Download Causes behind insect folivory patterns in latitudinal gradients

Journal of Ecology 2011, 99, 367–369
doi: 10.1111/j.1365-2745.2010.01707.x
FORUM
Causes behind insect folivory patterns in latitudinal
gradients
Christer Björkman1*, Åsa Berggren1,2 and Helena Bylund1
1
Department of Ecology, Swedish University of Agricultural Sciences, PO Box 7044, SE-750 07 Uppsala, Sweden;
and 2Swedish Species Information Centre, Swedish University of Agricultural Sciences, PO Box 7007, SE-750 07
Uppsala, Sweden
Summary
1. Adams and Zhang recently published one of the best studies so far of patterns of insect folivory
along a latitudinal (climatic) gradient. They show clear negative trends in foliage loss in relation to
temperature for certain groups of insect herbivores.
2. Although their suggestion that the plant–herbivore interaction may be more important in cooler
climates could be valid, they did not bring up the complementary explanation that interactions
between predators and herbivores could also vary with climate. There are indications that insect
natural enemies may respond more positively than insect herbivores to an increase in temperature.
We argue that higher predator pressure in warmer climates may partly explain the patterns
observed by Adams and Zhang.
3. Synthesis. To further develop the important research concerning herbivory in a changing
climate, both theoretically and empirically, plant ecologists and entomologists would mutually
benefit from joining forces.
Key-words: climate, herbivory, plant–herbivore interactions, temperature, trophic interactions
The hypothesis that herbivore damage should be higher in
warmer climates (e.g. Coley & Barone 1996), predicting that
climate warming should lead to more herbivory at a given
latitude (Wolf, Kozlov & Callaghan 2008), was recently
questioned by Adams & Zhang (2009). The authors made a
survey of levels of insect folivory on a subset of common tree
species over a latitudinal gradient along the North American
east coast. The results clearly showed negative relationships
between foliage loss (%) and temperature; the r-values,
including trends with P-values < 0.07, ranged between
)0.243 and )0.695. Similar results have been reported elsewhere (e.g. Lowman 1984), but there are examples showing
opposite trends (Coley & Barone 1996) and the most common observation seems to be no trends (e.g. Andrew &
Hughes 2005; Sinclair & Hughes 2008). The study by Adams
& Zhang (2009) is one of the best of its kind, partly because
the authors distinguish between damage caused by different
types of insect herbivores, which has not been done in any
of the previous studies. In addition, the study was repeated
in time over 2 years. Still, Adams & Zhang (2009) neglects
*Correspondence author. E-mail: [email protected]
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one important aspect, i.e. the possible role of the herbivores’
natural enemies, an important factor that can partly explain
the observed pattern.
The theoretical framework referred to in Adams & Zhang
(2009) focuses on plant–herbivore interactions and the evolution of plant defences. The third trophic level is mentioned but
without reflecting on how temperature might influence predators, parasitoids or diseases. To not consider the influence of
higher trophic level is unexpected, especially as the link
between plants, herbivores and natural enemies has long been
recognized (Lawton & McNeill 1979; Price et al. 1980). It is
likely that different trophic levels respond differently to the
same climate change (Voigt et al. 2003). In some cases, there is
evidence indicating that plants respond more than herbivores
and that the response to temperature becomes more indirect
further up in the food chain (Forchhammer et al. 2008). However, these patterns have been found in studies of mammals
and birds. When we consider insects, as is the case here, and in
the study Adams & Zhang (2009), a different pattern emerges:
plants respond least, (insect) herbivores intermediately and
natural enemies the most to the same temperature change
(Dunn 1952; Campbell et al. 1974; Virtanen & Neuvonen
1999; van Nouhuys & Lei 2004; ). Acknowledging these findings, we have recently developed a conceptual model where the
anticipated response of all three trophic levels to climate
Ó 2010 The Authors. Journal of Ecology Ó 2010 British Ecological Society
368 C. Björkman, Å. Berggren & H. Bylund
change is presented (Berggren et al. 2009). When viewing the
observations by Adams & Zhang (2009) from this perspective,
their findings can at least partly be explained from a higher
pressure from natural enemies on herbivores in warmer climates. However, the observed amount of folivory would
depend on the temperature response of each species involved
in the tritrophic interaction. In addition, regional climate may
affect plant quality, which in turn affects the success of insect
natural enemies (e.g. effects of immune competence, Haviola
et al. 2007; Klemola et al. 2007).
To what extent there is a fundamental difference between
different groups of herbivores and predators (mammals, birds
and insects) and how they interact with plants and their
response to temperature needs further investigation. Largescale analyses including a vast array of taxonomical groups
give a mixed picture. For example, Root et al. (2003) found
that during the last decades non-tree plants showed a stronger
phenological shift in spring than trees, whereas invertebrates
and particularly birds showed a stronger phenological
response than plants. Although broad-scale comparisons over
many systems and taxonomical groups give important insights
about trends and thus function as early warning signals (Walther et al. 2002), a more mechanistic understanding and better
predictive ability is more likely to be achieved by in-depth studies of specific systems.
If we have the ambition to make predictions about how climate change might influence herbivore damage in the future,
an understanding of the causes behind patterns of herbivory in
relation to climate is crucial. We suggest that novel attempts to
look for patterns in insect herbivory over climatic gradients
should also include estimates of responses at the third trophic
level. How this should be studied more explicitly will depend
on the systems involved. Cage experiments could be used in
many cases where the access of natural enemies to the cages is
manipulated, to study the survival and performance of common insect herbivores that occur in the whole study area. This
would give an estimate of plant quality effects and predator
pressure in the area. The impact of different natural enemies
(e.g. predators and parasitoids) can be separated with cleverly
designed experiments that involve different types of cages. To
use the cage method for estimating the relative contribution of
bottom-up and top-down effects properly, one has to account
for possible non-additive effects (Moreau et al. 2006). An
alternative method is to experimentally study the disappearance rate of individuals in different introduced insects’
life-stages (eggs, larvae or pupae) in a range of study sites.
However, these two methods mainly measure the pressure
from predation and miss the effect of parasiotoids and disease.
Despite this, predation pressure may be a good enough measure of interactions with a third trophic level, considering the
fact that it has recently been recognized that the combined
effect of several species of generalist predators may actually
regulate the densities of many insect herbivores (Symondson,
Sunderland & Greenstone 2002). To date, there are very few
studies on how trophic interactions are affected by temperature in terrestrial habitats. A well-designed experiment –
involving two plant types (herbs and grasses), one dominant
herbivore (grasshopper) and two common predators (spiders)
showed that experimental warming strengthened the effect of
single predators (Barton & Schmitz 2009). Eventually, intraguild predation leads to the extinction of one of the spider species. A loss of predator diversity as a consequence of warming
may have large consequences for the function and the stability
of food webs.
Even more could be gained in our understanding of patterns
of folivory if we knew the species involved. It would then be
possible to study leaf damage at the edge of the distribution
area of the plants, and from the colonizations and re-colonizations of herbivores, predators and parasitoids in these patches
we would acquire a greater understanding of the dynamics of
the different trophic levels. A carefully planned study would
make it possible to unearth the mechanisms behind the
observed insect folivory in different climates.
If theories on abiotic effects on biotic interactions of plant
and insects were incorporated in studies on climate effects, we
would achieve a greater understanding of how herbivores and
their predators affect plant systems in a changing climate. We
therefore emphasize the importance and benefits of greater collaboration between entomologists and plant ecologists. Such
collaborations are becoming increasingly valuable as interactions between changes in climate and land-use patterns result
in complex system responses.
Acknowledgements
Matt Low provided valuable comments and corrected the English. Financial
support was provided by the MISTRA-project ‘‘Future Forests’’ and the EUproject ‘‘BACCARA’’.
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Received 21 January 2010; accepted 28 June 2010
Handling Editor: Martin Heil
Ó 2010 The Authors. Journal of Ecology Ó 2010 British Ecological Society, Journal of Ecology, 99, 367–369