Download reduced wind insect herbivore

Ecology, 95(9), 2014, pp. 2375–2381
Ó 2014 by the Ecological Society of America
Reduced wind strengthens top-down control of an insect herbivore
BRANDON T. BARTON1
Department of Zoology, University of Wisconsin, 430 Lincoln Drive, Madison, Wisconsin 53706 USA
Abstract. Global wind speeds have decreased 5–15% over the last 30 years and are
expected to continue decreasing in the future. However, little is known about how wind affects
species and their interactions within communities. I experimentally tested the effects of wind
on predator–prey interactions using soybean aphids and predatory multicolored Asian
ladybeetles. First, I examined the direct effect of wind on aphids in a greenhouse without
predators under three treatments: no wind, wind (oscillating fan), or simulated wind
movement. Aphid abundances did not differ among treatments. Next, I conducted a field
experiment in soybean plots assigned to either control or wind-block treatments. Predators
were more abundant in wind-block treatments and reduced aphid abundance by 40%
compared to control plots. To elucidate why wind indirectly increased aphid density in open
plots, I conducted a feeding trial with ladybeetles foraging for aphids on plants that were
assigned to either control or simulated wind movement treatments. Plant movement doubled
the amount of time it took predators to begin consuming aphids and decreased predation rate
by two-thirds. These experiments illustrate how wind can have indirect effects on prey by
altering predator behavior and show the importance of this under-studied effect of global
change.
INTRODUCTION
A long-standing goal in ecology is to understand how
the abiotic environment affects species and their
interactions with one another (e.g., Park 1954). This
line of investigation has become especially important
because our abiotic environment is changing at an
unprecedented rate (Wisconsin Initiative on Climate
Change Impacts 2011). Increases in atmospheric greenhouse gases during the 20th century are expected to
induce widespread changes in climate, and since species
are intimately linked to their climate, we also expect
widespread changes in species abundances, distributions, and interactions (Tylianakis et al. 2008). Now,
more than ever, ecologists are not only charged with the
task of understanding how the abiotic environment
affects species, but also how predicted future climates
will affect species and their interactions within ecological
communities.
The effects of warming have seemingly taken center
stage in climate change studies, rivaled only by the
effects of altered precipitation regimes (Parmesan 2006,
Tylianakis et al. 2008). However, other elements
contribute to a region’s climate and have important
ecological effects, including humidity (e.g., Park 1954),
barometric pressure (e.g., Paige 1995), cloud cover (e.g.,
Orrock and Danielson 2009), and wind (e.g., Damschen
Manuscript received 26 November 2013; revised 2 April
2014; accepted 21 May 2014. Corresponding Editor: B. D.
Inouye.
1 E-mail: [email protected]
et al. 2008). Although it has received little attention
outside of green energy discussions, wind speeds have
decreased across the contiguous United States (Pryor et
al. 2009) and worldwide (Vautard et al. 2010, McVicar
et al. 2012) by 5–15% during the last 30 years, and are
generally expected to continue decreasing during the
21st century. Two mechanisms have been suggested to
explain slowing wind (Vautard et al. 2010). First, the
planet’s climate is warming faster at the poles than lower
latitudes, which reduces the equatorial-polar thermal
gradient (Ren 2010, McVicar et al. 2012). This gradient
is responsible for atmospheric circulation, and as the
gradient decreases wind speeds are expected to decrease
as well (McVicar et al. 2012). Second, reforestation,
agricultural abandonment, and manmade structures
have increased the number of physical obstacles on the
landscape (Strack et al. 2008, Vautard et al. 2010). These
obstacles slow wind speeds by physically impeding air
flow (Sud et al. 1988, Strack et al. 2008) and can have
reciprocating effects on temperature and precipitation
patterns (Sud et al. 1988, Nair et al. 2011).
Much has been written on the effects of wind on
dispersal, pollination, and environmental disturbance
(reviewed in Regal 1982, Everham and Brokaw 1996,
Gatehouse 1997), but little is known about how wind
affects predator–prey interactions. Investigations into
the effects of wind on predators have generally focused
on prey detection by chemical olfactory cues (MacKenzie and Leggett 1991, Wyatt et al. 1993) or flight costs to
aerial predators (Verboom and Spoelstra 1999, Weimerskirch et al. 2012). However, there are a priori reasons to
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Key words: behavior; climate change; indirect effects; ladybeetles; predator–prey interactions; soybean
aphids; wind.
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BRANDON T. BARTON
expect wind to affect predator-prey interactions. First,
predators and prey typically differ in shape, and
therefore may respond differently to the physical flow
of air across their bodies (Vogel 1994:50–80). For
example, the streamlined body plan of Sparrowhawks
generally makes them quite stable, but under high winds
their stocky shorebird prey retain more flight control
and can evade most hawk attacks (Quinn and Cresswell
2004). Similarly, predators and prey often differ in size
and mobility, which are traits that affect evaporation,
convection, and other physiological processes (Church
1960, Denny 1993). Finally, wind destabilizes the
physical environment, which can impede locomotion
or crush organisms (Cannon 1986, Vogel 1994, Mann et
al. 1995).
I report on an experimental investigation of the effects
of wind on soybean aphids (Aphis glycines) and
multicolored Asian ladybeetle (Harmonia axyridis).
Soybean aphids are sap-sucking herbivorous pests of
soybean and native to Asia (Ragsdale et al. 2011).
Soybean aphids are consumed by many predators, but
multicolored Asian ladybeetles are widely recognized as
the most important (Ragsdale et al. 2011), contributing
to about one-third of total soybean aphid predation in
the field (Costamagna and Landis 2007). In the midwest
United States where these species are now common (see
Plate 1), wind is a prominent component of the abiotic
environment (Wisconsin Initiative on Climate Change
Impacts 2011) and is expected to decrease 10–15%
during the 21st century (Segal et al. 2001, Pryor and
Barthelmie 2011). Predicting the effects of slowed winds
on species like ladybeetles and aphids is difficult because
little is known about how wind affects predator–prey
interactions in general.
I tested the hypothesis that wind indirectly affects
aphid density by altering top-down control by predators. The indirect effects of wind on aphids can be
density mediated (i.e., change predator abundance) or
trait mediated (i.e., change predator behavior). I
predicted that wind would negatively affect predator
hunting performance and reduce local abundance, and
in turn indirectly increase aphid abundance. I tested
both mechanisms in a series of field and greenhouse
experiments. First, I tested for a direct effect of wind on
aphid abundance in a greenhouse experiment. Next, I
manipulated wind speed in a field experiment and
measured aphid abundance in the presence and absence
of predators. Finally, I conducted a behavioral experiment to quantify the effects of wind on predator
hunting behavior.
METHODS
Study sites and organisms
I conducted this research in 2011 at the University of
Wisconsin in Madison, Wisconsin, USA (greenhouse
experiment) and the nearby Arlington Agricultural
Research Station (field experiment). To reduce potential
differences between wild and experimental populations,
Ecology, Vol. 95, No. 9
I cultivated a colony of aphids from individuals collected
at the field site three weeks prior to the experiments. I
reared aphids on potted soybean plants in a greenhouse
at ;238C. Ladybeetles used in the behavioral experiment were wild caught and maintained in the greenhouse on a diet of soybean aphids for no more than one
week (range 3–6 days) before experimentation.
Direct effect of wind on aphids in the greenhouse
I conducted an experiment to determine if wind had a
direct effect on aphid density by using 3-L pots planted
with three soybean plants. Pots were planted with
soybean seeds and grown in a greenhouse at ;238C.
When the first set of true leaves emerged, I stocked each
pot of plants with 10 aphids and assigned each pot to
one of three treatments: control, wind, or movement.
Control plants were not subjected to any wind or
movement, although a minimal amount of air movement
occurred as the climate control system circulated air
throughout the greenhouse. Plants in the wind treatment
were placed 0.5 m from an oscillating fan that blew a
;10 km/h pulse of wind on the plants 10 times per
minute for ;1 s per pulse, creating a disturbance similar
to that experienced in the field (mean ¼ 8.3 km/h;
Appendix A). Simulated wind movement treatments
were used to isolate the convective effects of wind from
the effects of physical disturbance caused when wind
pushes plants past each other. I built a machine that
pulled lightweight monofilament line attached to a plant
at a rate of 10 times per minute to match the frequency
of wind from the oscillating fan (Appendix B: Fig. B1a).
This caused the plants in the pot to brush against each
other as if they were subjected to wind, but without
affecting evaporation or the thermal environment. After
17 days, I ended the experiment and counted the total
number of aphids in each pot. I replicated this
experiment four times. After confirming that assumptions of the statistical test were met, I tested for
differences in aphid abundance among treatments using
an analysis of variance (ANOVA).
Effects of wind on aphids and predators in the field
On 19 May 2011, I planted 16 3 3 3 m plots
containing four rows of soybean plants (;40 per row)
within an alfalfa field. Plots were randomly assigned as
either control or reduced-wind treatments. I reduced
wind by constructing 0.5 m tall v-shaped wind blocks
that pointed west into the prevailing wind (Appendix B:
Fig. B1b). Wind blocks were constructed by supporting
clear plastic sheeting (Film-Gard, Minneapolis, Minnesota, USA) between three posts. Control plots were
exposed to ambient wind, while wind blocks protected
plots from nearly all wind (confirmed with an anemometer; Kestrel, Downington, Pennsylvania, USA). Within
all plots, I placed a 1 3 1 3 1 m mesh exclosure over a
section of a soybean row prior to plant emergence to
exclude predators. The mesh allowed wind to pass
through the exclosure, however reduced wind speed by
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INDIRECT EFFECTS OF WIND
2377
50% (measured with an anemometer; B. T. Barton,
unpublished data).
After plants emerged in early June, I surveyed the
open plots several times each week to determine when
aphids colonized the plots. When aphids were found in
the open plots in early July, I stocked the exclosures with
10 aphids from the greenhouse colony (wild-caught
aphids were not used to prevent introduction of
parasitoids and pathogens). Once each week from 1
August to 3 September 2011, I surveyed 50 soybean
leaves in the open plot, recording the number of
ladybeetles I encountered. On the last sampling day, I
also recorded the number of aphids on 50 soybean leaves
in the open plot as well as inside the mesh exclosure. I
calculated the magnitude of top-down control of aphid
abundance by predators for each plot as ln(N2/N1)
where N1 was the number of aphids observed inside the
exclosure (predators absent), and N2 was the number of
aphids observed in the open plot (predators present).
I tested for differences in predator abundance between
wind treatments using a repeated measures ANOVA
after confirming that the assumptions of the test were
met. I used Welch’s t tests to determine if wind
treatment affected aphid abundance inside the exclosure,
aphid abundance in the open plot, or the magnitude of
top-down control because variance was not equal
between treatments.
Effects of plant motion on predators
I investigated the effects of plant motion on foraging
ladybeetles in a series of greenhouse experiments.
Approximately two weeks before initiating the experiment, I planted 30 3-L pots with three soybeans. When
the first set of true leaves emerged, I inoculated the pot
with ;10 aphids. When densities reached ;100 aphids
per pot, I initiated predator feeding trials aimed at
understanding how plant motion caused by wind affects
predator hunting behavior and feeding rate. I randomly
assigned pots to control (no movement) or simulated
wind movement treatments, using the machine described
previously to move plants (Appendix B).
I conducted the experiment with wild-caught H.
axyridis ladybeetles that had been starved for 36 h
before the experiment. In the field ladybeetles consume
aphids as larvae and adults. However, adults often fly
away and therefore are difficult to work with in a
greenhouse setting, so experiments were conducted with
third- and fourth-instar larvae. To initiate the experiment, I recorded the total number of aphids on each
plant then transferred a single ladybeetle to the soil at
the base of the plant. I observed each ladybeetle as it
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PLATE 1. Harmonia axyridis in an windy soybean field (;15 km/h) at the University of Wisconsin Arlington Agricultural
Research Station (USA). This photograph was taken using an exposure time of 1/3 s to capture the motion of the plants and an
external flash to freeze the ladybeetle in focus. Photo credit: B. Barton.
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BRANDON T. BARTON
Ecology, Vol. 95, No. 9
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FIG. 1. Wind treatments altered predator abundance and indirectly affected aphid abundance in open soybean plots. (a)
Ladybeetles were more abundant in soybean plots with wind blocks than control plots subjected to ambient wind. (b) Aphids were
less abundant in soybean plots with wind blocks than control plots subjected to ambient wind. Plots show median (center line), 75th
percentiles (top of box), 25th percentiles (bottom of box), and whiskers connect the largest and smallest values within 1.5
interquartile ranges.
moved from the soil surface to the plant and recorded
the number of seconds it took it to begin feeding on
aphids. After 60 minutes, I removed the ladybeetle and
recorded the number of remaining aphids. I replicated
feeding trials 15 times using new plants and ladybeetles
each time. Because of unequal variances, I used Welch’s
t tests to compare the time it took ladybeetles to begin
eating aphids and the total number of aphids consumed
under control and movement treatments.
All analyses were conducted in the statistical computing language R (v3.0.2; R Development Core Team
2013).
RESULTS
Direct effect of wind on aphids
After 17 days, mean aphid abundance on potted
soybean plants in the greenhouse did not differ among
the three wind treatments (ANOVA, F2,3 ¼ 0.424, P ¼
0.67; Appendix C: Fig. C1a). Similarly, at the conclusion
of the field experiment aphid abundance inside mesh
exclosures (no predators) did not significantly differ
between control and wind blocked plots (Welch’s t test, t
¼ 0.38, P ¼ 0.71; Appendix C: Fig. C1b).
Effects of plant motion on predators
Predators exposed to moving plants took almost five
times longer to find and begin consuming aphids than
predators in control treatments (Welch’s t test, t ¼
3.84, P ¼ 0.0026; Fig. 3a). Predators exposed to
moving plants also ate less than half as many aphids as
predators in control treatments (Welch’s t test, t ¼ 6.46,
P , 0.0001; Fig. 3b).
DISCUSSION
Even on the calmest days, some wind is almost always
present on a landscape (Denny 1993). Wind has wellknown effects on pollination, dispersal, and disturbance
(Regal 1982, Everham and Brokaw 1996, Gatehouse
1997) yet relatively little is known about how it affects
interactions between species. I show here that wind can
Field experiment
The only ladybeetles I encountered during the
experiment were adult H. axyridis. Ladybeetles were
two-thirds more abundant in plots with wind blocks
than control plots exposed to ambient wind (repeatedmeasures ANOVA, F1,7 ¼ 157.6, P ¼ 0.0011; Fig. 1a).
Aphids were almost twice as abundant in control plots
than with wind blocks (Welch’s t test, t ¼ 3.90, P ¼
0.0017; Fig. 1b). Predator effect size was almost twice as
large in wind-block treatments than in control treatments (Welch’s t test, t ¼ 2.45, P ¼ 0.028; Fig. 2).
FIG. 2. Wind blocks increased the magnitude of top-down
control of soybean aphids by predators in the field. Error bars
give standard deviation of the mean.
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INDIRECT EFFECTS OF WIND
2379
FIG. 3. Effects of plant motion from simulated wind movement on predator foraging. (a) Predators were slower to begin eating
aphids when plants were moving than stationary control plants. (b) Predators ate fewer aphids when plants were moving than
stationary control plants. Box plot components are described in Fig. 1. Values outside whiskers are outliers (circles).
foraging ladybeetles must struggle against the forces of
drag and momentum on a moving substrate (Vogel
1994:50–80, 132–155), soybean aphids remain motionless and attached to the underside of leaves by their
stylet. Therefore, another testable prediction is that wind
has a larger effect on active species. This is a reasonable
prediction because sedentary species often have morphological adaptations to decrease the effects of wind
and other moving fluids, whereas active species are more
anatomically constrained (Vogel 1994:50–80).
There are, of course, benefits to being mobile. The
sedentary nature of aphids requires them to stay on one
plant and experience any wind force that occurs there. In
contrast, mobile species have the ability to seek out
environments that are favorable and avoid those that are
not. In this study, ladybeetles moved into the plots that
were sheltered from wind and avoided those exposed to
ambient wind. The behavioral experiments suggest that
ladybeetles avoid windy plots because the physical
disturbance makes it difficult for them to move among
plants and locate their prey, but there could be other
reasons. For example, wind may interfere with visual or
olfactory cues that ladybeetles use to find their prey
(Obata 1986, Meisner and Ives 2013), which could also
explain why it took longer for them to find aphids when
plants were moving.
This study is not without limitations. My experiment
was relatively short in duration and created a landscape
of heterogeneous wind speeds in relatively small patches.
This design emphasized the role of predator immigration
over predator reproduction, a point reinforced by my
failure to detect any larval ladybeetles during the
surveys. However, this is a reasonable emphasis because
ladybeetles are mobile generalist predators and consequently their population dynamics are not strongly tied
to aphid density within a single field (Forbes and
Gratton 2011, Ragsdale et al. 2011, Barton and Ives
2014a). So, what would happen if the entire landscape
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influence interactions between predators and their prey.
Wind had no direct effect on aphid abundance, but
negatively affected predator hunting performance (Fig.
3) and abundance (Fig. 1a). Consequently, wind had a
positive indirect effect on aphid abundance (Fig. 1b) by
weakening top-down control (Fig. 2). These findings are
consistent with other examples of how wind alters
predation by asymmetrically affecting predators and
their prey (e.g., Quinn and Cresswell 2004), as well as a
broader literature showing that species interactions can
propagate indirect effects of an abiotic factor throughout a community (Tylianakis et al. 2008, Barton and
Ives 2014a).
I did not detect a direct effect of wind on aphids,
indicating that wind did not alter the environment in
ways that hinder aphid feeding, growth, and reproduction. This may be because aphids are small (height ,1
mm) and are probably within the boundary layer of the
leaf surface. Within this layer of non-moving air, small
insects experience stable microclimates that can differ
greatly from the ambient environment outside the
boundary layer (Woods 2010). In contrast, ladybeetles
are considerably larger than aphids, thus they are
exposed to the ambient conditions outside the leaf
boundary layer. Their larger size also means ladybeetles
have more surface area for wind to exert a force on and
more momentum pulling them from wind-blown plants.
Therefore, it is reasonable to predict that wind would
have higher energetic costs for a larger animal. Testing
this prediction with some of the smaller predators that
are present in this system (e.g., Orius insidiosus) would
be a valuable next step.
Soybean aphids and ladybeetles also differ in their
mobility and foraging behavior. Ladybeetles are mobile
predators that actively search for prey (Forbes and
Gratton 2011, Meisner and Ives 2013), whereas soybean
aphids are sap-sucking herbivores and are relatively
sedentary (Whalen and Harmon 2012). Thus, while
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BRANDON T. BARTON
slowed homogenously? In that case, we would not
expect a numerical effect due to aggregations, but
ladybeetle abundance could still increase: larval feeding
rates were higher without wind, and increasing feeding
rate are positively related to development rate, adult
fitness, and population growth rates (Dmitriew et al.
2009). Thus, it is possible that slower wind could
increase ladybeetle population abundance, but this
remains untested. Finally, I have focused on the
dominant soybean aphid predator (H. axyridis), but
wind may also affect other aphid predators. How wind
may affect the abundance and behavior of other
predators remains unknown.
This experiment compared ambient wind treatments
to treatments with almost no wind, whereas projected
wind reduction for the midwestern United States is more
modest (10–15% reduction during the 21st century).
Experiments often require relatively large treatment
effects in order to detect the direct and indirect effects of
an abiotic manipulation within reasonable time scales
and replication (Newman et al. 2011, Barton and Ives
2014a). It was not my goal in this study to specifically
predict how wind will affect ladybeetle and aphid
interactions in a future, less windy environment. Instead,
I offer an experimental demonstration that wind can
affect predator–prey interactions and encourage ecologists to consider this changing component of climate in
future studies. Although I have emphasized the effects of
wind in this community, it is essential to remember that
these species can be simultaneously affected by other
components of climate change, such as temperature
(Harmon et al. 2009, Barton and Ives 2014b) and
precipitation (Barton and Ives 2014a). The task may
seem daunting, but integrating multiple abiotic factors,
including wind, into future studies is essential if we are
to understand the net effect of climate change on species
and their interactions within ecosystems.
ACKNOWLEDGMENTS
I thank J. Breuer, N. Dietz, M. Miesner, and T. Thalhuber
for field assistance; M. Barton, E. Damschen, E. Murrell, and J.
Harmon for feedback on experimental design and the
manuscript; and, A. Ives for just about everything (except help
with field work). I also thank three anonymous reviewers for
their constructive comments on the manuscript. This research
was funded by NSF-DEB-Dimensions 1240804 to A. Ives.
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SUPPLEMENTAL MATERIAL
Appendix A
Five years of temperature, precipitation, and wind data from the study area (Ecological Archives E095-212-A1).
Appendix B
Illustrations of movement machine and wind blocks (Ecological Archives E095-212-A2).
Appendix C
Figures showing no direct effect of wind on aphid abundance (Ecological Archives E095-212-A3).
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