Ecology, 96(11), 2015, pp. 2902–2911� 2015 by the Ecological Society of America

Varying predator personalities generates contrasting preycommunities in an agroecosystem

RAPHAEL ROYAUTE1,3

AND JONATHAN N. PRUITT2

1Department of Biological Sciences, North Dakota State University, Fargo, North Dakota 58102 USA2Department of Biological Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania 15260 USA

Abstract. Most taxa show consistent individual differences in behavior, a phenomenonoften referred to as animal ‘‘personalities.’’ While the links between individual personality andfitness have received considerable attention, little information is available on how animalpersonality impacts higher-order ecological processes, such as community dynamics. Using amesocosm experiment, we subjected a representative community of alfalfa pests to differentcompositions of personality types of the wolf spider Pardosa milvina. We show that subtlevariation in the personality composition of P. milvina populations generate wildly differentprey communities, where a mixture of both active and sedentary individuals performs best atsuppressing prey abundance. Our results provide the first experimental evidence that predatorpersonality types can generate contrasting prey communities. Moreover, our results suggestthat manipulating the representation of predator personality types may be a profitable avenueby which one can maximize the biocontrol potential of predator populations.

Key words: arthropod generalist predators; behavioral type 3 behavioral type interactions; biocontrol;Lycosidae; personality; pests community dynamics; predator–prey dynamics.

INTRODUCTION

Animal personality (also referred to as ‘‘tempera-

ment’’ or ‘‘behavioral syndromes’’) is a field of study

devoted to understanding the drivers and consequences

of consistent individual differences in behavior. Within

virtually any population, some individuals are consis-

tently more active, more aggressive, or are more willing

to engage in risk-taking behavior (Sih et al. 2004a, b,

Reale et al. 2007). Such personality differences are an

important determinant of an individual’s fitness (Dinge-

manse et al. 2004, Dingemanse and Reale 2005). These

individual differences have also been associated with

various underlying physiological and genetic mecha-

nisms (Careau et al. 2008, Bell and Aubin-Horth 2010,

Norton et al. 2011) and often exhibit a significant

heritability (Stirling et al. 2002). In addition, personality

differences have the potential to influence larger

ecological and evolutionary processes (Sih et al. 2012,

Wolf and Weissing 2012), including invasion success,

metapopulation dynamics, succession, species interac-

tions, and even extinction risk. In this manuscript, we

will refer to separate classes or categories of personalities

as behavioral types or personality types interchangeably.

The ecological consequences of animal personality

have been considered most rigorously in the context of

predator–prey interactions. Dozens of studies from a

wide variety of systems have demonstrated, for instance,

that prey personalities can influence prey growth rate

(reviewed in Stamps 2007), susceptibility to predation

(Bell and Sih 2007), and the intensity of trait-mediated

species interactions (Griffen et al. 2012, Toscano and

Griffen 2014). Other studies have shown that predator

personality types can influence predator feeding rate,

diet breadth, and the kinds of prey that individuals tend

to encounter and consume (Riechert and Hedrick 1993,

Matich et al. 2011; reviewed in Araujo et al. 2011). Still

other studies have shown that the outcome of predator–

prey interactions depend on subtle differences in the

representation of different personality types in both

predator and prey populations, hence the performance

of either predator or prey depends on the strategies

present in the opposing trophic level (Pruitt et al. 2012,

DiRienzo et al. 2013, McGhee et al. 2013, Sweeney et al.

2013). This last scenario is referred to as behavioral type

3 behavioral type interactions, and implies that no one

strategy in either predator or prey consistently experi-

ences superior performance. Yet, such interactions have

mostly been studied in the context of single-predator–

single-prey-species experiments and are therefore limited

in their ability to inform how predator personality

influences community dynamics.

A useful framework for predicting the community-

level consequences of behavioral type 3 behavioral type

interactions stems from the classic literature on foraging

mode. Huey and Pianka (1981) argued that the kinds of

prey consumed by predators would be different and

predictable depending on predators’ foraging mode:

sedentary predators should tend to catch active roving

prey whereas active predators would tend to capture

sedentary prey. Although the locomotor crossover

Manuscript received 17 December 2014; revised 2 April 2015;accepted 7 May 2015. Corresponding Editor: W. E. Snyder.

3 E-mail: raphael.royaute@gmail.com

2902

hypothesis has been mostly investigated in the context of

interspecific variation in foraging modes (Perry 2007, see

also Schmitz and Suttle 2001), a small number of studies

have revealed that similar dynamics can play out among

intraspecific trait variants in predator and prey (Pruitt et

al. 2012, DiRienzo et al. 2013, McGhee et al. 2013,

Sweeney et al. 2013) or in simulations (Scharf et al.

2006). Thus, an important question that remains to be

answered is whether variation in foraging mode within a

single predator species is of sufficient magnitude to

shape the interactions between a predator population

and myriad prey species, simultaneously. By extending

the locomotor crossover hypothesis to variation in

foraging mode within species, one might predict that

an assemblage of sedentary and active behavioral types

would be more effective at suppressing a community of

prey that exhibit a variety of locomotor and foraging

patterns. In contrast, we predict that if only a narrow

range of predators personality types are represented

within a population, then their top-down control on

prey assemblages should be weaker. In the study

described herein we probe more deeply into the role of

personality types in governing predator–prey interac-

tions to explore how the mixture of personality types in

populations of predators can impact entire communities

of prey using an agroecosystem model.

Spiders are ideal systems to explore the influence of

personality differences in ecological processes. Spiders

are dominant generalist arthropod predators in most

terrestrial ecosystems and can exert top-down control on

invertebrate prey assemblages, making them important

biocontrol agents in agroecosystems (Riechert and

Bishop 1990, Young and Edwards 1990, Carter and

Rypstra 1995). Their efficiency in biocontrol is also

mediated by a variety of behavioral processes, including

the timing of dispersal into agricultural habitats

(Hibbert and Buddle 2008, Sackett et al. 2009, Royaute

and Buddle 2012), intraguild predation and cannibalism

(Buddle 2002, Balfour et al. 2003, Buddle and Rypstra

2003), and the tendency to consume multiple prey items

beyond satiation (i.e., ‘‘wasteful killing’’; Maupin and

Riechert 2001). Fortuitously, spiders have also become a

model taxon for studying personality traits (Riechert

and Hedrick 1993, Johnson and Sih 2005, 2007, Pruitt et

al. 2008, Kralj-Fiser and Schneider 2012, Royaute et al.

2014) and personality differences are widespread across

more than a dozen families of spiders (reviewed in Pruitt

and Riechert 2012).

Our objective in this study was to test whether

personality differences in a generalist predator can

generate contrasting prey communities in an agro-

ecosystem. In particular, we focus on the extraordinarily

abundant wolf spider Pardosa milvina (see Plate 1). We

first classified individual P. milvina into either ‘‘active’’

or ‘‘inactive’’ personality types using a standardized

laboratory assay. We then deployed groups of active

spiders, inactive spiders, or a mixture of both active and

inactive spiders in experimental mesocosms that each

contained an identical assemblage of prey species. We

asked the following questions: (1) Does varying the

personality composition of the predator populations

generate contrasting prey communities? (2) If so, which

compositions (active, inactive, mixed) perform best at

diminishing which prey species or does one composition

work well universally? (3) Do some personality compo-

sitions generate more or less predictable prey commu-

nity structures? Addressing these questions is of broad

ecological interest for at least two reasons. First,

exploring the ecological consequences of personality

helps us understand when and how this aspect of

functional diversity trickles up to affect community

dynamics. Second, from a practical perspective, answer-

ing these questions can inform why integrative pest

management programs can succeed or fail, since

particular personality types (or combinations of person-

alities) may be more or less effective at controlling

particularly troublesome species of pests or entire pest

communities.

METHODS

Spider collection and laboratory maintenance.—Pardo-

sa milvina is a small wolf spider (Araneae: Lycosidae)

with high affinity for disturbed habitat and is extremely

common across many crop systems of North America

(Dondale and Redner 1990, Young and Edwards 1990,

Marshall and Rypstra 1999). P. milvina were collected as

late instar juveniles at an old field site in Powell,

Tennessee, USA in May–June 2010. Spiders were

collected at night using their eye shine. Spiders were

then transported back to laboratory at the University of

Tennessee, Knoxville. Spiders were housed individually

in 490-mL plastic cups containing a 2-cm pad of moist

sphagnum moss as substrate. Spiders were maintained

on a diet of size-matched domestic crickets provided ad

libitum twice weekly. Upon reaching maturity, we

selected only the females for use in our experiments,

ran them through a behavioral assay to assess their

activity level, measured their cephalothorax width at its

widest point using digital calipers as a proxy for body

size, and then assigned them to one of our experimental

treatments.

Activity level assay.—Open-field activity tests are

commonly used to test movement patterns in a

standardized manner (Carducci and Jakob 2000, Mon-

tiglio et al. 2010). These assays have been successfully

incorporated in personality studies to reveal patterns of

individual differences in activity and exploration strat-

egies in a wide variety of organisms, including spiders

(Dochtermann and Nelson 2014, Montiglio et al. 2014,

Royaute et al. 2014). Activity assays were conducted by

placing a single P. milvina in a clean 18 3 18 cm plastic

arena lined with 1 3 1 cm graphing paper. We then

covered the spider with a black cover object (4 cm high,

8 cm radius). After 30 s acclimation, we removed the

cover object and placed the lid on the arena. We waited

until the spider started movement and then counted the

November 2015 2903PREDATOR PERSONALITY AND PREY COMMUNITY

number of 1-cm lines crossed over the next 3 minutes.

We deemed individuals that traversed further in these

environments as more active. To ensure that this

behavior was a repeatable trait of individual spiders,

we measured a pool of 19 P. milvina once daily for eight

consecutive days. This pool of individuals was not used

in our mesocosm studies.

Single-predator–single-prey assays.—A pool (n ¼ 78)

of mature female P. milvina were collected to test

whether differences in predators’ willingness to accept

various prey species was associated with their personal-

ity type. Females were starved two weeks before being

presented with a single prey item in a structurally

depauperate arena. These arenas consisted of a 490-mL

plastic deli container lined with filter paper. The arena

perimeter was lined with petroleum jelly 2 cm above the

base, in order to prevent prey items from escaping into

the tops of the containers. A single spider of known

activity level was first released into the arena and given

20 minutes to acclimate. A single prey item was then

placed centrally within the arena using forceps. We left

the spider to interact with the prey for the next 24 hours.

At the end of this time we recorded whether the spider

consumed the prey item or not. Instances where the prey

item escaped into the top of the container we removed

from our analysis. A separate group of spiders was used

for each prey species. Sample sizes for each prey species

were as follows: blister beetles (n ¼ 12), potato

leafhoppers (n ¼ 12), beet armyworms (n ¼ 12), pea

aphids (n ¼ 14), sharpshooters (n ¼ 14), and alfalfa

weevils (n ¼ 14).

Alfalfa establishment.—We selected a 5 3 20 m plot

with direct sun atop a hill to seed our alfalfa. Prior to

planting, we cleaned the area, worked the soil, and

removed any and all debris. Certified organic alfalfa

seeds (Sustainable Seed Company, Covelo, California,

USA) were planted by sprinkling seed atop the bare soil

and covering the seeds with an additional 2 cm of loose

soil. Seeds were planted in rows spaced 32 cm apart,

with approximately 115 g of seeds deployed every 7 m.

Seeds were permitted to sprout and grow until they

reached approximately 18 cm in height. Throughout this

initial growth phase, we meticulously checked the alfalfa

beds for weeds and insects twice daily, since young

alfalfa beds are extremely susceptible to infestation by

potato leafhoppers (Empoasca fabae).

Pest species collection and release.—Pest species were

collected opportunistically on nearby alfalfa fields,

roadsides, and old field habitats by sweep netting. We

focused on six of alfalfa’s most voracious insect pests:

blister beetles (Epicauta sp.), potato leafhoppers (Em-

poasca fabae), pea aphids (Acyrthosiphon pisum), sharp-

shooters (Xyphon), alfalfa weevils (Hypera postica), and

beet armyworms (Spodoptera exigua). Moreover, each

of these pest species possesses distinct activity patterns,

varying from sap-suckers with relatively sedentary

foraging mode (pea aphids, potato leafhoppers, and

sharpshooters) to more free-living leaf chewers that are

generally more active (armyworms, alfalfa weevils, and

blister beetles [Price et al. 2011]). These biological

differences allowed to test whether specific predator

personality types are more likely to consume certain

prey species. Stock populations of pests were housed in

52 3 52 3 52 cm Lumite mesh mesocosms (BioQuip

1450DSV; Rancho Dominguez, California, USA),

which were placed over beds of alfalfa. We were unable

to collect larval S. exigua of a suitable size for P. milvina

to devour. Thus, we purchased our S. exigua (instar 2–3)

from a nearby hobbyist herpetologist.

Mesocosm experiment.—Fifty-five 52 3 52 3 52 cm

Lumite mesh mesocosms (BioQuip 1450DSV) were

deployed shortly after the alfalfa reached approximately

18 cm in height. Mesocosms were deployed by unscrew-

ing and removing their bottom panels and setting them

atop two adjacent rows of alfalfa. We then trimmed and

adjusted the alfalfa that was immediately adjacent to the

sides so that the mesocosms set flat against the ground.

We then placed an 18 cm skirt of plastic sheeting around

the edge of the mesocosm and molded a layer of potting

soil around the base to seal any remaining gaps between

the bottom of the mesocosm and the ground. Meso-

cosms were stocked with a standardized community of

pest arthropods and P. milvina. The pest community

consisted of 15 blister beetles, 15 potato leafhoppers, 10

beet armyworms, 9 pea aphids, 5 sharpshooters, and 8

alfalfa weevils. These numbers were selected based on

the number of prey caught using sweep nets in adjacent,

untreated alfalfa beds and old field habitats. Predator

populations consisted of eight active, eight inactive, or a

mixture of four inactive and four active P. milvina.

Spiders that exhibited activity scores in the top 50% of

the distribution of activity levels were labeled ‘‘active,’’

and spiders that exhibited activity scores in the bottom

50% of the distribution were labeled ‘‘inactive.’’ This

classification resulted in significant differences in activity

levels among all treatments (Appendix: Fig. A1). We

elected not to create predator populations with more

extreme compositions (e.g., only the top and bottom

deciles) because we were interested in creating distribu-

tions of predator personality types that might commonly

be found together in nature. Predators were starved for

two weeks prior to being deployed within the meso-

cosms. We deployed 15 mesocosms of each treatment

(active, inactive, mixture) plus 10 no-spider controls

(total n¼ 55). The latches to the tops of the mesocosms

were then closed, and we allowed the experimental

community to interact for seven days. At the end of this

time, we collected all of the surviving pests and noted the

resulting community structures and the number of P.

milvina that were recovered at the end of the experiment.

Statistical analyses.—All analyses were performed in

R version 3.0.2 (R Development Core Team 2013).

We first determined the repeatability of activity using

a linear mixed model with the package lme4 (Bates et al.

2014). We included body size and measurement number

as a fixed effect, individuals as random effects, and

RAPHAEL ROYAUTE AND JONATHAN N. PRUITT2904 Ecology, Vol. 96, No. 11

scaled activity values to standard deviation units to ease

convergence. The repeatability of activity was calculated

from the random component of the mixed model as R¼VID/(VID þ VR), where VID represents the among-

individual variance and VR represents the within-

individual, or residual variance. The 95% confidence

intervals (CI) were calculated using bootstrapping with

1000 simulation to assess the magnitude and precision of

activity repeatability and the significance of fixed effects.

We used generalized linear models (GLM) with

Poisson error to evaluate the effects of spider predation

from treatment groups with differing personality com-

positions on pest abundance. Each of the six pest species

was included in a separate GLM with pest abundance

used as the dependent variable and treatment group

included as a fixed effect. We used likelihood ratio tests

to test for an overall treatment effect and Tukey’s

multiple comparison test to detect significant differences

among treatments. We further compared the overlap of

95% CI in the mixture treatment with the average

predation in the active and inactive treatments combined

in order to test for the presence of risk enhancement

(lower survival than that expected by the combined

effect of both phenotypes), risk reduction (higher

survival than that expected by the combined effect of

both phenotypes) or substitutive effects (lack of risk

enhancement or reduction) in the mixture treatment (Sih

et al. 1998). We used a similar procedure for determining

potential differences in cannibalism among treatments.

In order to test for an effect of predator behavioral

type and prey species on capture propensity in single

predator–prey assay, we used a GLM with binomial

error structure. As above, we used likelihood ratio tests

to estimate the strength of the spider activity 3 prey

species interaction. We used nonmetric multidimension-

al scaling (NMDS) in the package vegan (Oksanen et al.

2007) to compare pest community composition between

treatment groups. NMDS is a nonparametric ordination

technique that allows robust representation of commu-

nity structures while not requiring linear relationships

between variables (McCune et al. 2002). Abundance

data were log10(x þ 1)-transformed to reduce the

influence of dominant species and results are based on

the Bray-Curtis dissimilarity matrix. To further test the

effects of treatment group on pest community compo-

sition, we used PERMANOVA to detect an effect of

treatment on average community composition (i.e., to

compare whether treatments differed in their centroids)

and tested for multivariate homogeneity of variance in

community composition between treatments (i.e., to

compare whether treatments differed in their distance to

their centroids).

RESULTS

Activity had moderate repeatability (R ¼ 0.36 [0.30,

0.44] [95% CI]) with similar values to that reported in the

behavioral literature for this trait (Bell et al. 2009). Note

that neither individuals’ body size nor measurement

number was associated with their activity levels (body

size¼�0.003 [�1.44, 1.27]; measurement number¼ 0.03

[�0.02, 0.09]). Taken together, these results demonstrate

that individuals showed consistent differences in activity

levels that are independent of body size and the number

of behavioral measurements (Appendix: Fig. A2).

Spiders’ tendency to attack the various prey species in

isolation was not significantly related to spider activity

(LRT, v2 ¼ 1.358, P ¼ 0.24), nor did we found any

indication of a significant species 3 spider activity

interaction (LRT, v2 ¼ 7.307, P ¼ 0.20). We did,

however, detect strong indication of difference in prey

preference (LRT, v2 ¼ 32.366, P , 0.0001). Potato

leafhoppers and sharpshooters were both more strongly

preyed upon (capture probability .0.5), while alfalfa

weevils, beet armyworms, and pea aphids were generally

rejected in single-predator–single-prey encounters (cap-

ture probability , 0.3; Fig. 1).

Based on the number of spiders recovered at the end

of the experiment, we did not detect any significant

difference in cannibalism rates among treatments (P ¼0.72; Fig. A3). With the exception of beet armyworms,

all pests showed a substantial decrease in abundance

when spiders were added (P , 0.05; Table 1). Three

species (alfalfa weevils, blister beetles, and sharpshoot-

ers) showed significantly lower pest abundance with a

mix of active and inactive personality types (Fig. 2).

These species also showed evidence of risk enhancement

effects since the prey survival in the mixed treatment was

lower than that expected by the sum of the two

personality types (mean pest survival [CI]; alfalfa

weevils, mixed treatment, 3.27 [2.47, 4.32], expected,

5.87; blister beetles, mixed treatment, 6.13 [5.00, 7.52],

expected, 10; sharpshooters, mixed treatment, 2.20 [1.56,

FIG. 1. Effect of predator behavioral type on capturepropensity for each prey species. Values represent averageprobability of capture with 95% confidence intervals based onpredicted values from generalized linear models. Pest species areAw, alfalfa weevil; Ba, beet armyworm; Bb, blister beetle; Pa,pea aphids; Pl, potato leafhopper; and Sh, sharpshooter.

November 2015 2905PREDATOR PERSONALITY AND PREY COMMUNITY

3.09], expected, 3.50). Potato leafhoppers showed no

differences in abundance between mixed and active

groups but both differed significantly from the inactive

treatment. This suggests that either the active pheno-

types contributed most to the control of this species or

that interference among personality types reduced pest

suppression in the mixed treatment. Pea aphids had

significantly lower abundance in all spider treatments,

suggesting that all personality types contributed equally

to the control of this species. In addition, personality

composition generated differences in pest abundance

community composition with the mixed group being the

most distinct from all other treatments (Fig. 3). This

result was corroborated by a significant treatment effect

in the PERMANOVA (P , 0.001). However, the mixed

treatment also showed highest variance in community

composition when performing the multivariate homo-

geneity of variance test (Table 2, P , 0.0001). This

means that the mixed phenotype produced the most

variable results in terms of reduction of pest abundance.

DISCUSSION

The objective of our experiment was to understand

whether varying the representation of predator person-

ality types has an effect on prey community structure.

Our results show that prey regulation depended highly

on the personality types of predators: varying the

representation of active vs. sedentary P. milvina

generated wildly different prey communities over the

course of only a few days. For one-half of the pest

species that we tested, deploying a mixture of active and

inactive personality types led to significant risk enhance-

ment effects compared to monotypic predator groups.

Single-predator–single-prey encounters revealed that

different personality types are equally willing to attack

prey when they are presented to them, thus suggesting

TABLE 1. Effects of phenotypic group composition on pest abundance post treatment.

Speciesand term Estimate SE Z P

LRT

ComparisonsStatistic P

Blister beetles (Epicauta sp.)

Intercept 2.54 0.09 28.64 ,0.0001 31.04 ,0.0001 inactive , controlInactive �0.25 0.12 �2.09 ,0.05 mixed , control***Mixed �0.73 0.14 �5.32 ,0.0001 active , controlActive �0.23 0.12 �1.88 0.06 mixed , inactive**, active . inactive,

active . mixed***

Potato leafhoppers (Empoasca fabae)

Intercept 2.46 0.09 26.61 ,0.0001 64.76 ,0.0001 inactive , controlInactive �0.31 0.13 �2.41 ,0.05 mixed , control***Mixed �0.85 0.15 �5.75 ,0.0001 active , control***Active �1.09 0.16 �6.83 ,0.0001 mixed , inactive***, active ,

inactive***, active , mixed

Pea aphids (Aphis pisum)

Intercept 4.23 0.04 110.63 ,0.0001 44.75 ,0.0001 inactive , control***Inactive �0.34 0.05 �6.47 ,0.0001 mixed , control***Mixed �0.27 0.05 �5.13 ,0.0001 active , control***Active �0.24 0.05 �4.65 ,0.0001 mixed , inactive, active . inactive,

active . mixed

Sharpshooters (Xyphon sp.)

Intercept 1.46 0.15 9.57 ,0.0001 9.6 ,0.05 inactive , controlInactive �0.25 0.21 �1.22 0.22 mixed , control*Mixed �0.67 0.23 �2.9 ,0.005 active , controlActive �0.16 0.2 �0.78 0.43 mixed , inactive, active . inactive,

active . mixed

Alfalfa weevils (Hypera postica)

Intercept 1.81 0.13 14.12 ,0.0001 16.74 ,0.001 inactive , controlInactive 0.01 0.17 0.03 0.97 mixed , control**Mixed �0.62 0.19 �3.26 ,0.005 active , controlActive �0.09 0.17 �0.51 0.61 mixed , inactive**, active , inactive,

active . mixed*

Beet armyworms (Spodoptera exigua)

Intercept 1.99 0.12 16.98 ,0.0001 1.33 0.72 inactive . controlInactive 0.07 0.15 0.5 0.62 mixed , controlMixed �0.04 0.15 �0.28 0.78 active , controlActive �0.07 0.15 �0.46 0.64 mixed , inactive, active , inactive,

active , mixed

Notes: Values represent results of generalized linear models with Poisson error with the control group set as the reference (i.e.,the intercept). Boldface type indicates significance for a , 0.05. Abbreviations are SE, standard error associated with the estimate,and LRT, likelihood ratio test value for the treatment term. Comparisons based on Tukey HSD test.

* P , 0.05; ** P , 0.01; *** P , 0.001.

RAPHAEL ROYAUTE AND JONATHAN N. PRUITT2906 Ecology, Vol. 96, No. 11

that the patterns observed in our mesocosms reflect

more than variation in individuals’ willingness to attack

prey or personality-dependent differences in diet

breadth. When investigating the effects of predator

personality composition at the community level, our

results reveal that deploying a group of only active

predators or combination of both active and inactive

predators created communities with no overlap with our

no-predator controls (Fig. 2). Yet, we also noted that

the active/inactive mixture treatment generated the

greatest variety of experimental outcomes (i.e., the

outcomes were less predictable and more broadly

scattered), whereas the inactive-only and active-only

treatments had very consistent outcomes across repli-

cates.

The fact that a mixture of active and inactive predator

types performs best at suppressing a variety of prey

populations is notable. Although we failed to observe

any instance where sedentary P. milvina were more

effective than active individuals in suppressing any one

prey species, a mixture of active and inactive individuals

was always at least as effective as monotypic groups at

suppressing prey populations and often performed much

better. Similar consequences of intraspecific behavioral

FIG. 2. Changes in pest abundance in relation to phenotypic group composition. Values represent average pest abundance post-treatment with 95% confidence intervals based on predicted values from generalized linear models. Solid line represents pestabundance at the beginning of the experiment, dotted line represents the expected performance of the mixed treatment (calculatedas the average of the active and inactive treatments). Treatments are C, control; I, inactive; M, mixed; and A, active.

FIG. 3. Change in pest community composition dependingon spider phenotypic group. Values are based on nonmetricmultidimensional scaling (NMDS) ordination with 95% densityellipses overlain for each group. Stress¼ 0.15.

November 2015 2907PREDATOR PERSONALITY AND PREY COMMUNITY

variation in predators have been noted in at least one

other experimental system (Finke and Snyder 2008).

Yet, a closer examination of the pest species most

affected by sedentary vs. active foraging types reveals

more curious patterns, which appear at odds with Huey

and Pianka’s predictions (1981). Sap-sucker species tend

to spend extended periods of time with their stylet

inserted into plant vascular tissues (Auclair 1963,

Weintraub and Beanland 2006), yet none of these

species showed evidence for increased predation pres-

sure in the active predator treatment. Similarly, free-

roaming leaf chewers either showed evidence of risk

enhancement in the mixed predator treatment (alfalfa

weevils, blister beetles) or no significant effect of spider

predation (beet armyworms). Overall, it seems that the

results of results of variation in predator personality

composition yields more predictive power at the

community level rather than by examining the effects

on individual prey species.

These details are important to consider because the

outcome of predatory encounters can depend on a

multitude of factors, including prey defenses (e.g., alarm

pheromones and dropping behavior in aphids; Nault et

al. 1973, Losey and Denno 1998) or changes in prey

habitat use in response to predator presence (Schmitz

2005). Current theory on predator–prey dynamics

predicts that the direction and magnitude of multiple

predator effects (MPE; risk enhancement/reduction or

substitutive effects) will depend strongly on the interac-

tion between predator and prey foraging mode as well as

the overlap in habitat domain among predator and prey

species (Schmitz 2007). Risk enhancement is expected to

happen whenever prey species have narrow habitat

domains and their predators have broad and overlap-

TABLE 2. Effect of predator personality type on pest community composition based onPERMANOVA.

Response df F P R2 Comparisons

Treatment 3 9.05 ,0.001 0.35 inactive . controlResiduals 51 mixed . control****, active . control,

mixed . inactive***, active . inactive,active , mixed***

Note: Comparisons based on Tukey HSD test indicating multivariate homogeneity of groupdispersion among treatments.

**** P , 0.0001; *** P , 0.001.

PLATE 1. Male Pardosa milvina. Photo credit: Matthew Persons.

RAPHAEL ROYAUTE AND JONATHAN N. PRUITT2908 Ecology, Vol. 96, No. 11

ping habitat domains and similar hunting strategies. In

this configuration, prey cannot find predator-free space

and predators encounter little risk of intraguild preda-

tion or interference as they do not need to rely

exclusively on a unique prey species (Griffen 2006). P.

milvina has a relatively broad habitat domain (Sitvarin

and Rypstra 2014) but how individual variation in

activity level relates to habitat use remains unknown in

this species. We do not have strong data on the habitat

domains of our various prey species either. Yet, we

detected risk enhancement for three prey species (alfalfa

weevils, blister beetles, and sharpshooters) in our mixed

treatment, thus theory predicts that active and sedentary

P. milvina should have broad and overlapping habitat

domains and that these three prey species will exhibit

narrow habitat domains (Schmitz 2007). Taken togeth-

er, given the necessary data, we reason that the MPE

framework could become a powerful tool for predicting

the relative influence of intra- and inter-specific variation

in predator foraging mode in shaping prey communities.

Some mixtures of predator personality types generat-

ed more variable outcomes than others. While both the

active-only and inactive-only treatments tended to have

very similar outcomes on prey community structure

across replicates, the mixed treatment created wildly

different communities across replicates. This is an

intriguing finding because it suggests that intraspecific

variation in predator populations could be a major

determinant of spatiotemporal variation in prey com-

munity structure, where the same mix of predator

personality types could generate surprisingly different

prey communities across space and time. In contrast,

given our results, one would predict that the erosion of

intraspecific variation in apex predators would generate

a homogenization of prey community composition

across space and time, even when predator abundance

remains constant. This, in turn, has important conser-

vation implications and casts doubt on conventional

management schemes that tend to focus on species

abundance and/or persistence and tend to discount

subtle shifts in key functional traits, like behavior

(Watters et al. 2003, Watters and Meehan 2007).

The findings herein have intriguing ecological impli-

cations because they suggest that any factor that

imposes a selective pressure on predator personality

types (e.g., human-induced rapid environment change,

selective hunting, climate change) is likely to have non-

intuitive consequences for lower trophic levels. For

instance, any selective pressure that reduces trait

variation in predator populations (e.g., via hunting

and poaching, Biro and Post 2008) could yield surprising

rises in the abundance of various prey species, even if

predator population numbers remain largely consistent

through time, since an assemblage of personality types is

predicted to suppress prey communities more effectively

than an equal number of monotypic individuals (Fig. 1).

Likewise, directional selection on predator personality

types could result in either increases or decreases in the

abundance of various prey species, depending on the

direction of selection considered.

One of the most important consequences of our study

is that it brings the animal personality framework to

bear on a classic question in applied ecology: When and

how can natural enemies be used to combat pests? In a

generic sense, our results demonstrate that varying the

personality type of predators has the potential to change

their efficacy as biocontrol agents. Consistent with the

established theory on animal personalities, we show that

a mix of personality types best suppresses an assemblage

of pest species, although the pest communities generated

were also highly variable. Our results lead to several

interesting recommendations for integrative pest man-

agement (IPM) plans. For instance, IPM plans may

benefit by promoting selection regimes that preserve

intraspecific variation in their key and ancillary control

agents. Yet, an alternative could be to deploy manage-

ment practices that favor the persistence of active

individuals, since in our system the active-only treatment

diminished pest numbers reasonably well and generated

highly stereotyped pest communities. Consequently, in

terms of biocontrol potential, it seems the ‘‘optimal’’

personality composition of P. milvina populations

depends on the precise goal in mind: diminish a

particular pest species to the lowest level possible (or

some ‘‘ideal’’ level), diminish the broadest suite of pests

to the lowest levels possible (or some ‘‘ideal’’ level), or

generate a highly predictable prey community, which

may be easier to control with additional regulatory

mechanisms.

It is, of course, important to note that top-down

control on pests resulting from spiders and other

generalist predators is a community process provided

by all species present in an agroecosystem, rather than a

single species (Riechert and Bishop 1990, Symondson et

al. 2002). Intra-guild predation and cannibalism are

common phenomena in such systems and also reduce the

top-down effect of predator assemblages (Buddle 2002,

Balfour et al. 2003). Thus, we argue that an important

way forward would be to quantify which types of

personality compositions have the largest impact on pest

communities whilst minimizing undesired effects (e.g.,

competition within guilds) by considering personality

types in multiple predator species simultaneously.

CONCLUSIONS

We show that altering the composition of personality

types in a top arthropod predator can magnify their top-

down effects by 200–300% (Fig. 1). A mixture of active

and sedentary spiders provided the best pest regulation

service for three of the six pest species tested and the

resulting pest community structure was most variable

with this treatment (Fig. 2). Understanding how this

variation among replicates comes about is essential in

order to move this field forward. These findings also

have practical importance as they show a clear link

November 2015 2909PREDATOR PERSONALITY AND PREY COMMUNITY

between personality composition and the performance

of natural enemies in pest biocontrol.

ACKNOWLEDGMENTS

We thank Jamie Troupe, Austin Dillon, and Jeffrey Taylorfor assistance collecting wolf spiders and the establishment ofour mesocosms. We are indebted to the University ofPittsburgh’s Department of Biological Sciences and theUniversity of Tennessee’s Department of Ecology and Evolu-tionary Biology for support for this research. We thank Ned A.Dochtermann for comments on an earlier draft of this article.We also thank William Snyder and two anonymous reviewersfor their thoughtful comments.

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SUPPLEMENTAL MATERIAL

Ecological Archives

The Appendix is available online: http://dx.doi.org/10.1890/14-2424.1.sm

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