Effects of Chiton granosus (Frembly, 1827) and other molluscan grazers on algal succession in wave exposed mid-intertidal rocky shores of central Chile

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<ul><li><p>mid-intertidal algal succession and to isolate the effects of Chiton granosus, the most conspicuous member of the assemblage at thesetidal elevations. At sites heavily impacted by humans themolluscan grazer assemblage had strong negative effects on colonization and</p><p>1. Introduction</p><p>Journal of Experimental Marine Biology andabundance of green algae such as ulvoids and Blidingia minima. In doing so, the grazer assemblage had a strong negative indirecteffect on the establishments of chironomid fly larvae, which were only observed on green algal mats and rarely on bare rock. Nosignificant effects were detected on epilithic microalgae, and effects on sessile invertebrates were highly variable over space and time.C. granosus also had significant negative effects on green algae but did not account for the total grazing pressure exerted by the guild.Limited foraging excursions (ca. 35 cm) from refuges and moderate site (crevice) fidelity in this species may contribute to thepatchiness in green algal distribution observed in the field. Nearly 13 months after rock surface were experimentally cleared,M. laminarioides appeared in all experimental plots, but increased over three times faster in enclosures containingC. granosus than inexclosures plots or controls, suggesting that moderate levels of herbivory could actually facilitate the establishment of this alga in thesuccession and that the green algal cover found in the absence of grazers may delay its establishment. 2007 Elsevier B.V. All rights reserved.</p><p>Keywords: Ecological redundancy; Epilithic algae; Foraging behaviour; Grazing; Refuges; Successiongrazers on algal succession in wave exposed mid-intertidalrocky shores of central Chile</p><p>Moiss A. Aguilera, Sergio A. Navarrete </p><p>Estacin Costera de Investigaciones Marinas, Las Cruces, and Center for Advanced Studies in Ecology and Biodiversity,Pontificia Universidad Catlica de Chile, Casilla 114-D, Santiago, Chile</p><p>Received 15 January 2007; received in revised form 28 April 2007; accepted 7 May 2007</p><p>Abstract</p><p>Molluscan grazers can have important effects on the abundance, colonization rates, and successional pathways of algalassemblages and the entire intertidal community. In general, early successional algae are more readily consumed than corticated algaeand kelps, which usually get established later in the community succession. To generalize, however, the effect of different grazers onalgal assemblages must be examined on different coasts and under different scenarios. This information could help us understand themechanisms of ecosystem processes and situations in which general models do not apply. Along the coast of Chile, humans harvestlarge keyhole limpets, which seem to be the only invertebrate grazers capable of controlling the dominant corticated algaMazzaellalaminarioides, a canopy-forming species that can cover extensive areas of the mid intertidal zone. In this scenario, where large limpetsare harvested, the overall effects of the diverse molluscan assemblage of limpets, chitons and snails on algal succession and oncorticated algae in particular are not clear. We conducted a 26-month-long experiment to evaluate the effects of molluscan grazers onEffects of Chiton granosus (Frembly, 1827) and other molluscan Corresponding author. Tel.: +56 35 431670; fax:+56 35 431720.E-mail address: snavarrete@bio.puc.cl (S.A. Navarrete).</p><p>0022-0981/$ - see front matter 2007 Elsevier B.V. All rights reserved.doi:10.1016/j.jembe.2007.05.002Ecology 349 (2007) 8498www.elsevier.com/locate/jembeExperimental manipulations in different parts of theworld have demonstrated that invertebrate herbivores</p></li><li><p>mentacan determine the structure and diversity of intertidalalgal assemblages by controlling the abundance (bio-mass, cover) of established dominant macrophytes, bypreventing or severely decreasing colonization by algaeand sessile invertebrates, or by selectively removingedible algal species and, through this, altering succes-sional pathways (see Lubchenco and Gaines, 1981;Hawkins and Hartnoll, 1983; Santelices, 1990; Branchand Moreno, 1994; Fernndez et al., 2000; Duffy andHay, 2001 for reviews). Along most temperate coasts ofthe world, the intertidal grazer assemblage is numericallydominated by several species of mollusks and crusta-ceans (Lubchenco and Gaines, 1981; Brawley, 1992;Duffy and Hay, 2001). Several studies have shown thatmost of these grazers prefer early successional algae overthe more herbivore-resistant corticated algae and kelps(sensu Steneck and Dethier, 1994). These algal groupsusually become established later in succession. Excep-tions to these broad generalizations abound, however.Algal responses to grazers depend, among other things,on a) attributes of the grazer assemblage, such as speciescomposition, overall size and the range of feedingpossibilities, which is in part determined by the radularapparatus (Steneck and Watling, 1982), b) attributes ofthe algal species composition and their chemical ormechanical defenses (e.g. Branch, 1981; Gaines, 1985;Hay and Fenical, 1988), c) the rates of algal growth,which are usually determined by external environmentalfactors (Underwood and Jernakoff, 1981; Nielsen andNavarrete, 2004; Coleman et al., 2006; Wieters, 2005),and d) the relative effects of stress gradients on algalversus grazer species (Menge and Olson, 1990; Jenkinsand Hartnoll, 2001; Menge et al., 2002). Since humansare dramatically reducing the biomass of many grazersand top predator species, targeting mostly the largestspecies in these assemblages (Botsford et al., 1997;Jackson et al., 2001; Worm et al., 2002), there is anurgent need to understand how biodiversity and speciescomposition determines the dynamics of benthic com-munities (Coleman et al., 2006). Here, we evaluate theeffect of an entire molluscan grazer assemblage on algalcolonization and succession in an intertidal ecosystemstrongly influenced by humans on the central coast ofChile.</p><p>Several intertidal mollusks can control the abun-dance of corticated algae and kelps (Lubchenco, 1978;Moreno and Jaramillo, 1983; Hawkins et al., 1992;Bustamante et al., 1995), but many others can feedefficiently only on benthic microalgae. While they havethe capacity to diminish considerably or even totallyeliminate the thin algal films (diatoms, sporelings and</p><p>M.A. Aguilera, S.A. Navarrete / Journal of Expericyanobacteria), they have virtually no direct effects onestablished macroalgae (Castenholz, 1961; Nicotri,1977; Underwood, 1984; Hill and Hawkins, 1991;Hawkins et al., 1992). It has also been observed thatsome molluscan grazers can affect the settlement andrecolonization of sessile invertebrates (mostly barna-cles), by eating or exerting a bulldozing effect on larvaeor post-metamorphic stages (e.g. Lottia pelta and Tec-tura scutum Dayton, 1971; Berlow and Navarrete,1997; Scurria (=Collisella) digitalis Paine, 1981; Pa-tella vulgata Hill and Hawkins, 1991; Katharinatunicata Wootton et al., 1996; Collisella grata Chanand Williams, 2003). These differences are primarilydetermined by mechanical restrictions of the feedingapparatus and individual body size. Moreover, differentkinds of molluscan grazers, even those with similarfeeding apparatus and sizes can influence spatialpatterns of algal and sessile invertebrate abundance indifferent ways because of differences in foragingbehavior (see Creese and Underwood, 1982; Chelazziet al., 1987) and the spatial range of foraging excursions(Williams et al., 2000). For example, the mosaics ofsessile species in the intertidal seascape appear to begreatly modified by the distribution of grazers and theirforaging performances, which are directly related tospecific behavioral adaptations (eg. Mackay andUnderwood, 1977; Branch, 1981; Focardi and Chelazzi,1990; Chapman, 2000). In this context, homingbehavior, which is the repeated return of individualsto the same resting site after foraging excursions (seeStimson, 1970; Chelazzi et al., 1987; Focardi andChelazzi, 1990), can have important consequences foralgal community structure and spatial patterns ofvariance (Benedetti-Cecchi, 2000a,b; Coleman et al.,2004).</p><p>1.1. The system</p><p>A diverse array of herbivores inhabit the mid andupper intertidal zones of the wave-exposed coast ofcentral Chile, including several species of patellid,keyhole and pulmonate limpets, littorinid, turbinid andtrochid snails, as well as several chiton species(Santelices, 1990; Rivadeneira et al., 2002). A fewspecies of grapsid crabs also form part of thisheterogeneous grazing guild, but their abundance isgenerally low in central Chile. At high tide fish also formpart of this guild during some life stages and their effecton macroalgae can be very important, especially in semi-protected areas (Muoz and Ojeda, 1997). The coast isintensively harvested by humans, who target largeindividuals of the fissurellids, Fissurella crassa and</p><p>85l Marine Biology and Ecology 349 (2007) 8498F. limbata (Oliva and Castilla, 1986). Inside the marine</p></li><li><p>mentareserve of Las Cruces, in central Chile, where noharvesting takes place, Oliva and Castilla (1986)suggest that large keyhole limpets are responsible forthe low abundance of the corticated alga Mazzaellalaminarioides as well as green algae. This result agreeswell with results inside a marine reserve in southernChile involving another large keyhole limpet species(Jara and Moreno, 1984). On the other hand, at sites incentral Chile impacted by human harvesting, andtherefore with low abundances of large limpets, Nielsenand Navarrete (2004) observed that molluscan grazerscan exert strong control on the abundance of ephemeral(mostly green) algae that settled soon after the rocksurface is cleared. However, they also noted that thesegrazers had no significant effects on late successionalspecies, such as Mazzaella, regardless of variation innutrient loadings produced by coastal upwelling.Similarly, Otaza (1986) found only transient effects onephemeral algae exerted by Chiton granosus, andvirtually no effects on corticated algae. All of thesestudies were conducted on areas of relatively smoothrock surface, away from crevices and therefore poten-tially beyond the reach of most grazers as most non-fissurellid grazers, especially chitons, tend to aggregatein crevices and forage some distance around them.Therefore, their effects on benthic algae might have beenunderestimated in these experiments. Moreover, obser-vations in southern Chile suggest that some of the samegrazer species can control the abundance of corticatedalgae (Jara and Moreno, 1984; Moreno and Jaramillo,1983), in contrast to Nielsen and Navarrete's (2004)results.</p><p>Here we explore whether small molluscan grazersplay a role in regulating algal and barnacle colonizationin areas of the coast heavily exploited by humans.We concentrate on the potential effects of the chitonC. granosus, the most abundant grazer in the mid inter-tidal zone in terms of biomass (Otaza and Santelices,1985), which occurs in crevices during low tides.</p><p>2. Methods</p><p>2.1. Study site and grazers assemblage</p><p>The study was conducted in the mid intertidal zone ofa wave-exposed site outside the Estacin Costera deInvestigaciones Marinas (ECIM) of the PontificiaUniversidad Catlica de Chile in the locality of LasCruces (3330S, 71 30W), central Chile. Las Cruces islocated between two upwelling centers and is itselfwithin an upwelling shadow (Wieters et al., 2003;</p><p>86 M.A. Aguilera, S.A. Navarrete / Journal of ExperiNarvaz et al., 2004; Nielsen and Navarrete, 2004),where sea surface temperatures remain higher andnutrients lower than at upwelling centers to the northand south (Nielsen and Navarrete, 2004; Wieters, 2005).The experimental site is characterized by exposedbenches oriented SENW and separated by widechannels with strong water flux.</p><p>To quantify invertebrate herbivore abundance at theexperimental site, we conducted 3 transects perpendicularto the coastline from the highest intertidal fringe (littorinidzone), to lowest intertidal fringe (LessoniaCorallinezone), spaced ca. 50 cm apart. Along each transect wepositioned 9 to 12 625 cm2 (2525 cm) quadrats at 30 cmintervals. Sampling was conducted three times during thefirst year of the study (April, September and November2003). Biomass of each species was estimated throughwet weight to length regressions.</p><p>2.2. C. granosus diet</p><p>To characterize the diet of C. granosus through theyear and relate it to experimental results, we examinedstomach contents of individuals collected monthly tobimonthly in the field, several meters away from theexperimental areas. Preliminary samples and rarefactioncurves (Gotelli and Colwell, 2001) indicated that asample size of 8 individuals was sufficient to charac-terize diet diversity of this species on each samplingdate. Individuals were collected manually from the midand high intertidal zones during night time low tides,injected immediately with a 10% formaldehyde solutionto stop the digestion process, labeled, and taken to thelaboratory for analysis. The gut contents of eachindividual were examined under a dissecting scope toidentify food items to the lowest possible taxonomiclevel. Furthermore, to estimate the relative abundance ofalgal items, we placed a 1 ml gut sample on a glass slidereticulated with 30 points, recording the number ofpoints intersected by each item. Note that more than onefood item could intersect a given point (e.g. microalgaeand sections of macroalgae), and therefore the totalabundance can be higher than 1.</p><p>2.3. Movement and foraging activity of C. granosus</p><p>To assess the spatial scale of the foraging excursionsof C. granosus from the aggregation crevices andquantify potential homing behavior, we monitored themovement of marked individuals in November 2002(n=50 individuals) and again in February 2003 (n=67individuals) at the same site where the herbivoryexperiments where later set up (see below) and at</p><p>l Marine Biology and Ecology 349 (2007) 8498another site 500 m away, respectively. The spatial</p></li><li><p>mentapositions of individuals found inside crevices during theday were recorded on an XY coordinate system andindividuals were marked in situ with bee tags withoutprying them off the substratum. A total of 40 markedindividuals were lost in the first site and 34 in the secondone (due to lost tags, migration of the survey area andsome to predation in successive days), leaving 10 and 33individuals respectively at each site. High tag losswas the tradeoff of marking individuals in situ to causethem as little disturbance as possible. To set up thecoordinate reference, we fixed two screws parallel to theshoreline and 5 m apart, along which we extended ameasuring tape to register the position of individualsalong the X-axis. With another measuring tape, extendedperpendicular to the first axis, we recorded the positionof the individuals along the Y-axis. Individuals werefollowed every 12 h, during diurnal and nocturnal lowtides for seven consecutive days. Movement wascalculated as the minimal Euclidian di...</p></li></ul>


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