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

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    Masakazu Hori Takashi Noda 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-nicant eects on algal assemblages and small herbivo-rous invertebrates. The eects of the birds on algae weredierent 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 indirectlyaected 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 modiersrather 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 dierent to invertebrate herbi-vores in rocky intertidal habitats.

    Keywords Amphipods Ecosystem engineering Gulls Isopods Monostroma angicava


    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 eects of herbivores have been categorizedinto the following three types: (1) direct and indirecteects on algae (e.g., Paine and Vadas 1969; Lubch-enco 1978; Branch 1981; Duy and Hay 2000), (2)direct and indirect eects on sessile animals by theirgrazing/bulldozing (e.g., Dayton 1971; Underwood1986; Petraitis 1990), and (3) indirect eects 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 eect on algae and invertebratesthrough habitat modication. However, there havebeen few studies of habitat modication 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 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@arc.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) 21:768775DOI 10.1007/s11284-006-0192-8

  • eects of habitat modication on small organisms aswell as the food related eects of grazing/herbivory.

    Shorebirds feed on a variety of marine organisms,including shes, invertebrates, and seaweed in variousnear-shore habitats (Jacobs et al. 1981; Hocky andUnderhill 1984; Baird et al. 1985; Brown andMcLachlan 1990; Raaelli 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; Raaelliand Milne 1987; Raaelli 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 ats, 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-specic juveniles (Kent and Day 1983; Thrush et al.1994).

    Studies of bird herbivory on mud ats 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 eects seem to dier from thoseof invertebrate herbivores because of substantial sizeand morphological dierence. Birds, with greater size,eyesight and mobility, are likely to be selective, and eatpreferable seaweeds as well as avian predators on mudats. 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 eects of birds on seaweeds or theindirect eects 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 theeects of avian grazers on the algal assemblage thatcreates a high canopy on the rocky benches, andexamined indirect eects 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 (4144N,14104E). 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 fth was the wildgoose species, the black brent goose (Branta berniclaorientalis Tougarinov), which was less abundant thanthe herring gulls (Hori and Noda 2001a). These vespecies 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 ood-tide period, the herbivorous birdsfeed on algae from when the algal fronds start to oat 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 ood 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 ingestM. 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 shery wastes in shing 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


  • 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 shes 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 eectsof 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 505015 cm3 andmade from 13-mm diameter poly-vinyl chloride pipes(see Hori and Noda 2001b for details). In order to avoidany articial eects 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 2525 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 2060 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 nished 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 ShannonWeiner 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 eect on the percent coverofM. angicava, algal species richness and diversity index(H), and the densities of amphipods and isopods. Theassumption of variance homogeneity was assessed usingCochrans C-test. Mauchlys sphericity test for within-subject factors was also performed, and GreenhouseGeisser 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 dierences in algalcover and amphipod density between exclosures andcontrols.


    Of the ve 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 theocks 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 signicantlydierent 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 dierence was insignicant in early May afterthe avian herbivores had left the study site (Fig. 2,








    Brent gooseGulls


    . num

    ber o

    f ind


    al (d

    ay1 )

    MonthDec. 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


  • Table1Repeated-measuresANOVAontheeectofaviangrazing(controlversusexclosure)onpercentcoverofM.angicava,algalrichness,algalevenness,amphipods,andisopods




























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