Ecology, 91(11), 2010, pp. 3177–3188� 2010 by the Ecological Society of America

Differential tree and shrub production in response to fertilizationand disturbance by coastal river otters in Alaska

AARON M. ROE,1 CAROLYN B. MEYER,1,2,3 NATHAN P. NIBBELINK,4 AND MERAV BEN-DAVID3,5

1Department of Botany, University of Wyoming, Laramie, Wyoming 82071 USA2ARCADIS U.S. Inc., Lakewood, Colorado 80401 USA

3Department of Zoology and Physiology, University of Wyoming, Laramie, Wyoming 82071 USA4Warnell School of Forestry and Natural Resources, University of Georgia, Athens, Georgia, 30602 USA

Abstract. We explored the interacting effects of marine-derived nutrient fertilization andphysical disturbance introduced by coastal river otters (Lontra canadensis) on the productionand nutrient status of pristine shrub and tree communities in Prince William Sound, Alaska,USA. We compared production of trees and shrubs between latrines and non-latrines, whileaccounting for otter site selection, by sampling areas on and off sites. Nitrogen stable isotopeanalysis (d15N) indicated that dominant tree and shrub species assimilated the marine-derivedN excreted by otters. In association with this uptake, tree production increased, but shrubdensity and nonwoody aboveground shrub production decreased. The reduced shrubproduction was caused by destruction of ramets, especially blueberry (Vaccinium spp.),through physical disturbance by river otters. False azalea (Menziesia ferruginea) ramets wereless sensitive to otter disturbance. Although surviving individual blueberry ramets showed atendency for increased production per plant, false azalea allocated excess N to storage inleaves rather than growth. We found that plant responses to animal activity vary amongspecies and levels of biological organization (leaf, plant, ecosystem). Such differences shouldbe accounted for when assessing the influence of river otters on the carbon budget of Alaskancoastal forests at the landscape scale.

Key words: aquatic–terrestrial linkages; disturbance; feces; latrine; d15N; Lontra canadensis; nitrogen;Prince William Sound, Alaska; ramets; river otter; stable isotopes.

INTRODUCTION

Transfer of energy and nutrients across ecosystem

boundaries can elicit variable responses in the recipient

ones depending on trophic position, ecological process,

biotic and abiotic conditions, and the ratio between the

subsidy and local resources (Knight et al. 2005,

Marczak et al. 2007, Michelutti et al. 2009). In some

cases, cross-ecosystem nutrient fluxes can be as

important as transfers within individual ecosystems

(Polis et al. 1997, Reiners and Driese 2001). For

example, terrestrial animals feeding in freshwater and

marine habitats transfer nutrients from these aquatic to

adjacent terrestrial ecosystems, leading to increases in

primary production in the latter (e.g., Anderson and

Polis 1999, Sanchez-Pinero and Polis 2000, Croll et al.

2005). Such increases in production are comparable in

magnitude to positive effects of moderately elevated

local herbivory observed in some systems (e.g.,

McNaughton et al. 1988, Frank and McNaughton

1993, Singer and Schoenecker 2003, Holdo et al. 2007),

or nitrogen fixation by alder (Alnus spp; Binkley 1983,

Vogel and Gower 1998, Helfield and Naiman 2006).

Several studies in temperate forests have shown

increased nitrogen (N) concentration in plant tissue

or increased plant production in response to such

animal-mediated nutrient transfers (Ben-David et al.

1998a, b, Hilderbrand et al. 1999, Helfield and Naiman

2001, 2002, Crait and Ben-David 2007).

Aside from deposition of nutrients, animal activities

can physically damage plants through feeding or

disturbance. Impacts of herbivory on plant productiv-

ity vary in magnitude and direction depending on

environmental conditions and feeding intensity, al-

though heavy browsing and grazing usually reduce

plant production (Huntly 1991, Paige 1992, Post and

Pedersen 2008). Similarly, non-herbivorous animals

can decrease plant production through physical distur-

bance such as digging, cratering, and trampling (e.g.,

Huntly and Inouye 1988, Naiman 1988, Jones et al.

1997, Tardiff and Stanford 1998). Thus, the interaction

between negative effects of animal disturbance, unre-

lated to herbivory, and positive cross-ecosystem nutri-

ent deposition may affect plant production in

unforeseen ways at the level of the individual and at

the ecosystem scale.

Coastal river otters (Lontra canadensis) forage on

marine prey from the intertidal and pelagic zones

(Blundell et al. 2002, Ben-David et al. 2005) and come

ashore to scent mark via defecation and urination in

Manuscript received 6 July 2009; revised 4 January 2010;accepted 1 March 2010; final version received 24 March 2010.Corresponding Editor: N. J. Sanders.

5 Corresponding author. E-mail: bendavid@uwyo.edu

3177

specific locations along the shoreline known as latrines.

Through these activities, otters serve as a vector for the

transport and deposition of marine-derived nutrients to

the terrestrial landscape. Latrines, particularly commu-

nal ones, can receive substantial quantities of potentially

limiting nutrients over the course of several decades

(Ben-David et al. 2005). Such nutrient additions can

increase N content in leaves and potentially enhance

plant growth because of alleviation of N deficiency

(Vitousek and Howarth 1991). Alternatively, when

excess N is not allocated to growth as a result of

limitation by other factors, such as light or water

(George et al. 1999), plants may store these nutrients in

tissues as luxury consumption, making N available in

the future should the limiting conditions change (Chapin

1980). Localized responses of plants to otter fertilization

may translate into large-scale changes in ecosystem

production because river otter latrines are common

along both the Atlantic and Pacific coastlines (Bowyer et

al. 2003).

Although latrines serve mainly as olfactory commu-

nication centers, river otters also use these sites for

resting, denning, and as rubbing platforms to restore the

thermoregulatory capacity of their fur (Estes et al.

2008). Thus, the repeated visitations of latrines by

individual otters can introduce considerable physical

disturbance in the form of trampling, digging, and

rubbing, which may confound any positive response of

plants to nutrient fertilization. It is likely that different

growth forms (e.g., trees, shrubs, or herbaceous plants)

or different levels of organization (e.g., individuals vs.

community) would be differentially susceptible to otter

disturbance.

To assess the interacting effects of nutrient deposition

and physical disturbance from coastal river otters, we

investigated the production and nutrient status of the

shrub and tree communities on latrines in Prince

William Sound, Alaska, USA. Specifically, we addressed

three questions. (1) Does nutrient deposition from otters

increase availability and uptake of marine-derived N

(enriched in 15N relative to N derived from terrestrial

sources; Ben-David et al. 1998a), evident from enrich-

ment in the foliar d15N of shrubs and trees on latrine

sites relative to areas not used by otters? (2) Does the

increased assimilation of marine-derived N translate

into increased production of individual shrubs and trees

and an increase in foliar N content? (3) Does increased

individual plant production correspond to higher

aboveground production at the ecosystem level? A

concurrent increase in individual- and ecosystem-level

production on latrines at both canopy layers (shrubs and

trees) would indicate that nutrient deposition is the

main factor influencing plant responses. In contrast,

reduction in ecosystem production of the shrub layer

would suggest that disturbance from trampling is the

more important process dominating understory plant

responses.

STUDY AREA

The study area consisted of 145 km of shoreline along

northern Knight, Ingot, and Eleanor Islands (608230 N,

1478400 W; Fig. 1) in western Prince William Sound,

Alaska, USA. A maritime climate in Prince William

Sound results in cool, wet summers and deep snow

accumulations during the winters (2400 mm average

annual precipitation for 1971 to 2000), and at lower

elevations, the snow-free period extends from early May

to early November (data from the Alaska Climate

Research Center, available online).6

Vegetation is dominated by a coastal, old-growth

western hemlock (Tsuga heterophylla)–Sitka spruce

(Picea sitchensis) forest. Sitka spruce is the most

common tree in the nearshore margin, whereas western

hemlock occurs on the upland portions of the landscape

(Bowyer et al. 2003). The shrub layer is well developed,

consisting of several species of blueberry (Vaccinium

spp.), false azalea (Menziesia ferruginea), Devil’s club

(Oplopanax horridus), and salmonberry (Rubus specta-

bilis; Viereck et al. 1992) with blueberry (30% canopy

FIG. 1. Location of river otter (Lontra canadensis) latrinesand non-latrine sites on Knight, Ingot, and Eleanor Islands inPrince William Sound (PWS), Alaska, USA, used for vegeta-tion sampling in the summers of 2006 and 2007. Sampled latrinesites are a subset of the 100 sites selected for fecal depositionsurveys and the 320 total latrines identified in the study area.

6 hhttp://climate.gi.alaska.edui

AARON M. ROE ET AL.3178 Ecology, Vol. 91, No. 11

cover) and false azalea (27% canopy cover) dominating

in most locations. Sitka alder (Alnus viridis), which relies

on atmospheric N fixation, grows on disturbed sites and

near the boundary between the terrestrial vegetation and

the intertidal zone (Ben-David et al. 1998a). The

herbaceous layer consists of a mixture of perennial

vascular plants (e.g., Cornus canadensis and Maianthe-

mum dilatatum), ferns (e.g., Gymnocarpium dryopteris),

and bryophytes (e.g., Hylocomium splendens and Rhyti-

diadelphus loreus).

METHODS

Site selection and sampling design

We selected a subsample (30 in 2006 and 53 in 2007)

of latrine sites previously chosen for monitoring of fecal

deposition (Appendix A) for evaluation of woody plant

response to otter latrine activity (Fig. 1). To ensure that

these latrines were representative, we used stratified

random sampling, stratifying by activity level (high and

low use) and geographic location within the study area

(Appendix A). We also randomly selected 19 non-latrine

sites in 2006 and 9 in 2007 along the same coastline (Fig.

1; see Roe 2008). The range of sizes of non-latrines

sampled was similar to the range of sizes of actual

latrines. Variables were measured on both (1) the

actively used area of the latrine (‘‘on’’-latrine) or

similarly located area on each non-latrine (surrogate

‘‘on’’ area) and (2) an adjacent unused vegetated area of

each latrine (‘‘off ’’-latrine) and non-latrine (surrogate

‘‘off ’’ area), either along two parallel transects or in

randomly selected 1-m2 plots (Appendix A: Fig. A1).

Stable isotope analysis

We collected current-year foliage of blueberry, false

azalea, and western hemlock for determination of d15Nand d13C. Each sample was dried for 48 hours at 60–

708C, ground using a dry tissue grinder (Glenn Mills,

Clifton, New Jersey, USA), and analyzed in duplicate

using a Finnigan Deltaplus XP spectrometer (Thermo

Electron North America, West Palm Beach, Florida,

USA) attached to a Costech ECS elemental analyzer

(Costech Analytical Technologies, Valencia, California,

USA) at the University of Wyoming Stable Isotope

Facility, Laramie, Wyoming, USA. Results were ac-

cepted only if variance between every two replicates did

not exceed the peptone (d13Cstd ¼�15.17 and d15Nstd ¼5.48) or acetil (d13Cstd ¼ �30.07 and d15Nstd ¼ 0.34)

standards, and machine linearity did not deviate from

0.99. Samples that had coefficient of variation greater

than that of these standards after two additional

replications were discarded.

Shrub cover and ramet density

We measured percent canopy cover of blueberry and

false azalea using the line-intercept method (Lucas and

Seber 1977) along the two transects. The canopy cover

for each transect for the ‘‘on’’ and ‘‘off ’’ portions of each

site was calculated and the values from the two transects

in each portion were averaged.

Because of vegetative reproduction, a single shrub

may have several shoots (ramets; Antos and Zobel 1985,

Haeussler and Coates 1986) and these individual ramets

may share resources (e.g., Wijesinghe and Hutchings

1997, Pennings and Callaway 2000). Nonetheless, we

sampled individual ramets as if they were independent of

each other because it was impossible to determine the

extent of individual plants. To estimate density of

blueberry and false azalea, we counted ramets in five

1-m2 plots randomly located within each of the ‘‘on’’ and

‘‘off ’’ portions of all sites in 2006 and 2007.

Aboveground annual nonwoody shrub production

Shrub production for the year was sampled at two

levels: production per ramet (grams per plant) and

production per unit area (referred to as ecosystem

production; grams per square meter).

Production per ramet.—To estimate production per

ramet, we collected the current-year leaves and twigs

from individual ramets of blueberry and false azalea in

2006, and then dried and weighed them to the nearest

0.1 g. Because plant production increases with increasing

plant size, we measured three morphological variables

that scale with leaf number and, subsequently, mass of

new production (Appendix B; see also West et al. 1999,

Enquist 2002). We developed allometric relationships

for each species, in which log10-transformed shrub

production was the predicted variable and base diam-

eter, height, and number of branches were the indepen-

dent variables (Appendix B). The back-transformed

residuals from these allometric relationships were used

to represent the nonwoody production per ramet

relative to predicted production based on plant size

(hereafter relative production; where 1.0 ¼ same as

predicted (Drezner 2003); Appendix B).

Ecosystem shrub production.—To estimate ecosystem

shrub production, we multiplied ramet density of

blueberry and false azalea by the production per ramet

for the ‘‘on’’ and ‘‘off ’’ portions of each site during 2006.

In 2007, samples of all new nonwoody growth of

blueberry and false azalea from one randomly selected

1-m2 plot on each ‘‘on’’ and ‘‘off ’’ portion of sites were

collected and weighed. Although we estimated fruit

production separately, we included it in overall ecosys-

tem shrub production because fruit biomass was

substantially lower than biomass of leaves and twigs

(3–6% of production) and did not change the patterns

that we observed for nonwoody production.

Shrub leaf area index (LAI).—We estimated effective

shrub leaf area index (LAI; Chen 1996), defined as half

the total green leaf area per unit ground (Chen and

Black 1992), for the shrub layer from 0.3 to 2 m above

the ground in 2006 using a Decagon AccuPAR LP-80

ceptometer (hereafter AccuPAR; Decagon Devices,

Pullman, Washington, USA). Transmittance of photo-

synthetically active radiation (PAR) was sampled every

November 2010 3179OTTER ACTIVITY AND PLANT PRODUCTION

2 m along a portion of both parallel transects on both

the ‘‘on’’ and ‘‘off ’’ portions of each site. We included

only those sites that had .50% overstory cover in the

sampled area, based on 36 PAR transmittance readings

(Decagon Devices 2004) over a 103 10 m grid to restrict

interpretation of the results to sites with a closed canopy

(4 latrines and 1 non-latrine were excluded). This

measured PAR transmittance through the canopy was

used to calculate the effective shrub LAI using the

inverted equation for predicting scattered and transmit-

ted PAR proposed by J. Norman (Decagon Devices

2004) in conjunction with Campbell’s (1986) light

extinction model.

Tree production

Tree leaf area index.—To provide an estimate of

ecosystem production of the overstory layer, we

estimated tree effective LAI using PAR measurements

above and below the tree canopy (.2 m height) using

the same equations and measured at the same locations

as described for the shrub effective LAI. We obtained

incoming PAR measurements (above the canopy), by

placing a second AccuPAR that logged data every

minute (Decagon Devices 2004) on the unshaded

shoreline or on a boat.

A negative relationship existed between transmittance

and the beam fraction, resulting in an overestimation of

LAI values on days with partly cloudy to clear skies.

Therefore, we limited our subsequent analyses to data

that did not deviate from a beam fraction of 0.01 (18

latrines and 5 non-latrines excluded) to verify that all

measurements were taken under similar light conditions.

Similar to the shrub LAI procedure, sites with ,50%tree cover were excluded, yielding a final sample size of

15 latrine and 14 non-latrine sites.

Tree basal area.—We estimated tree density using the

point-centered quarter method every 5 m along the two

transects for each site, using the equations by Eberhardt

(1967). Additionally, we measured the diameter at

breast height for each tree sampled for density. To

remove the effect of tree size (cross-sectional stem area)

and density on LAI, we calculated the basal area of trees

on each site and divided effective LAI estimates by basal

area to provide an index of leaf production per unit of

stem area.

Foliar nitrogen content

Subsamples of leaves collected from western hem-

lock, blueberry, and false azalea were analyzed for leaf

N concentration (calculated as percentage). Analyses

were performed with an ECS4010 Elemental Analyzer

(Costech Analytical Technologies, Valencia, Califor-

nia, USA) at the University of Wyoming Stable Isotope

Facility.

Statistical analysis

Because observed differences between latrine and non-

latrine sites may result from otter site selection (Crait

and Ben-David 2007), and not nutrient deposition

alone, it was important to account for the former in

our analyses. To evaluate the effect of otter activity

independent of latrine site selection, we calculated the

difference in measured variables between the ‘‘on’’ and

‘‘off ’’ portion of each latrine and contrasted it with the

difference between the surrogate ‘‘on’’ and ‘‘off ’’

portions of each non-latrine site (hereafter the contrast

in the differences is called the otter interaction effect).

Our sampling design is equivalent to a before–after

control–impact study (McDonald et al. 2000), where

before–after are replaced with off–on. We assumed that

otter activity on latrines accounted for the differences if

the on/off trends were not similar for the two site types.

To test for the statistical significance of this otter

interaction effect, we used independent sample random-

ization tests with 10 000 resamples or the number of

possible unique combinations (to a minimum of 1000

resamples), whichever was smaller (Manly 2007), using

the module Resampling Stats (Resampling Stats, Ar-

lington Virginia, USA). We used an a level of 0.05 to

designate statistical significance on all tests except those

where sample sizes per group were less than 10. In such

cases, we assessed significance at the a ¼ 0.1 level.

Because d15N, foliar N, and effective tree LAI were

expected to only be influenced by the positive effect of

fertilization, we used one-sided rather than two-sided

tests (Manly 2007). The rest of the randomization tests

were two-sided independent tests.

We used leaf-level nutrient vector analysis, an

evaluation of leaf nutrient concentration, content, and

mass, to determine plant nitrogen status (Timmer and

Armstrong 1987). Vector analysis allows for detection

and isolation of dilution effects, nutrient imbalances,

and element interactions in a graphic format known as a

nomogram (Haas and Rose 1995). We tested for

changes in each of the vector components with a two-

sided independent sample randomization test between

the ‘‘on’’ latrine areas and ‘‘on’’ portions of non-latrines.

RESULTS

Stable isotopes

Values of d15N in blueberry, false azalea, and western

hemlock foliage were higher on latrines (means 6.0% to

6.8%) than on areas without otter activity (means

�4.0% to 4.0%; Fig. 2). The otter interaction effect in

d15N was significant and positive, indicating that

marine-derived N was assimilated by all three species

(blueberry, P ¼ 0.04; false azalea, P ¼ 0.07; western

hemlock, P ¼ 0.01; Fig. 2).

Mean values of foliar d13C for all three species

showed no significant otter interaction effect between

latrine and non-latrine sites (blueberry P ¼ 0.63, false

azalea P ¼ 0.11, western hemlock P ¼ 0.55; Fig. 2),

indicating that sampled sites did not differ in properties

that led to water stress in shrubs or trees (Dawson et al.

2002).

AARON M. ROE ET AL.3180 Ecology, Vol. 91, No. 11

Shrub cover and ramet density

Otter activity was associated with reduced shrub cover

and ramet density, but the magnitude and significance

varied depending on the species. Blueberry cover showed

a large negative otter interaction effect (P , 0.005; Fig.

3). Although the pattern was similar, the reduction in

cover for false azalea was not significant (otter

interaction effect, P ¼ 0.21; Fig. 3). Otter activity

reduced ramet density of both blueberry and false

azalea, but the effect on blueberry was larger than on

false azalea (blueberry P , 0.005, false azalea P , 0.005;

Fig. 3).

Aboveground annual nonwoody shrub production

Individual shrub production.—After accounting for

ramet size, we found no significant otter interaction

effect in the relative shrub production for either species.

Nonetheless, surviving blueberry ramets showed a

moderate trend of increased relative production on

latrine sites, as might be expected if individual ramets

were responding to increased N availability (P ¼ 0.23;

Fig. 3); no such trend was detected in false azalea (P ¼0.96; Fig. 3).

Ecosystem shrub production.—Otter activity negative-

ly affected blueberry ecosystem production. A negative

otter interaction effect existed for the estimated relative

FIG. 2. (A) Stable isotope d15N and d13C values of foliage (mean 6 SE) of blueberry (Vaccinium spp.), false azalea (Menziesiaferruginea), and western hemlock (Tsuga heterophylla) collected from river otter latrines and non-latrines in Prince William Sound,Alaska in the summers of 2006 and 2007. Variables were measured on both (1) the actively used area of the latrine (‘‘on’’-latrine) orsimilarly located area on each non-latrine (surrogate ‘‘on’’ area) and (2) an adjacent unused vegetated area of each latrine (‘‘off ’’-latrine) and non-latrine (surrogate ‘‘off ’’ area), either along two parallel transects or in randomly selected 1-m2 plots. Gray symbolsrepresent latrines, and open symbols are non-latrines. Triangles indicate the ‘‘on’’ portions of sites while squares indicate the ‘‘off ’’portions of sites. (B) The otter interaction effect (comparison of the ‘‘on’’ and ‘‘off ’’ stable isotope values of latrine and non-latrines,respectively) for blueberry (n ¼ 9 and 6), false azalea (n ¼ 16 and 2), and western hemlock (n ¼ 8 and 5). Significant differencesbetween latrines and non-latrines at a¼ 0.05 (for n . 10) or a ¼ 0.10 (for n , 10) are represented by different lowercase letters.

November 2010 3181OTTER ACTIVITY AND PLANT PRODUCTION

production for 2006 and for the production per 1-m2

plot collected in 2007 (P ¼ 0.10 for each year; Fig. 3).

Ramet density for all 1-m2 plots measured on latrine and

non-latrine sites explained 50% of the variability in

ecosystem-level shrub production (log–log regression, b

¼ 0.83, F1, 117 ¼ 115.58, P , 0.005; Fig. 4), suggesting

that reduction in ramet density from otter disturbance

was an important factor influencing production.

Ecosystem-level shrub production of false azalea,

unlike blueberry, did not show evidence of negative

otter effects, despite the observed reduction in ramet

density. We detected no significant otter interaction

effect in either 2006 (P¼ 0.12; Fig. 3) or 2007 (P¼ 0.39;

Fig. 3). The ramet density for all 1-m2 plots measured on

latrine and non-latrine sites in 2007 only explained

23.7% of the variability in the nonwoody production

(log–log regression; b¼ 0.67, F1, 117¼ 36.00, P , 0.005;

Fig. 4), indicating lower magnitude of the effect of otter

disturbance.

Shrub leaf area index.—Similar to the results for

blueberry, shrub effective LAI values suggest that

ecosystem-level production was reduced by otter activ-

FIG. 3. The otter interaction effects (mean 6 SE) on the five shrub production variables on river otter latrine (gray bars) andnon-latrine (open bars) sites in Prince William Sound, Alaska: percent cover, ramet density, relative production of individualramets (normalized to zero), the estimated ecosystem production for 2006 sites, and the measured ecosystem production for 2007sites. Left-hand panels for each species depict the results for response variables at each site type; right-hand panels represent theotter interaction effect, i.e., difference between ‘‘on’’ (hatched bars) and ‘‘off ’’ (open bars) plots. Significant differences betweenlatrines and non-latrines at a¼ 0.05 (for n . 10) or a¼ 0.10 (for n , 10) are represented by different lowercase letters.

AARON M. ROE ET AL.3182 Ecology, Vol. 91, No. 11

ity, as noted by a strong negative otter interaction effect

(effective LAI ‘‘on’’ latrine ¼ 0.50 6 0.07 m2/m2 (mean

6 SE), ‘‘off ’’ latrine ¼ 0.85 6 0.08, ‘‘on’’ non-latrine ¼0.69 6 0.12, ‘‘off ’’ non-latrine ¼ 0.69 6 0.11; latrine

difference ¼�0.33 6 0.08, non-latrine difference ¼ 0.00

6 0.13 m2/m2; P ¼ 0.02).

Tree production

There was no significant otter interaction effect for

tree effective LAI (P¼ 0.43; Fig. 5), dbh, (P¼ 0.08, Fig.

5) or basal area (P ¼ 0.55; Fig. 5), but tree density

showed a negative otter interaction effect (P , 0.005;

Fig. 5). Mean tree leaf production per woody basal area

(leaf area per stem area), which removes effects of tree

basal area on LAI, showed a positive otter interaction

effect, with mean value on latrines 2.45 times greater

than on non-latrines (P ¼ 0.03; Fig. 5).

We found no relationship between tree effective LAI

and relative production for individual blueberry ramets

(R2 ¼ 0.04, P ¼ 0.23) or for individual ramets of false

azalea (R2 ¼ 0.00, P ¼ 0.95).

Foliar nitrogen content

Vector analysis indicated that blueberry ramets

growing on otter latrines may exhibit some luxury

consumption of N, but that this may be driven by site

differences rather than otter fertilization (Fig. 6A).

There was an increase in foliar N concentration for the

‘‘on’’ portion of latrines compared to the ‘‘on’’ portion

of non-latrines in blueberries (P , 0.005; Fig. 6A), but

there was no difference in the average leaf mass between

latrines and non-latrines (P¼ 0.72; Fig. 6A), suggesting

some N storage in leaves. Also, N content, although not

statistically significant (P ¼ 0.19; Fig. 6A), was 38%

higher on latrines than non-latrines. Nonetheless, the

otter interaction effect for the relative difference in foliar

N concentration was neither significant nor large (P ¼0.50; Fig. 6B).

False azalea also showed evidence of luxury con-

sumption, with an increase in the foliar N concentration

and content between latrines and non-latrines (P ,

0.005 and P¼ 0.04; Fig. 6A), but no difference between

FIG. 4. Relationships between measured ramet density ofblueberry and false azalea and estimated ecosystem-level shrubproduction on river otter latrine and non-latrines in PrinceWilliam Sound, Alaska in 2007. All values plotted are log-transformed; ramet density was originally measured as ramets/m2, and shrub production was measured as g/m2. Theserelationships were calculated for all the plots from the ‘‘on’’and ‘‘off ’’ portions of both latrines and non-latrines. Values forzero ramet density represent production inside the 1-m2 plotsfrom individuals growing outside but leaning into the sampledarea. This phenomenon was more pronounced in false azalea,which grows in thick clumps.

FIG. 5. The otter interaction effects (mean 6 SE) for thetree production metrics of effective LAI, tree density, treediameter at breast height (dbh), basal area, and the ratio of leafarea to basal area on river otter latrines (gray bars) and non-latrines (open bars) in Prince William Sound, Alaska. Left-handpanels depict the results for response variables at each site type;the right-hand panels represent the otter interaction effect, i.e.,difference between ‘‘on’’ (hatched bars) and ‘‘off ’’ (open bars)plots. Significant differences between latrines and non-latrinesat a¼ 0.05 are represented by different lowercase letters.

November 2010 3183OTTER ACTIVITY AND PLANT PRODUCTION

latrines and non-latrines in leaf mass (P¼0.53; Fig. 6A).

However, for false azalea there was a positive otter

interaction effect for the relative difference in foliar N

concentration (P , 0.005; Fig. 6B), which suggests that

otter activity caused changes in the plant N status

beyond the environmental differences between latrines

and non-latrines.

There was no significant otter interaction effect on the

relative difference in foliar N concentration for western

hemlock (P¼ 0.12; Fig. 6B). Nonetheless, the difference

between ‘‘on’’ and ‘‘off ’’ portions of sites was 6.11 times

higher on latrines than non-latrines, and the N

concentration in needles of western hemlock linearly

increased as the fecal deposition rate per unit area

increased on the latrine (R2¼ 0.434, b1 ¼ 73.217, F1,8¼5.363, P ¼ 0.027; Fig. 6C), suggesting some effect from

otter fertilization. We could not construct nomograms

for western hemlock because the mass of needles was not

available.

DISCUSSION

Our results suggest that the interaction between two

concurrent ecological processes that may have opposing

effects in singularity (fertilization and disturbance) could

FIG. 6. (A) Vector nomograms of relative changes in dry mass, N content, and N concentration (mean 6 SE) of foliage samplescollected from ‘‘on’’ latrines (gray symbols) and ‘‘on’’ non-latrines (open symbols) from river otter latrines and non-latrines inPrince William Sound, Alaska. (B) The otter interaction effects for the relative difference in N concentration for each species(relative differences from the mean for each species are shown together for comparisons, where mean blueberry ¼ 2.17%, falseazalea¼1.88%, and western hemlock¼1.30%). Left-hand panels depict the results for response variables at each site type; the right-hand panels represent the otter interaction effect, i.e., difference between ‘‘on’’ (hatched bars) and ‘‘off ’’ (open bars) plots.Significant differences between latrines and non-latrines at a¼ 0.05 are represented by different lowercase letters. (C) The observedlinear relationship between the N concentration of western hemlock foliage from the ‘‘on’’ portions of latrine sites and the fecaldeposition rate. N concentration values (mean 6 SE) of foliage collected from the ‘‘on’’ portions of non-latrines and the ‘‘off ’’portions of latrines are provided for reference (along the y-axis), demonstrating that the regression intercept (i.e., no otterfertilization on latrines) is not significantly different than these values.

AARON M. ROE ET AL.3184 Ecology, Vol. 91, No. 11

yield differential responses in various ecosystem com-

ponents. Although all three dominant woody species

showed uptake of the marine-derived N deposited by

otters on latrines, shrubs showed no increase in

ecosystem-level production from otter fertilization, but

rather a decrease in production because of physical

disturbance. Although individual surviving blueberry

ramets may have allocated some excess N to annual

production, surviving ramets of false azalea stored

excess N in leaves rather than increased growth. Finally,

established trees, which have low susceptibility to

disturbance, exhibited elevated aboveground production

in response to otter fertilization, and western hemlock

concurrently increased N concentration in needles.

Thus, we found that the response of different woody

plant species to otter activity at latrine sites is not

uniform and probably depends on the species growth

form (tree vs. shrub) and the level of biological

organization (individual vs. ecosystem).

Our observation of elevated d15N in woody plants in

response to animal-mediated N transport was noted in

previous studies (Ben-David et al. 1998a, Hilderbrand et

al. 1999, Helfield and Naiman 2002, Crait and Ben-

David 2007). Similar to Crait and Ben-David (2007), we

were able to unequivocally demonstrate that such

elevation in d15N is not solely a function of otter latrine

site selection, but rather is indicative of plant uptake of

marine-derived N. In contrast with Crait and Ben-David

(2007), who compared post hoc the d15N values of

plants from sites correctly classified (by resource

selection functions) as latrines and non-latrines with

those that were collected from misclassified sites, we

compared plants growing ‘‘on’’ and ‘‘off ’’ plots of each

site type. This approach probably provided better

control for the effects of unmeasured edaphic factors

that could affect values of d15N, such as nitrification

rates (Hogberg 1997), rooting depth (Nadelhoffer and

Fry 1988), the form of assimilated N (Dawson et al.

2002), differences in mycorrhizal associations (Dawson

et al. 2002), differences in plant demand for N (Hogberg

1997), and site age (Chang and Handley 2000), as well as

plant community composition (Roe 2008).

Although the two dominant shrub species assimilated

marine-derived N deposited by otters, this fertilization

did not increase ecosystem production. Instead, it

appears that disturbance overrode the benefits of

fertilization, probably because shrubs, with their high

perennating bud location and erect leaf-stem architec-

ture, are susceptible to chronic disturbance (Cole 1995,

Whinam and Chilcott 2003). Although both species

exhibited a reduction in ramet density, false azalea

showed a lesser reduction in density, cover, and

production compared with blueberry. False azalea

ramets had a mean base diameter that exceeded 30

mm, which is 50% larger than the mean value for

blueberries (Appendix B). This high mean basal

diameter, together with a clumped growth form that

protected smaller ramets, probably afforded higher

resistance to trampling (Cole 1995).

Despite exhibiting higher resistance to disturbance,

the surviving false azalea ramets on latrines allocated

little excess marine-derived N to growth, but rather

experienced luxury consumption. This suggests that

equating foliar percentage N with production (Math-

ewson et al. 2003, Hannan et al. 2007) may lead to

erroneous conclusions. It is possible that false azalea

growth is constrained by low light or deficiency in other

nutrients (Wainhouse et al. 1998, George et al. 1999).

Crait and Ben-David (2007) showed that after account-

ing for the effect of light infiltration, residual shoot

growth of currants (Ribes ssp.) was higher on otter

latrines compared with non-latrines, suggesting that

under similar light conditions, fertilized currants allocate

excess N to growth. Nonetheless, we found no relation

between tree effective LAI and relative production of

individual ramets, suggesting that the effects of distur-

bance were stronger than those of light. Alternatively,

the increased foliar N concentration may have encour-

aged increased herbivory (Mattson 1980, Tripler et al.

2002), negating the increased production from N

fertilization. Nonetheless, we suspect that herbivory

probably played a lesser role in reducing shrub

production, given the depauparate arthropod and

mammalian fauna in our study area. Indeed, in all our

destructive sampling we did not encounter a single

herbivorous insect and found few galls. Experimental

exclusion of herbivores from shrubs on latrines and non-

latrines as well as sampling of sites with canopy gaps

(such as those created by windthrow) will allow for more

adequate assessment of the influence of concurrent

fertilization, disturbance, herbivory, and light depriva-

tion on woody plant growth in this system.

Regardless of the factors that constrained production

in false azalea, this species adopted a strategy of storing

N for a future time when conditions become more

suitable for growth, consistent with the expectations of

species adapted to low and pulsed fertility sites (Chapin

1980). In contrast, blueberry ramets that survived otter

trampling and rubbing may have allocated some of the

excess N to increased production of leaves and stems. It

is likely that, following abandonment of a latrine,

growth of false azalea will be accelerated compared

with that of blueberries that lack the advantage of

stored nutrients in their vegetative tissues. Whether

blueberries store N in roots is unclear and merits further

investigation.

Other studies found that disturbance by animals can

damage the shrub layer, although the net effect on

production at the individual and ecosystem level was not

quantified. Sobey and Kenworthy (1979) who studied

colonies of Herring Gulls (Larus argentatus) found that

gulls physically destroyed plants during boundary

clashes, despite nutrient enrichment from guano depo-

sition. Similarly, Mulder and Keall (2001) found that

burrowing and guano fertilization by the Fairy Prion

November 2010 3185OTTER ACTIVITY AND PLANT PRODUCTION

(Pachyptila turtur), a seabird, increased nutrient avail-

ability in the soil, but N uptake in leaves occurred in

only one of three shrub species measured. Most

importantly, the uric acid in guano lowered the soil

pH, which decreased tree seedling establishment. Both

of these studies and ours suggest that although nutrient

inputs from animals can enhance plant production in

certain ecosystems (Anderson and Polis 1999, Sanchez-

Pinero and Polis 2000, Croll et al. 2005), the associated

disturbance may cancel those positive effects in others.

The reduction in ecosystem production in the

understory shrub layer may be offset by increased

production of the overstory tree layer, as shown by the

increase in effective LAI per basal area. River otters

select sites with large, old-growth trees (Bowyer et al.

2003, Ben-David et al. 2005), and such sites often have

lower tree density. This may be a result of stand self-

thinning as the increase in biomass of individual

maturing tree stems causes shading and death in others

(Enquist and Niklas 2001). Nonetheless, radial woody

growth of trees could be caused partially by decades of

otter fertilization. Our observations are consistent with

those reported by Helfield and Naiman (2001, 2002)

and Drake et al. (2002) in other areas of Alaska. In

those studies, Sitka spruce in southeast Alaska and

white spruce (Picea glauca) in southwest Alaska

responded to inputs of marine-derived N from spawn-

ing salmon (Oncorhynchus spp.) with an increase in the

relative annual wood production. Further, our obser-

vation of an increase in effective LAI per basal area is

likely to equate to an increase in annual production

rather than increased retention of previous years’

needles because research has shown that conifers

exhibit reduced needle longevity when grown on high-

fertility sites compared to trees grown on control sites

(e.g., Balster and Marshall 2000, Amponsah et al.

2005). Indeed, the positive relation between leaf N

concentrations in western hemlock and fecal deposition

suggests that N availability from otter activity allevi-

ated N deficiency for the tree layer of these forests.

Thus, it appears that established trees, which are

unaffected by otter disturbance, and possibly experi-

ence lower competition because of the reduction in

understory production, can take full advantage of this

marine-derived fertilization.

In conclusion, our results, illustrating differential

responses of various ecosystem components to the

activity of animal vectors, emphasize the importance of

concurrently investigating multiple species of multiple

growth forms (herbs, shrubs, and trees) at multiple

levels of organization (leaf, plant, and ecosystem). We

demonstrated that, in addition to the effects of nutrient

inputs from aquatic systems to the plant community by

marine feeding river otters, the disturbance associated

with the behavior of the animals on land has important

implications for production of the plant community. In

order to obtain a more comprehensive understanding

of ecosystem responses to the effects of animal vectors,

future studies should include multiple ecosystem

compartments, including soil processes, at multiple

scales. Finally, after accounting for the differential

responses of trees and shrubs, extrapolation of our

results to the landscape scale could elucidate the

influence of river otters on the carbon budget of

Alaskan coastal forests.

ACKNOWLEDGMENTS

We thank M. Wood, B. Myers, J. Herreman, T. Whitaker,and K. Pope for assistance in the field and lab; S. Albeke forhis contributed GIS expertise and advice; K. Ott for her timeand expertise in studying otter latrine use; B. Ewers and G.Brown for comments on early drafts of this manuscript; andK. Gerow for statistical advice. Funding for this project wasprovided by NSF Grant #0454474 and the University ofWyoming Ecology EPSCoR. Additional logistical support wasprovided by the Alaska Department of Fish and Game andBabkin Charters.

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APPENDIX A

Methods for measuring fecal deposition rates and vegetation sampling design on coastal river otter latrine sites on Knight, Ingot,and Eleanor Islands in Prince William Sound, Alaska, USA (Ecological Archives E091-223-A1).

APPENDIX B

Methods and results for allometric relationships between nonwoody production of individual ramets of blueberry and falseazalea in relation to plant morphology and size (Ecological Archives E091-223-A2).

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