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General introduction: In which I attempt to briefly put the present thesis in a
historical, global, social and scientific context.
Background:
Life on earth may have started as early as 3.5 billion years ago (Brasier et al. 2002,
Schopf et al. 2002, Furnes et al. 2004, Kerr 2004) and since that time many new life
forms have evolved, flourished and gone extinct. Insects appeared about 300 million
years ago, and the Lepidoptera (the order in which butterflies are placed) some 100
million years ago (Gaunt & Miles 2002), whilst our species, Homo sapiens sapiens,
appeared only about 150,000 years ago (Shields 2000). We are a species with an
intellectual capacity and cultural development that has added a new dimension to
evolution since we can consciously strive to manage our own and other species to
persist for many generations to come.
Man has had a dramatic influence on the ecosystems on earth and will
continue to do so (Houghton et al. 2001). To which degree and how this will
influence the human population itself is still unclear, but an important negative impact
can be expected as ecosystems and the biodiversity therein provide invaluable
services (Myers 1996, Gitay et al. 2001). One disputable point may be the intrinsic
value of biodiversity: perhaps extinction is likely to be followed by a new round of
diversification with evolution of life forms that would be equally valuable and
interesting.
With this in mind and considering the intellectual capacities and cultural
development noted in man, it may seem surprising that most people are more
concerned with the short term (Lagerspetz 1999). In most cases however, poverty or
suppressive regimes can easily explain this, since they form a more imminent life
threat. Perhaps more surprisingly, many well-off people in developed countries also
prefer a short-term approach and occasionally attempt to back this up with corrupted
data presented as real science (Pimm & Harvey 2001, Wilson et al. 2001).
If natural ecosystems and biodiversity are to be maintained, serious
conservation measures have to be taken. This requires awareness of the problem and
funding for conservation efforts, as well as knowledge on the structure and spatial
distribution of this biodiversity to allocate funding and effort efficiently (Peuhkuri &
Jokinen 1999). Therefore, studies that enhance our understanding of ecosystem
functioning and biodiversity that potentially lead to predictions on how ecosystems
will react to expected changes or management efforts are of critical importance for
conservation. However, in the current age of artificial intelligence, human genomics,
perceptual robotics, flow visualisation, advanced astrophysics and other high-tech
wizardry, it is both disturbing and ironic that our understanding of vital ecological
processes is rudimentary (Harvey 2001).
Tropical forests
Tropical forests have been identified as major hotspots of biodiversity (Myers et al.
2000), and especially the canopy is thought to harbour a diverse and poorly known
fauna and flora (Basset 2001, Mitchell 2001, Stork 2001). However, the area of
tropical forest has decreased rapidly over recent decades and most forests are subject
to disturbance. Undisturbed forest will soon be confined to isolated reserves
surrounded by cultivated land (FAO 1999).
Most tropical forests are situated in developing countries where the awareness
of the value and vulnerability of biodiversity is generally low, government budgets
are limited, and human pressure on the land is high. According to the
Intergovernmental Panel on Climate Change (McCarthy et al. 2001), third world
countries are especially vulnerable to global change due to their poor economic
development and stability, and a generally low level of knowledge. However,
sacrificing the National Parks in Uganda to agriculture, for example, will only
compensate for 1.5 years of population growth, whilst at the same time diminishing
the possibilities for eco-tourism, not to mention the loss of ecosystem services.
The governments of most countries are to some degree aware of the value of
wilderness areas and do protect them. However, such protected areas cost more than
the income they generate and aid from western donors who appreciate their more
global value will be necessary (Balmford et al. 2000, Balmford et al. 2002, Balmford
et al. 2003, Balmford & Whitten 2003, Williams et al. 2003). Law enforcement is of
critical importance to the effectiveness of protective measures, even though some
local use may well be sustainable (Gordon & Ayiemba 2003). Sadly, political
instability and corruption can easily lead to periods of anarchy in which poaching and
habitat degradation flourish (Draulans & Van Krunkelsven 2002). So, conservation of
biodiversity can not be viewed independently of global policies that affect peace,
good governance and development (Kahn & McDonald 1995, Pimentel et al. 1997,
Avery 1998, Haila 1999, Swanson 1999, Kremen et al. 2000, Campbell & VainioMattila 2003).
Sustainable development is a key concept in this discussion. This is defined
as: “development that meets the needs of the present without compromising the ability
of future generations to meet their own needs”, noting that: “even the narrow notion
of physical sustainability implies a concern for social equity between generations, a
concern that must logically be extended to equity within each generation”
(Brundtland Commission; WCED, 1987). The goal of sustainable development is a
stable human environmental system in which available resources are sufficient to
meet the needs of society in perpetuity. Questions have been asked about whether
“needs,” as conceived in the Brundtland Commission report, should be limited to
basic necessities of food, clothing, shelter, and health or should include more
qualitative aspects such as comfort, convenience, or other “quality of life” measures.
There is no consensus in the literature regarding what constitutes the limits of “needs”
in this context.
Extinction and rarity:
Insights from both evolutionary biology and ecology are necessary to understand
biodiversity. The number of species in the world is the outcome of both speciation
and extinction. Speciation is mostly viewed as an evolutionary process which takes
place in an ecological arena, whilst extinction is usually viewed from an ecological
perspective where evolved traits clearly play an important role.
Palaeontology has demonstrated that diversification and extinction rates have
varied considerably through time, with mass extinction’s followed by diversification.
The study of biogeography has made major contributions to our appreciation of how
migration between continents and from continents to islands shaped biodiversity on a
taxonomic level. To explain biodiversity on a local scale, immigration can be added to
the key-factors of speciation and (local) extinction. One successful approach in
describing the outcome of immigration and local extinction is found in island biology.
The distance of an ‘island’ to a source area can largely explain immigration rate
whilst the size of the island can predict the extinction rate. These ‘islands’ can be
habitats of different types and scales, including forest patches and lakes.
Extinction rate can be viewed as a function of size and stability (amount of
fluctuation) of populations (Hanski 2003). The size of a population is dependent on
the area of the habitat, and also on the population density, which again depends on the
ecology and life history of the species. The stability of a population can depend on a
host of biotic and abiotic factors, and also on the life history. Moreover, genetic
diversity plays a role in the capacity of a species to adapt to a changing environment
and genetic health in general (Frankham et al. 2004).
Natural selection results in adaptation of a species to the environment.
However, when the environment changes, the amount of pre-adaptation of the present
species to this new environment can depend largely on chance. Generalist species are
more likely to be pre-adapted to a new environment than are specialists. Therefore,
from a long-term evolutionary perspective, specialisation can be viewed as a dead
end, even though selection can temporarily favour specialisation in a particular
location.
From a conservationist’s perspective, it is important to know why certain
species have low abundances and limited geographical ranges, and thus why they
have a more threatened status. Surprisingly few studies address this question
systematically. These studies include those in mosses (Cleavitt 2002, Heinlen & Vitt
2003), higher plants (Bevill & Louda 1999, Hegde & Ellstrand 1999, Gitzendanner &
Soltis 2000, Kelly et al. 2001, Cadotte & Lovett-Doust 2002, Lloyd, Lee & Wilson
2002b, a, Rogers & Walker 2002), insects (Didham et al. 1998, Malmqvist 2000,
Lewis 2001), fish (Dulvy, Sadovy & Reynolds 2003), and primates (Harcourt,
Coppeto & Parks 2002). Plant species with narrow geographical distributions were
found to produce significantly fewer seeds (per unit measurement) than common
species (in four of six studies), but did not differ with respect to breeding system (five
of five studies). The majority of traits (including seed size, competitive ability, growth
form and dispersal mode) were related to rarity in different ways from one study to
the next.
Studies on butterflies and aquatic insects have suggested that species with a
restricted distribution tended to have limited dispersal behaviour or abilities (Hill et
al. 1995, Lewis, Wilson & Harper 1998, Malmqvist 2000). However, data on leaf
litter beetles showed that rarer species are predicted to be better dispersers, and more
likely to persist in a given habitat. In this case, rarity and population variability (in
undisturbed forests) were significant predictors of susceptibility to fragmentation.
Common species were significantly more likely to become locally extinct in small
fragments than rarer species, lending empirical support to models of multi-species
coexistence under disturbance that suggest competitively dominant but poorly
dispersing species are the first to become extinct due to habitat destruction (Didham et
al. 1998). Studies on invertebrate herbivore communities in a forest in Papua New
Guinea indicated that host-plant specialization did not affect rarity (Novotny & Basset
2000). In primates however, specialization was the only trait that correlated with
rarity (Harcourt et al. 2002).
The highly context-dependent nature of most trait relationships with rarity
implies that application of knowledge concerning rare-common differences and
similarities to management plans will vary substantially for different organisms,
vegetation types, and possibly among different continents. This is a serious problem
for management decisions in the light of scant data.
Evolution
The process of diversification and speciation, the source of biodiversity, has received
ample attention from biologists. Evolutionary biologists are currently very successful
in the application of new molecular and population genetical techniques that have
become available. These studies investigate how natural selection together with
constraints affects adaptive evolution and speciation.
An important field within evolutionary biology is life history evolution.
Among species, growth and reproduction occur at different rates with different
timing, and result in, for example, differences in adult size. Central to life history
theory is the distribution of energy, time and nutrients to maintenance, storage,
growth and reproduction (Stearns 1992). The possible allocation of resources
obviously depends on these resources themselves, and diet is, therefore, an important
factor in life history. A diet shift is, therefore, likely to be accompanied by life history
evolution. To elucidate such relations, one can compare different clades in which a
similar diet shift has occurred. For example, it is striking that filter-feeding in marine
vertebrates is found in the largest species of sharks, rays and whales. Possibly,
plankton is a rich food-source that facilitated the evolution of large adult sizes.
Additionally, the strength and nature of nutritional constraints within a species can be
studied by manipulation of the diet and exploring plastic responses.
Fruit-feeding in butterflies provides an example of diet shifts that are
accompanied by changes in nutritional ecology, since the quality and spatial and
temporal availability of fruits differs from that of nectar. In this thesis, data are
presented on nutritional ecology of fruit-feeding butterflies in the field (chapters 3, 4
and 6), whilst most of the life history data still await analysis. Additionally, we
performed three experiments in which we manipulated the protein (chapter 5) and
sodium content (chapter 7) of the adult diet of the small fruit-feeding tropical butterfly
Bicyclus anynana and measured lifespan and egg-production.
Within research in evolutionary biology, sexual selection takes an important
place. However, sexual differences can also have an ecological background. Sexual
differences give an extra dimension to diversity and often diversify the habitat use of
a species. A fine example can be found in hummingbirds where the sexes can have
different bill morphologies, each adapted to a certain flower type (Temeles et al.
2000). If this species had split into two species with their own flower specialisation,
both populations would presumably be of about one-half the size of the current
population and thus be more prone to extinction.
Butterflies provide excellent examples of sexual dimorphism, and in the field
it can be difficult to match males and females of the same species. The feeding
behaviour of males and females can differ too. Generally, male butterflies are more
often trapped on fruit baits, possibly because they feed more frequently (Fermon,
Waltert & Muhlenberg 2003), and in many species, males are almost exclusively the
only sex to puddle (= feeding on mud, dung or carrion). In this thesis, I will discuss
sexual size dimorphism and mating system in relation to possible functions of
puddling behaviour in a community of fruit-feeding butterflies (Chapter 6).
Ecology
Despite extreme geographical variation in species composition, some similarities in
patterns of biodiversity can be found in similar habitats on different continents. This
indicates that ecological processes have substantial effects on patterns in biodiversity.
However, it is still poorly understood to what extent and how fundamental biotic
interactions, such as competition, facilitation and trophic interactions, determine
community patterns (Peres-Neto 2004). Such information is essential for
understanding the effects of disturbance, and with massive anthropogenic global
disturbance, highly relevant for conservation (Harvey 2001). The complexity of
ecosystems is so high that science has only begun to understand how the food webs,
nutrient cycles and physical traits of an ecosystem interact. Two approaches can be
distinguished: investigating community patterns in time and space for complete
guilds, and case studies of focal taxa. In this thesis, vertical and temporal patterns in
abundance and biodiversity of fruit-feeding butterflies are described (Chapter 2).
These data will later be used by Prof. Russel Lande (San Diego) and Prof. Steinar
Engen (Oslo) to estimate to what degree the fruit-feeding butterfly community is
structured in time and space.
The description of temporal and spatial diversity patterns of tropical
Lepidoptera has now reached a stage where the search for causal explanations should
be intensified. Some phenomena that have been recognised as important to
understanding patterns in biodiversity will be elaborated on below in relation to this
thesis.
Specialisation is expected to be accompanied by efficient resource use and
high competitive abilities on the specific resource, as well as by superior defence
against natural enemies. However, generalists need less time to find suitable resources
and may adapt more easily to a changing environment. It has long been believed that
the high diversity of insects in tropical forest is due to high floral diversity and high
levels of specialisation (Owen 1966). However, recent studies have shown that
catholic food choice is common amongst herbivorous insects in tropical forests, and
tropical Lepidoptera are no more host-specific than temperate species (Basset &
Burckhardt 1992, Fiedler 1998, Novotny et al. 2002).
In the case of butterflies, host-plant specialisation is most likely to be
associated more with natural enemies than with competition, since caterpillar
densities are usually low. Although it was not a prime goal of the project, we found a
host-plant specialist, Gnophodes chelys (Satyrinae), that was particularly well
camouflaged on the stripy leaves of its host-plant (Setaria poiretiana). I monitored the
reproduction of this species and two students, Mechteld van Dijk and Peter Boons,
have made more detailed surveys of parasitoid loads in eggs and larvae. The results
showed that almost all eggs are laid in a four-week period at the beginning of the
rainy season. By the time the parasitoids can develop a second generation, very few
caterpillars are available, and these few late caterpillars are typically parasitised.
These findings are in accordance with the idea that parasitoids can be a selective force
in the evolution of seasonal reproduction in environments where the seasonality of
plant availability is not very marked. In this butterfly species, other life history traits
facilitate the evolution of seasonal reproduction, including the large egg-batches that
reduce the host-plant searching time (only one host-plant is needed), and the large
host-plant that allows for large egg-batches. This could potentially be an example of
how life history and trophic interactions together affect the phenology of individual
species and thus community dynamics. It would be interesting to know to what extent
predator and parasitoid faunas’ overlap between butterfly species, plants and habitats,
and thus how these natural enemies connect butterfly species ecologically.
Indications for host-plant specialisation were also found in Euphaedra
species, with typically one host-plant species recorded. The caterpillars of one
gregarious Euphaedra species possess clear warning colours, a phenomenon
commonly associated with sequestration of toxins from particular host-plants.
Adult butterflies may be specialised with respect to feeding substrates,
particular patterns of activity levels during the day, and phenology. Occasionally,
butterflies fight over specific fruit-items. However, this occurs when both fruits and
butterflies are plentiful and it may just save time for an individual to chase another
butterfly, instead of seeking a suitable fruit. It may, therefore, not qualify as a pure
example of competition. Aggregations on dung and carrion seem more peaceful, even
though the strongly-build species of Charaxes may dominate, displacing others by
sudden, powerful, wing-flaps. I collected some data on conflicts over fruits, but these
are beyond the scope of this thesis.
Competition may be avoided by differences in adult food-choice. Food-choice
is linked with intake rates, and thus with mouthpart morphology. In fruit-feeding
butterflies two different feeding techniques are distinguished. In collaboration with
Harald Krenn (Vienna) and Monique van Alphen, I investigated the proboscis
morphology and feeding efficiency of fruit-feeding butterflies species that use each of
these feeding techniques. I reflected on possible associations between proboscis
morphology and food-choice, as well as on their evolutionary consequences (Chapter
3). Food choice was investigated for both fruit-feeding and puddling in this guild.
With Maartje Liefting and Roy van Grunsven, I collected data on puddling behaviour
(Chapter 6), and with Monique van Alphen on the relative attractiveness of fruits for
different groups of butterflies (Chapter 4). To which extent variation in adult food
preferences (and associated morphologies and behaviours) is a result of interactions
between species remains, however, unclear. My data on activity levels during the day
and on phenology (Kop et al. in preparation) do not appear in this thesis.
An interesting example of how habitat preferences affect species turnover in a
disturbance gradient has been found in forest butterflies (Hamer et al. 2003). Whilst
in primary forest both very shady patches and light gaps occur, secondary forests are
shaded. Recently (selectively) logged forest consists mostly of light gaps. Therefore,
logging was shown by Hamer et al. (2003) to lead to a butterfly fauna that is poor in
light gap specialists. Their study highlights the need to sample at a sufficiently large
spatial scale to account for the impacts of disturbance on heterogeneity in forest
environments. It also demonstrates how understanding the responses of species to
natural variation in environmental conditions within undisturbed forest is crucial to
interpreting responses of species to anthropogenic habitat modification. The results
further indicate that selectively logged forests can make an important contribution to
the conservation of tropical biodiversity, provided that they are managed in a way that
maintains environmental heterogeneity.
The opposite of competition, namely facilitation and symbiosis can also
influence biodiversity. Detailed studies of larval associations with ants, use of
warning colours and mimicry are popular among evolutionary biologists and have
contributed to our understanding of biodiversity. The function of butterfly colour
patterns has fascinated biologists for centuries and studies on mimicry (a form of
facilitation) in butterflies have a long tradition. Butterflies can be cryptic or possess
warning colours or predator deflections. Central in the theory of mimicry is the cooccurrence of models and mimics in time and space in particular proportions. In
tropical forests, complex mimicry rings are present, probably based on differences in
palatability or agility in which the two sexes can often play different roles. Especially
in butterflies, understanding this inter-relatedness could be crucial to understanding
community composition and its change along disturbance gradients. For achieving
this goal, detailed studies have to be supplemented by community wide monitoring of
butterfly abundance in time and space and quantification of key traits such as colour
patterns, flight characteristics and palatability.
This thesis aims to contribute to the unravelling of ecological complexity and
to understand better how ecosystems evolve, how they assemble themselves, and how
they function. The research is carried out at different levels ranging from description
of patterns in biodiversity, to experiments in nutritional ecology. This approach is
essential to close the gap between the study of macro-ecological and individual level
processes, so that we can better understand how the complex biosphere has emerged
from processed operating on the scale of individual organisms.
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