9
Ecology, 92(12), 2011, pp. 2258–2266 Ó 2011 by the Ecological Society of America Landscape of fear influences the relative importance of consumptive and nonconsumptive predator effects CATHERINE M. MATASSA 1 AND GEOFFREY C. TRUSSELL Marine Science Center, Northeastern University, East Point, Nahant, Massachusetts 01908 USA Abstract. Predators can initiate trophic cascades by consuming and/or scaring their prey. Although both forms of predator effect can increase the overall abundance of prey’s resources, nonconsumptive effects may be more important to the spatial and temporal distribution of resources because predation risk often determines where and when prey choose to forage. Our experiment characterized temporal and spatial variation in the strength of consumptive and nonconsumptive predator effects in a rocky intertidal food chain consisting of the predatory green crab (Carcinus maenas), an intermediate consumer (the dogwhelk, Nucella lapillus), and barnacles (Semibalanus balanoides) as a resource. We tracked the survival of individual barnacles through time to map the strength of predator effects in experimental communities. These maps revealed striking spatiotemporal patterns in Nucella foraging behavior in response to each predator effect. However, only the nonconsumptive effect of green crabs produced strong spatial patterns in barnacle survivorship. Predation risk may play a pivotal role in determining the small-scale distribution patterns of this important rocky intertidal foundation species. We suggest that the effects of predation risk on individual foraging behavior may scale up to shape community structure and dynamics at a landscape level. Key words: Carcinus maenas; consumptive effect; nonconsumptive effect; Nucella lapillus; predation risk; Semibalanus balanoides; trait-mediated indirect interaction; trophic cascade. INTRODUCTION Predators can strongly influence ecological communi- ties through trophic cascades. Trophic cascades, in the classical sense, occur when predators eat prey (a consumptive effect or CE), thereby reducing prey density and relaxing consumer pressure on basal resources (Hairston et al. 1960, Paine 1980). Predators can also initiate trophic cascades by scaring prey (a nonconsumptive effect or NCE), because prey often reduce foraging rates in response to predation risk (Sih 1980, Lima and Dill 1990, Abrams et al. 1996, Peacor and Werner 1997, Werner and Peacor 2003). Although both forms of predator effect can enhance the abun- dance of basal resources, the effects of predation risk may more strongly dictate when, where, and what prey eat (for review, see Schmitz et al. [2004]). For example, many prey shift their foraging activities from risky to refuge habitats when they detect predation risk (Werner et al. 1983, Turner and Mittelbach 1990, Trussell et al. 2006). Hence, nonconsumptive effects may play a primary role in determining the distribution and abundance of resources over space and time. The consumptive and nonconsumptive effects of predators are important features of rocky intertidal systems (Trussell et al. 2002, 2004). Carnivorous whelks are common and effective consumers of mussels and barnacles and their impact on the abundance of these resources can strongly influence the structure and dynamics of rocky intertidal communities (Connell 1961, Menge 1976, 1978a, b, Lubchenco and Menge 1978, Hughes and Burrows 1993). The impact of whelk foraging in these systems is determined by a suite of abiotic (e.g., refuge availability, wave exposure, thermal stress; Menge 1978a, b, Fairweather 1988b, Burrows and Hughes 1989, 1990) and biotic factors (e.g., whelk density, age, size, energetic state, and diet history, the availability of mussel or barnacle resources, presence/ absence of predators [Dunkin and Hughes 1984, Hughes and Drewett 1985, Fairweather 1988a, b, Burrows and Hughes 1990, 1991, Palmer 1990, Hughes et al. 1992, Vadas et al. 1994, Trussell et al. 2006, 2008]) that can influence whelk population sizes and shape their foraging decisions. On the rocky shores of New England, risk cues from the predatory green crab (Carcinus maenas) strongly suppress the foraging rates of the Atlantic dogwhelk (Nucella lapillus), driving trait- mediated trophic cascades that rival or exceed the strength of density-mediated cascades driven by reduc- tions in whelk density (Trussell et al. 2006, 2008). Moreover, the absolute and relative strength of non- consumptive effects in this system strongly depends upon habitat type (risky vs. refuge) and resource identity (barnacles [Semibalanus balanoides] vs. mussels [Mytilus edulis]). In risky habitats, green crab predation risk reduces Nucella foraging rates by over 50%, with strong, positive indirect effects on resources, but has little to no Manuscript received 3 March 2011; revised 8 June 2011; accepted 13 June 2011. Corresponding Editor: S. G. Morgan. 1 E-mail: [email protected] 2258

Landscape of fear influences the relative importance of consumptive and nonconsumptive predator effects

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Page 1: Landscape of fear influences the relative importance of consumptive and nonconsumptive predator effects

Ecology, 92(12), 2011, pp. 2258–2266� 2011 by the Ecological Society of America

Landscape of fear influences the relative importance of consumptiveand nonconsumptive predator effects

CATHERINE M. MATASSA1

AND GEOFFREY C. TRUSSELL

Marine Science Center, Northeastern University, East Point, Nahant, Massachusetts 01908 USA

Abstract. Predators can initiate trophic cascades by consuming and/or scaring their prey.Although both forms of predator effect can increase the overall abundance of prey’s resources,nonconsumptive effects may be more important to the spatial and temporal distribution ofresources because predation risk often determines where and when prey choose to forage. Ourexperiment characterized temporal and spatial variation in the strength of consumptive andnonconsumptive predator effects in a rocky intertidal food chain consisting of the predatorygreen crab (Carcinus maenas), an intermediate consumer (the dogwhelk, Nucella lapillus), andbarnacles (Semibalanus balanoides) as a resource. We tracked the survival of individualbarnacles through time to map the strength of predator effects in experimental communities.These maps revealed striking spatiotemporal patterns in Nucella foraging behavior in responseto each predator effect. However, only the nonconsumptive effect of green crabs producedstrong spatial patterns in barnacle survivorship. Predation risk may play a pivotal role indetermining the small-scale distribution patterns of this important rocky intertidal foundationspecies. We suggest that the effects of predation risk on individual foraging behavior may scaleup to shape community structure and dynamics at a landscape level.

Key words: Carcinus maenas; consumptive effect; nonconsumptive effect; Nucella lapillus; predationrisk; Semibalanus balanoides; trait-mediated indirect interaction; trophic cascade.

INTRODUCTION

Predators can strongly influence ecological communi-

ties through trophic cascades. Trophic cascades, in the

classical sense, occur when predators eat prey (a

consumptive effect or CE), thereby reducing prey

density and relaxing consumer pressure on basal

resources (Hairston et al. 1960, Paine 1980). Predators

can also initiate trophic cascades by scaring prey (a

nonconsumptive effect or NCE), because prey often

reduce foraging rates in response to predation risk (Sih

1980, Lima and Dill 1990, Abrams et al. 1996, Peacor

and Werner 1997, Werner and Peacor 2003). Although

both forms of predator effect can enhance the abun-

dance of basal resources, the effects of predation risk

may more strongly dictate when, where, and what prey

eat (for review, see Schmitz et al. [2004]). For example,

many prey shift their foraging activities from risky to

refuge habitats when they detect predation risk (Werner

et al. 1983, Turner and Mittelbach 1990, Trussell et al.

2006). Hence, nonconsumptive effects may play a

primary role in determining the distribution and

abundance of resources over space and time.

The consumptive and nonconsumptive effects of

predators are important features of rocky intertidal

systems (Trussell et al. 2002, 2004). Carnivorous whelks

are common and effective consumers of mussels and

barnacles and their impact on the abundance of these

resources can strongly influence the structure and

dynamics of rocky intertidal communities (Connell

1961, Menge 1976, 1978a, b, Lubchenco and Menge

1978, Hughes and Burrows 1993). The impact of whelk

foraging in these systems is determined by a suite of

abiotic (e.g., refuge availability, wave exposure, thermal

stress; Menge 1978a, b, Fairweather 1988b, Burrows and

Hughes 1989, 1990) and biotic factors (e.g., whelk

density, age, size, energetic state, and diet history, the

availability of mussel or barnacle resources, presence/

absence of predators [Dunkin and Hughes 1984, Hughes

and Drewett 1985, Fairweather 1988a, b, Burrows and

Hughes 1990, 1991, Palmer 1990, Hughes et al. 1992,

Vadas et al. 1994, Trussell et al. 2006, 2008]) that can

influence whelk population sizes and shape their

foraging decisions. On the rocky shores of New

England, risk cues from the predatory green crab

(Carcinus maenas) strongly suppress the foraging rates

of the Atlantic dogwhelk (Nucella lapillus), driving trait-

mediated trophic cascades that rival or exceed the

strength of density-mediated cascades driven by reduc-

tions in whelk density (Trussell et al. 2006, 2008).

Moreover, the absolute and relative strength of non-

consumptive effects in this system strongly depends

upon habitat type (risky vs. refuge) and resource identity

(barnacles [Semibalanus balanoides] vs. mussels [Mytilus

edulis]). In risky habitats, green crab predation risk

reduces Nucella foraging rates by over 50%, with strong,

positive indirect effects on resources, but has little to no

Manuscript received 3 March 2011; revised 8 June 2011;accepted 13 June 2011. Corresponding Editor: S. G. Morgan.

1 E-mail: [email protected]

2258

Page 2: Landscape of fear influences the relative importance of consumptive and nonconsumptive predator effects

effect on consumers or resources in refuge habitats

(Trussell et al. 2006). In contrast, consumptive effects

(reductions in Nucella density) enhance resource abun-

dance in both risky and refuge habitats. Hence,

predation risk may more strongly dictate the spatial

distribution of resources according to the location of

risky vs. refuge habitats within a consumer’s environ-

ment, i.e., the ‘‘landscape of fear’’ (Laundre et al. 2001).

It is becoming increasingly clear that ecological

context can shape the interactions between predators,

consumers, and resources. Studies that have mapped

landscapes of fear for ecologically important consumers

found spatiotemporal correlations among habitat types,

resources, consumers, and predators in the field (Van

der Merwe and Brown 2008, Valeix et al. 2009).

However, to determine the relative importance of

predation risk (NCE) vs. consumer removal (CE) across

a landscape of fear, it is necessary to manipulate each

predator effect independently. In this study, we exam-

ined how the NCEs and CEs of the green crab influenced

spatiotemporal patterns of barnacle survival by altering

Nucella foraging behavior within experimental meso-

cosm communities. Although we recognize the limita-

tions of mesocosm experiments, an advantage of our

experimental system is that we are able to independently

apply both forms of predator effect across an entire

landscape of fear, thereby allowing us to directly map

the strength of each predator effect in isolation and

together (the total predator effect) through time. We

predicted that the strength and relative importance of

NCEs on whelk foraging would increase with distance

from whelk refuges and lead to pronounced spatial

gradients in barnacle survival. Our maps revealed

spatiotemporal patterns in consumer foraging behavior

in response to both NCEs and CEs, but only NCEs

produced strong spatial patterns in resource survival.

MATERIALS AND METHODS

We explored how the predatory green crab (Carcinus

maenas) influenced spatial variation in the foraging

behavior of the whelk Nucella lapillus feeding on

barnacles (Semibalanus balanoides). We fully crossed

two levels of predation risk (crab cues, no crab cues)

with two levels of Nucella removal (removal, no

removal) and randomly applied each treatment combi-

nation to 20 independent flow-through mesocosms (n ¼5) for 36 days. The four treatment combinations of this

design allowed us to obtain independent estimates of

nonconsumptive (NCEs), consumptive (CEs), and total

predator effects (TEs) relative to predator-free controls.

Mesocosms were modified plastic utility boxes (27 3 15

3 5 cm) divided into two chambers with a perforated

barrier. Seawater was delivered to the upstream crab

chamber, which was stocked weekly with 10 Nucella (as

crab food) plus a single green crab (crab cues) or no crab

(no crab cues) to manipulate predation risk. An

experimental barnacle community (15 3 15 cm granite

tile; mean 6 SE, 3150 6 90 barnacles/tile, approximate-

ly 14 barnacles/cm2) and 20 experimental Nucella

( juveniles, shell length 8–10 mm) were placed in the

downstream chamber. Nucella were collected from the

mid- to upper-intertidal near Chamberlain, Maine,

USA. Field estimates of Nucella density at this site

range from 36–152 adults/m2, but reach densities of 436

whelk/m2 when juveniles are included in these estimates

(Menge 1976, 1978b). During our spring–summer

sampling (using 0.263 0.26 m quadrats, n¼ 10), Nucella

densities ranged from 192 to 828 snails/m2 (mean 6 95%CI; 402 6 152 snails/m2) in and around favorable

habitats such as crevices or shaded rock overhangs, and

we observed feeding/breeding aggregations having even

higher densities (Feare 1971).

To simulate green crab consumptive effects, we

manually removed either 0% (no removal) or 16%(removal) of the experimental Nucella present in

appropriate mesocosms every three days (see Peacor

and Werner 2001 and Trussell et al. 2006 for similar

approaches). This simulated ‘‘predation rate’’ (;0.5

snails�crab�1�d�1) exceeds field estimates of green crab

predation on Nucella by more than an order of

magnitude (see Trussell et al. 2006). In addition, we

have also found that the effects of green crab predation

risk on Nucella foraging rates are surprisingly similar for

a broad range of risk cue exposures (Trussell et al. 2011).

For example, exposure to risk cues 25% vs. 100% of the

time (as in this experiment) suppressed Nucella foraging

to the same degree. Hence, we think that our estimates

of the relative strength of NCEs compared to CEs are

likely conservative.

We examined how predator effects on Nucella foraging

behavior and resulting indirect effects on barnacles varied

over space and time by mapping and tracking the survival

of individual barnacles within experimental communities.

We digitally photographed barnacle communities in the

same orientation every 12 d (see Appendix for details).

We divided each community into a 103 10 grid (1.531.5

cm squares; see Appendix: Fig. A1) and determined the

number of live barnacles (B) within each grid square, s, at

time x as Bsx. We calculated the number of barnacles

consumed in each square as Bs0 � Bsx, where Bs0 is the

number of barnacles initially alive in square s at time 0.

To evaluate how predators influenced Nucella–barnacle

interactions, we first calculated the per capita consump-

tion (C ) of barnacles by Nucella (N ) in each square using

the formula Csx¼ (Bs0 – Bsx)/Nx, where Nx is the average

number of Nucella present in the mesocosm through time

x. We then estimated the size of nonconsumptive

(NCEsx), consumptive (CEsx), and total (TEsx) predator

effects on Nucella–barnacle interactions using the follow-

ing equations:

NCEsx ¼ 1� ðCsx Crab;NoRemoval=Csx NoCrab;NoRemovalÞ ð1Þ

CEsx ¼ 1� ðCsx NoCrab;Removal=Csx NoCrab;NoRemovalÞ ð2Þ

TEsx ¼ 1� ðCsx Crab;Removal=Csx NoCrab;NoRemovalÞ: ð3Þ

December 2011 2259LANDSCAPE OF FEAR

Page 3: Landscape of fear influences the relative importance of consumptive and nonconsumptive predator effects

The denominator was the mean Csx for square s at time x,

averaged across all five no-predator control replicates.

This technique yielded five replicate estimates of NCEsx,

CEsx, and TEsx for each square, s, at each time period.

For example, an effect size of 0.65 means that Nucella

reduced per capita foraging rates by 65% relative to no-

predator controls. A negative effect size indicates an

increase in foraging rates, while zero indicates no effect

(see Peacor and Werner 2004 and Trussell et al. 2008 for

similar approaches).We could not calculate the strength of indirect effects

on barnacle abundance using similar equations (e.g.,

TMII or DMII; Okuyama and Bolker 2007, Trussell et

al. 2008) because of the high frequency of zero-value

denominators (BsxNoCrab,No removal¼ 0) by day 24 of the

experiment. Instead, we calculated barnacle survival rate

as the proportion of barnacles in each square that

survived as Psx¼Bsx/Bs0. Comparing Psx in the predator

treatments to the no-predator controls allowed us to

evaluate the indirect effects of predation risk and snail

removal on barnacles.

We constructed contour maps of predator effect size

and barnacle survival at days 12, 24, and 36 across our

experimental communities using values from our 10310

grid. We mapped NCEs, CEs, and TEs on Nucella

foraging behavior by averaging our five replicate

estimates of NCEsx, CEsx, and TEsx, to obtain a single

value per square per time period. We similarly averaged

our five replicate estimates of Psx to map barnacle

survival rates in the no-predator controls (no crab, no

removal) and in each of the three predator treatments

(NCE, CE, and TE) at each time period. From these

contour maps, as well as in our previous work (e.g.,

Trussell et al. 2006, 2008) using the same mesocosm

design, we found that snails under predation risk

retreated to the edges of the tiles for refuge. Presumably

these areas, where the tile contacts the walls of the

mesocosm, simulate the cracks and crevices that snails

utilize in the field. To quantitatively analyze these

patterns, we binned squares from the 10 3 10 grid into

‘‘risk zones’’ that ran parallel to the tile edge (0.0–1.5

cm, 1.5–3.0 cm, 3.0–4.5 cm and 4.5–6.0 cm from the tile

edge; see Appendix: Fig. A1). At each time period, we

randomly selected 10 squares from each risk zone and

calculated the mean effect size and mean proportion of

barnacles that survived for each zone within each

replicate.

We analyzed predator effect sizes using a split-plot

ANOVA that fully crossed effect type (NCE, CE, and

TE), zone (1–4), and day (12, 24, and 36), and

considered these factors as fixed effects. Replicate tiles

were nested within effect type, crossed with zone and

day, and considered random effects (REML methods

used with the ANOVA). To correct for correlated errors

over space (i.e., zone) and time (i.e., day), we used

Greenhouse-Geisser estimates of Box’s epsilon to correct

the degrees of freedom for tests involving zone and day

(PG-G). Because NCE, CE, and TE are ratios, we also

analyzed the data using permutation tests (N¼ 5000) for

comparison (Pperm). We report the most conservative P

values in our results, but provide full details of statistical

tests in the Appendix (Tables A1 and A2).

We analyzed barnacle survival (Psx) in a similar

fashion, with predation risk, removal, zone, and day as

fully crossed, fixed effects. Replicate tiles were nested

within predation risk and removal, crossed with zone

and day, and considered random effects. Assumptions

of normality and equal variances were satisfied for

analyses of both predator effect size and barnacle

survival rates. Analyses were performed using R (R

Development Core Team 2010) with package ‘‘ez’’

(available online).2 We used JMP software (SAS

Institute, Cary, North Carolina, USA) to conduct post

hoc comparisons and to construct contour maps.

RESULTS

Predator effects on the per capita foraging rates

of Nucella

Differences in the size of each predator effect emerged

quickly, but these differences depended on distance from

refuge and varied over time (effect type 3 zone 3 day;

PG-G ¼ 0.035; Fig. 1; Appendix: Table A1). During the

first 12 days, predators had no effect on Nucella foraging

rates in areas closest (0–1.5 cm) to refuge habitat (Fig. 1,

Day 12). However, the size of NCEs and TEs increased

with distance from refuge (zone, F3,16 ¼ 13.5 and 17.6,

respectively, both P , 0.0001), while zone had no effect

on the size of CEs (F3,16¼ 1.3, P¼ 0.3). In habitats more

than 1.5 cm from Nucella refuges, NCEs reduced

Nucella foraging rates by (mean 6 SE) 68 6 8%. NCEs

were 4.4 times stronger than CEs (effect type, F1,8¼20.2,

P ¼ 0.002), and drove the total predator effect through

day 12 in these habitats (Fig. 1, day 12).

NCEs remained stronger than CEs throughout the

experiment in risky habitats (areas . 1.5 cm from

refuge; F1,8 ¼ 95.0, P , 0.0001; Fig. 1, day 36). As a

result, the strong foraging reductions caused by TEs (53

6 12%) were more strongly driven by NCEs (69 6 5%)

than by CEs (�7 6 8%) in risky habitats. In habitats

near refuge, however, NCEs reduced foraging (22 6

4%), but CEs enhanced Nucella per capita foraging rates

(�53 6 5%), perhaps by reducing intraspecific compe-

tition for resources in this preferred habitat. Based on

the absolute value of each effect size, CEs were 2.4 times

stronger than NCEs near refuge (F1,8¼ 21.0, P¼ 0.002),

but TEs remained weak (�8 6 6%) near refuges because

of the opposing contributions of CEs (foraging en-

hancement) and NCEs (foraging reduction) in this

habitat.

Indirect effects of predators on barnacle survival

Changes in Nucella foraging in response to predation

risk quickly produced spatial patterns in barnacle

2 hhttp://CRAN.R-project.org/package¼ezi

CATHERINE M. MATASSA AND GEOFFREY C. TRUSSELL2260 Ecology, Vol. 92, No. 12

Page 4: Landscape of fear influences the relative importance of consumptive and nonconsumptive predator effects

survival that became more pronounced over time (risk3

removal 3 zone 3 day; PG-G¼ 0.007; Fig. 2; Appendix:

Table A2). At day 12, barnacle survival was lowest

within 1.5 cm of refuge (mean 6 SE, 65 6 2%) but

increased with distance from refuge (zone; F3,48¼57.5, P

, 0.0001). The relative increase in barnacle survival with

increasing distance from refuge depended on the

presence of predation risk (risk 3 zone; F3,48 ¼ 5.5, P ¼0.002), but not on snail removal (removal3 zone; F3,48¼0.4, P¼ 0.7) or their interaction (risk3 removal3 zone;

FIG. 1. Size of nonconsumptive (blue), consumptive (red), and total (black) predator effects of the green crab (Carcinus maenas)at days 12, 24, and 36 on the per capita foraging rates of dogwhelks (Nucella lapillus) feeding on barnacles (Semibalanus balanoides).Predator effects were measured across 15 3 15 cm experimental communities (top contour maps) and along a spatial gradient ofhabitat riskiness extending away from the edge of the barnacle community (bottom graphs). Positive values indicate reducedforaging rates, while negative values indicate increased foraging rates. The dotted line indicates no predator effect (size¼ 0). Valueson graphs are means and 95% confidence intervals obtained by bootstrapping (5000 iterations). See Appendix: Table A1 forcorresponding analyses.

December 2011 2261LANDSCAPE OF FEAR

Page 5: Landscape of fear influences the relative importance of consumptive and nonconsumptive predator effects

F3,48 ¼ 0.5, P ¼ 0.7; Fig. 2, day 12). Predation risk

marginally enhanced barnacle survival within 1.5 cm of

refuge (F1,16 ¼ 3.8, P ¼ 0.07), but strongly enhanced

barnacle survival in habitats 1.5–3.0 cm from refuge

(F1,16 ¼ 17.5, P ¼ 0.0007) and further away. In these

riskier habitats, barnacle survival rates were 91 6 1% in

the presence of predation risk, but only 73 6 2% in the

absence of risk (Fig. 2, day 12).

Over time, the complete absence of predator effects

(i.e., no-predator controls) led to uniform depletion of

barnacles throughout the experimental community

(zone; F3,16 ¼ 0.6, P ¼ 0.6), with only 9 6 2% of

barnacles surviving to the end of the experiment.

Predator effects increased barnacle survival in general,

but the magnitude of this increase depended on effect

type and risk zone (risk3 removal3 zone; F3,48¼ 8.7, P

, 0.0001; Fig. 2, day 36). In habitats closest to refuge

(,1.5 cm), NCEs and CEs had similar effects on

barnacle survival (F1,8 ¼ 0.2, P ¼ 0.7), allowing 33 6

4% of barnacles to survive 36 days. In the same habitat

(,1.5 cm from refuge), the combined effects of risk and

removal (the total predator effect, TE) enhanced

barnacle survival to 53 6 4% (F1,12 ¼ 6.6, P ¼ 0.02).

Moving further from refuge habitats (e.g., 3–4.5 cm

from refuge), CEs and TEs enhanced barnacle survival

slightly (0.5 times) more (to 51 6 5% and 776 8%;

respectively). However, NCEs more than doubled

survival rates across the same distance (to 75 6 3%),

causing a strong spatial gradient in barnacle survival.

Though many factors in addition to predation by

Nucella contribute to barnacle survival in the field

(Connell 1961, Bertness 1989, Hancock and Petraitis

2001, Petraitis et al. 2003), the survival rates we observed

in our experiment fall within the range of published

values for S. balanoides during spring/summer (from 0%

to ;67% per 12 weeks; see Bertness 1989 and Petraitis et

al. 2003).

DISCUSSION

Consumptive and nonconsumptive predator effects

influenced the foraging behavior of Nucella, but these

effects varied over space and time, with different

consequences for barnacle survival. The strength of

nonconsumptive effects (NCEs) increased with distance

from consumer refuges, reducing Nucella foraging rates

in all habitats except those closest to refuge. In contrast,

consumptive effects (CEs) enhanced per capita foraging

by Nucella near refuges, but had little to no effect in

other habitats. In the absence of predators, barnacle

survival was low and similar in all habitat types after 36

days (;9%). Both NCEs and CEs enhanced barnacle

survival overall, but NCEs resulted in a much stronger

spatial pattern than CEs or the total predator effect

(TE). This distinction emerged largely because of

differences in how the per capita effects of predators

on consumers scaled up to population-level effects of

consumers on resources.

Our results are consistent with optimal foraging

theory, which predicts that consumers will forage in a

given habitat until resources fall below some threshold

density that balances the costs (search time, vulnerability

to predators) and benefits (energy gain, growth) of

foraging (MacArthur and Pianka 1966, Sih 1980). This

threshold resource density, or ‘‘giving up density’’

(Brown 1988), is likely to vary across a forager’s

landscape of fear (Laundre et al. 2001) because

consumers may tolerate lower per capita resource levels

in refuge habitats when other habitats, despite their

having more resources, are also more risky (Brown 1999,

Brown and Kotler 2004). In the absence of predator

effects, Nucella initially displayed a slight preference for

barnacles close to refuge, but quickly expanded their

foraging area once resources near refuge declined.

Eventually, resources were depleted across the entire

landscape. Nonconsumptive effects caused Nucella to

remain in habitats near refuge despite their declining

barnacle supply and despite an abundance of barnacles

only a few centimeters away from refuge. Predation risk

effectively lowered the giving-up density of barnacles in

safer habitats, resulting in weak NCEs near refuge but

strong NCEs in riskier habitats. Furthermore, because

nonconsumptive effects impacted all Nucella simulta-

neously, the high density of ‘‘scared’’ Nucella quickly

consumed barnacle resources near the refuge, while

leaving other resources intact. This foraging behavior

created a strong barnacle survival gradient between

areas near the refuge (32% survival) and areas further

away (72% survival), producing distinct patches of low

(;5 barnacles/cm2) and high (;11 barnacles/cm2)

barnacle density, respectively.

In contrast, consumptive and total predator effects

produced a more homogeneous pattern of barnacle

survival because reductions in conspecific density slowed

the depletion of barnacles. When consumptive effects

acted alone, slow barnacle depletion allowed per capita

foraging rates to remain high relative to no-predator

controls in preferred habitats, resulting in strong CEs on

foraging rates near refuge. However, this effect did not

produce a strong barnacle survival gradient because the

increase in per capita foraging rates near the refuge only

influenced the few remaining Nucella that ‘‘survived’’

our simulated predation. Furthermore, in the absence of

predator risk cues, the remaining Nucella continued to

forage in riskier habitats at the same per capita rate as

Nucella without predators (CE¼ 0). When both risk and

consumptive effects were operating (i.e., the total

predator effect), surviving Nucella avoided risky habits

and allowed barnacle survival to remain high (77%survival). Unlike NCEs, however, TEs did not cause a

strong barnacle survival gradient because reductions in

Nucella density diminished the total foraging impact of

Nucella on barnacles near the refuge (51% survival).

Our results support previous work suggesting that the

strong influence of nonconsumptive effects in natural

systems emerges because predators can quickly and

CATHERINE M. MATASSA AND GEOFFREY C. TRUSSELL2262 Ecology, Vol. 92, No. 12

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FIG. 2. Contour maps (top) of the proportion of barnacles (Semibalanus balanoides) surviving (Psx) to days 12, 24, and 36within 15315 cm experimental communities. Graphs (bottom) indicate the proportion barnacles surviving (mean 6 SE) at varyingdistances from refuge habitats in no-predator controls (open symbols) or in treatments testing for nonconsumptive (blue),consumptive (red), and total (black) predator effects of the green crab (Carcinus maenas) on dogwhelks (Nucella lapillus). At right,we present photographs of representative barnacle communities at days 12, 24, and 36; the bottom photograph is a samplecommunity at the beginning of the experiment (0 d). See Appendix: Table A2 for corresponding analyses.

December 2011 2263LANDSCAPE OF FEAR

Page 7: Landscape of fear influences the relative importance of consumptive and nonconsumptive predator effects

simultaneously scare many prey, with strong and rapid

effects on resources (Peacor and Werner 2001, Werner

and Peacor 2003). Increased attention to the effects of

predation risk is changing views of how communities are

structured and ecosystems function over space and time

(e.g., Schmitz et al. 2008). For example, the reintroduc-

tion of wolves in Yellowstone National Park has had

significant impacts on this ecosystem that appear to be

strongly driven by elk responses to wolf predation risk

(Creel et al. 2005). When wolves are present, elk retreat

from open grasslands and riverbeds to the protective

cover of forest edges (Creel et al. 2005, Fortin et al.

2005). This behavior has fostered the recovery of woody

vegetation along riverbeds and helped to restore beaver

populations, riparian ecosystem functions, and hydro-

logical processes (Ripple and Beschta 2004). In addition,

changes in elk habitat use alter spatial patterns of energy

and nutrient dynamics across the Yellowstone landscape

(Frank 2008). However, determining the relative impor-

tance of NCEs and CEs to the dynamics of this system

has been difficult (Creel and Christianson 2009) because

the experiments necessary to do so are particularly

challenging at this scale.

Although our experiment involved considerably

smaller spatial scales, we suggest that the observed

effects of predation risk on the spatial distribution of

barnacles may scale up to influence rocky intertidal

community dynamics on a landscape level. Indeed,

community structure can be driven by interactions

operating on an even smaller spatial scale. Raimondi

et al. (2000) found that the greater structural complexity

afforded by conic vs. predator-induced bent morphs of

barnacles (Chthamalus anisopoma) dictated whether a

patch became mussel or algae dominated. The small-

scale patterns of barnacle survival caused by predation

risk in our experiment are similar to the gradients in

barnacle population structure and ‘‘predation haloes’’

around cracks and crevices often noted by others

working in the field (Fairweather 1988d, Johnson et al.

1998). For example, the risk of dislodgement due to high

wave energy restricts the foraging range of whelks on

exposed headlands, resulting in areas of bare space or

reduced prey density near crevices used by whelks for

refuge (Menge 1978b). The risk of desiccation or thermal

stress may cause similar patterns on more protected

shores, where crevices, the undersides of boulders, tide

pools, or algal patches provide cool, moist refuges

(Fairweather 1988d, Johnson et al. 1998). By altering the

spatial foraging patterns of consumers, predation risk

may have a broad influence on the structure and

dynamics of rocky shore communities by creating the

striking spatial patterning in barnacle distributions that

are often observed in the field (Fairweather 1988c, d,

1990).

On the rocky shores of New England, barnacles

strongly influence community succession (Menge 1976,

1978a, b, 1995, Bertness et al. 2002, 2004, Kordas and

Dudgeon 2010) because they buffer thermal stress,

provide physical structure for settlement of other

species, and interfere with herbivore grazing on algal

recruits (Lubchenco 1983, Bertness 1989, Navarrete and

Castilla 1990). The prominent role of barnacles is

partially due to their ability to preempt space because

they are one of first organisms to recruit in early spring

after winter storm disturbances, and their density

influences the subsequent recruitment of other species,

such as canopy-forming seaweeds (e.g., Ascophyllum

nodosum, Fucus spp.) and mussels (Mytilus edulis)

(Lubchenco 1983, Bertness et al. 2002). For example,

depending on their development stage (e.g., Kordas and

Dudgeon 2010), barnacle density can facilitate seaweed

recruitment by creating spatial refuges that limit the

effectiveness of herbivore grazing (Lubchenco 1983).

We suggest that the strength of positive interactions

between barnacles and other species may be determined

by how the effects of risk on Nucella foraging behavior

shape the abundance and distribution of barnacles.

Predation risk should allow positive interactions be-

tween barnacles and other species to be strong in areas

away from Nucella refuges (high barnacle survival), but

weak in areas close to refuges (low barnacle survival).

Spatial patterns in barnacle survival could also shape

density-dependent intraspecific interactions, growth

rates, morphology (e.g., hummock formation), and

fitness of individual barnacles (Bertness 1989, Bertness

et al. 1998). Furthermore, by increasing heterogeneity or

patchiness of the barnacle community (i.e., causing

adjacent patches of high and low barnacle survival or

density), nonconsumptive effects may influence diversi-

ty, productivity, and dynamics at the community and

landscape level (Duggins 1983, Sousa 1984, Fairweather

1988c, Dunstan and Johnson 2006). Indeed, predation

risk and the landscape of fear (i.e., the distribution of

consumer refuges) may provide an explanation for why

consumer pressure and community structure is often

patchy on rocky shores (Lubchenco and Menge 1978,

Fairweather 1988c, d, 1990).

The scale of our experiment allowed us to indepen-

dently estimate the influence of nonconsumptive, con-

sumptive, and total predator effects on individual prey

foraging decisions that, in turn, determined the survival

and distribution of resources. Our study highlights that

the effects of predators on Nucella–barnacle interactions

are ultimately context dependent: they rely upon the

location of barnacles within Nucella’s landscape of fear.

Nonconsumptive effects on foraging behavior are much

stronger than consumptive effects in habitats where

Nucella are more vulnerable to predators. Noncon-

sumptive effects drive the total predator effect in these

habitats and strongly influence the distribution of

resources. In contrast, consumptive effects on foraging

behavior develop slowly and only in refuge habitats,

with much weaker effects on resource distribution. We

suggest that mapping the strength of predator effects

across landscapes of fear at larger spatial scales may

allow more robust assessment of where, when and how

CATHERINE M. MATASSA AND GEOFFREY C. TRUSSELL2264 Ecology, Vol. 92, No. 12

Page 8: Landscape of fear influences the relative importance of consumptive and nonconsumptive predator effects

predators influence community structure and ecosystem

function. Such maps may reveal the contexts in whichpredator introduction or removal can be an effective

management strategy.

ACKNOWLEDGMENTS

We thank the Marine Science Center for providing anexcellent work environment, our families for their support, andP. Ewanchuk, G. Bernatchez, E. Bryson, and J. Page forenduring winters on the river. We thank an anonymousreviewer and P. Petraitis for especially helpful comments thatimproved this manuscript. This study is part of the Ph.D.dissertation of C. M. Matassa and was generously supported byNSF grants OCE-0648525 and OCE-0727628 to G. C. Trussell.This is contribution #274 from Northeastern University’sMarine Science Center.

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APPENDIX

Description of techniques used to map and monitor barnacles and tables of statistical results (Ecological Archives E092-196-A1).

CATHERINE M. MATASSA AND GEOFFREY C. TRUSSELL2266 Ecology, Vol. 92, No. 12