ORIGINAL ARTICLE

Masakazu Hori Æ Takashi Noda Æ Shigeru Nakao

Effects of avian grazing on the algal community and smallinvertebrates in the rocky intertidal zone

Received: 4 August 2005 / Accepted: 17 March 2006 / Published online: 2 June 2006� The Ecological Society of Japan 2006

Abstract In this study of a rocky intertidal habitat innorthern Japan, feeding by avian consumers had sig-nificant effects on algal assemblages and small herbivo-rous invertebrates. The effects of the birds on algae weredifferent from those of invertebrate grazers such asurchins and gastropods. The abundance of the dominantalgal species decreased during the grazing period, in-creased again after the grazing period, and indirectlyaffected algal species richness and evenness. Aviangrazing also decreased the density of tube-dwelling am-phipods on the dominant alga, but did not change thedensity of mobile and free-living isopods. These resultssuggest that avian grazers may act as habitat modifiersrather than exploitative competitors for the small her-bivorous crustaceans. Avian herbivores consumed onlythe upper parts of large algal fronds, apparently reduc-ing the amount of suitable microhabitat for the smallherbivorous crustaceans, which are subject to a varietyof physical or biological stress. Thus, avian herbivoresfunction as ecosystem engineers, regulating communitystructure in a manner different to invertebrate herbi-vores in rocky intertidal habitats.

Keywords Amphipods Æ Ecosystem engineering ÆGulls Æ Isopods Æ Monostroma angicava

Introduction

Herbivore-plant interactions play an important role inregulating community structure and dynamics. Herbiv-ory is qualitatively distinct from predation becauseherbivory does not always result in the death of one ofthe participants. Plant responses occur at the individual,population and community level, resulting in complexinteraction pathways (Ricklefs and Miller 1999).

In coastal ecosystems, grazing by limpets, gastro-pods, arthropods, and sea urchins has been shown toimpact algal assemblages and other animals (e.g.,Lubchenco and Gaines 1981; Hawkins and Hartnoll1983). The effects of herbivores have been categorizedinto the following three types: (1) direct and indirecteffects on algae (e.g., Paine and Vadas 1969; Lubch-enco 1978; Branch 1981; Duffy and Hay 2000), (2)direct and indirect effects on sessile animals by theirgrazing/bulldozing (e.g., Dayton 1971; Underwood1986; Petraitis 1990), and (3) indirect effects on motileherbivores through exploitative competition or othercomplex pathways (e.g., Creese and Underwood 1982;Hawkins and Hartnoll 1983; Underwood et al. 1983;Branch 1984). Additionally, because seaweed serves asrefuge from disturbance and predation (Buschmann1990; Pohle et al. 1991; Bertness and Leonard 1997;Bertness et al. 1999; Hori and Noda 2001b), herbivoresmay have some effect on algae and invertebratesthrough habitat modification. However, there havebeen few studies of habitat modification resulting fromalgal consumption by herbivores. Moreover, as algalassemblages serve as both food and habitat resourcesfor small herbivores, there is a complex indirect inter-action between them. To estimate the functions ofherbivory/grazing on community regulation in therocky intertidal habitat, it is necessary to clarify the

M. HoriLaboratory of Biodiversity Science, School of Agricultureand Life Science, The University of Tokyo,Bunkyo-ku, Tokyo 113-8657, Japan

T. Noda Æ S. NakaoDepartment of Marine Biodiversity,Graduate School of Fisheries Science,Hokkaido University, Hakodate, Hokkaido 041-8611, Japan

Present address: M. Hori (&)National Research Institute of Fisheriesand Environment of Inland Sea, Fisheries Research Agency,2-17-5 Maruishi, Hatsukaichi, Hiroshima 739-0452, JapanE-mail: mhori@affrc.go.jpTel.: +81-829-550666Fax: +81-829-541216

Present address: T. NodaGraduate School of Environmental Science,North 10 West 5, Kita-ku, Sapporo 060-0810, Japan

Ecol Res (2006) 21:768–775DOI 10.1007/s11284-006-0192-8

effects of habitat modification on small organisms aswell as the food related effects of grazing/herbivory.

Shorebirds feed on a variety of marine organisms,including fishes, invertebrates, and seaweed in variousnear-shore habitats (Jacobs et al. 1981; Hocky andUnderhill 1984; Baird et al. 1985; Brown andMcLachlan 1990; Raffaelli and Hall 1996; Hori andNoda 2001a). Although most previous food-web stud-ies have suggested that the contribution of shorebirdsto community regulation are relatively minor in coastalecosystems (e.g., Menge and Sutherland 1987; Raffaelliand Milne 1987; Raffaelli and Hall 1992), recent studieshave indicated that their feeding can sometimes changeprey density and community structure (Frank 1982;Kent and Day 1983; Marsh 1986; Good 1992; Wootton1992, 1993a, b, 1997; Thrush et al. 1994; Coleman et al.1999; Hamilton 2000; Hori and Noda 2001b). Forexample, on mud flats, avian predators probably showsize-selective predation on larger-size individuals sothat large-size individual elimination by birds occa-sionally causes the increase of the abundance of con-specific juveniles (Kent and Day 1983; Thrush et al.1994).

Studies of bird herbivory on mud flats have alsosuggested that avian grazing can largely depress sea-weed abundance (Charman 1977; Jacobs et al. 1981;Reise 1985; Baldwin and Lovvorn 1994; Portig et al.1994). However, their effects seem to differ from thoseof invertebrate herbivores because of substantial sizeand morphological difference. Birds, with greater size,eyesight and mobility, are likely to be selective, and eatpreferable seaweeds as well as avian predators on mudflats. In contrast, many invertebrate herbivores may beopportunistic grazers. Also, avian herbivory may occurwith high temporal variability (e.g., highly seasonal butperhaps intense due to migration) in comparison withinvertebrate herbivory. However, few studies have di-rectly examined the effects of birds on seaweeds or theindirect effects of birds on invertebrates due to changesin the seaweed assemblage.

The rocky shore of Hiura coast in Hokkaido,northern Japan, is covered with ephemeral algae dur-ing winter and summer (Hori and Noda 2001a).Herbivorous invertebrates, such as tube-dwelling am-phipods (Hyale sp. and Amphithoe sp.) and free-livingisopods (Cymodoce sp.), are common on the rockybenches in this area. From winter to spring, aviangrazers appear in these rocky benches and feed mainlyon the dominant green alga (Monostroma angicavaKjellman) (Hori and Noda 2001a, b). Major avianherbivores are geese and gulls, which do not feed di-rectly on amphipods or isopods during this period(Hori and Noda 2001a). Here, we investigated that theeffects of avian grazers on the algal assemblage thatcreates a high canopy on the rocky benches, andexamined indirect effects on small invertebrates with amanipulative experiment.

Materials and methods

The study site was located on a 1.2-ha rocky bench inHiura, in southern Hokkaido, Japan (41�44¢N,141�04¢E). At the study site, the mid-intertidal zone iscovered with ephemeral algae dominated byM. angicavafrom January to July (Hori and Noda 2001a). The les-ser-algae, such as Porphyra sp., also appears in the zone.The herbivorous amphipods (Hyale sp. and Amphithoesp.) dwell in tubes mainly attached to the base of therhizoid of M. angicava (Hori, personal observation) andfeed on M. angicava and epiphytic diatoms (Hori 2003).The herbivorous isopod (Cymodoce sp.) is a free-livingbut less mobile species and feeds on M. angicava andepiphytic diatoms (Hori 2003). Of the 15 bird speciesforaging at Hiura shore, 5 were observed ingesting theephemeral algae, mostly on M. angicava, between Jan-uary and April (Hori and Noda 2001a). Four were gullspecies, herring gull (Larus argentatus vegas Palmen),slaty-backed gull (L. schistisagus Stejneger), glaucousgull (L. hyperboreus pallidissimus Portenko), and glau-cous-winged gull (L. glaucescens Naumann). Amongthem, herring gull was normally the most abundant,slaty-backed gull was second, and others were probablyvagrant with quite few individuals. The fifth was the wildgoose species, the black brent goose (Branta berniclaorientalis Tougarinov), which was less abundant thanthe herring gulls (Hori and Noda 2001a). These fivespecies appeared in the study site in early January andleft in late April (Hori and Noda 2001a). During theebb-tide period, the herbivorous birds start their feedingon algae as soon as their bills can reach the algal frondsof M. angicava even when the rocky intertidal benchesare still submerged in sea-water, and stop their feedingwhen the rocky benches are completely exposed to theair. During the flood-tide period, the herbivorous birdsfeed on algae from when the algal fronds start to float inthe sea-water until their bills can no longer reached thefronds. However, the birds usually foraged on the algaeduring the ebb-tide period because, in the tidal cycle ofthe study site during the study period, the flood tideoften started at nightfall when the birds no longer foragedue to lack of visibility. The observation of avian for-aging and analyses of their pellets and feces revealed thatgulls actually ingest M. angivaca and presumably do notfeed on any intertidal invertebrates on the rocky shoreduring this season (Hori and Noda 2001a, b; Hori 2003),although they were sometimes observed foraging on seaurchins which had migrated from the subtidal habitatand on fishery wastes in fishing ports at the high-tideperiod. Therefore, in this study, the gulls were consid-ered apparent grazers in this rocky intertidal habitat,since it was still unknown whether the gulls can digestthe algae. Except for the gulls and the goose, a carniv-orous avian species, carrion crow (Corvus corone orien-talis Eversmann), appears to forage in the study site

769

during the study period. The crows do not feed on anyplant materials, but take the small amphipods and iso-pods (Hori and Noda 2001b). As there were no herbiv-orous fishes in this system, located in a cold-temperateregion, the cage-exclosure experiment was intended onlyfor these avian species.

Field experiment

An exclosure experiment, designed to estimate the effectsof avian grazing on the algal community and inverte-brate grazers, was performed from December 1998 toMay 1999. Avian herbivores were excluded from plotsusing prefabricated cages, measuring 50·50·15 cm3 andmade from 13-mm diameter poly-vinyl chloride pipes(see Hori and Noda 2001b for details). In order to avoidany artificial effects of cage structure on organisms in theplots, this cage was without any mesh and no othermaterials were used. However, this was enough to pre-vent just the birds from grazing (Hori and Noda 2001a).Twelve cages were randomly placed on the mid-inter-tidal zone by attaching them to rocks with screws at thebeginning of December when the birds had not yet be-gun feeding on M. angicava. Each cage was paired withan adjacent open control area of the same size locatedwithin 1 m of the exclusion plot. A permanent quadratof 25·25 cm2, marked with small stainless nails at thefour corners, was placed in the center of each of theexclosure and control plots. These quadrats were todetermine the percent cover of algae and the density ofinvertebrates. In the census of the algal cover, thepresence/absence of each algal species was counted usingpoint-intercept with 100 points. In case the quadratswere covered with the dominant algal canopy, theunderstory of the algal canopy directly attached on therock surface was also counted. Each cage-control pairwas regarded as one treatment block.

Every 2 weeks from December 1999 to July 2000,avian grazing on algae was observed from the timewhen the birds entered the study site for feeding at thebeginning of the ebb-tide period during daytime. Usinga 20–60· spotting scope, we counted the daily maxi-mum number of each bird species grazing on algae overthe whole study site. At each census, the percentage ofeach permanent quadrat covered by each algal specieswas recorded after the birds had finished grazing. Itwas possible to determine algal cover without disturb-ing avian feeding, because herbivorous bird speciesstarted to feed on algae when their bills could reach thealgal mat beneath the surface of the sea, and stoppedfeeding when the rocky benches were exposed com-pletely to the air during the census. Using these data,we calculated the Shannon–Weiner diversity index asan indicator of algal species diversity (Tokeshi 1993).The census of invertebrates was conducted at thebeginning of January when avian herbivores started tofeed on M. angicava, in late April when birds had justleft the study site, and in late May well after the birds

had left the study site. More frequent censuses wouldhave disturbed the algal mat.

Repeated-measures ANOVA were conducted toexamine the gulls’ exclosure effect on the percent coverof M. angicava, algal species richness and diversity index(H¢), and the densities of amphipods and isopods. Theassumption of variance homogeneity was assessed usingCochran’s C-test. Mauchly’s sphericity test for within-subject factors was also performed, and Greenhouse–Geisser corrected probabilities were given for the Uni-variate within-subject analysis when the sphericityassumption was not met. Additionally MANOVA wasalso conducted, because it has suggested that MANOVAis more robust occasionally when time is the within-subject factor (von Ende 2001), but the results of ourunivariate and multivariate analyses were similar. Posthoc tests were performed to examine differences in algalcover and amphipod density between exclosures andcontrols.

Results

Of the five avian species observed grazing during theexperiment, the herring gull was the dominant species,and brent geese were the second most common aviangrazers (Fig. 1). Only very small numbers of slaty-backed gulls, glaucous gulls, and glaucous-winged gullswere observed, and they were intermingled with theflocks of herring gulls. The number of gulls increasedrapidly in January, to 40 individuals/1.2-ha on average,until early April, and then decreased sharply from earlyApril. The number of brent geese per day surged threetimes, once in January and twice in February, and wereabsent in all other months.

The percent cover of M. angicava was significantlydifferent between the avian exclosure and control plotsduring the avian feeding period (Table 1), being 25%lower in the open control cages that were accessible tobirds. The difference was insignificant in early May afterthe avian herbivores had left the study site (Fig. 2,

0

10

20

30

40

50

60

Brent gooseGulls

Max

. num

ber

of in

divi

dual

(da

y–1)

Month

Dec. Jan. Feb. Mar. Apr. May

Fig. 1 The maximum number of each avian species feeding M.angicava per day in the study site. All four gull species are includedin the line with open circles

770

Table

1Repeated-m

easuresANOVA

ontheeff

ectofaviangrazing(controlversusexclosure)onpercentcover

ofM.angicava,algalrichness,algalevenness,amphipods,andisopods

duringtheavianforagingseason

Source

df

Percentcover

of

M.angicava

df

Algalrichness

Algalevenness(H

¢)df

Amphipods

Isopods

MS

FP

MS

FP

MS

FP

MS

FP

MS

FP

Univariate

analysis

Betweensubjects

Treatm

ent

11.310

130.452

<0.001

1145.200

145.200

<0.001

7.674

269.174

<0.001

1276.212

132.409

<0.001

1.589

0.069

0.798

Block

11

0.110

11

6.633

0.179

11

13.318

Treatm

ent

·block

11

0.010

11

1.000

0.029

11

2.086

Residual

00

0Within

subjects

Season

1.881

4.801

436.443

<0.001

418.479

41.519

<0.001

0.204

8.949

<0.001

2644.892

152.676

<0.001

488.793

37.746

<0.001

Season

·treatm

ent

1.881

0.239

21.741

<0.001

411.054

24.837

<0.001

0.849

37.191

<0.001

288.828

21.030

<0.001

7.703

0.595

0.560

Season

·block

20.69

0.046

44

0.916

0.056

22

15.891

15.193

Season

·treatm

ent

·block

20.69

0.011

44

0.445

0.023

22

4.224

12.950

Residual

00

0

df

Wilks’k

FP

df

Wilks’k

FP

Wilks’k

FP

df

Wilks’k

FP

Wilks’k

FP

Multivariate

analysis

Season

40.008

236.435

<0.001

40.031

63.344

<0.001

0.170

9.770

0.004

20.045

106.671

<0.001

0.102

44.256

<0.001

Season

·treatm

ent

40.048

39.900

<0.001

40.048

39.877

<0.001

0.044

43.343

<0.001

20.254

14.652

0.001

0.912

0.483

0.631

Season

·block

44

0.005

2.165

44

0.005

2.224

0.011

1.664

22

0.048

3.220

0.249

0.913

Analyseswereperform

edusingthedata

from

earlyJanuary,earlyFebruary,earlyMarch,earlyAprilandearlyMayforAlgae,andthedata

from

earlyJanuary,earlyApril,andlate

Mayforinvertebrates.Thedata

ofpercentcover

ofM.angicavawerelog-transform

edto

meettheassumptionofhomogeneity

ofvariance.Justforthecover

data,Greenhouse–Geisser

(G–G)correctedprobabilitieswerealsogiven

fortheunivariate

within-subject

analysis(G

–Gepsilon=

0.470),because

thesphericityassumptionforwithin-subjectsfactors

wasnotmet

(Mauchly’ssphericitytest:df=

9,W=

0.112,P=

0.016)

771

ANOVA; early May: F=0.058, P=0.814), and algalcover in control plots was actually greater in avian-ex-closure plots at the end of May (Fig. 2, ANOVA; lateMay: F=20.568, P=0.001).

Concordant with the changes in the dominant alga,M. angicava, algal species richness and diversity indexbegan to increase in January (Fig. 3), and became sig-nificantly higher in the control versus the avian-exclo-sure plots (Table 1). This difference was maintainedthroughout the avian foraging period, starting in Feb-ruary continuing then the end of May (ANOVA; rich-ness: F=82.831, P<0.0001, evenness: F=106.903,P<0.0001), after the avian herbivores had left the studysite (ANOVA; richness: F=35.200, P<0.0001, even-ness: F=69.109, P<0.0001). Avian exclusion changedthe algal species composition, relative to controls(Table 2).

Although the density of the isopods did not differbetween exclosure and control plots at any time during

the experimental period (Fig. 4, Table 1), the amphipoddensity was significantly higher in avian exclosures thanin control plots during two census periods: when theavian herbivores had just finished feeding on M. angi-cava (ANOVA; F=55.723, P<0.0001) and when theyhad already left the study site (ANOVA; F=46.361,P<0.0001).

ControlExclosure

Month (per two weeks)

Co

ver

(%)

0

25

50

75

100

ControlExclosureControlExclosure

Month (per two weeks)

Co

ver

(%)

Dec. Jan. Feb. Mar. Apr. May

Fig. 2 The difference of seasonal change in mean percent cover ofM. angicava (mean±1 SE) between control and bird-exclosureplots. The period from January to April corresponded to the seasonwhen gulls and brent geese fed M. angicava in the study site

Richness - ControlRichness - Exclosure

Evenness - ControlEvenness - Exclosure

No.

ofal

gals

peci

es(6

25cm

2-1)

Shanon-W

einerindex

0

2

4

6

8 Richness - ControlRichness - Exclosure

Evenness - ControlEvenness - Exclosure

0

0.25

0.5

0.75

1

1.25Richness - ControlRichness - Exclosure

Evenness - ControlEvenness - ExclosureRichness - ControlRichness - Exclosure

Evenness - ControlEvenness - Exclosure

Month (per two weeks)

No.

ofal

gals

peci

es(6

25cm

2-1)

Shanon-W

einerindex

Dec. Jan. Feb. Mar. Apr. May

Fig. 3 Results of mean algal richness and evenness (mean±1 SE)in both control and exclosure plots. The algal evenness wasexhibited as Shanon–Weiner index

Table 2 Algal species appeared in both control and exclosure plotsduring the whole experiment period

Plot

Control Exclosure

Class chlorophyceaeEnteromorphora compressa(Linnaeus) Nees

+ +

Ulva pertusa Kjellman +M. angicava Kjellman + +Class PhaeophyceaeSargassum thunbergii(Mertens ex Roth) Kuntze

+ +

Alaria crassifolia Kjellman +Laminaria japonica Areschoug +Petalonia fascia (O. F. Muller)Kuntze

+

Leathesia difformis (Linnaeus)Areschoug

+

Analipus japonicus (Harvey) Wynne +Scytosiphon lomentaria (Lyngbye) Link + +Pelvetia wrightii (Harvey) De Toni +Colpomenia bullosa (Saunders) Yamada + +Class RhodophyceaePolysiphonia morrowii Harvey +Champia parvula (C Agardh) Harvey +Chondrus occellatus Holmes +Porphyra yezoensis Ueda +Porphyra pseudolinearis Ueda + +Neorhodomela aculeata(Perestenko) Masuda

+

OthersEpihytic diatoms + +

Isopod -Control

Isopod -Exclosure

Amphipod -Control

Amphipod -Exclosure

Month

Density(No.625cm2-1)

0

5

10

15

20

Isopod -Control

Isopod -Exclosure

Amphipod -Control

Amphipod -Exclosure

Isopod -Control

Isopod -Exclosure

Amphipod -Control

Amphipod -Exclosure

Month

Density(No.625cm2-1)

Jan. Apr. May

Fig. 4 The differences of the amphipod and the isopods density(mean±1 SE) between control and exclosure plots. The data inJanuary, April, and May correspond to the period when avianherbivores started to feed on M. angicava, when they finished theirfeeding and left the study site, and a sufficient time after they hadleft study site, respectively

772

Discussion

Avian grazing significantly decreased abundance of thedominant algal prey during their foraging period, butincreased it after they left the study site. This decreased-increase pattern may be due to size-selective feeding bythe birds, followed by plant regrowth and new growthby smaller conspecific recruits (Hori and Noda 2001a).Avian grazers appeared to consume only large fronds ofalgae and could not collect smaller ones (probably newrecruits) with their bills. Thus, smaller algae that settledduring the avian foraging period tended to remain in theplots, and grew rapidly after the avian herbivores mi-grated away. In addition, avian grazing could haveprovided free space for new recruits, which can survivemuch longer than old ones that settled much earlier.Furthermore, algal fronds of M. angicava that are tornby avian grazers have the potential to re-grow and re-cover from physical damage (Lobban and Harrison1994). The cost is that avian grazing prolongs the growthperiod of the dominant algal species (Hori and Noda2001b), and may reduce the allocation to reproductionversus somatic growth. The similar effect of avian for-aging, the release of new recruits or juveniles fromintraspecific competitive depression by larger size-classindividuals was sometimes reported in mudflat inverte-brates and avian predator interactions (e.g., Kent andDay 1983; Thrush et al. 1994).

A prolonged growth period seems to be similar to‘‘over-compensation’’ in terrestrial plants. Plant indi-viduals sometimes alter patterns of growth/reproductionduring intense herbivory, making morphological andphysiological adjustments to counter losses (Jefferies1988; Trumble et al. 1993). Our results suggest that theprocess of prolonged algal growth might be a popula-tion-level compensatory response.

In addition, avian herbivores indirectly increased al-gal species diversity. This indirect effect suggests a‘‘keystone’’ role for the birds, as the herbivory appearedto release small understory algal species from competi-tive exclusion by the dominant alga, similar to Paine(1966) and Menge (1995). In rocky shores, althoughsome sea urchins and snails occasionally decrease algaldiversity due to their feeding on a wide range of algalspecies (e.g., Lubchenco 1978; Wootton 1995), mostother grazers, including snails (e.g., Lubchenco 1978),limpets (e.g., Hawkins and Hartnoll 1983; Farrell 1991),and fish (e.g., Hixon and Brostoff 1996), have keystoneroles with respect to algal communities. This is becausethe algae on rocky shores often exhibit negative intra-specific trade-offs between palatability and competitiveability (Lubchenco and Gaines 1981; Watson and Nor-ton 1985).

Manipulation of avian grazing caused significantdifferences in the amphipod density between exclosureand control plots. However, the isopod did not showclear differences in density between treatments andcontrols. We could not perform the additional experi-

ments to clarify the effect of the dominant algal structureon the small invertebrates because of the impossibility ofthe algal frond manipulation, so that we cannot exactlyspecify the process making these patterns of both theamphipod and the isopod density. However, there are atleast four possible interpretations for this result. Thefirst is that avian grazing significantly decreased both theamphipod and the isopod density (i.e., exploitativecompetition or habitat modification), but the motileisopods may have emigrated to control plots from thelush exclosure areas. However, the isopod with lessmobility, probably due to low air and water temperaturein winter (Hori, personal observation), is unlikely toemigrate from profitable exclosure plots with lush algalgrowth to control plots with less resource.

The second explanation is that the cages excluded notonly avian grazers but also some predators of the am-phipods. In this case, the observed pattern of the differ-ence in the amphipod density between treatments andcontrols was not a consequence of the indirect effect ofavian grazers but the direct effect of predator exclusion.However, any other avian predators that often consumethe small invertebrates, such as passerines and smallsandpipers, were absent from this study site (Hori andNoda 2001b). Moreover, the carrion crow does notconsume such small amphipods and isopods and theseinvertebrates were not actually included in the prey itemsof the crow in this study period (Hori and Noda 2001b).

The third explanation is that the gulls consumedamphipods directly; they could have targeted them asprey or eaten them incidentally when the algal frondswere grazed. If the gulls are really carnivores that cannotdigest algae, the algal ingestion by the gulls can beconsidered as foraging on the amphipods with the algalfrond. However, we believe this differential direct pre-dation to be unlikely, for concurrent research found thatthe gulls rarely consume small intertidal invertebrates inthe study site in winter (Hori and Noda 2001b). Therewere no regurgitated pellets or feces from gulls that in-cluded traces of amphipod, which are sometimes foundat other seasons (Hori and Noda 2001b). Furthermore,birds tend to consume only the upper part of largefronds of M. angicava, whereas amphipods occupy thebase of the rhizoids of M. angicava (Hori, personalobservation). These indirect meaures suggest that thegulls are likely to ingest only M. angicava and not toforage the amphipod, although it was unknown whetherthe gulls can be considered as the real grazers.

The final explanation is one of differential suscepti-bility to habitat modification. During the experiments,most of the tubes of amphipods disappeared from thelower parts of algal fronds a few days after birds fed onthe upper parts of the fronds. Presumably, the upperalgal canopy protects amphipods from physical stress(i.e., waves, heat-stress, desiccation) or predation byother animals. Moreover, there were lots of algal frondsin the exclusion plots, meaning that more habitat surfacearea for the amphipod was established in the exclusion

773

plots and thus may have facilitated the settlement of theamphipods. We believe the habitat modification theoryto be the most plausible, and further studies are neededto clarify the causes and consequences of herbivory onassociated animals.

Our study suggests that there are at least two fun-damental differences in the foraging behavior betweenavian and invertebrate herbivores (i.e., limpets, snails,and sea urchins) with a strongly top-down effect on thealgal community. First, avian herbivores feed on theupper parts of algal fronds while the lower parts remainon the rock surface (Hori and Noda 2001b, this study),while invertebrate herbivores can sometimes feed onalgal holdfasts and remove them from the rock surface(e.g., Castenholz 1961; Paine and Vadas 1969; Iwasaki1993a, b). This difference may be due to differences infeeding morphology; avian herbivores hold the algalfrond in their bills and bite them, while the invertebrateherbivores rasp algal material using their radulae (e.g.,Branch 1981). The second difference is that avian her-bivores prefer larger algae, which sometimes have thickblades that are less vulnerable to attack by small inver-tebrates. These differences in foraging behavior wouldcause the observed differences in the grazing effect on thealgal assemblage and on community structure betweenavian and invertebrate herbivores. In addition, the aviangrazing on more abundant and dominant algae mayincrease algal diversity through reductions in competi-tive exclusion in the algal assemblage to a greater extentthan invertebrate grazing, which tended to reduce thenumber of many algal species and total algal abundance(e.g., Paine and Vadas 1969; Wootton 1995). Aviangrazing occurs only on a certain part of the dominantalgal frond and may not create space for the recruitmentby other algae, which contrasts with the impact of someinvertebrate grazers that remove the entire algal frond.This behavior could also help maintain virtuallymonospecific expansion of M. angicava.

In general, most marine benthic communities aregenerated by the presence of a few foundation species(Bruno and Bertness 2001), e.g., kelp forests, musselbeds, oyster reefs, seagrass meadows, and coral reefs(Abele 1976; Peterson et al. 1984; Tsuchiya and Nishihira1985; Duggins et al. 1990; Seed 1996; Peterson et al.2003), greatly modifying habitats for other associatedspecies. Moreover, most of these associated species areclosely-dependent on the individual traits or structure oftheir foundation species, and these interactions havebeen well studied and demonstrated (e.g., Mukai 1971;Abele 1976; Lassig 1977; Vance 1978; Tsuchiya and Ni-shihira 1985; Bertness et al. 1999; Peterson et al. 2003). Inthe present study, the algal fronds are an importanthabitat element. The avian herbivores consume and dis-turb the algal canopy, and thereby have strong indirecteffects on other species. Our results may imply that theeffects of modification on structurally important speciesare likely to regulate community dynamics (Jones et al.1994; Bruno and Bertness 2001; Odling-smee et al. 2003)and are therefore important for further study.

Acknowledgments We would like to thank S. Thrush, D. Lohrer,and T. Wootton for their number of beneficial comments on theMS. We also thank S. Goshima, H. Ogi, A. S. Ilano, M. Nakaoka,and T. Miyashita for a number of helpful suggestions. T. Amanogave us some suggestions about avian foraging. This work wasmade possible by the generous hospitality of the fishery officers ofthe Hiura Fishermen’s Cooperative Association. We would alsolike to thank the members of the Laboratory of Marine Biodiver-sity of Hokkaido University for their help in the field.

References

Abele LG (1976) Comparative species richness in fluctuating andconstant environments; coral-associated decapod crustaceans.Science 192:461–463

Baird D, Evans PR, Milne H, Pienkowski MW (1985) Utilizationby shorebirds of benthic invertebrate production in intertidalareas. Oceanogr Mar Biol Annu Rev 23:573–597

Baldwin JR, Lovvorn JR (1994) Expansion of seagrass habitat bythe exotic Zostera japonica, and its use by dabbling ducks andbrant in Boundary Bay, British Columbia. Mar Ecol Prog Ser103:119–127

Bertness MD, Leonard GH (1997) The role of positive interactionsin communities: lessons from intertidal habitats. Ecology78:1976–1989

Bertness MD, Leonard GH, Levine JM, Schmidt PR, IngrahamAO (1999) Testing the relative contribution of positive andnegative interactions in rocky intertidal communities. Ecology80:2711–2726

Branch GM (1981) The biology of limpets: physical factors, energyflow and ecological interactions. Oceanogr Mar Biol Annu Rev19:235–379

Branch GM (1984) Competition between marine organisms: eco-logical and evolutionary implications. Oceanogr Mar BiolAnnu Rev 22:429–593

Brown AC, McLachlan A (1990) Ecology of sandy shores. Elsevier,Amsterdam

Bruno JF, Bertness MD (2001) Habitat modification and facilita-tion in benthic marine communities. In: Bertness MD, GainesSD, Hay ME (eds) Marine community ecology. Sinauer Asso-ciates, Sunderland, pp 201–218

Buschmann AH (1990) Intertidal macroalgae as refuge and foodfor amphipoda in central Chili. Aquat Bot 36:237–246

Castenholz RW (1961) The effect of grazing on marine littoraldiatom populations. Ecology 42:783–794

Charman K (1977) The grazing of Zostera by wildfowl in Britain.Aquaculture 12:229–233

Coleman RA, Goss-Custard JD, Durell SEA le V dit, Hawkins SJ(1999) Limpet Patella spp. consumption by oystercatchersHaematopus ostraleegus: a preference for solitary prey items.Mar Ecol Prog Ser 183:253–361

Creese RG, Underwood AJ (1982) Analysis of inter- and intra-specific competition amongst intertidal limpets with differentmethods of feeding. Oecologia 53:337–346

Dayton PK (1971) Competition, disturbance and communityorganization: the provision and subsequent utilization of spacein a rocky intertidal community. Ecol Monogr 41:351–389

DuffyJE,HayME(2000) Strong impacts of grazing amphipodson theorganization of a benthic community. Ecol Monogr 70:237–263

Duggins DO, Eckman JE, Sewell AT (1990) Ecology of understorykelp environments II. Effects of kelps on recruitment on benthicinvertebrates. J Exp Mar Biol Ecol 143:27–45

Farrell TM (1991) Models and mechanisms of succession: anexample from a rocky intertidal community. Ecol Monogr61:95–113

Feare CJ, Summers RW (1985) Birds as predators on rocky shores.In: Moore PG, Seed R (eds) The ecology of rocky coast.Columbia University Press, New York, pp 249–264

Frank PW (1982) Effects of winter feeding on limpets by BlackOystercatchers, Haematopus bachmani. Ecology 63:1352–1362

774

Good TP (1992) Experimental assessment of gull predation on theJonah crab Cancer borealis (Stimpson) in New England rockyintertidal and shallow subtidal zones. J Exp Mar Biol Ecol157:275–284

Hamilton DJ (2000) Direct and indirect effects of predation bycommon eiders and abiotic disturbance in an intertidal com-munity. Ecol Monogr 70:21–43

Hawkins SJ, Hartnoll RG (1983) Grazing of intertidal algae bymarine invertebrates. Oceanogr Mar Bio Annu Rev 21:195–282

Hixon MA, Brostoff WN (1996) Succession and herbivory: effectsof differential fish grazing on Hawaiian coral-reef algae. EcolMonogr 66:67–90

Hocky PAR, Underhill LG (1984) Diet of the African black oys-tercatcher Haematopus moquini on rocky shores: spatial, tem-poral and sex-related variation. S Afr J Zool 19:1–11

Hori M, Noda T (2001a) An unpredictable indirect effect of algalconsumption by gulls on crows. Ecology 82:3251–3256

Hori M, Noda T (2001b) Spatio-temporal variation of avian for-aging in the rocky intertidal food web. J Anim Ecol 70:122–137

Hori M (2003) Food web structure and dynamics attributed toavian foraging and allochthonous input in the rocky intertidalhabitat. PhD thesis, Hokkaido University, Hokkaido, Japan

Iwasaki K (1993a) Synergistic effects of mixed grazing by intertidallimpets on sessile organisms: consequences of differences ingrazing ability and feeding habit. Physiol Ecol Jpn 30:1–30

Iwasaki K (1993b) The roles of individual variability in limpets’resting site fidelity and competitive ability in the organization ofa rocky intertidal community. Physiol Ecol Jpn 30:31–70

Jacobs RPWN, Denhartog C, Braster BF, Carriere FC (1981)Grazing of the seagrass zostera noltii by birds at terschelling(Dutch Wadden sea). Aquat Bot 10:241–259

Jefferies RL (1988) Vegetational mosaics, plant-animal interactionsand resources for plant growth. In: Gottlieb LD, Jain SK (eds)Plant evolutionary biology. Chapman & Hall, London, pp 341–369

Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystemengineers. Oikos 69:373–386

Kent AC, Day RW (1983) Population dynamics of an infaunalpolychaete: the effect of predators and adult-recruit interaction.J Exp Mar Biol Ecol 73:185–203

Lassig BR (1977) Communication and coexistence in a coralcommunity. Mar Biol 42:85–92

Lobban CS, Harrison PJ (1994) Seaweed ecology and physiology.Cambridge University Press, Cambridge

Lubchenco J (1978) Plant species diversity in a marine intertidalcommunity: importance of herbivore food preference and algalcompetitive abilities. Am Nat 112:23–39

Lubchenco J, Gaines SD (1981) A unified approach to marineplant-herbivore interactions. 1. Populations and communities.Annu Rev Ecol Sys 12:405–437

Marsh CP (1986) Rocky intertidal community organization; theimpact of avian predators on mussel recruitment. Ecology67:771–786

Menge BA (1995) Indirect effects in marine rocky intertidal inter-action webs: patterns and importance. Ecol Monogr 65:21–74

Menge BA, Sutherland JP (1987) Community regulation, variationin disturbance, competition and predation in relation to envi-ronmental stress and recruitment. Am Nat 130:730–757

Mukai H (1971) The phytal animals on the thalli of sargassum inthe sargassum region, with reference to their seasonal fluctua-tions. Mar Biol 8:170–182

Odling-Smee SE, Laland KN, Feldman MW (2003) Niche con-struction: the neglected process in Evolution. Princeton Uni-versity Press, Princeton

Paine RT, Vadas RL (1969) The effects of grazing by sea urchinsStrongylocentrotus spp. on benthic algal populations. LimnolOceanogr 14:710–719

Peterson CH, Summerson HC, Duncan PB (1984) The influence ofseagrass cover on population structure and individual growth ofa suspension-feeding bivalve, Mercenaria mercenaria. J MarRes 42:123–138

Peterson CH, Grabowski JH, Powers SP (2003) Estimatedenhancement of fish production resulting from restoring oysterreef habitat: quantitative valuation. Mar Ecol Prog Ser264:249–264

Petraitis PS (1990) Direct and indirect effects of predation, her-bivory, and surface rugosity on mussel recruitment. Oecologia83:405–413

Pohle DG, Bricevj VM, GarciaeSquivel Z (1991) The eelgrasscanopy—an above-bottom refuge from benthic predators fromjuvenile bay scallop Agropecten irradians. Mar Ecol Prog Ser74:47–59

Portig AA, Mathers RG, Mkontgomery WI, Govier RN (1994)The distribution and utilization of Zostera species in StrangfordLough, Northern Ireland. Aquat Bot 47:317–328

Raffaelli DG, Hall SJ (1992) Compartments and predation in anestuarine food web. J Anim Ecol 61:551–560

Raffaelli DG, Hall SJ (1996) Assessing the relative importance oftrophic links in food webs. In: Polis GA, Winemiller KO (eds)Food webs: integration of patterns and dynamics. Chapman &Hall, New York, pp 185–191

Raffaelli DG, Milne H (1987) An experimental investigation of theeffects of shorebird and flatfish predation on estuarine inverte-brates. Est Coast Shelf Sci 24:1–13

Reise K (1985) Tidal flat ecology: an experimental approach tospecies interactions. Springer, Berlin Heidelberg New York

Ricklefs RE, Miller GL (1999) Ecology, 4th edn. Freeman, NewYork

Seed R (1996) Patterns of biodiversity in the macro-invertebratefauna associated with mussel patches on the rocky shores.J Mar Biol Assoc 76:203–210

Thrush SF, Pridmore RD, Hewitt JE, Cummings VJ (1994) Theimportance of predators on a sandflat: interplay between sea-sonal changes in prey densities and predator effects. Mar EcolProg Ser 107:211–222

Tokeshi M (1993) Species abundance patterns and communitystructure. Adv Ecol Res 24:111–186

Trumble JT, Kolodyn-Hirsch DM, Ting IP (1993) Plant compen-sation for arthropod herbivory. Annu Rev Entomol 38:93–119

Tsuchiya M, Nishihira M (1985) Islands of mytilus as a habitat forsmall intertidal animals-effect of island size on communitystructure. Mar Ecol Prog Ser 25:71–81

Underwood AJ (1986) Physical factors and biological interactions:the necessity and nature of ecological experiments. In: MoorePG, Seed R (eds) The ecology of rocky coast. Columbia Uni-versity Press, New York, pp 372–390

Underwood AJ, Denley EJ, Moran MJ (1983) Experimentalanalyses of the structure and dynamics of mid-shore rockyintertidal communities in New South Wales. Oecologia 56:202–219

Vance RR (1978) A mutualistic interaction between a sessile marineclam and its epibionts. Ecology 59:679–685

von Ende CN (2001) Repeated-measures Analysis: growth andother time-dependent measures. In: Scheiner SM, Gurevitch J(eds) Design and analysis of ecological experiments. OxfordUniversity Press, New York, pp 134–157

Watson DC, Norton TA (1985) Dietary preferences of the commonperiwinkle Littorina littorea (L). J Exp Mar Biol Ecol 88:193–211

Wootton JT (1992) Indirect effects, prey susceptibility, and habitatselection: impacts of birds on limpets and algae. Ecology73:981–991

Wootton JT (1993a) Indirect effects and habitat use in an intertidalcommunity: interaction chains and interaction modifications.Am Nat 141:71–89

Wootton JT (1993b) Size-dependent competition: effects on thedynamics vs. the end point of mussel bed succession. Ecology74:195–206

Wootton JT (1995) Effects of birds on sea urchin and algae: alower-intertidal trophic cascade. Ecoscience 2:321–328

Wootton JT (1997) Estimates and tests of per capita interactionstrength: diet, abundance, and impact of intertidally foragingbirds. Ecol Monogr 67:45–64

775