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Population ecology
rsbl.royalsocietypublishing.org
Response of insect parasitism to elevation
depends on host and parasitoid lifehistory strategies
Christelle Péré1,2,3, Hervé Jactel2,3 and Marc Kenis1
Research
1
CABI, 2800 Delémont, Switzerland
University of Bordeaux, BIOGECO, UMR1202, 33400 Talence, France
3
INRA, BIOGECO, UMR1202, 33610 Cestas, France
2
Cite this article: Péré C, Jactel H, Kenis M.
2013 Response of insect parasitism to elevation
depends on host and parasitoid life-history
strategies. Biol Lett 9: 20130028.
http://dx.doi.org/10.1098/rsbl.2013.0028
Received: 10 January 2013
Accepted: 22 May 2013
Subject Areas:
ecology
Keywords:
parasitoids, elevation gradient, global
warming, meta-analysis
Author for correspondence:
Marc Kenis
e-mail: [email protected]
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rsbl.2013.0028 or
via http://rsbl.royalsocietypublishing.org.
How global warming will affect insect parasitoids and their role as natural
enemies of insect pests is difficult to assess within a short period of time.
Considering that elevation gradients can be used as analogues for global
warming, we carried out meta-analyses of 27 correlations between parasitoid richness and elevation and 140 correlations between parasitism rate
and elevation in natural and semi-natural environments. We also explored
various covariates that may explain the observed responses. Both parasitism
rates and parasitoid species richness significantly decreased with increasing
elevation. The decrease was greater for ectoparasitoids and parasitoids of
ectophagous insects than for endoparasitoids and parasitoids of endophagous hosts, possibly because these latter are better protected from adverse
and extreme climatic conditions occurring at higher elevations. Although
our results suggest an increase of parasitism with increasing temperature,
other factors regulating herbivorous insects have to be considered before
concluding that climate warming will lead to a decrease in pest density.
1. Introduction
Parasitoids play an essential role in regulating insect populations and preventing pest outbreaks. Climate change will affect their action, either through a
direct effect on their life cycle or through disturbance of trophic interactions
with their host insects and host plants [1,2]. Recent reviews have suggested
that climate change will increase the incidence of insect pests, particularly via
increased population growth and reduced plant resistance [3]. The same studies
pointed out that increasing temperature might also benefit natural enemies and
thus negatively affect herbivores but failed to estimate the strength of this topdown effect due to lack of data. Furthermore, life-history traits can affect host
and parasitoid species and community responses to climate. For example, we
may expect different responses by ecto- versus endoparasitoids (i.e. the larval
stage of the parasitoid develops outside or inside the herbivorous host body,
respectively) and ecto- versus endophagous hosts (i.e. the larval stage of the
herbivorous insect develops externally on the plants or within plant tissues,
respectively) because of differences in exposure to weather.
A major issue in studying ecological effects of climate change is the slowness
of the process. Ideally, observations should be made over decades, which is rarely
possible. Elevation gradients are a powerful tool for testing ecological responses of
biota to geophysical influences such as temperature [4], and the influence of changing environment experienced along such gradients has been suggested as
analogous to climate warming [5,6]. Hodkinson [6] provided a series of examples
where parasitism was measured along elevation gradients. In most cases, parasitism declined with increasing elevation, possibly because of low temperature
affecting the survival and behaviour of parasitoids at higher elevations. These
& 2013 The Author(s) Published by the Royal Society. All rights reserved.
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We searched published studies reporting (i) species-specific parasitism rates of herbivorous insects and (ii) species richness of
parasitoid complexes of herbivorous insects, at different elevations
in bibliographic databases, using the combination of ‘parasit*’ and
‘insect’ and (‘altitud*’ or ‘elevation*’ or ‘mountain’). We also
surveyed the references cited in the relevant articles and
unpublished CABI reports.
Studies were included in the meta-analyses if they met the following criteria: (i) parasitism rates were reported by individual
parasitoid species or genus, or number of parasitoid species, in
at least four different elevations separated by a distance of less
than 250 km with elevation range of more than 300 m, or a distance of less than 50 km with elevation range of more than
100 m; (ii) parasitism rates were based on at least 10 individuals;
(iii) parasitoid and host species were native to the study area
and studies were carried out in a natural or semi-natural ecosystem (grasslands, scrublands or woodlands) to capture natural
responses to elevation; and (iv) parasitoid richness varied among
elevations by at least two species.
This resulted in the selection of 32 publications that
accounted for 140 parasitoid species-specific responses to
elevation gradients and 20 publications that reported on parasitoid species richness changes along 27 elevation gradients (see
the electronic supplementary material, appendix S1 and references in appendix S2). Most of the studies were from central
Europe, reflecting a lack of data from other regions in the
world, notably in the tropics (electronic supplementary material,
appendix S3).
In many cases, the parasitism rates of several parasitoid species
were reported for the same insect herbivore within the same
elevation gradient. These particular response patterns are not
truly independent. We therefore calculated an averaged effect
size at the insect herbivore elevation gradient level (n ¼ 36)
using the method proposed by Borenstein et al. [9] for multiple comparisons within a study. The outcome was similar to that obtained
with the complete dataset (electronic supplementary material,
appendix S4a). To keep the maximum of information and benefit
from higher statistical power, we therefore decided to use the 140
parasitoid species-specific response patterns.
We quantified the relationship between parasitism rate or
parasitoid species richness and elevation by using correlation
coefficient (r) and regression slope values (b) (electronic supplementary material, appendix S5). We systematically extracted
numerical values from tables or by digitizing figures and plotted
simple linear regressions.
coefficient of correlation, r
0.6
0.4
0.2
0
–0.2
–0.4
–0.6
2
–0.8
–1.0
–1.2
Figure 1. Coefficients of correlation (r) between the species richness of parasitoids and elevation (n ¼ 27 elevational gradients). Each bubble represents one r
value, the diameter of the bubble is proportional to its weight in the meta-analysis (inverse of variance). The dashed line represents the grand mean effect size
(20.31), and the shaded area represents the bootstrap confidence interval.
We tested the effect of four covariates on the magnitude of
the relationship between parasitism rate or parasitoid species
richness and elevation: (i) herbivore-feeding strategy: herbivorous
hosts of the parasitoids were defined as ‘ectophagous’ (e.g.
chewers, skeletonizers, leaf-rollers, leaf-tiers and sap-feeders) or
‘endophagous’ (e.g. leaf-miners, gall-makers, cone, seed and
fruit insects, bark and root borers); (ii) parasitoid-feeding strategy:
parasitoids were classified as ‘ectoparasitoids’ or ‘endoparasitoids’;
(iii) latitude of the lower median step of the elevation gradient; (iv)
mean annual temperature of the mean elevation of the gradient,
extracted from the WorldClim database at 1 km spatial resolution
[10]. To avoid problems associated with confounding factors, we
tested hierarchically the effect of parasitoid-feeding strategy
within each type of host-feeding strategy and then the effect of latitude and temperature within the four categories of host parasitoid-feeding strategies [11].
We also tested other attributes for each parasitoid species,
including host stage attacked or killed (egg, larval, pupal and
adult), parasitoid taxonomy (Diptera versus Hymenoptera),
development mode of parasitoid (koinobiont, i.e. parasitoid
that allows the host to continue its development after being
parasitized versus idiobiont, i.e. parasitoid that permanently
paralyzes the host and thereby prevents any further development
of the host) and the range of elevations (difference between the
highest and the lowest elevations).
We used a mixed-effect model to assess between-class heterogeneity (for each categorical covariate, i.e. host and parasitoid
types) and to evaluate the significance of the class effect [12],
assuming a fixed effect across classes and a random effect
within classes [9]. The weighted mean effect size and a biascorrected bootstrap confidence interval (CI) were then calculated
for each class of covariate. Effects were considered statistically
significant if the 95% bias-corrected bootstrap CI calculated
with 9999 iterations did not include zero. We checked the dataset
for publication bias with the weighted Rosenthal’s fail-safe
number [13] and normal quantile plots to identify abnormalities
in data structure. All meta-analyses were conducted with METAWIN v.
2.0 software [14].
3. Results
The species richness of insect parasitoids significantly decreased
with increasing elevation (rgrand mean ¼ 20.31; CI ¼ 20.53 to
20.12; figure 1). The mean slope of regression across the 27
elevation gradients was significantly negative (bgrand mean ¼
Biol Lett 9: 20130028
2. Material and methods
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observations are supported by laboratory experiments showing
that the functional efficiency of parasitoids decreasing with
decreasing temperature [7]. However, studies on the effect of
elevation on parasitism and parasitoid complexes have focused
mostly on single insect herbivores and their parasitoid complex
and did not predict climate change effects on natural enemies
in a wide range of ecosystems.
Meta-analyses provide excellent tools with which to
recognize common responses of organisms to climate or
other ecological variables and to explore covariates explaining the observed patterns [8]. Here, we present the results
from meta-analyses testing the hypotheses that parasitism
rate and parasitoid richness decrease with elevation. We
also test whether the decrease in parasitism rate is greater
for ectoparasitoids and parasitoids of ectophagous insects,
which are more exposed to variable climatic conditions
than endoparasitoids and parasitoids of endophagous hosts.
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3
rate of parasitism (%)
ectoparasitoid–endophagous
endoparasitoid–ectophagous
–0.5
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endoparasitoid–endophagous
0
ectoparasitoid–ectophagous
100 m
Figure 2. Effect of the feeding strategy of insect parasitoid (ecto- versus endoparasitoid) and insect herbivore host (ecto- versus endophagous) on mean slopes of
linear regressions between parasitism rate and elevation. Lines represent the weighted mean value of slopes. Shaded areas represent the bias-corrected bootstrap
confidence intervals of mean slopes.
20.21; CI ¼ 20.38 to 20.07), indicating the average loss of one
species of parasitoid every 475 m.
The meta-analysis of the 140 parasitism rates of individual
parasitoid species along elevation gradients also revealed
that 61 per cent of the correlations were negative (electronic supplementary material, appendix S1). The mean correlation and
slope value across all studies were significantly negative (rgrand
mean ¼ 20.22; CI ¼ 20.35 to 20.08 and bgrand mean ¼ 20.21;
CI ¼ 20.35 to 20.08). The normal quantile plot identified no
outliers, which means that data can be assumed to come from
a single normal distribution, and no gap around zero, indicating
the absence of publication bias (electronic supplementary
material, appendix S4b). The high Rosenthal’s number (1082),
which was about 1.5 times the conservative value of 710,
confirmed the absence of publication bias.
The mean coefficient of correlation between parasitism rate
and elevation was more than twice as negative for ectophagous (rmean ¼ 20.37) as for endophagous insect herbivores
(rmean ¼ 20.14) and for ectoparasitoids (rmean ¼ 20.32) as
for endoparasitoids (rmean ¼ 20.14). The effect of the combination of the two covariates on the coefficient of correlation
was significant (d.f. ¼ 3, QB ¼ 10.8, p ¼ 0.01). Although not
significantly different (d.f. ¼ 3, QB ¼ 132.6, p ¼ 0.13), the
slopes of regression between parasitism and elevation followed the same pattern (figure 2). Only those involving
ectophagous insect herbivores were significantly negative,
with a steeper slope for ectoparasitoids parasitizing ectophagous herbivores than for ectoparasitoids parasitizing
endophagous herbivores. The weighted mean slope for parasitoids of ectophagous herbivores corresponded to a loss of ca
20.44 per cent of parasitism per 100 m for a median parasitism
rate of 3.7 per cent in the 140 case studies (figure 2). We
never observed any significant effect of latitude and mean
annual temperature on parasitism rate or parasitoid richness
(electronic supplementary material, appendix S4c,d).
None of the other species-related covariates, including
host stage attacked or killed, parasitoid taxonomy, development mode of parasitoid and range of elevation, had any
significant effect on the correlations between parasitism rate
and elevation when tested within each combination of
herbivore parasitoid-feeding strategies.
4. Discussion
These meta-analyses provide the first quantitative evidence that insect parasitism and parasitoid richness
generally decrease with elevation. They show a decrease in
parasitism rate of ectophagous herbivores of 0.44 per cent
per 100 m elevation, which represents a relative loss of ca
15 per cent per 100 m (when related to a median speciesspecific parasitism rate of 3.7%). Considering that a parasitoid
complex is often composed of a large number of species, the
cumulative effect of decreasing species-specific rates of parasitism is likely to result in significantly higher host survival.
Our analysis also shows that the decrease with elevation
was greater in ectoparasitoids and parasitoids living in or
on ectophagous hosts, whereas endoparasitoids of endophagous hosts did not show any reduction in parasitism. This
may be due to a better protection by endoparasitoids and
parasitoids of endophagous hosts against adverse or extreme
weather conditions. It is also possible that, as ectoparasitoids
are usually more generalist than endoparasitoids [15], they
may be more affected by the possible absence of their
alternative hosts at higher elevations [16]. Unfortunately,
the available information on parasitoid host ranges is largely
unreliable and so the influence of parasitoid specificity on the
response to climate change could not be tested.
Parasitism often depends positively on host density [17].
Consequently, it cannot be ruled out that the general decrease
in parasitism is caused by decreases in host density. In most
cases, host density was not indicated in the studies used for
the meta-analyses and, thus, this variable could not be tested.
Although reviews [6] suggest that responses of herbivores to
elevation are largely idiosyncratic, with different species showing increasing, declining or no elevational trends in abundance,
host density affects parasitism and needs to be considered in
further studies on the effect of climate change on parasitoids.
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elevation
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We thank A. Battisti and M. Cock for their helpful comments to the
manuscript, and A. Roques, W. Grodzki and C.-E. Imbert for unpublished data. We also acknowledge support from the European
Commission FP7 via the Project BACCARA (GA no. 226299).
References
1.
2.
3.
4.
5.
6.
7.
Thomson LJ, Macfadyen S, Hoffmann AA. 2010
Predicting the effects of climate change on natural
enemies of agricultural pests. Biol. Control 52,
296–306. (doi:10.1016/j.biocontrol.2009.01.022)
Hance T, van Baaren J, Vernon P, Boivin G. 2007 Impact
of extreme temperatures on parasitoids in a climate
change perspective. Annu. Rev. Entomol. 52, 107–126.
(doi:10.1146/annurev.ento.52.110405.091333)
Klapwijk MJ, Ayres MP, Battisti A, Larsson S. 2011
Assessing the impact of climate change on outbreak
potential. In Insect outbreaks revisited (eds P
Barbosa, DK Letourneau, AA Agrawal), pp. 429–
450. Chichester, UK: John Wiley & Sons.
Körner C. 2007 The use of ‘altitude’ in ecological
research. Trends Ecol. Evol. 22, 569 –574. (doi:10.
1016/j.tree.2007.09.006)
Dainese M. 2012 Using natural gradients to infer a
potential response to climate change: an example on
the reproductive performance of Dactylis glomerata L.
Biology 1, 857–868. (doi:10.3390/biology1030857)
Hodkinson ID. 2005 Terrestrial insects along
elevation gradients: species and community
responses to altitude. Biol. Rev. 80, 489– 513.
(doi:10.1017/S1464793105006767)
Mills NJ, Getz WM. 1996 Modelling the biological
control of insect pests: a review of host –parasitoid
8.
9.
10.
11.
12.
13.
models. Ecol. Model. 92, 121 –143. (doi:10.1016/
0304-3800(95)00177-8)
Jactel H, Petit J, Desprez-Loustau M-L, Delzon S,
Piou D, Battisti A, Koricheva J. 2012 Drought effects
on damage by forest insects and pathogens: a
meta-analysis. Glob. Change Biol. 18, 267–276.
(doi:10.1111/j.1365-2486.2011.02512.x)
Borenstein M, Hedges LV, Higgins JPT, Rothstein HR.
2009 Introduction to meta-analysis. Chichester, UK:
John Wiley & Sons.
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis
A. 2005 Very high resolution interpolated climate
surfaces for global land areas. Int. J. Climatol. 25,
1965 –1978. (doi:10.1002/joc.1276)
Whittaker RJ. 2010 Meta-analyses and megamistakes: calling time on meta-analysis of the
species richness-productivity relationship. Ecology
91, 2522–2533. (doi:10.1890/08-0968.1)
Gurevitch J, Hedges LV. 1999 Statistical issues in
ecological meta-analyses. Ecology 80, 1142–1149.
(doi:10.1890/0012-9658)
Rosenberg MS. 2005 The file-drawer problem
revisited: a general weighted method for calculating
fail-safe numbers in meta-analysis. Evolution
59, 464–468. (doi:10.1111/j.0014-3820.2005.
tb01004.x)
14. Rosenberg MS, Adams DC, Gurevitch J. 2000
MetaWin: statistical software for meta-analysis,
version 2.0. Sunderland, MA: Sinauer Associates.
15. Quicke DLJ. 1997 Parasitic wasps. London, UK:
Chapman & Hall.
16. Gaston KJ, Williams PH. 1996 Spatial patterns in
taxonomic diversity. In Biodiversity (ed. KJ Gaston),
pp. 202–229. Oxford, UK: Blackwell Science.
17. Wade SJ, Murdoch WW. 1988 Spatial density
dependence in parasitoids. Annu. Rev. Entomol. 33,
441–466. (doi:10.1146/annurev.en.33.010188.
002301)
18. Messing RH, Klungness LM, Jang EB. 1997 Effects of
wind movement on Diachasminorpha longicaudata,
a parasitoid of tephritid fruit flies, in a laboratory
flight tunnel. Entomol. Exp. Appl. 82, 147 –152.
(doi:10.1046/j.1570-7458.1997.00124.x)
19. Stireman III JO et al. 2005 Climatic unpredictability
and caterpillar parasitism: implications of
global warming. Proc. Natl Acad. Sci. USA
102, 17 384 –17 387. (doi:10.1073/pnas.
0508839102)
20. Sunday JM, Bates AE, Dulvy NK. 2011 Global
analysis of thermal tolerance and latitude in
ectotherms. Proc. R. Soc. B 278, 1823–1830.
(doi:10.1098/rspb.2010.1295)
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central and northern Europe, in particular in the Alps.
While this largely reflects the absence of such studies in
other continents, it is not clear whether the same patterns
would have been found on tropical or subtropical gradients
where climate is less seasonal [4] and thermal tolerance of
insects to extreme temperatures is usually lower [20].
Our analysis provides a quantitative contribution to the
debate on the effect of climate warming on insect pests and
their control by natural enemies [3]. It also reveals that host
and parasitoid-feeding strategies can be used to build up
functional groups showing similar responses to climate
change. However, parasitoids are only one group of natural
enemies regulating herbivorous insect populations, and
further investigations are needed to evaluate the responses
of predators and pathogens to climate change.
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While a decrease in temperature is the most consistent
environmental response to increasing elevation, other factors
can be affected as well [4]. Other climate variables such as precipitation, mist, atmospheric turbulence and wind speed
change with elevation, but the analogy between elevation
and climate change is less straightforward for these variables
than for temperature. Harsh weather conditions encountered
at higher elevation may affect mating, host foraging and oviposition behaviour in adult parasitoids [18], but the fact that
endoparasitism of endophagous insects does not seem to
decline at higher elevations suggests that the effects of weather
conditions on adults may not be the main driver. In an analysis of climatic factors affecting parasitism of Lepidoptera along
a latitudinal gradient, Stireman et al. [19] found that parasitism
was mainly driven by precipitation, with parasitism decreasing as yearly precipitation variability and drought periods
increase. However, annual precipitation is less likely to vary
in elevation gradients than in latitudinal gradients.
Another limitation of our study is that the vast majority of
the gradients included in the meta-analyses are situated in