constant dynamics
(e.g. Brown and Benson, 1974). Most subsequent Heliconius exam-
ples have shown relatively stable population dynamics, though in
all cases seasonal uctuations still occur (Quintero, 1988; Ramos
and Freitas, 1999; de-Andrade and Freitas, 2005; Fleming et al.,
2005).
Ithomiine butteries are another uniquely tropical buttery
complex that has been relatively well studied. The primarily
forest-inhabiting species typically associate with specic
microhabitats based on soil, light and microclimatic conditions
(Vasconcellos-Neto, 1991). Populations exhibit seasonal dynamics,
with increases in the wet season and decreases in the dry season
(Vasconcellos-Neto, 1991; Freitas, 1996; Freitas et al., 2001).
Furthermore, there is a seasonal geographic shift among most
ithomiines (Freitas et al. (2001) give an exception), in which but-
teries contract their range to moist forest habitats producing
so-called ithomiine pockets during the dry season (Vasconcel-
los-Neto, 1991).
Although the heliconiines and ithomiines do not generally exhi-
bit the drastic uctuations in population size often seen in temper-
ate butteries, outbreaks do occur in tropical buttery populations
(Owen, 1971; DeVries, 1987; Larsen, 2005). For example, Azerefe-
gne et al. (2001) show that the afrotropical buttery, Acraea acera-
ta, has high amplitude population uctuations correlated with
changes in rainfall that rival the uctuations of many temperate
butteries populations (see also Tiple et al., 2009). While alterna-
tive methods of coping with seasonal environments (long lives,
reproductive diapause and migration) likely contribute to the ab-
sence of seasonal outbreaks for some species, the causal mecha-
nisms of outbreaks require further exploration.
3.2.2. Spatial structure
As discussed in the introduction, metapopulation theory is a
dominant paradigm for recent temperate buttery conservation ef-
forts (Schultz and Crone, 2008). However this does not appear to be
the case with tropical butteries. Shahabuddin and Terborgh
(1999) suggest that butteries on the islands of Lago Guri, Venezu-
ela may exhibit mainlandisland metapopulation dynamics. Be-
yond this example however, to our knowledge there are no
explicit uses of metapopulation theory in any tropical buttery
population studies or conservation efforts. This very likely reects
the paucity of population studies in the tropics rather than an over-
sight by tropical conversation biologists or an actual absence of
metapopulation dynamics in tropical populations.
Due largely to that lack of population studies, we know rela-
tively little about the spatial structure and dispersal capabilities
of most tropical butteries. Heliconius are known for their high site
delity or home-range behaviors, returning daily to the same plant
and roosting sites (Turner, 1971; Brown, 1981; Mallet, 1986).
Kronforst and Gilbert (2008) also found signicant population sub-
division using genetic markers within several species of Heliconius,
further suggesting limited dispersal and home-range behavior at
small spatial scales. However, some butteries disperse/migrate
long distances, particularly in response to changing wet and dry
seasons (e.g. Jones and Rienks, 1987; Shahabuddin and Terborgh,
1999; Haber and Stevenson, 2004). Given the many in-depth stud-
ies of dispersal and metapopulation dynamics in temperate butter-
ies (e.g., Ehrlich, 1984; Ehrlich and Hanski, 2004) and the
subsequent incorporation of metapopulation theory into temper-
ate buttery conservation (Schultz and Crone, 2008), we suggest
that further study of the spatial structure of tropical buttery
populations may improve the success of tropical buttery
conservation.
The life histories of tropical butteries can be very different
from their temperate counterparts. Efforts to conserve tropical but-
teries should draw on lessons learned from well-studied temper-
ate examples while incorporating strategies specic to tropical
buttery life histories.
4. Species interactions
The complex array of species interactions, or the biotic envi-
ronment, may be the most dening characteristic of tropical envi-
ronments (Dobzhansky, 1950). In particular, the close relationship
between butteries and their host plants has been a recent focus as
one explanation for tropical megadiversity, though patterns
globally remain unclear (see for discussion and examples: Stork,
2007; Lewinsohn and Roslin, 2008). Beyond larval host plant and
adult resource interactions, predatory, parasitic, competitive and
 T.C. Bonebrake et al. / Biological Conservation 143 (2010) 18311841
mutualistic interactions also inuence the diversity, life histories
and population dynamics of buttery communities in the tropics.
4.1. Predation
Lepidopteran larvae form a critical food base for tropical forest
ecosystems (Janzen, 1988), but predation of adults is also a key ele-
ment in the evolution of those butteries. To escape predation,
adult butteries will y, hide (e.g. mimicry) or ght using toxic
compounds that make them distasteful to predators. In fact, tropi-
cal buttery communities are split between butteries with strong
ight capability that are typically palatable to predators and those
that are slow ying but unpalatable (Chai and Srygley, 1990).
A buttery hides from its predators in multiple ways. Cryptic
coloration is exemplied by particular species of Charaxinae,
whose ventral wing patterns strongly resemble dried leaves and
provide cryptic protection within forest litter layers (Muyshondt,
1973). Wet season forms of Bicyclus have wing eyespots which pro-
vide a slight but important selective crypsis advantage as well
(Lyytinen et al., 2004).
The evidence for mimicry in tropical butteries is striking. Bates
(1862) and Mller (1879) were the rst to describe the mimicry con-
cept and did so using heliconiines, ithomiines, papilionids, and pier-
ids. Mimicry has important effects on the habitat distribution of
tropical butteries (Hill, 2010) and on the vertical stratication of
butteries within forests (DeVries et al., 1997). Mimicry also can
have temporal activity consequences, such that mimics are more
likely to y later in a given day, after the models have own for a
while and taught the predators who to avoid (Pinheiro, 2007).
These microhabitat and temporal segregations have important ram-
ications. Changes in adaptive microhabitat use among ithomiine
mimics have been shown to have cascading evolutionary effects
and even cause speciation (Mallet and Joron, 1999; Elias et al., 2008).
4.2. Parasites and parasitoids
Parasites are known to be crucial components of some temper-
ate buttery communities (e.g. in Melitea cinxia; Lei and Hanski,
1997), and while parasites are present in tropical buttery popula-
tions, their importance and prevalence are unclear. On the one
hand, the speciose group of ichneumonid parasites exhibits a lati-
tudinal gradient in species richness with lower diversity in the tro-
pics (Skillen et al., 2000). On the other hand, tachinid lepidopteran
parasites appear to reach their greatest diversity in the tropics
(Stireman et al., 2009). The complicated patterns of parasitoid bio-
geography and their under-studied natural histories could equally
complicate conservation of the Lepidoptera that they inhabit
(Smith et al., 2006).
4.3. Competition
Competition, both intra- and inter-specic, can be a structuring
process in tropical environments. Competition for heliconiine lar-
val resources (passion vine host plants) can be intense in some
populations and this competition has important consequences for
community dynamics (Benson, 1978). We also might expect com-
petition for adult resources in tropical buttery communities given
their importance in life history strategies. Indeed, Kunte (2008) re-
moved butteries of the very abundant and numerically dominant
genus Anartia from a buttery community in Costa Rica and found
that the availability of nectar resources, and subsequently the but-
tery community diversity, increased. The circumstances in which
competition plays a critical role in population and community
dynamics need further study.
1835
4.4. Ant association
Approximately a third of Papilionoidea are blue and metalmark
butteries (Lycaenidae: Lycaeininae and Riodininae) and a large
majority of these butteries have close associations with ant spe-
cies (Pierce et al., 2002). Ant association within Lycaenidae is usu-
ally mutualistic, but the association can also be parasitic,
competitive, neutral, or commensalic (for reviews see Fiedler,
1998; Pierce et al., 2002). The conservation consequences for ant-
associated butteries are that if a host ant species becomes extinct
there is a good chance the afliated buttery will go along with it
(Koh et al., 2004).
4.5. Mate recognition and species boundaries
The complexity of these inter-specic buttery interactions
within tropical communities has led researchers to focus on the
process of intra- and inter-specic individual recognition and spe-
ciation (Chamberlain et al., 2009). For example, Jiggins et al. (2001)
found Heliconius melpomene and Heliconius cydno recently diverged
to mimic different model taxa, and the mimetic shift caused both
pre-mating and post-mating isolation of the two sister species.
Additionally, in Heliconius, quantitative trait locus mapping places
a coloration recognition locus coincident with the locus that deter-
mines forewing color, which itself is linked to the wing patterning
candidate gene, wingless, suggesting wing color and color prefer-
ence are controlled by loci that are linked, or are pleiotropic effects
of a single locus (Kronforst et al., 2006). Therefore, the study of spe-
cies interactions and the mechanisms of individual recognition in
tropical butteries continue to revolutionize our understanding
of evolutionary patterns in the tradition of Bates (1862) and Mller
(1879).
Species interactions play a signicant role in the ecology and
evolution of tropical butteries. A holistic conservation approach
aimed at preserving the evolutionary mechanisms that generate
diversity should therefore consider the maintenance of species
interactions. Also, predictions of future anthropogenic impacts on
tropical buttery communities should carefully consider the role
of species interactions on population and species persistence.
5. Monitoring
As dened by Yoccoz et al. (2001), monitoring efforts seek to
gather information at different points in time for the purpose of
assessing system state and drawing inferences about changes in
state over time. The goals and objectives of specic monitoring
programs are critical in devising monitoring methodology. That is
unfocused or omnibus surveillance monitoring can be an inef-
cient use of conservation resources (New, 2006; Nichols and Wil-
liams, 2006). Extensive and exemplary buttery monitoring
programs in Europe have been vital sources for documenting the
effects of habitat and climate change on biodiversity (Pollard and
Yates, 1993; van Swaay et al., 2008). In the tropics however, mon-
itoring schemes of comparable spatial and temporal magnitude are
not present (New, 2009). Tropical buttery monitoring has primar-
ily focused on their use as indicators of habitat degradation but re-
cently there have also been efforts to document changes in
buttery communities through time as well as comprehensive uses
of DNA barcoding to catalogue these highly diverse ecosystems.
5.1. Indicator species
With shortages of time and resources for monitoring tropical
biodiversity, conservation biologists have been searching for meth-
ods that reduce time and costs. Indicator species are one way to do
1836 T.C. Bonebrake et al. / Biological Conservation 143 (2010) 18311841
this. Kremen (1992) found that in Madagascar, buttery diversity
correlated well with habitat heterogeneity but was a poor predic-
tor of anthropogenic disturbance. Additionally, Lawton et al.
(1998) found that while buttery species richness decreased with
anthropogenic disturbance in a tropical forest in Cameroon, the
change in species composition was poorly correlated with changes
in other taxonomic groups. The sometimes poor correlation be-
tween buttery diversity and both other species or human impacts
on habitat make the use of buttery communities as indicators
problematic (Ghazoul, 2002; Fleishman and Murphy, 2009). The
complex vertical structuring of tropical forests and tropical butter-
y communities can further complicate matters (DeVries et al.,
1997; DeVries and Walla, 2001; Molleman et al., 2006).
In general, while butteries are an imperfect indicator species,
their sensitivity to environmental change, short generation time
and relatively resolved systematics make them more suitable than
other candidates (Brown, 1997; Thomas, 2005). In particular,
ithomiines have attracted signicant attention as good indicators
for habitat quality, habitat fragmentation and patterns of total but-
tery diversity (Beccaloni and Gaston, 1995; Brown, 1997; Uehara-
Prado and Freitas, 2009). However, uctuations in their population
sizes and distributions (see Section 3.2.1) can complicate utility of
ithomiines as indicators as well (Brown and Freitas, 2000).
5.2. Techniques
Monitoring butteries in tropical environments can be chal-
lenging given the complexity of the habitat and the sheer number
of species. One of the most reliable and unbiased methods of sur-
veying tropical butteries is through using fruit traps for fruit-
feeding butteries (Daily and Ehrlich, 1995; Hughes et al., 1998).
Caldas and Robbins (2003) also highlight the effectiveness of timed
transects and hand-nets in monitoring tropical butteries. These
two monitoring techniques can be used in conjunction with one
another to provide the best results (Sparrow et al., 1994). These
methods can also be used in a rapid assessment framework to
characterize tropical buttery communities to a rough rst esti-
mate, when resources are very limited (Bonebrake and Sorto,
2009). However, in addition to multiple monitoring techniques,
long-term data are critical for true representations of buttery
diversity (DeVries et al., 1997, 2009).
Advances in genetic technology have made possible the advent
of the DNA barcode, which employs standardized gene regions as
species tags to assist in identifying unknown species (Hajibabaei
et al., 2006). The prime example highlighting the utility of DNA
barcoding is the case of the neotropical skipper, Astraptes fulgera-
tor, which upon barcoding was discovered to be ten cryptic species
rather than one (Hebert et al., 2004). While the prospect of using
standardized DNA sequencing to assist in characterizing tropical
buttery communities is appealing and promising, there are limi-
tations to the approach, including that the identication system re-
lies upon only a single locus (Valentini et al., 2009).
6. Threats to tropical buttery diversity
6.1. Habitat loss
Habitat loss in the tropics can take many forms including con-
version to agriculture, logging or fragmentation. For Lepidoptera,
conversion to agriculture might be the most destructive form of
habitat loss (Dunn, 2004; Sodhi et al., 2009). However, making
denitive claims about habitat disturbance effects on buttery spe-
cies diversity is difcult given the variety of responses butteries
exhibit to disturbance (Koh, 2007; Table 1). Koh (2007) reviewed
20 studies that examined the impacts of land use changes and hab-
itat loss on buttery communities in South-east Asia. Seven of the
studies showed decreased diversity in anthropogenically disturbed
sites as compared to protected forests, but interestingly, nine stud-
ies showed the opposite trend. We reviewed 20 more studies from
the neotropics and afrotropics (Table 1) and found similarly that
six of the studies reported decreases in diversity with disturbance,
but four found increases. The other ten studies were equivocal on
this point, but examined other aspects of land use change and but-
tery diversity. Much of the confusion stems from methodological
differences among studies, which make comparisons difcult (Koh,
2007). Spatial scale (extent and grain) and regional differences can
have important consequences for species richness relationships
(e.g. Hess et al., 2006) and likely further obscure habitat loss effects
on buttery diversity. One of the consistent patterns found in most
of these studies, however, is that species with narrow ranges tend
to be the most vulnerable to the impacts of habitat loss and usually
require natural forest to persist (Thomas, 1991; Spitzer et al., 1993;
Horner-Devine et al., 2003).
Spatial and temporal scales are complicating factors that must
be considered when comparing effects of habitat loss on butter-
ies. For example, studies at small spatial scales are more likely
to report increases in diversity when comparing disturbed and
undisturbed sites than are studies at larger spatial scales (Hill
and Hamer, 2004). This effect is likely a sampling artifact of species
pooling, such that at smaller spatial scales rare or patchy species
are more likely to be detected differentially among sites of varying
habitat loss pressures (Cleary, 2003). Also, the time interval be-
tween the disturbance event and buttery sampling could affect
the results. Brown and Hutchings (1997) analyzed the buttery
communities before and after the controlled fragmentation of the
Biological Dynamics of Forest Fragments Project in the Brazilian
Amazon. Based on their results, they proposed a dynamic model
of fragmentation effects on butteries such that increases in diver-
sity are expected after an initial disturbance (in this case burning).
Diversity steadily increases with the growth of secondary forest,
but then species diversity is expected to decrease slowly later as
heterogeneity decreases with the re-establishment of the primary
forest. This study considered all buttery species including the
widespread and sun-loving species that would colonize after a dis-
turbance and probably compensate for the loss suffered by forest-
adapted species (Brown and Hutchings, 1997; see also Leidner
et al., 2010).
On a much larger scale, in a survey of West Africa Larsen (2008)
found that no buttery species are known to have gone extinct
over the past 150 years, despite over 80% destruction of the forest
in the area. Conversely, in Singapore, deforestation over 183 years
led to the recorded extinctions of 38% of buttery species in the
country (Brook et al., 2003). These examples highlight how little
we know about the effects of habitat loss processes on buttery
communities.
6.2. Global climate change
The effects of climate change over the next several decades are
predicted to signicantly impact populations worldwide (Thomas
et al., 2004) and are already being felt in many taxa (Parmesan,
2006). Butteries are certainly no exception and climate change ef-
fects have been seen among many temperate buttery populations
(e.g. McLaughlin et al., 2002; Parmesan and Yohe, 2003; Pelini
et al., 2009). Chen et al. (2009) estimated that the altitudinal
ranges of 102 montane moth species in Mount Kinabalu, Borneo,
increased by a mean of 67 m in 42 years. However, there are cur-
rently few additional empirical studies linking changes in climate
to distribution changes or extinctions in tropical Lepidoptera.
Without the high resolution phenological and spatial distribu-
tion data of buttery populations and species that we have for
 T.C. Bonebrake et al. / Biological Conservation 143 (2010) 18311841 1837

Table 1
Habitat loss effects on tropical buttery populations in the neotropics and afrotropics.

Site Region Buttery Disturbance type Effect on community

community
Brazilian Amazoniaa,b Neotropics Fruit-feeding Conversion to Eucalyptus Decrease in species richness
plantation
c
Chiqibul Forest, Belize Neotropics Fruit-feeding Selective logging None
Lago Guri, Venezuelad,e,f Neotropics Fruit-feeding Fragmentation Larger and slower ying species were more vulnerable to
extinction
Brazilian Atlantic forestg,h Neotropics Fruit-feeding Fragmentation No effect on species richness, but changes in dominance and
composition
Victoria Mayaro, Trinidadi Neotropics All Selective logging Increase in species richness, supports intermediate disturbance
hypothesis
j
Las Cruces, Costa Rica Neotropics All Conversion to coffee, pasture Increase in overall species richness in coffee but decreased
abundance of species with narrow ranges
San Fernando, Chiapas Mexicok Neotropics Fruit-feeding Conversion to agro-pasture The agro-pasture matrix did not hinder diversity or migration
between sampled forest fragments
Soconusco, Chiapas Mexicol,m,n Neotropics Fruit-feeding Conversion to coffee, Decrease in species richness with decreasing shade and increasing
agroforestry management intensity
o
Manaus, Brazil Neotropics All Fragmentation Edge effects increase species richness and composition
Korup, Cameroonp Afrotropics Fruit-feeding Conversion to agroforestry Diversity highest in secondary forest but species with narrow
ranges prefer primary forest
Ashanti Region, Ghanaq Afrotropics Fruit-feeding Fragmentation Decrease in species diversity and composition
Muhaka forest, Kenyar Afrotropics All Fragmentation Decrease in species richness though some true forest species
also persisted in forest fragments
Mbalmayo, Cameroons Afrotropics All Conversion to agriculture, Decrease in species richness with disturbance intensity, replanted
silviculture plots had intermediate diversity
t
Sango Bay and Iriiri, Uganda Afrotropics All Conversion to pasture, charcoal Decrease in diversity with increased anthropogenic disturbance;
burning, cultivation and logging context dependent
a
Barlow et al. (2007).
b
Barlow et al. (2008).
c
Lewis (2001).
d
Shahabuddin and Terborgh (1999).
e
Shahabuddin et al. (2000).
f
Shahabuddin and Ponte (2005).
g
Uehara-Prado et al. (2007).
h
Uehara-Prado and Freitas (2009).
i
Wood and Gillman (1998).
j
Horner-Devine et al. (2003).
k
Marin et al. (2009).
l
Perfecto et al. (2003).
m
Mas and Dietsch (2003).
n
Mas and Dietsch (2004).
o
Brown and Hutchings (1997).
p
Bobo et al. (2006).
q
Bossart et al. (2006).
r
Rogo and Odulaja (2001).
s
Stork et al. (2003).
t
Akite (2008).

places like North America and the UK, it remains to be seen
whether or not tropical butteries have been or will be impacted
by warming temperatures. However, theory and some data show
that tropical organisms in general should have smaller thermal
niches than temperate organisms based on the low annual thermal
variability (Janzen, 1967; Ghalambor et al., 2006). As a result, Deu-
tsch et al. (2008) show that even though the magnitude of warm-
ing will be greater at the poles, given this difference in thermal
tolerance between temperate and tropical organisms, tropical
ectotherms appear to be more vulnerable to changes in climate.
Temperature is not the only climatic variable predicted to
change as a result of climate change. Changes in rainfall can have
large effects on tropical buttery populations (e.g. Azerefegne
et al., 2001) and in particular, changes in ENSO (El Nio Southern
Oscillation) are likely to affect buttery population outbreaks and
migratory behavior (Srygley et al., 2010). Furthermore, climate
change is predicted to disrupt species interactions (Schweiger
et al., 2008), which, because of the close relationship among but-
teries, their host plants and other species (e.g. parasitoids: Stir-
eman et al., 2005), may have ramications for tropical buttery
abundances and distributions as well.
6.3. Invasive species
After development (habitat loss), invasive species pose one of
the greatest contemporary threats to the conservation of lepidopt-
erans in North America (Wagner and Van Driesche, 2009). In the
tropics, the impact of invasive species on native buttery popula-
tions is less well known, though clearly invasive species can have
large affects on native tropical insects generally and especially
within island ecosystems (Gillespie and Roderick, 2002).
The invasion of non-native species can lead to disruption in spe-
cies interactions involving tropical buttery systems. For example,
oviposition mistakes are known to occur in the tropics when fe-
males lay eggs on invasive plants upon which offspring cannot de-
velop (e.g. Straatman, 1962). Also, Ghazoul (2004) found that the
invasion of an understory herbaceous plant (Chromolaena odorata)
into logged sites of tropical dry forest habitat in Thailand caused a
shift in buttery pollination activity away from the native canopy
owers to the understory. The effect of the non-native in this case
(and likely others) is facilitated by habitat loss through logging and
represents a likely route through which non-native species may af-
fect native populations in the tropics (Didham et al., 2007).
1838 T.C. Bonebrake et al. / Biological Conservation 143 (2010) 18311841
6.4. Toxins
Anthropogenic toxins disruptive to buttery development and
survival include pesticides, herbicides, pollution, and genetically
modied organisms. In general, the effects of environmental toxins
on buttery populations are poorly understood and toxins may or
may not have appreciable or primary consequences for populations
in the tropics. In the monarch buttery (Danaus plexippus) for
example, it is unclear if the butteries suffer effects of transgenic
Bacillus thuringiensis (Bt) pollen in the eld as a non-target taxon
(Andow and Zwahlen, 2006). Furthermore, Marvier et al. (2007)
considered the effects of pesticides on non-target insect taxa and
found greater impacts resulting from pesticides compared to Bt
transgenics. Thus, the importance of toxins for buttery population
trends requires more study and the relative effects of different tox-
ins and non-toxic effects (e.g. habitat loss, climate change, and
invasive species) on populations could have implications for trop-
ical buttery conservation.
6.5. Exploitation and harvest
Some of the largest, and arguably most beautiful, butteries in-
habit tropical forests. Their appeal to human collectors has resulted
in very large population declines, leading to endangerment for
some butteries. These include large swallowtail butteries (Pap-
ilionidae), such as the famous birdwings (Ornithoptera) of New
Guinea and Australia (New et al., 1995). These butteries are one
of the few exceptions to the habitat focus of tropical buttery con-
servation, in that conservation efforts directed at them are often
species-specic. For example, all of the CITES listed buttery spe-
cies are Papilionidae (Collins and Morris, 1985). Harvesting of trop-
ical butteries in these circumstances can be devastating, but
beyond those large Papilionidae and possibly the spectacular Mor-
pho, harvesting probably does not have a signicant effect on most
tropical buttery populations, particularly when compared to
more imminent threats such as habitat loss.
7. Future research
Studies of butteries as indicators of disturbance and environ-
mental change have been useful for conservation efforts that focus
on reserve design (Kremen, 2003) and landscape connectivity or
corridor establishment (Hill, 1995; Brown and Freitas, 2000). How-
ever, the difculty in reaching generalizations about the effects of
anthropogenic development or habitat loss on buttery diversity
(e.g. Koh et al., 2004) stems from a poor understanding of basic
tropical buttery ecology. If we are to develop a predictive theory
of habitat loss impacts on buttery diversity (or effectively use
tropical butteries as indicators of anthropogenic impacts), more
research is required into the specic biogeographic patterns,
demographic and life history strategies, and the importance of spe-
cies interactions in tropical buttery communities.
However, butteries are more than just indicators. In temperate
buttery conservation efforts, population- and species-specic ap-
proaches are used because people want to conserve species, not for
butteries inherent utility in estimating human impacts on biodi-
versity in habitat fragments. Buttery conservation efforts in the
tropics would benet greatly from more long-term population
studies (e.g. Papilio homerus; Garraway et al., 2008), such as those
that have pervaded temperate buttery conservation (e.g. Euphydr-
yas editha and Melitaea cinxia; Ehrlich and Hanski, 2004). Yet, as the
rule more than the exception in the tropics, it seems that the ab-
sence of sufcient time and resources limit the use of targeted,
population-specic conservation. As an alternative, model system
development may be useful (Ehrlich, 1992) as has been the case
to some extent for heliconiines and ithomiines (Brown, 1981).
More research into economic alternatives to habitat or forest
exploitation will almost certainly aid the cause of tropical buttery
conservation and should be explored as well. Butteries provide
ecosystem services in tropical ecosystems by, for example, provid-
ing pollination services (Kremen et al., 2007), and because of their
beauty providing life-fullling aesthetic services (Ehrlich and Ehr-
lich, 1992). The aesthetic services can also translate into direct eco-
nomic value. The sustainable use of buttery farming, for example,
can provide an additional source of income for local communities
looking to combat logging threats (Slone et al., 1997; Morgan-
Brown et al., 2010).
Ultimately, effective tropical buttery conservation will require
the utilization of multiple approaches. It may be very difcult to
replicate the success seen in large scale temperate buttery con-
servation efforts in the tropics without similar depths of ecological
knowledge (e.g. high resolution distributional data and annual
censusing). While understanding the exact utility of tropical but-
teries as indicators (and of what) would be of interest, it is now
time to consider tropical butteries as more than just indicators
but targets of conservation in their own right. We conclude by urg-
ing further studies on all aspects of tropical buttery biology: if
they are done, then in the future it will be possible to review trop-
ical buttery ecology and conservation more completely and
denitively.
Acknowledgments
This review would not be possible of course without the many
tropical buttery biologists around the world who have inspired
and laid the foundations for present and future research. We are
very grateful to Jan Beck, Larry Gilbert, Lian Pin Koh, Krushnamegh
Kunte and one anonymous reviewer for extensive comments on
previous drafts. We also thank members of the Boggs, Daily and
Ehrlich labs for helpful input.
References
Akite, P., 2008. Effects of anthropogenic disturbances on the diversity and
composition of the buttery fauna of sites in the Sango Bay and Iriiri areas,
Uganda: implications for conservation. African Journal of Ecology 46, 313.
Andow, D.A., Zwahlen, C., 2006. Assessing environmental risks of transgenic plants.
Ecology Letters 9, 196214.
Azerefegne, F., Solbreck, C., Ives, A.R., 2001. Environmental forcing and high
amplitude uctuations in the population dynamics of the tropical buttery
Acraea acerata (Lepidoptera: Nymphalidae). Journal of Animal Ecology 70,
10321045.
Barlow, J., Overal, W.L., Araujo, I.S., Gardner, T.A., Peres, C.A., 2007. The value of
primary, secondary and plantation forests for fruit-feeding butteries in the
Brazilian Amazon. Journal of Applied Ecology 44, 10011012.
Barlow, J., Araujo, I.S., Overal, W.L., Gardner, T.A., Mendes, F.D., Lake, I.R., Peres, C.A.,
2008. Diversity and composition of fruit-feeding butteries in tropical
Eucalyptus plantations. Biodiversity and Conservation 17, 10891104.
Bates, H.W., 1862. Contributions to an insect fauna of the Amazon valley.
Lepidoptera: Heliconidea. Transactions of the Linnean Society of London 23,
495566.
Beccaloni, G.W., Gaston, K.J., 1995. Predicting the species richness of neotropical
forest butteries Ithomiinae (Lepidoptera, Nymphalidae) as indicators.
Biological Conservation 71, 7786.
Beck, J., 2007. The importance of amino acids in the adult diet of male tropical
butteries. Oecologia 151, 741747.
Beck, J., 2008. Phylogenetic and ecological correlates with male adult life span of
rainforest butteries. Evolutionary Ecology 22, 507517.
Beck, J., Fiedler, K., 2009. Adult life spans of butteries (Lepidoptera:
Papilionoidea + Hesperioidea): broadscale contingencies with adult and larval
traits in multi-species comparisons. Biological Journal of the Linnean Society 96,
166184.
Beck, J., Kitching, I.J., Linsenmair, K.E., 2006. Wallaces line revisited: has vicariance
or dispersal shaped the distribution of Malesian hawkmoths (Lepidoptera:
Sphingidae)? Biological Journal of the Linnean Society 89, 455468.
Beldade, P., Brakeeld, P.M., Long, A.D., 2005. Generating phenotypic variation:
prospects from evo-devo research on Bicyclus anynana wing patterns.
Evolution and Development 7, 101107.
 T.C. Bonebrake et al. / Biological Conservation 143 (2010) 18311841
Benson, W.W., 1978. Resource partitioning in passion vine butteries. Evolution 32,
493518.
Bigger, M., 1976. Oscillations of tropical insect populations. Nature 5540, 207209.
Bobo, K.S., Waltert, M., Fermon, H., Njokagbor, J., Mhlenberg, M., 2006. From forest
to farmland: buttery diversity and habitat associations along a gradient of
forest conversion in Southwestern Cameroon. Journal of Insect Conservation 10,
2942.
Boggs, C.L., 1986. Reproductive strategies of female butteries: variation in and
constraints on fecundity. Ecological Entomology 11, 715.
Boggs, C.L., 1997. Reproductive allocation from reserves and income in buttery
species with differing adult diets. Ecology 78, 181191.
Boggs, C.L., 2009. Understanding insect life histories and senescence through a
resource allocation lens. Functional Ecology 23, 2737.
Boggs, C.L., Dau, B., 2004. Resource specialization in puddling Lepidoptera.
Environmental Entomology 33, 10201024.
Boggs, C.L., Watt, W.B., Ehrlich, P.R., 2003. Butteries: Ecology and Evolution Taking
Flight. University of Chicago Press, Chicago.
Bonebrake, T.C., Sorto, R., 2009. Buttery (Papilionoidea and Hesperioidea) rapid
assessment of a coastal countryside in El Salvador. Tropical Conservation
Science 2, 3451.
Bossart, J.L., Opuni-Frimpong, E., Kuudaar, S., Nkrumah, E., 2006. Richness,
abundance, and complementarity of fruit-feeding buttery species in relict
sacred forests and forest reserves of Ghana. Biodiversity and Conservation 15,
333359.
Braby, M.F., 1995. Reproductive seasonality in tropical satyrine butteries
strategies for the dry season. Ecological Entomology 20, 517.
Brakeeld, P.M., Reitsma, F., 1991. Phenotypic plasticity, seasonal climate and
population biology of Bicyclus butteries. Ecological Entomology 16, 291303.
Brakeeld, P.M., Pijpe, J., Zwaan, B.J., 2007. Developmental plasticity and
acclimation both contribute to adaptive responses to alternating seasons of
plenty and of stress in Bicyclus butteries. Journal of Biosciences 32, 465475.
Brook, B.W., Sodhi, N.S., Ng, P.K.L., 2003. Catastrophic extinctions follow
deforestation in Singapore. Nature 424, 420423.
Brower, L.P., 1995. Understanding and misunderstanding the migration of the
monarch buttery (Nymphalidae) in North America (18571995). Journal of the
Lepidopterists Society 49, 304385.
Brown, K.S., 1981. The biology of Heliconius and related genera. Annual Review of
Entomology 26, 427456.
Brown, K.S., 1996. Diversity of Brazilian Lepidoptera: history of study, methods for
measurement, and use as indicator for genetic, specic and system richness. In:
Bicudo, C.E.M., Menezes, N.A. (Eds.), Biodiversity in Brazil, a First Approach.
Instituto de Botnica/CNPq, So Paulo, pp. 221253.
Brown, K.S., 1997. Diversity, disturbance and sustainable use of Neotropical forests:
insects as indicators for conservation monitoring. Journal of Insect Conservation
1, 2542.
Brown, K.S., Benson, W.W., 1974. Adaptive polymorphism associated with multiple
Mullerian mimicry in Heliconius numata. Biotropica 6, 205228.
Brown, K.S., Freitas, A.V.L., 2000. Atlantic forest butteries: indicators for landscape
conservation. Biotropica 32, 934956.
Brown, K.S., Hutchings, R.W., 1997. Disturbance, fragmentation, and the dynamics
of diversity in Amazonian forest butteries. In: Laurance, W.F., Bierregaard, R.O.
(Eds.), Tropical Forest Remnants: Ecology, Management, and Conservation of
Fragmented Communities. University of Chicago Press, Chicago, pp. 91110.
Brown, K.S., Sheppard, P.M., Turner, J.R.G., 1974. Quaternary refugia in tropical
America: evidence from race formation in Heliconius butteries. Proceedings of
the Royal Society of London Series B Biological Sciences 187, 369378.
Caldas, A., Robbins, R.K., 2003. Modied Pollard transects for assessing tropical
buttery abundance and diversity. Biological Conservation 110, 211219.
Chai, P., Srygley, R.B., 1990. Predation and the ight, morphology, and temperature
of neotropical rain-forest butteries. American Naturalist 135, 748765.
Chamberlain, N.L., Hill, R.I., Kapan, D.D., Gilbert, L.E., Kronfurst, M.R., 2009.
Polymorphic buttery reveals the missing link in ecological speciation.
Science 326, 847850.
Chen, I.-C., Shiu, H.-J., Benedick, S., Holloway, J.D., Chey, V.K., Barlow, H.S., Hill, J.K.,
Thomas, C.D., 2009. Elevation increases in moth assemblages over 42 years on a
tropical mountain. Proceedings of the National Academy of Sciences of the
United States of America 106, 14791483.
Cleary, D.F.R., 2003. An examination of scale assessment, logging and ENSO-induced
res on buttery diversity in Borneo. Oecologia 135, 313321.
Collins, N.M., Morris, M.G., 1985. Threatened Swallowtail Butteries of the World:
The IUCN Red Data Book. IUCN, Gland and Cambridge.
Daily, G.C., Ehrlich, P.R., 1995. Preservation of biodiversity in small rain-forest
patches rapid evaluations using buttery trapping. Biodiversity and
Conservation 4, 3555.
de-Andrade, R.B., Freitas, A.V.L., 2005. Population biology of two species of
Heliconius (Nymphalidae: Heliconiinae) in a semi-deciduous forest in
southeastern Brazil. Journal of the Lepidopterists Society 59, 223228.
Deutsch, C.A., Tewksbury, J.J., Huey, R.B., Sheldon, K.S., Ghalambor, C.K., Haak, D.C.,
Martin, P.R., 2008. Impacts of climate warming on terrestrial ectotherms across
latitude. Proceedings of the National Academy of Sciences of the United States
of America 105, 66686672.
DeVries, P.J., 1987. The butteries of Costa Rica and their natural history. Vol 1.
Papilionidae, Pieridae, and Nymphalidae. Princeton University Press, Princeton.
DeVries, P.J., Walla, T.R., 2001. Species diversity and community structure in
neotropical fruit-feeding butteries. Biological Journal of the Linnean Society
74, 115.
1839
DeVries, P.J., Murray, D., Lande, R., 1997. Species diversity in vertical, horizontal, and
temporal dimensions of a fruit-feeding buttery community in an Ecuadorian
rainforest. Biological Journal of the Linnean Society 62, 343364.
DeVries, P.J., Austin, G.T., Martin, N.H., 2009. Estimating species diversity in a guild
of Neotropical skippers (Lepidoptera: Hesperiidae) with articial lures is a
sampling problem. Insect Conservation and Diversity 2, 125134.
Didham, R.K., Tylianakis, J.M., Gemmell, N.J., Rand, T.A., Ewers, R.M., 2007.
Interactive effects of habitat modication and species invasion on native
species decline. Trends in Ecology and Evolution 22, 489496.
Dobzhansky, T., 1950. Evolution in the tropics. American Scientist 38, 209221.
Dunn, R.R., 2004. Managing the tropical landscape: a comparison of the effects of
logging and forest conversion to agriculture on ants, birds, and lepidoptera.
Forest Ecology and Management 191, 215224.
Dunn, R.R., 2005. Modern insect extinctions, the neglected majority. Conservation
Biology 19, 10301036.
Ehrlich, P.R., 1984. The structure and dynamics of buttery populations. In: Vane-
Wright, R.I., Ackery, P.R. (Eds.), The Biology of Butteries. Academic Press,
London, pp. 2540.
Ehrlich, P.R., 1992. Population biology of checkerspot butteries and the
preservation of global biodiversity. Oikos 63, 612.
Ehrlich, P.R., Ehrlich, A.H., 1992. The value of biodiversity. Ambio 21, 219226.
Ehrlich, P.R., Gilbert, L.E., 1973. Population structure and dynamics of the tropical
buttery Heliconius ethilla. Biotropica 5, 6982.
Ehrlich, P.R., Hanski, I., 2004. On the Wings of Checkerspots: A Model System for
Population Biology. Oxford University Press, Oxford.
Elias, M., Gompert, Z., Jiggins, C., Willmott, K., 2008. Mutualistic interactions drive
ecological niche convergence in a diverse buttery community. Plos Biology 6,
26422649.
Elias, M., Joron, M., Willmott, K., Silva-Brandao, K.L., Kaiser, V., Arias, C.F., Pinerez,
L.M.G., Uribe, S., Brower, A.V.Z., Freitas, A.V.L., Jiggins, C.D., 2009. Out of the
Andes: patterns of diversication in clearwing butteries. Molecular Ecology
18, 17161729.
Erhardt, A., Baker, I., 1990. Pollen amino acids an additional diet for a nectar
feeding buttery? Plant Systematics and Evolution 169, 111121.
Fiedler, K., 1998. Lycaenidant interactions of the Maculinea type: tracing their
historical roots in a comparative framework. Journal of Insect Conservation 2,
314.
Fischer, K., Brakeeld, P.M., Zwaan, B.S., 2003. Plasticity in buttery egg size: why
larger offspring at lower temperatures? Ecology 84, 31383147.
Fischer, K., OBrien, D.M., Boggs, C.L., 2004. Allocation of larval and adult
resources to reproduction in a fruit-feeding buttery. Functional Ecology 18,
656663.
Fisher, R.A., Corbet, S.A., Williams, C.B., 1943. The relation between number of
species and the number of individuals in a random sample of an animal
population. Journal of Animal Ecology 12, 4258.
Fleishman, E., Murphy, D.D., 2009. A realistic assessment of the indicator potential
of butteries and other charismatic taxonomic groups. Conservation Biology 23,
11091116.
Fleming, T.H., Serrano, D., Nassar, J., 2005. Dynamics of a subtropical population of
the zebra longwing buttery Heliconius charithonia (Nymphalidae). Florida
Entomologist 88, 169179.
Freitas, A.V.L., 1996. Population biology of Heterosais edessa (Nymphalidae) and its
associated Atlantic forest Ithomiinae community. Journal of the Lepidopterists
Society 50, 273289.
Freitas, A.V.L., Vasconcellos-Neto, J., Vanini, F., Trigo, J.R., Brown, K.S., 2001.
Popualtion studies of Aeria olena and Tithorea harmonia (Nymphalidae,
Ithomiinae) in Southeastern Brazil. Journal of the Lepidopterists Society 55,
150157.
Garraway, E., Bailey, A.J.A., Freeman, B.E., Parnell, J.R., Emmel, T.C., 2008. Population
studies and conservation of Jamaicas endangered swallowtail buttery Papilio
(Pterorous) homerus. Journal of Insect Conservation 12, 383397.
Gaston, K.J., 1991. The magnitude of global insect species richness. Conservation
Biology 5, 283296.
Ghalambor, C.K., Huey, R.B., Martin, P.R., Tewksbury, J.J., Wang, G., 2006. Are
mountain passes higher in the tropics? Janzens hypothesis revisited.
Integrative and Comparative Biology 46, 517.
Ghazoul, J., 2002. Impact of logging on the richness and diversity of forest
butteries in a tropical dry forest in Thailand. Biodiversity and Conservation 11,
521541.
Ghazoul, J., 2004. Alien abduction: disruption of native plantpollinator interactions
by invasive species. Biotropica 36, 156164.
Gilbert, L.E., 1972. Pollen feeding and reproductive biology of Heliconius butteries.
Proceedings of the National Academy of Sciences of the United States of
America 69, 14031407.
Gilbert, L.E., 1991. Biodiversity of a Central American Heliconius community:
pattern, process, and problems. In: Price, P.W., Lewinsohn, T.M., Wilson
Fernandes, G., Benson, W.W. (Eds.), PlantAnimal Interactions: Evolutionary
Ecology in Tropical and Temperate Regions. Wiley, New York.
Gilbert, L.E., Singer, M.C., 1975. Buttery ecology. Annual Review of Ecology and
Systematics 6, 365395.
Gillespie, R.G., Roderick, G.K., 2002. Arthropods on islands: colonization, speciation,
and conservation. Annual Review of Entomology 47, 595632.
Haber, W.A., Stevenson, R.D., 2004. Diversity, migration, and conservation of
butteries in northern Costa Rica. In: Frankie, G.W., Mata, A., Vinson, S.B. (Eds.),
Biodiversity Conservation in Costa Rica: Learning the Lessons in a Seasonal Dry
Forest. University of California Press, Berkeley and Los Angeles.
1840 T.C. Bonebrake et al. / Biological Conservation 143 (2010) 18311841
Hajibabaei, M., Janzen, D.H., Burns, J.M., Hallwachs, W., Hebert, P.D.N., 2006. DNA
barcodes distinguish species of tropical Lepidoptera. Proceedings of the
National Academy of Sciences of the United States of America 103, 968971.
Hall, J.P., Willmott, K.R., 2000. Patterns of feeding behavior in adult male riodinid
butteries and their relationship to morphology and ecology. Biological Journal
of the Linnean Society 69, 123.
Hawkins, B.A., DeVries, P.J., 2009. Tropical niche conservatism and the species
richness gradient of North American butteries. Journal of Biogeography 36,
16981711.
Hebert, P.D.N., Penton, E.H., Burns, J.M., Janzen, D.H., Hallwachs, W., 2004. Ten
species in one: DNA barcoding reveals cryptic species in the neotropical skipper
buttery Astraptes fulgerator. Proceedings of the National Academy of Sciences
of the United States of America 101, 1481214817.
Hess, G.R., Bartel, R.A., Leidner, A.K., Rosenfeld, K.M., Rubino, M.J., Snider, S.B.,
Ricketts, T.H., 2006. Effectiveness of biodiversity indicators varies with extent,
grain, and region. Biological Conservation 132, 448457.
Hill, C.J., 1995. Linear strips of rain forest vegetation as potential dispersal corridors
for rain forest insects. Conservation Biology 9, 15591566.
Hill, R.I., 2010. Habitat segregation among mimetic ithomiine butteries
(Nymphalidae). Evolutionary Ecology 24, 273285.
Hill, J.K., Hamer, K.C., 2004. Determining impacts of habitat modication on
diversity of tropical forest fauna: the importance of spatial scale. Journal of
Applied Ecology 41, 744754.
Horner-Devine, M.C., Daily, G.C., Ehrlich, P.R., Boggs, C.L., 2003. Countryside
biogeography of tropical butteries. Conservation Biology 17, 168177.
Hughes, J.B., Daily, G.C., Ehrlich, P.R., 1998. Use of fruit bait traps for monitoring of
butteries (Lepidoptera: Nymphalidae). Revista De Biologia Tropical 46, 697
704.
Jablonski, D., Roy, K., Valentine, J.W., 2006. Out of the tropics: evolutionary
dynamics of the latitudinal diversity gradient. Science 314, 102106.
Janzen, D.H., 1967. Why mountain passes are higher in the tropics. American
Naturalist 101, 233249.
Janzen, D.H., 1987. Insect diversity of a Costa Rican dry forest why keep it, and
how. Biological Journal of the Linnean Society 30, 343356.
Janzen, D.H., 1988. Ecological characterization of a Costa Rican dry forest caterpillar
fauna. Biotropica 20, 120135.
Jervis, M.A., Boggs, C.L., Ferns, P.N., 2005. Egg maturation strategy and its associated
trade-offs: a synthesis focusing on Lepidoptera. Ecological Entomology 30, 359
375.
Jiggins, C.D., Naisbit, R.E., Coe, R.L., Mallet, J., 2001. Reproductive isolation caused by
colour pattern mimicry. Nature 411, 302305.
Jones, R.E., Rienks, J., 1987. Reproductive seasonality in the tropical genus Eurema
(Lepidoptera, Pieridae). Biotropica 19, 716.
Kemp, D.J., 2001. Reproductive seasonality in the tropical buttery Hypolimnas
bolina (Lepidoptera: Nymphalidae) in northern Australia. Journal of Tropical
Ecology 17, 483494.
Knapp, S., Mallet, J., 2003. Refuting refugia. Science 300, 7172.
Koh, L.P., 2007. Impacts of land use change on South-east Asian forest butteries: a
review. Journal of Applied Ecology 44, 703713.
Koh, L.P., Dunn, R.R., Sodhi, N.S., Colwell, R.K., Proctor, H.C., Smith, V.S., 2004. Species
coextinctions and the biodiversity crisis. Science 305, 16321634.
Kremen, C., 1992. Assessing the indicator properties of species assemblages for
natural areas monitoring. Ecological Applications 2, 203217.
Kremen, C., 2003. Butteries and conservation planning in Madagascar: from
pattern to practice. In: Boggs, C.L., Watt, W.B., Ehrlich, P.R. (Eds.), Butteries:
Ecology and Evolution Taking Flight. University of Chicago Press, Chicago.
Kremen, C., Williams, N.M., Aizen, M.A., Gemmill-Harren, B., LeBuhn, G., Minckley,
R., Packer, L., Potts, S.G., Roulston, T., Steffan-Dewenter, I., Vazquez, D.P.,
Winfree, R., Adams, L., Crone, E.E., Greenlead, S.S., Keitt, T.H., Klein, A.M., Regetz,
J., Ricketts, T.H., 2007. Pollination and other ecosystem services produced by
mobile organisms: a conceptual framework for the effects of land-use change.
Ecology Letters 10, 299314.
Kronforst, M.R., Gilbert, L.E., 2008. The population genetics of mimetic diversity in
Heliconius butteries. Proceedings of the Royal Society B: Biological Sciences
275, 493500.
Kronforst, M.R., Young, L.G., Kapan, D.D., McNeely, C., ONeill, R.J., Gilbert, L.E., 2006.
Linkage of buttery mate preference and wing color preference cue at the
genomic location of wingless. Proceedings of the National Academy of Sciences
United States of America 103, 65756580.
Kunte, K., 2004. Species composition, sex-ratios and movement patterns in danaine
buttery migrations in southern India. Journal of the Bombay Natural History
Society 102, 280286.
Kunte, K., 2008. Competition and species diversity: removal of dominant species
increases diversity in Costa Rican buttery communities. Oikos 117, 6976.
Lamas, G., 2004. Atlas of Neotropical Lepidoptera (Checklist Part 4A. Hesperioidea
Papilionoidea). Association of Tropical Lepidoptera, Gainesville.
Larsen, T.B., 2005. Butteries of West Africa. Apollo Books, Stenstrup.
Larsen, T.B., 2008. Forest butteries in West Africa have resisted extinction... So far
(Lepidoptera: Papilionoidea and Hesperioidea). Biodiversity and Conservation
17, 28332847.
Lawton, J.H., Bignell, D.E., Bolton, B., Bloemers, G.F., Eggleton, P., Hammond, P.M.,
Hodda, M., Holt, R.D., Larsen, T.B., Mawdsley, N.A., Stork, N.E., Srivastava, D.S.,
Watt, A.D., 1998. Biodiversity inventories, indicator taxa and effects of habitat
modication in tropical forest. Nature 391, 7276.
Lei, G.C., Hanski, I., 1997. Metapopulation structure of Cotesia melitaearum, a
specialist parasitoid of the buttery Melitaea cinxia. Oikos 78, 91100.
Leidner, A.K., Haddad, N.M., Lovejoy, T.E., 2010. Does tropical forest fragmentation
increase long-term variability of buttery communities? PLoS One 5, e9534.
Lewinsohn, T.M., Roslin, T., 2008. Four ways towards tropical herbivore
megadiversity. Ecology Letters 11, 398416.
Lewis, O.T., 2001. Effect of experimental selective logging on tropical butteries.
Conservation Biology 15, 389400.
Lyytinen, A., Brakeeld, P.M., Lindstrm, L., Mappes, J., 2004. Does predation
maintain eyespot plasticity in Bicyclus anynana? Proceedings of the Royal
Society B: Biological Sciences 271, 279283.
Mallet, J., 1986. Hybrid zones of Heliconius butteries in Panama and the stability
and movement of warning colour clines. Heredity 56, 191202.
Mallet, J., 2004. Poulton, Wallace, and Jordan: how discoveries in Papilio butteries
led to a new species concept 100 years ago. Systematics and Biodiversity 1,
441452.
Mallet, J., Joron, M., 1999. Evolution of diversity in warning color and mimicry:
polymorphisms, shifting balance, and speciation. Annual Review of Ecology and
Systematics 30, 201233.
Marin, L., Leon-Cortes, J.L., Stefanescu, C., 2009. The effect of an agro-pasture
landscape on diversity and migration patterns of frugivorous butteries in
Chiapas, Mexico. Biodiversity and Conservation 18, 919934.
Marvier, M., McCreedy, C., Regetz, J., Kareiva, P., 2007. A meta-analysis of
effects of Bt cotton and maize no nontarget invertebrates. Science 316,
14751477.
Mas, A.H., Dietsch, T.V., 2003. An index of management intensity for coffee
agroecosystems to evaluate buttery species richness. Ecological Applications
13, 14911501.
Mas, A.H., Dietsch, T.V., 2004. Linking shade coffee certication to biodiversity
conservation: butteries and birds in Chiapas, Mexico. Ecological Applications
14, 642654.
McLaughlin, J.F., Hellmann, J.J., Boggs, C.L., Ehrlich, P.R., 2002. Climate change
hastens population extinctions. Proceedings of the National Academy of
Sciences of the United States of America 99, 60706074.
Megens, H., van Moorsel, C.H.M., Piel, W.H., Pierce, N.E., de Jong, R., 2004. Tempo of
speciation in a buttery genus in the Southeast Asian tropics, inferred from
mitochondrial and nuclear DNA sequence data. Molecular Phylogenetics and
Evolution 31, 11811196.
Molleman, F., Kop, A., Brakeeld, P.M., DeVries, P.J., Zwaan, B.J., 2006. Vertical and
temporal patterns of biodiversity of fruit-feeding butteries in a tropical forest
in Uganda. Biodiversity and Conservation 15, 107121.
Molleman, F., Zwaan, B.J., Brakeeld, P.M., Carey, J.R., 2007. Extraordinary long life
spans in fruit-feeding butteries can provide window on evolution of life span
and aging. Experimental Gerontology 42, 472482.
Molleman, F., Ding, J., Wang, J.L., Brakeeld, P.M., Carey, J.R., Zwaan, B.J., 2008.
Amino acid sources in the adult diet do not affect life span and fecundity
in the fruit-feeding buttery Bicyclus anynana. Ecological Entomology 33, 429
438.
Molleman, F., Ding, J., Carey, J.R., Wang, J.L., 2009. Nutrients in fruit increase fertility
in wild-caught females of large and long-lived Euphaedra species (Lepidoptera,
Nymphalidae). Journal of Insect Physiology 55, 375383.
Morgan-Brown, T., Jacobson, S.K., Wald, K., Child, B., 2010. Quantitative assessment
of a Tanzanian integrated conservation and development project involving
buttery farming. Conservation Biology 24, 563572.
Mller, F., 1879. Ituna and Thyridia: a remarkable case of mimicry in butteries.
Transactions of the Entomological Society of London 1879, xxxxix.
Muyshondt, A., 1973. Notes on the life cycle and natural history of butteries of El
Salvador. II. Anaea (Zaretis) itys (Nymphalidae). Journal of the Lepidopterists
Society 27, 294302.
New, T.R., 2006. Does inventory of insect species in the tropics really help in their
conservation? Journal of Insect Conservation 10, 211213.
New, T.R., 2009. Forty years of buttery conservation! Journal of Insect
Conservation 13, 12.
New, T.R., Pyle, R.M., Thomas, J.A., Thomas, C.D., Hammond, P.C., 1995. Buttery
conservation management. Annual Review of Entomology 40, 5783.
Nichols, J.D., Williams, B.K., 2006. Monitoring for conservation. Trends in Ecology
and Evolution 21, 669673.
OBrien, D.M., Boggs, C.L., Fogel, M.L., 2003. Pollen feeding in the buttery Heliconius
charitonia: isotopic evidence for essential amino acid transfer from pollen to
eggs. Proceedings of the Royal Society B: Biological Sciences 270, 26312636.
Owen, D.F., 1971. Tropical Butteries. Clarendon, Oxford.
Parmesan, C., 2006. Ecological and evolutionary responses to recent climate change.
Annual Review of Ecology Evolution and Systematics 37, 637669.
Parmesan, C., Yohe, G., 2003. A globally coherent ngerprint of climate change
impacts across natural systems. Nature 421, 3742.
Pelham, J., 2008. Catalogue of the butteries of the United States and Canada.
Journal of Research on the Lepidoptera 40, xiv658.
Pelini, S.L., Prior, K.M., Parker, D.J., Dzurisin, J.D.K., Lindroth, R.L., Hellmann, J.J.,
2009. Climate change and temporal and spatial mismatches in insect
communities. In: Letcher, T.M. (Ed.), Climate Change: Observed impacts on
Planet Earth. Elsevier, The Netherlands, pp. 215231.
Perfecto, I., Mas, A., Dietsch, T., Vandermeer, J., 2003. Conservation of biodiversity in
coffee agroecosystems: a tri-taxa comparison in southern Mexico. Biodiversity
and Conservation 12, 12391252.
Pianka, E.R., 1970. On r- and K-selection. American Naturalist 104, 367372.
Pierce, N.E., Braby, M.F., Heath, A., Lohman, D.J., Mathew, J., Rand, D.B., Travassos,
M.A., 2002. The ecology and evolution of ant association in the Lycaenidae
(Lepidoptera). Annual Review of Entomology 47, 733771.
 T.C. Bonebrake et al. / Biological Conservation 143 (2010) 18311841
Pimm, S.L., Raven, P., 2000. Biodiversity extinction by numbers. Nature 403, 843
845.
Pinheiro, C.E.G., 2007. Asynchrony in daily activity patterns of buttery models and
mimics. Journal of Tropical Ecology 23, 119123.
Pollard, E., Yates, T.J., 1993. Monitoring Butteries for Ecology and Conservation.
Chapman & Hall, London.
Quintero, H.E., 1988. Population dynamics of the buttery Heliconius charitonius L.
in Puerto Rico. Caribbean Journal of Science 24, 155160.
Ramos, R.R., Freitas, A.V.L., 1999. Population biology and wing color variation in
Heliconius erato phyllis (Nymphalidae). Journal of the Lepidopterists Society 53,
1121.
Rogo, L., Odulaja, A., 2001. Buttery populations in two forest fragments at the
Kenya coast. African Journal of Ecology 39, 266275.
Roskam, J.C., Brakeeld, P.M., 1999. Seasonal polyphenism in Bicyclus (Lepidoptera:
Satyridae) butteries: different climates need different cues. Biological Journal
of the Linnean Society 66, 345356.
Samways, M.J., 2007. Insect conservation: a synthetic management approach.
Annual Review of Ecology and Systematics 52, 465487.
Schultz, C.B., Crone, E.E., 2008. Using ecological theory to advance buttery
conservation. Israel Journal of Ecology and Evolution 54, 6368.
Schweiger, O., Settele, J., Kudrna, O., Klotz, S., Kuhn, I., 2008. Climate change can
cause spatial mismatch of trophically interacting species. Ecology 89, 3472
3479.
Scoble, M.J., 1992. The Lepidoptera: Form, Function, and Diversity. Oxford
University Press, Oxford.
Shahabuddin, G., Ponte, C.A., 2005. Frugivorous buttery species in tropical forest
fragments: correlates of vulnerability to extinction. Biodiversity and
Conservation 14, 11371152.
Shahabuddin, G., Terborgh, J.W., 1999. Frugivorous butteries in Venezuelan forest
fragments: abundance, diversity and the effects of isolation. Journal of Tropical
Ecology 15, 703722.
Shahabuddin, G., Herzner, G.A., Aponte, C., Gomez, M.D., 2000. Persistence of a
frugivorous buttery species in Venezuelan forest fragments: the role of
movement and habitat quality. Biodiversity and Conservation 9, 16231641.
Shields, O., 1989. World numbers of butteries. Journal of the Lepidopterists
Society 43, 178183.
Skillen, E.L., Pickering, J., Sharkey, M.J., 2000. Species richness of the Campopleginae
and Ichneumoninae (Hymenoptera:Ichneumonidae) along a latitudinal
gradient in eastern North America old-growth forests. Environmental
Entomology 29, 460466.
Slone, T.H., Orsak, L.J., Malver, O., 1997. A comparison of price, rarity, and cost of
buttery specimens: implications for the insect trade and for habitat
conservation. Ecological Economics 21, 7785.
Smith, M.A., Woodley, N.E., Janzen, D.H., Hallwachs, W., Hebert, P.D.N., 2006. DNA
barcodes reveal cryptic host-specicity within the presumed polyphagous
members of a genus of parasitoid ies (Diptera: Tachinidae). Proceedings of
the National Academy of Sciences of the United States of America 103, 3657
3662.
Sodhi, N.S., Lee, T.M., Koh, L.P., Brook, B.W., 2009. A meta-analysis of the impact of
anthropogenic forest disturbance on Southeast Asias biotas. Biotropica 41,
103109.
Sparrow, H.R., Sisk, T.D., Ehrlich, P.R., Murphy, D.D., 1994. Techniques and guidelines
for monitoring neotropical butteries. Conservation Biology 8, 800809.
Spitzer, K., Novotny, V., Tonner, M., Leps, J., 1993. Habitat preferences, distribution
and seasonality of the butteries (Lepidoptera, Papilionoidea) in a montane
tropical rain forest, Vietnam. Journal of Biogeography 20, 109121.
Srygley, R.B., Dudley, R., Olveira, E.G., Aizpra, R., Pelaez, N.Z., Riveros, A.J., 2010. El
Nio and dry season rainfall inuence host plant phenology and an annual
buttery migration from Neotropical wet to dry forests. Global Change Biology
16, 936954.
Stireman, J.O., Dyer, L.A., Janzen, D.H., Singer, M.S., Lill, J.T., Marquis, R.J., Ricklefs,
R.E., Gentry, G.L., Hallwachs, W., Coley, P.D., Barone, J.A., Greeney, H.F., Connahs,
H., Barbosa, P., Morais, H.C., Diniz, I.R., 2005. Climatic unpredictability and
parasitism of caterpillars: implications of global warming. Proceedings of the
National Academy of Sciences of the United States of America 102, 17384
17387.
Stireman, J.O., Greeney, H.F., Dyer, L.A., 2009. Species richness and host associations
of Lepidoptera-attacking Tachinidae in the northeast Ecuadorian Andes. Journal
of Insect Science 9, 119.
1841
Stocks, G., Seales, L., Panlagua, F., Maehr, E., Bruna, E.M., 2008. The geographical and
institutional distribution of ecological research in the tropics. Biotropica 40,
397404.
Stork, N.E., 2007. Biodiversity: world of insects. Nature 448, 657658.
Stork, N.E., Srivastava, D.S., Watt, A.D., Larsen, T.B., 2003. Buttery diversity and
silvicultural practice in lowland rainforests of Cameroon. Biodiversity and
Conservation 12, 387410.
Straatman, R., 1962. Notes on certain Lepidoptera ovipositing on plants which are
toxic to their larvae. Journal of the Lepidopterists Society 16, 99103.
Thomas, C.D., 1991. Habitat use and geographic ranges of butteries from the wet
lowlands of Costa Rica. Biological Conservation 55, 269281.
Thomas, J.A., 2005. Monitoring change in the abundance and distribution of insects
using butteries and other indicator groups. Philosophical Transactions of the
Royal Society B: Biological Sciences 360, 339357.
Thomas, C.D., Cameron, A., Green, R.E., Bakkenes, M., Beaumont, L.J., Collingham,
Y.C., Erasmus, B.F.N., de Siqueira, M.F., Grainger, A., Hannah, L., Hughes, L.,
Huntley, B., van Jaarsveld, A.S., Midgley, G.F., Miles, L., Ortega-Huerta, M.A.,
Peterson, A.T., Phillips, O.L., Williams, S.E., 2004. Extinction risk from climate
change. Nature 427, 145148.
Tiple, A., Agashe, D., Khurad, A.M., Kunte, K., 2009. Population dynamics and
seasonal polyphenism of Chilades pandava buttery (Lycaenidae) in central
India. Current Science 97, 17741779.
Tolman, T., Lewington, R., 2008. Collins Buttery Guide: The Most Complete Field
Guide to the Butteries of Britain and Europe. Harper Collins, London.
Turner, J.R.G., 1971. Two thousand generations of hybridisation in a Heliconius
buttery. Evolution 25, 471482.
Turner, J.R.G., 1981. Adaptation and evolution in Heliconius: a defense of
NeoDarwinism. Annual Review of Ecology and Systematics 12, 99121.
Uehara-Prado, M., Freitas, A.V.L., 2009. The effect of rainforest fragmentation on
species diversity and mimicry ring composition of ithomiine butteries. Insect
Conservation and Diversity 2, 2328.
Uehara-Prado, M., Brown, K.S., Freitas, A.V.L., 2007. Species richness, composition
and abundance of fruit-feeding butteries in the Brazilian Atlantic Forest:
comparison between a fragmented and a continuous landscape. Global Ecology
and Biogeography 16, 4354.
Valentini, A., Pompanon, F., Taberlet, P., 2009. DNA barcoding for ecologists. Trends
in Ecology and Evolution 24, 110117.
van Swaay, C.A.M., Nowicki, P., Settele, J., van Strien, A.J., 2008. Buttery monitoring
in Europe: methods, applications, and perspectives. Biodiversity and
Conservation 17, 34553469.
Vasconcellos-Neto, J., 1991. Interactions between Ithomiine butteries and
Solanaceae feeding and reproductive strategies. In: Price, P.W., Lewinsohm,
T.M., Fernandes, G.W., Benson, W.M. (Eds.), PlantAnimal Interactions:
Evolutionary Ecology in Tropical and Temperate Regions. Wiley-Interscience,
New York.
Wagner, D.L., Van Driesche, R.G., 2009. Threats posed to rare or endangered insects
by invasions of nonnative species. Annual Review of Entomology 55, 547568.
Wahlberg, N., Leneveu, J., Kodandaramaiah, U., Pea, C., Nylin, S., Freitas, A.V.L.,
Brower, A.V.Z., 2009. Nymphalid butteries diversify following near demise at
the cretaceous/tertiary boundary. Proceedings of the Royal Society B: Biological
Sciences. doi:10.1098/rspb.2009.1303.
Wallace, A.R., 1865. On the phenomena of variation and geographical distribution as
illustrated by the Papilionidae of the Malayan region. Transactions of the
Linnean Society of London 25, 171.
Wallace, A.R., 1879. The Geographical Distribution of Animals. Macmillan,
London.
Whinnett, A., Zimmerman, M., Willmott, K.R., Herrera, N., Millarino, R., Simpson, F.,
Joron, M., Lamas, G., Mallet, J., 2005. Strikingly variable divergence times
inferred across an Amazonian buttery suture zone. Proceedings of the Royal
Society B: Biological Sciences 272, 25252533.
Wolda, H., 1978. Fluctuations in abundance of tropical insects. American Naturalist
112, 10171045.
Wolda, H., 1988. Insect seasonality why? Annual Review of Ecology and
Systematics 19, 118.
Wood, B., Gillman, M.P., 1998. The effects of disturbance on forest butteries using
two methods of sampling in Trinidad. Biodiversity and Conservation 7, 597
616.
Yoccoz, N.G., Nichols, J.D., Boulinier, T., 2001. Monitoring of biological diversity in
space and time. Trends in Ecology and Evolution 16, 446453.