The functional roles of herbivores in the rocky intertidal

FUNCTIONAL ROLE OF INTERTIDAL HERBIVORES 241

Revista Chilena de Historia Natural 84: 241-261, 2011 © Sociedad de Biología de Chile

REVIEW ARTICLE

REVISTA CHILENA DE HISTORIA NATURAL

The functional roles of herbivores in the rocky intertidal systems inChile: A review of food preferences and consumptive effects

Los roles funcionales de los herbívoros en sistemas intermareales rocosos en Chile:Una revisión de las preferencias alimenticias y efectos de consumo

MOISÉS A. AGUILERA

Centro de Estudios Avanzados en Zonas Áridas (CEAZA), Facultad de Ciencias del Mar, Universidad Católica del Norte,Larrondo 1281, Coquimbo, Chile

Estación Costera de Investigaciones Marinas, Las Cruces, and Center for Advanced Studies in Ecology and Biodiversity,Pontificia Universidad Católica de Chile, Casilla 114-D, Santiago, Chile

Corresponding author: [email protected]

ABSTRACT

This paper reviews recent knowledge about the functional roles that herbivores have in intertidal communities inChile. Specifically, I review field and laboratory studies dealing with the food preferences of herbivores, theresponses of algae to herbivore attacks and reports of negative and positive functional effects of herbivores on algalpopulations and communities. Most herbivores studied are characterized as generalist species. Green ephemeraland a few corticated algae dominate diets, while all species considered ingest larvae and post-metamorphic stagesof invertebrates challenging classical characterizations of the herbivore guild. Functional redundancy andcomplementarity within the herbivore guild is discussed in relation to both quantitative and qualitative evidence.The magnitude of consumptive per capita effects of herbivores on algae can be related, although not entirely, tobody size. Feeding mode can determine differential species participation in different phases and stages ofcommunity succession. Positive effects of herbivores on algae via spore dispersion, and also compensatory potentialafter consumption, appear to match the classical model of the “grazing optimization hypothesis”. Only one speciesthat form “gardens” is reported, suggesting a lack of information regarding behavioural aspects of abundant taxafrom intertidal habitats in Chile. According to variation in oceanographic conditions and thermal regimes along thecoast of Chile, geographical variation in functional effects of herbivores and thereby shifts in the herbivore-algaebalance is expected. Future studies should consider the functional relationship within the herbivore guild atdifferent temporal and spatial scales, and compensatory potential after species loss. Whether herbivore specieshave either redundant or complementary roles in intertidal communities can help us to understand the intensityand direction of human impacts in both community structure and ecosystem functioning.

Key words: Chile, herbivores, functional role, guild, intertidal.

RESUMEN

Este trabajo revisa el conocimiento reciente sobre los roles funcionales que los herbívoros tienen en comunidadesintermareales en Chile. Específicamente, se revisaron estudios sobre preferencias tróficas de los herbívoros,respuestas de las algas al ataque de estos y reportes de efectos negativos y positivos de los herbívoros sobrepoblaciones y comunidades de algas. La mayoría de los herbívoros estudiados se caracterizan por ser generalistastróficos. Las algas verdes efímeras y pocas algas corticadas dominan la dieta, mientras que todas las especiesconsideradas ingieren larvas y postmetamórficos de invertebrados lo cual desafía la caracterización clásica delgremio. La ocurrencia de redundancia funcional y complementariedad al interior del gremio de herbívoros, esdiscutida en relación a las evidencias cuantitativas y cualitativas presentadas. La magnitud de los efectos deconsumo per cápita de los herbívoros sobre las algas puede estar relacionada, aunque no completamente, al tamañocorporal. Los modos de forrajeo pueden determinar la participación diferencial de las especies en distintas fases yestados de la sucesión comunitaria. Los efectos positivos de los herbívoros sobre las algas a través de dispersión deesporas, y potencial de compensación luego del consumo, parece coincidir con los modelos clásicos de la “hipótesisde optimización del forrajeo”. Solo una especie que forma “jardines” ha sido reportada en Chile, lo cual muestra lafalta de información sobre los patrones de comportamiento de taxa abundantes presentes en estos hábitats enChile, los cuales muestran comúnmente este tipo de comportamientos en otras costas. De acuerdo a la variación enlas condiciones oceanográficas y régimen termal a lo largo de la costa de Chile, se espera que existan variacionesgeográficas en los efectos funcionales de los herbívoros y en el balance herbívoro-alga. Futuros estudios deberíanconsiderar las relaciones funcionales al interior del gremio a diferentes escalas espaciales y temporales, y elpotencial de compensación en funciones luego de la pérdida de especies. Si los herbívoros tienen roles redundanteso complementarios en la comunidad intermareal, puede ser de gran interés para entender la intensidad y ladirección que tienen los impactos humanos en la estructura comunitaria y funcionamiento ecosistémico.

Palabras clave: Chile, gremio, herbívoros, intermareal, rol funcional.

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INTRODUCTION

Herbivory is commonly defined as theconsumption of living plant tissue by animals,and herbivores are considered all those animalsadapted to live solely consuming plant tissue.Thus, herbivory is related to the consumptiveeffects that animals can cause on populations orcommunities of plants, and is considered one ofthe most important ecological processes inmarine as well as in terrestrial ecosystemsaround the world (Lubchenco & Gaines 1981,Hawkins & Hartnoll 1983, Huntly 1991, Schmitz2008). In marine systems, herbivores candetermine temporal and spatial distribution ofalgae in both intertidal and subtidal habitats(Lubchenco & Gaines 1981, Hawkins &Hartnoll 1983). Through consumption of maturealgae and spores, different intertidal andsubtidal herbivores can affect successionalpathways, determining algae speciescomposition and abundance (Lubchenco 1978,Hawkins & Hartnoll 1983). Almost everydimension of algal life history and performancecan be influenced by marine herbivores (e.g.,succession, Sousa 1979; chemical defences,Duffy & Hay 1994). But although many speciescan cause negative effects on algae, positivedirect and indirect effects are also importantmechanisms recently considered as relevantfactors in the structure of intertidalcommunities (Branch et al. 1992, Plaganyi &Branch 2000). As herbivores are also consumedby high-level carnivores, including humans,they also have a central importance in food webdynamics and ecosystem function (Schmitz2008).

Diverse studies have been conducted inrocky intertidal systems, but lack of replicationhas hindered testing hypotheses regarding theeffect of herbivores on community structure.Widespread negative effects on algal biomassare common features. On the other hand,information from the diet of herbivoressuggests positive interactions between grazersand algae may occur in some intertidal habitatsand recent studies reporting frequentinvertebrate consumption by generalist grazerschallenges the basic definition of this guild.

In Chile, an important number of studiesdealing with the effect of herbivores oncommunity structure have been conducted insubtidal habitats examining for example the

dynamics of kelp forests (see Vásquez &Buschmann 1997 for review). Some of themost abundant herbivores in Chilean subtidalhabitats are amphipods (Lancelloti & Trucco1993), sea urchins, fishes and some molluscs(e.g., Vásquez et al. 1984, Santelices 1990). Inintertidal habitats, a similar pattern is seenwith amphipods (Lancellotti & Trucco 1993)molluscs (Otaíza & Santelices 1985, Santeliceset al. 1986, Valdovinos 1999, Rivadeneira et al.2002), some crustaceans, fish (Muñoz & Ojeda1997, Horn Ojeda 1999) and two commonspecies of sea urchins (Vásquez & Buschmann1997, Vásquez 2007) as the most abundant anddiverse herbivore species. Of all the taxonomicgroups, molluscs are one of the most diversein intertidal habitats (Rivadeneira et al. 2002)and are common in experimental studiesbecause they can be easily manipulated.

In this paper, I review the status of marineintertidal studies conducted in Chile dealingwith effects of herbivores on algae. Specifically,I consider studies on food preferences and algalresponses to herbivore attack, experimentalapproaches evaluating community-level effectsof herbivory and discuss studies reportingpositive effects of herbivores on algae. Finally, Ihighlight the importance of experimentalapproaches, as well as consideration of naturalhistory for better understanding the diversity offunctional roles herbivores play on Chileanintertidal rocky shores.

In general, studies dealing with the role ofherbivores in intertidal systems in Chile can beseparated into three categories; (a) studies thatcharacterize diet or food preferences ofherbivores and relate them with effects on algaepopulations; (b) studies that through field or labexperiments explicitly evaluate the consumptiveeffects (commonly negative) of herbivores onalgae and other sessile populations andcommunities and; (c) studies that observepositive relationships between herbivores andalgae (mutualistic interactions). Consideringthese studies altogether, they give us relevantinformation about the functional role thatherbivores play in intertidal ecosystems.

FOOD PREFERENCES OF HERBIVORES

From a functional perspective, the foodpreferences of herbivores are relevant to


understand the impacts that different speciesexert on algae community structure (e.g.,Lubchenco & Gaines 1981, Steneck & Dethier1994). Whether herbivores are generalist orspecialist consumers, could be of interest tounderstand the role that these species have onthe successional pathways of the system,increasing or decreasing the rate of succession(e.g., Lubchenco 1978).

Feeding modes

Food preferences of herbivores are linkedto algal handling mode and effects on algalcommunities. Diverse classifications of feedingmodes have been proposed by some authorswho utilize ingested food size (see Hawkins &Hartnoll 1983 for review). Thus, they separatethe different species into microphagous(mainly feeding in microalgae) andmacrophagous (feeding on macroalgae). Forexample, considering microphagous andmacrophagous feeding modes in limpetsBranch (1981) proposed four basic foragingpatterns; (i) species feeding on microalgae anddetritus, (ii) species feeding on macroalgae,(iii) territorial species closely linked to aparticular food plant, and finally (iv) epiphyticspecialist species feeding on their host plantand microalgal epiphytes. Despite ingestedfood size, almost all molluscan herbivores areconsidered “grazers”, in the sense that theymainly feed on microalgae and plantlets ofgreen ephemeral algae, and some fish andcrustaceans are considered “browsers” in thatthey can bite large pieces of adult algae(Hawkins & Hartnoll 1983, Horn 1992).

Feeding modes appear more variable introphic generalist than in specialist species,because it has been observed some generalistherbivores can alternate the feeding onmicroalgae with feeding on pieces of adultmacroalgae (e.g., fissurelids limpets and fish,see Horn & Ojeda 1999 and see below).According to a most general classification, itcould be more appropriate to consider“grazers” these species able to scrap thesubstratum removing spores, plantlets ofmacroalgae, epiphytes, microalgae, andrecently settled invertebrates (see below).Meanwhile, “browsers” could be considered allthose species removing pieces of adult orestablished algae through “biting” on their

fronds. These categories of feeding are similarto those which are commonly used for fish(Horn 1992) and for terrestrial herbivores(McNaughton 2001).

In particular, modes of feeding are directlyrelated to the morphology of the buccalapparatus of herbivores (Steneck & Watling1982, Horn & Ojeda 1999). Different feedingstructures can constrain the capacities ofherbivores to remove large pieces ofmacroalgae or to deeply scrape the rockysubstratum to ingest epilithic microalgae, butthey can’t determine specific food choice (seebelow). Feeding modes (browsing, grazing,and two alternating strategies) are importantcharacteristics that could help to understandqualitative effects of herbivores on either algaedevelopmental stages or morphologies, butpoorly determine quantity of algae removedwhich is mostly a matter of body size (seebelow).

Molluscs’ food preferences

One of the most diverse and locally abundantgroups of herbivores present in the rockyintertidal habitat in Chile are molluscs(Santelices et al. 1986, Valdovinos 1999,Rivadeneira et al. 2002). Most species aregeneralist grazers, and show considerablesimilarity in the items they consume. The mostfrequent items consumed by molluscan grazersare diatoms, ulvoids, and calcareous crusts(Santelices & Correa 1985, Santelices et al.1986, Camus et al. 2008). Seasonal variations inthe diet of grazers correlate with foodavailability (Santelices et al. 1986), suggestingthat most species have an opportunistic strategyin their feeding patterns.

Despite the fact that most molluscanherbivores present in the intertidal habitat inChile consume microalgae and microscopicstages of green ephemeral algae (i.e. plantules,spores), the browser/grazer Fissurella pictaappears to be also capable of consuming adultcorticated algae like Mazzaella laminarioides(hereafter Mazzaella, Moreno & Jaramillo1983, Godoy & Villouta 1986). Similarly, thePulmonate limpet Siphonaria lessoni has beenreported to consume adult stages of Mazzaella,and according to Jara & Moreno (1984)populations of this limpet can cause importantreductions in biomass of this alga (but see

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below). Interestingly, very low ingestion ofcorticated Mazzaella by Siphonaria orfissurellid limpets was reported by Santeliceset al. (1986)’s study conducted in central Chilecontrasting with the high availability ofMazzaella in this region (Santelices 1990).

Previous studies dealing with dietcomposition were not able to separateconsumption on adult or microscopic stages ofalgae thus constraining information onconsumptive effects of herbivores. In order toestablish the ability of molluscan herbivores toingest adult stages of both ephemeral andcorticated algae, Aguilera (2010) conductedshort term laboratory trials (replicate trials for7-10 days) evaluating consumptive effects ofthe species F. crassa, S. lessoni, C. granosusand S. araucana on ephemeral (ulvoids,Porphyra) and corticated (i.e. Mazzaella) algalbiomass. In general, it was observed that S.lessoni and F. crassa were the only speciescapable of consuming adult stages ofcorticated Mazzaella and the ephemeral Ulvarigida and Porphyra columbina (Aguilera2010). The pulmonate limpet S. lessoni eatssome portion of cystocarpic fronds, and canonly consume tiny pieces of adult gametophyteof Mazzaella. The ability to consume adultstages of algae was related to feeding modes(see above), whereas quantity of algaeconsumed showed a linear relationship withherbivore body size (see below). In general,body size correlates with consumption rates,handling times and the time animals spendforaging (Mittelbach 1981) thereby suggestinga scaling relation of food intake and body sizein consumer assemblages (see below). In thefield, in the higher intertidal zone, S. lessoni,together with the periwinkle Nodilittorinaperuviana, is able to feed upon bleachedfronds of Mazzaella (author personalobservations). The key-hole limpet F. crassacan consume entire fronds of adult plants ofMazzaella, and because of its large size (5.0-7.0cm shell length, see also Oliva & Castilla 1986)this herbivore can have strong effects onnatural populations of this alga (see below). Inconsequence, both F. crassa and S. lessonihave the potential to affect microscopic as wellas adult plants of both ephemerals andcorticated algae. These herbivores apparentlycan alternate grazing and browsing provokingan apparent differentiation in their trophic

niche and their functional role compared withother herbivores.

Are molluscan grazers omnivorous?

Many studies dealing with the diet ofherbivores report the presence ofinvertebrates, mainly barnacles, in the gut ofmolluscan grazers (Santelices & Correa 1985,Santelices et al. 1986, Aguilera 2005, Aguilera& Navarrete 2007). These herbivores may beconsidered omnivores owing to their ability tofeed (i.e. ingest, digest and assimilate) in morethan one trophic level (Pimm & Lawton 1978),in this case a basal (algae) and intermediate(animal) species. The ingestion of barnacles(i.e. cyprid larvae and post-metamorphics) bygrazers occurs when they scrape the substratein a “bulldozing-like” fashion. This foragingmode is an important mechanism of post-settlement mortality for diverse invertebrates,widely reported in other systems (e.g., Dayton1971, Chan & Williams 2001).

Studies conducted in northern Chile (20º S-70º W) (Aguilera 2005) report that the speciesChiton granosus frequently consume cypridlarvae (Frequency = 67 % of guts analysed) andpost-metamorphic spat (100 %) of chthamalidbarnacles beside other invertebrates (e.g.,dipteran larvae, Aguilera 2005). Previousauthors suggested cyprids are the main itemingested by C. granosus (see Jara & Moreno1984), but these larvae are able to passundamaged through the gut and the caecum ofthis chiton (Aguilera 2005). The proportion ofcyprids found in the faecal pellets of C.granosus is commonly high (e.g., Santelices &Correa 1985, Aguilera 2005) suggesting theselarvae may not be digested properly by thischiton.

Recently, an extensive study dealing withtrophic relationships among molluscanherbivores present in intertidal systems ofnorthern Chile (from 21º00’ S to 30º06’ S)(Camus et al. 2008) showed that 29 of the mostrepresentative species of molluscan herbivoresingest invertebrates. The animal items accountfor around 60 % of the food consumed by theseherbivores. In general, the chitons C. granosusand Enoplochiton niger and the scurrinidlimpets Scurria viridula and S. cecilianainclude barnacle larvae and post-metamorphicspat besides other invertebrate items in their


diet (Camus et al. 2008, Sanhueza et al. 2008).Camus et al. (2009) showed that fissurellidlimpets (formerly Fissurella limbata and F.picta) and C. granosus are able to digest andalso assimilate animal items. This findingappears to indicate the generality of animalconsumption by molluscan grazers, pointingout that most species behave like omnivoresrather than strict herbivores (Camus et al.2009). This information highlights theimportance of these species for trophic webdynamics and their broader functional roles inintertidal systems (Camus et al. 2008, Camuset al. 2009). Likely, consumption of barnacles(larvae and post-metamorphics) may supplyherbivores with both proteins and minerals notpresent in algae especially during theirreproductive peaks (J. Lubchenco personalcommunication). In this context, studies onthe diet of chitons (conducted in Siberia),suggest a selective shift in feeding patterns ofsome species from herbivore to omnivoreaccording to seasonal changes inenvironmental conditions (Latyshev et al.2004). Thus, ingestion of animal items byherbivores may vary in response to changes inthe physiological requirements of herbivores(e.g., development stages, reproductive peaks)and also seasonal variation in both algal spores(Santelices 1990) and animal settlement (e.g.,barnacles, Aguilera 2005, Aguilera &Navarrete 2007). Therefore, information onboth animal ingestion and assimilation analysissuggest consumption of invertebrates may notbe entirely incidental and nutrientrequirements of these herbivores, not presentin algae, might account for this kind of intake(see Bozinovic & Martinez del Río 1996) whichdeserve further studies. For example, foodchoice experiments could be conducted inorder to determine whether generalistherbivores are able to select animal items andhow environmental variability can modify thisfeeding behaviour.

Although some grazers frequently consumepost-metamorphics and larvae of differentinvertebrate species (e.g., Aguilera 2005,Camus et al. 2008), it is not entirely clearwhether this consumption can translate intosignificant effects in abundance of theseinvertebrates. Although grazers can remove aconsiderable number of barnacle cyprids andpost-metamorphics from the rock surface

(through bulldozing), some authors haveobserved that pedal mucus of grazers canpositively affect the settlement of cyprid larvae(e.g., Johnson & Strathmann 1989). Therefore,positive as well as negative effects of grazerson barnacle settlement have been observed inother systems (e.g., Berlow & Navarrete1997). Because grazers maintain bare spacefor new colonizers of barnacles, some speciesmay have indirect positive effects on theabundance of barnacles (see Aguilera &Navarrete 2007 for effects of C. granosus onbarnacle settlement).

Food preferences by other intertidal herbivores

The most abundant, non-molluscan herbivorespresent in the low intertidal fringe andintertidal pools are the sea urchins Tetrapygusniger and Loxechinus albus. These speciesaggregate underneath the kelp Lessonianigrescens forming “barren grounds” whengrazing (see Vásquez & Buschmann 1997 forreview). Analysis of the gut contents of T.niger showed crustose calcareous algae werethe most frequent and abundant food item inits diet, although drift of the kelp Lessonianigrescens and Macrocystis pyrifera are alsoconsumed in low intertidal habitats (e.g.,Rodríguez 2003, Navarrete et al. 2008). Similarto molluscan grazers, both sea urchins includea wide variety of invertebrates in their diets(González et al. 2008, Navarrete et al. 2008).

Despite the high similarity in the generalmorphology between T. niger and L. albus,these species have differential feedingmechanisms which were related to f inedifferentiation in the buccal apparatus(Contreras & Castil la 1987). Thesemorphological characteristics would appear toconstrain their diets; adult T. niger canconsume significantly more benthic algaeattached to rock than L. albus which consumemore drift algae (González et al. 2008).Ontogenetic shift in the diet of L. albus couldaccount for the diverse role this species mayplay in low intertidal habitats (see Rodríguez2003); juveniles of this species consumemostly Ulva spp. while adult individualsconsume drift Lessonia.

Other important components from theherbivore guild are fish, which can forage onboth microscopic and adult stages of algae

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(Horn 1992, Horn & Ojeda 1999). Some authorsreport that algae consumption by fish iscommon in the intertidal assemblage present inChile (Stepien 1990). Nevertheless, this couldbe due to ontogenetic changes in the diet ofmany species from omnivores to herbivores(e.g., Aplodactylus punctatus; Benavides et al.1994, Ojeda & Cáceres 1995). The bleniidScartichthys viridis appears to be the only strictherbivorous fish in intertidal habitats (Muñoz &Ojeda 1997, Quijada & Cáceres 2000). The dietof S. viridis consists of green ephemeral algae(i.e. ulvoids) and exceptionally corticated algaelike Gelidium spp. (Cáceres & Ojeda 2000,Muñoz & Ojeda 2000). Even though this fishcan remove microscopic stages of macroalgaein a “grazing-like” fashion (Muñoz & Ojeda1997, Horn & Ojeda 1999), animals are also ableto remove large pieces of ulvoids and red algaethrough browsing of the distal portion of thesealgae (Ojeda & Muñoz 1999). Therefore, thisfish could have consumptive effects on theintertidal algae community via different feedingmodes similar to fissurellid limpets (see below).

Omnivorous fish Girella laevifrons canconsume large proportions of algae inintertidal levels similar to those observed forS. viridis (Muñoz & Ojeda 1997). In contrast,G. laevifrons needs to complement energyfrom algae with protein of animal origin. Theother common fish in intertidal habitats, thespecies S. sanguineous (Cancino & Castilla1988), consume commonly ephemeral algaebut also animal items (e.g., gastropods,barnacles) showing no clear trophicrelationship with any guild (see Muñoz &Ojeda 1997). Regarding body size of adult fishspecies (commonly larger than 30 cm), theymay have large per capita consumption of bothephemeral and corticated algae speciessuggesting strong effects on mid-to lowintertidal populations (see below).

In general, all herbivores studied (grazersand browsers) show dietary changes whichindicate opportunistic shifts in their feedinghabits, perhaps in response to seasonal changesin algae abundance or/and physical factors orontogenetic changes related to shifts inenergetic demands and body size (Santelices1990, Cáceres et al. 1993, Muñoz & Ojeda2000). The algae consumed by intertidalherbivores studied were previously consideredindependent of calcareous matrices, phenolic

compound or caloric contents of the algae (seeSantelices 1987 for review). Recently, differentchemical and structural algal traits has beenconsidered relevant to understand herbivore-algae interaction because some herbivores can“induce” enhancement in the concentration ofchemical compounds (e.g., polypropionates),changing the palatability of algae (i.e. brownalgae, see Macaya et al. 2005, Rothausler et al.2005). Although the food preferences ofmolluscan herbivores may be related to radularand plant morphologies (Steneck & Watling1982, Steneck & Dethier 1994), modification ofthe algal chemical concentration can changethe susceptibility of algae to herbivoreconsumption at very low temporal scales(Macaya et al. 2005, Macaya & Thiel 2008) andlikely food preferences of herbivores.

Defensive anti-herbivore mechanisms havebeen suggested to be important in herbivore-algae interactions in both tropical andtemperate systems (Duffy & Hay 1994; Cronin& Hay 1996). Commonly “constitutive”defences of algae (i.e. defences presentpermanently in algae) predominate over“induced” defences in systems with eitherlarge herbivores or high intensity of herbivory,but they tend to be costly to maintain (Cronin& Hay 1996). Induced anti-herbivore defencescan be triggered only a few hours afterherbivore consumption, and disappear whengrazing pressure diminishes (Macaya & Thiel2008). In this way, algae chemical compoundsmay alter the food choice of herbivores butonly at very low temporal scales likely notaltering algal attractiveness for herbivores. Ingeneral, induced defences are related to lowconsumption intensity and both plant andherbivore identity (Rothausler et al. 2005). Forexample, field and laboratory experimentsconducted in central-north Chile showedpalatability of brown algae Glosophora kunthiiand Dyctiota kunthii can be reduced byconsumption of the amphipod Parhyalellaruffoi but not by other herbivores (Macaya etal. 2005, Rothausler et al. 2005). It has beenreported that chemical deterrents ofherbivores are mostly concentrated inreproductive blades of algae (i.e. Lessonianigrescens) (Pansch et al . 2008). Thesestructures have high fitness value for algaeand higher energetic content for herbivoresthus ensuring a close co-evolutionary


relationship between different herbivore andalga pairs. There is no information, however,whether induced defences can trigger a moresustained or consistent effect on herbivorediet. Furthermore, apparently only herbivoresof small body size (i .e. amphipods andisopods), characterized by low consumptionrates, are able to induce responses in algae(Cronin & Hay 1996).

Most herbivores studied appear to preferephemeral algae that have low chemicalcompounds or structures resistant toherbivory (see Duffy & Hay 1994, Steneck &Dethier 1994), but others like chitons orspecies with very strong buccal apparatus likesea urchins prefer calcareous and non-calcareous crusts which have been consideredto be tolerant to grazing (e.g., Steneck &Dethier 1994). Sea urchins can also consumedrift kelps in pools and low intertidal habitatsthereby broaden their feeding niche comparedwith other herbivores (Rodríguez 2003). Fewmolluscs appear to be able to consumecorticated algae when they reach the adultstage, which may be related to eitherconstraints of the morphology of its buccalapparatus or defensive mechanisms present inthese algae (e.g., Steneck & Watling 1982,Duffy & Hay 1994, Steneck & Dethier 1994).

Food preferences of herbivores, feedingmodes and reaction of algae to herbivoreattack have been correlated with the kind ofeffects that different species have oncommunity structure (Cronin & Hay 1996,Macaya et al . 2005, Schmitz 2008).Nevertheless, the effect of consumers onresources can not be easily related to eithertheir diet or functional traits (e.g., body size,see below). It is necessary to take into accountboth direct and indirect effect of herbivores ontheir food resources, and manipulativeexperiments are often the only way to testmechanistic hypotheses dealing with bothconsumptive effects of herbivores on algalcommunities and functional structure of theassemblages (Paine 1992).

CONSUMPTIVE EFFECTS OF HERBIVORES

In Chile, experimental studies dealing withherbivore-algae interactions in rocky intertidalsystems have been designed to evaluate the

role of molluscan grazers on abundance,distribution, and successional patterns of algaeand other sessile organisms (e.g., barnacles).Although many studies reproduce generalpatterns found in other coasts of the world(Underwood 1980, Lubchenco & Gaines 1981,Hawkins & Hartnoll 1983, Coleman et al.2006), often they have identified species inChile that have important roles and apparentlyno parallel in equivalent habitats. Througheither similarity or differentiation in the effectsreported for herbivores, it should be possibleto examine the functional relationship amongdifferent species (i .e. redundant orcomplementary roles) and the compensatorypotential of species. Redundant or equivalenteffects of species within assemblages, arehypothesized to provide a high insurance ofecosystem function after species loss (Walker1992, Naeem 1998). Complementary effects ofspecies are related to the diversity ordifferentiation of functions that species haveon community or ecosystems through nichedifferentiation and facil itation, thereby,enhancing ecosystem functions (Loreau &Hector 2001). Thus, how functionally relatedspecies are is of interest to understand howhuman disturbances can scale up to alterationof different ecosystem functions (see below).

Effects of herbivores on intertidal communitystructure

One of the first experimental studies dealingwith the effects of herbivores on intertidalcommunities in Chile was conducted byMoreno and Jaramillo (1983). This studyshowed the importance of molluscan herbivoreassemblages in the structure of sessilecommunities (algae and barnacles). Throughherbivore removal experiments (in non-replicated experimental platforms, 5×5 m)conducted inside a Marine reserve (Mehuín),these authors observed that the browser/grazer Fissurella picta has a key role on mid-intertidal algal communities throughconsumption of the corticated dominant algaeMazzaella laminarioides (= Iridaea boryana inthese study) (Moreno & Jaramillo 1983).Outside the marine reserve, however,consumptive effects of F. picta on Mazzaellawere suppressed by human gathering whichdrastically reduces the abundance of adult

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limpets (Jara & Moreno 1984, Moreno et al.1984). Thus, other grazers like Siphonarialessoni (not consumed by humans) appear tocompensate for the absence of F. picta incontrolling corticated Mazzaella (Jara &Moreno 1984). Similarly, in central Chile thefissurellid limpets appear to have key roles oncommunity structure (Oliva & Castilla 1986).Strong effects of the key-hole limpet F. crassaon Mazzaella’ biomass was observed in mid-intertidal levels through field experiments(Aguilera 2010). Although other herbivores,formerly S. lessoni, can consume this alga (seeabove) they can not compensate for F. crassain controlling corticated Mazzaella either atper capita or at population level (Aguilera &Navarrete, unpublished data). Highconsumption of corticated late-successionalgae (e.g., Mazzaella) by fissurellid limpetscan entirely modify the intertidal landscape,especially when abundance of large key-holelimpets is high (as inside the marine preserveof Las Cruces, Oliva & Castilla 1986). Hence,these limpets might be considered keystoneherbivores in Chilean intertidal habitats. Poorinformation, however, is yet available aboutthe role these herbivores play on successionaltrajectories of the algal community eitherenhancing or decreasing species diversity.

Small, but locally abundant, molluscangrazers (i.e. chitons, scurrinid limpets) appearto have important roles in removing ephemeralalgae, maintaining bare rock, and indirectlyenhancing barnacles and calcareous algaeduring colonizing phases of the emergentcommunity (Moreno & Jaramillo 1983, Jara &Moreno 1984, Aguilera & Navarrete 2007,Aguilera 2010, see Fig. 1 for summary ofeffects of these herbivores on earlysuccession). Studies dealing with the grazingeffect of one of the most abundant grazerspecies in intertidal habitats in central Chile,the chiton Chiton granosus , (Otaíza &Santelices 1985, Otaíza 1986, Aguilera &Navarrete 2007) show this species can reduceephemeral algae abundance and have positiveeffect in the production of bare rock (see Fig.1). Through scraping the substratum, chitonscan affect recently colonizing spores, plantlets,and sessile invertebrates (see above)accounting for patchiness in ulvoids and barerock distribution (Otaíza 1986, Aguilera &Navarrete 2007, Aguilera 2010). Owing to high

densities of C. granosus in mid-to highintertidal levels (i.e. both juvenile and adult~600 individuals m-2 Otaíza & Santelices 1985),this chiton can have important population-leveleffects during the colonizing phase of the algalcommunity (see Fig. 1, Otaíza 1986, Aguilera& Navarrete 2007, Aguilera 2010). Othergrazers, the limpet S. araucana, also haveimportant roles similar to those observed forC. granosus (Aguilera & Navarrete,unpublished data). Due to the high similarityin foraging effects between these species, theycould be considered functionally redundant(i.e. equivalents, see Walker 1992) in the rolethey play during early community succession(Aguilera 2010). In this context, theredundancy model (Walker 1992, Naeem 1998,Rosenfeld 2002) suggests that the more similarin morphology, behaviour or diet two speciesare, they tend to be most similar andinterchangeable in their functional roles.Chitons and Scurria limpets may be similar inthe mode they handle algae, because bothspecies have tough buccal apparatuses (i.e.polyplacophoran and doccoglossanrespectively, see Steneck & Watling 1982)allowing deep scraping of the substratum. Thisforaging mode allows ingestion of microalgae,spores and recently settled invertebratesduring the colonizing phase of communitysuccession (see Fig. 1). Nevertheless, themorphology of buccal apparatuses impede C.granosus and S. araucana from removingpieces of adult algae, even green algae,resulting in a similar reduction in themagnitude of their effects during theestablishment phase of ephemeral algae atearly succession (see Fig. 1, Aguilera 2010).Interestingly, contrary to the classic view ofthe guild, some studies suggest C. granosusand some Scurria species may have short timepositive effects on Mazzaella abundance(Aguilera & Navarrete 2007, Aguilera &Navarrete, unpublished data, Aguilera et al.,unpublished data) which await furtherconfirmation (see Fig. 1, punctuated arrows).According to the similarity of niches amongthese species it is suggested that redundantspecies should have higher levels of inter-specific competition and thus local coexistencewould be restrictive (Leibold 1998). Thesespecies have a comparatively similar diet(Santelices et al. 1986), but some form of


habitat segregation at the micro-scale has beenobserved in the mid-intertidal (Aguilera &Navarrete 2011) which might explain localcoexistence.

In the same context, high levels ofredundancy are expected within taxonomicallysimilar species in the role they play in thecommunity (e.g., by niche conservatism, seeWebb et al. 2002). Contrary to this view,studies dealing with the grazing effect ofscurrinid limpets in Chile (see Espoz et al.2004 for a general phylogenetic structure of

the group) show both similar and dissimilareffects of different species of this assemblage.For example, in northern Chile Correa et al.(2000) show that joint (i.e. additive) grazing bythe species Scurria araucana and S. viridula isthe key factor controlling ephemeral algaeabundance and diversity. Similarity in diet(Santelices et al. 1986, Camus et al. 2008), andfeeding behaviour between these grazers (notexplored by Correa et al. 2000) might accountfor the additive effects reported. In turn, theother abundant scurrinid l impet Scurria

Fig. 1: Scheme of the relative participation of molluscan herbivores during early and late algae communitysuccession in the mid-intertidal zone. Early community succession is separate in a colonization phase andestablishment of the adult plants. Magnitude of per capita effects (recorded through field and laboratoryexperiments, see Aguilera 2010) of different molluscan herbivores are presented as solid arrow of differentsize. Potential effects (those awaiting further confirmation) are presented as punctuated arrows. Direction ofeffects is presented in front of each arrow (- negative; + positive). Key of algal groups are presented below.

Esquema de la participación relativa de moluscos herbívoros durante la sucesión algal temprana y tardía en la zonaintermareal media. La sucesión temprana es separada en una fase de colonización y establecimiento de plantas adultas.La magnitud de los efectos per cápita (registrados a través de experimentos de terreno y laboratorio, ver Aguilera, 2010)de los diferentes moluscos herbívoros son presentados como flechas de distinto tamaño. Efectos potenciales (en esperade confirmación) se presentan como flechas punteadas. La dirección de cada efecto es presentada en frente de cadaflecha (- negativo; + positivo). La clave de identificación de los grupos de algas es presentada en la parte inferior.

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ceciliana (see Espoz et al. 2004), can havelocally important effects on intertidal habitatsthrough grazing on the shells of the musselPerumytilus purpuratus (Santelices & Martinez1988). Field experiments conducted bySantelices and Martinez (1988) suggests that,although mussels can trap spores of algaewhile immersed, feeding of S. ceciliana onspores and plantlets during the period ofemersion prevents P. pupuratus beingovercrowded by green algae which candiminish food availability for this mussels.This effect may be constant through timebecause limpets tend to forage persistently onthe same mussel (author personalobservation). Despite the potentialphylogenetic inertia (see Webb et al. 2002) ineither diet or morphology among scurrinids(Espoz et al. 2004), limited redundancy ineffects would be expected in this limpet groupbecause they could have differential habitatuse likely related to different physiologicaland/or behavioural responses accounting for“functional niche” differentiation (Rosenfeld2002). Both direct and indirect effects,commonly related to differences in behaviourand habitat use at micro-scales (cm) observedin some grazers present in the molluscassemblage (Aguilera & Navarrete 2011), cancontribute to the differences in the rolesscurrinid limpets play in intertidal community.Further investigation is required to explorecontribution of behavioural traits and thespatial niche of herbivores on the magnitudeand also direction of their effects.

In contrast to most molluscs, sea urchinscommonly exert strong per capita andpopulation level effects on algal communities,and some studies conducted in Chilecorroborate information recorded in othersystems about the magnitude of impacts (seeVásquez & Buschmann 1997, Vásquez 2007 forreview). Contreras and Castil la (1987)experimentally tested the effects of twosympatric sea urchins, Tetrapygus niger andLoxechinus albus. Utilizing intertidal rock pools(60 to 70 cm long; 45 to 50 cm wide) asexperimental arenas, these authors found thetwo sea urchin species have differentialfeeding mechanisms accounting for differentialeffects on the algae community. The species T.niger consumes both benthic algae (e.g.,Gelidium) and drift kelp (e.g., L. nigrescens),

but when kelp drift availability is low (seeRodríguez 2003), juvenile and adult individualscan generate “halos” (i.e. bare rock patches) inthe bed of intertidal pools. In turn, onlyjuveniles of L. albus can produce small halossimilar to T. niger while adult individuals ( > 3cm diameter) consume mostly floating algae(i.e. Lessonia , Macrocystis) (Contreras &Castilla 1987). Previous studies (e.g., Dayton1985) suggest populations of the two seaurchins can shift the algae assemblage to an“alternate state” (sensu Sutherland 1974) inthe low intertidal and subtidal community. Onestate in the presence of these grazers isdominated by calcareous crusts (“barrens”);meanwhile in the absence of these grazerskelp forest develop. In contrast, Contreras andCastilla (1987) found T. niger is the onlyspecies capable of forming barren grounds.These authors suggest that differences ineffects may be related directly to the differentfeeding apparatuses of these urchins; theAristotle’s lantern in T. niger is twice as longas that in L. albus , and this last speciespossesses modified aboral podia (“suckers”)which help mostly in the capture and transportof food (algal drift) to the mouth. In general,both species commonly aggregate formingdense patches in low-tidal pools (mainlyjuveniles in the case of L. albus, see Vásquez2007) generating high small -scale (cm)impacts in benthic habitats. According todifferentiation in their feeding patterns, seaurchin species might have dissimilar evencomplementary ecological roles in lowintertidal and subtidal habitats.

Although it was previously suggested thatherbivorous fish play minor roles in temperateshores (Lubchenco & Gaines 1981), fieldexperiments conducted in Chile suggest theycan have enormous effects on bothcolonization and establishment of differentfunctional groups of algae (see Muñoz & Ojeda1997, Horn & Ojeda 1999, Ojeda & Muñoz1999). The blennid fish Scartichthys viridiscommonly ventures into mid-to low intertidalhabitats grazing selectively on ephemeralalgae and epilithic microalgae (Muñoz & Ojeda1997, Ojeda & Muñoz 1999). Therefore, thisfish can reduce biomass of ulvoids and otherephemerals, drastically affecting algalcomposition of early successional community(Ojeda & Muñoz 1999, Muñoz & Ojeda 1997).


The effect of S. viridis resembles the effectthat molluscan grazers have on algalcommunities (Moreno & Jaramillo 1983,Aguilera 2010). Contrary to most molluscangrazers, the browser/grazer Girella laevifronsand the browser Aplodactylus punctatus canquickly remove large pieces of algae by cuttingthe distal portion of adult plants (Stepien 1990,Cáceres et al. 1993, Horn & Ojeda 1999). Inthis context, experimental exclusion of fish,molluscs and both taxa conducted in the mid-intertidal of a wave exposed platform in centralChile (see Aguilera 2010), showed that theeffect of the fish assemblage (un-identifiedbrowser species) was concentrated in thedistal portion of blades of both ephemeral (i.e.ulvoids) and corticated (i.e. Mazzaella) algae(Aguilera & Navarrete, unpublished data). Arecent study suggests the effect of browsingfish on corticated Mazzaella could be commoneven in the mid-intertidal zone during theimmersion period of the rock platforms(Escobar & Navarrete, unpublished data).

In functional terms, the fish S. viridis mayhave similar, even redundant, roles to thoseobserved for most molluscan grazers (i.e.chitons, scurria l impets) during earlysuccession. Browsing fish may entirelycompensate (according to their potential highper capita consumption, see below) the effectsof fissurellid limpets on adult established algae(both corticated and ephemerals). Commonly,molluscan herbivores forage during the low-tide period (when rock is wet, Aguilera &Navarrete 2011) while fish venture onto flatplatforms when they are completely immersed.Thus, these herbivores could have morecomplementary than redundant roles on thealgae community due to temporal nichedifferentiation (Carothers & Jaksic 1984)which needs to be further explored.

In general, because body size is related toconsumption rate, handling times and foragingrange (Mittelbach 1981), this could greatlydetermine the magnitude of consumers’effects. The magnitude of per capita effects ofdifferent species has been positively related tobody size in different assemblages (e.g.,Woodet al. 2010). For example, data on the percapita effect of herbivores on green ephemeralalgae measured through field experiments inthe mid-intertidal in central Chile, during thecolonizing phase of early succession (0 to 3

months of field experiments, see Aguilera2010), show a linear relationship between percapita effect and body size (see Fig. 2, greycircles). The magnitude of effect of differentherbivores appears to be also related to bodysize at different t imes of communitysuccession (early v/s late succession see Fig.1, Aguilera 2010). Although little publisheddata are available, based on reported body sizeof some herbivore species per capita effectsmay be estimated/predicted (see Fig. 2). Thisestimation, however, must be considered withcaution because other traits (e.g., foragingbehaviour) of the different species may wellmodify this picture (see below). Thus the fishScartichthys viridis (body size = 75.67 ± 97.44 g,Muñoz & Ojeda 1999) and the chitonEnoplochiton niger (body size = 75.26 ± 2.58 g,Broitman et al. unpublished data), can bepredicted to have a large mean per capitaeffect on ulvoids compared with mostmolluscan grazers (see Fig. 2 black square anddiamond respectively). The medium sizespecies Scurria viridula is predicted to havemoderate effects compared with otherscurrinids (i.e. S. araucana) and chitons (seeFig. 2 black triangle). In this context, fieldexperiments by Ojeda & Muñoz (1999) reportlarger effects for S. viridis on ulvoidabundance than the present analysis suggests(see Fig. 2 black square). Therefore, analysesbased solely on body size may underestimatereal per capita effects of large herbivores andneed to be considered with caution.

Both theoretical and experimental studiessuggest body size is positively related toforaging range (e.g., displacement length atforaging) (see Mittelbach 1981, Wood et al.2010). Range of movement during foragingcould explain the importance of body size ofherbivores on the magnitude of their effects.In contrast to this, studies by Aguilera &Navarrete (2011) showed that S. lessoni, thesmallest herbivore considered (0.97 cm ± 0.07cm shell length), had intermediate foragingexcursions of 24.6 cm (± 3.7 cm) from restingareas (i.e. crevices) with low effects on ulvoids(see Fig. 1 and 2). In turn, S. araucana amedium sized species (2.6 cm ± 1.2 cm shelllength) had shorter excursions (6.5 cm ± 3.9cm) from its homing scars and an intermediatesize effect on ulvoids (Fig. 1 and 2). Therefore,other behavioural traits related to consumption

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rate and/or responses of herbivores topredator pressure (for molluscs responses, seeEspoz & Castilla 2000, Escobar & Navarrete2011) may also be of interest to understandchanges in the magnitude of effect of differentherbivores on algae biomass.

It is worth noting that humans can act asselective herbivores harvesting different algaespecies (i.e. clipping, trimming or detachingentire plant), thereby modifying both intertidaland subtidal algal community structure (seeBranch & Moreno 1994, Moreno 2001 forreview). As presented above, some herbivoresare able to consume competitively dominantalgae species (e.g., Mazzaella) enhancingintertidal community diversity. Since humansalso harvest keystone herbivores (e.g.,fissurellid limpets) they can reduce algaldiversity through increasing the abundance ofdominant algae species (Moreno et al. 1984,Oliva & Castilla 1986). When harvesting isconcentrated on the dominant alga, communitydiversity can be enhanced again because

abundance of non-exploited species rise(Branch & Moreno 1994). Therefore, humanimpacts in both herbivores and algaeabundance (acting as predator and herbivorerespectively) can provoke dramatic alterationsof herbivore-algae interaction strengths andthus food web structure (Moreno et al. 1984,Oliva & Castilla 1986, Branch & Moreno 1994).Future studies should take into account thedirection and magnitude of human effects onconsumer-resource interactions, because thiscould shed light on the contribution of specificinteractions (e.g., Fissurella-Mazzaella) toecosystem resilience.

Physical regulation of herbivores’ effects

There is evidence that the abundance andcomposition of both herbivores and algae arestrongly affected by bottom up processes suchas coastal upwelling (Broitman et al. 2001,Camus 2001, Nielsen & Navarrete 2004, Thiel etal. 2007). Commonly, onshore larval transport is

Fig. 2: Linear regression between magnitudes of per cápita effect, recorded through field experiments at thecolonizing phase of intertidal succession, and body size (g) of molluscan herbivores: Siphonaria lessoni,Scurria araucana, Chiton granosus, Fissurella crassa. Each circle represents a replicate plot. Expected meaneffect are presented for Scurria viridula (black crossed triangle), Enoplochiton niger (black crossed dia-mond) and for intertidal fish Scartichthys viridis (black crossed square) (individuals mean size from Sanhue-za et al. 2008, Ojeda & Muñoz 1999 and Broitman et al., unpublished data).

Regresión lineal entre la magnitud de los efectos per cápita, estimados a través de experimentos de terreno durante la fasede colonización de la sucesión intermareal, y el tamaño corporal (g) de los siguientes moluscos herbívoros: Siphonarialessoni, Scurria araucana, Chiton granosus, Fissurella crassa. Cada círculo corresponde a una réplica experimental. Sepresentan los efectos promedio esperados para Scurria viridula (triángulo negro-cruzado), Enoplochiton niger (diamantenegro-cruzado) y para el pez intermareal Scartichthys viridis (cuadrado negro-cruzado) (tamaño individual promedio toma-do de Sanhueza et al. 2008, Muñoz & Ojeda 1999 y Broitman et al., datos no publicados).

Body mass (g)


affected by different oceanographic conditionslike upwelling which can alter the abundance ofbenthic species with free living larvae (e.g.,Shanks et al. 2000). Additionally, nutrientloading can greatly account for variation inbiomass and growth rates of different functionalgroups of algae affecting herbivore-algaeinteractions (Nielsen & Navarrete 2004).Therefore, differences in the magnitude of perpopulation effects of herbivores at large spatialscales (e.g., sites separated by 10s ofkilometers) are expected according to differentoceanographic processes operating alongcoastal ecosystems (e.g., Bustamante et al.1995, Thiel et al. 2007). In this context, throughexcluding small-non fissurellids molluscangrazers in sites with different upwellingintensity in central Chile, Nielsen & Navarrete(2004) showed that abundance of molluscangrazers (chitons, scurrinid limpets and S.lessoni) and both composition and abundance ofdifferent functional groups of algae differs withlevels of seashore productivity. Both theabundance of green ephemeral algae (formerlyulvoids) and the biomass of molluscan grazerswere observed to be high in zones of lowupwelling intensity (i.e. Las Cruces and ElQuisco); meanwhile the cover of corticatedalgae (formerly Mazzaella) was low. In turn,abundance of corticated algae increases in sitesof high upwelling intensity (i.e. Matanzas andPichilemu). This information suggestsconsumptive effects of herbivores on algae maybe compensated by increases in tolerances ofalgae to consumption. For example, despite thehigh densities of grazers in low upwellinglocalities the magnitude of their effects (at thepopulation-level) on green ephemeral may bedampened by high growth rates of these algae.Furthermore, since the growth rate ofcorticated algae are enhanced by upwelling(Nielsen & Navarrete 2004, Wieters 2005),biomass and even composition of these algaecould be regulated by oceanographic conditionsrather than herbivores (see Wieters 2005).Thus, “herbivory intensity”, which is a functionof herbivore consumption relative to plantgrowth rates (Lubchenco & Gaines 1981), couldbe modified, but not completely altered by, localoceanographic conditions. Some generality,however, in the foraging pattern of molluscangrazers (i.e. patellid limpets), over broadgeographical scales, has been reported in other

coasts (i.e. European) (e.g., Jenkins et al. 2001).Therefore, it is necessary to explore potentialgeographic variability in consumption effect ofdifferent herbivores in order to disentangletheir role in different communities.

In the same context, as communitycomposition is also determined by speciesresponses to local environmental stress, theycan also determine differential trajectories ofcommunity succession. In a grazer exclusionexperiment which considered thermal stressamelioration (by seawater drainage),Buschmann (1990) showed that in thepresence of grazers but without water drainagegreen ephemeral algae can persist throughdifferent seasons. However, in presence ofboth grazers and seawater drainage calcareouscrusts of Ralfsia sp. dominate the substratum,thus outcompeting the ulvoids (Buschmann1990). Thus, despite different studies showingthat green algae are consumed by diverseherbivore species (see above), thermal stressmay well modify foraging rates or herbivoreeffectiveness at low spatial scales (see below)and/or algae growth rates. This can beespecially relevant to explain among replicatevariabil ity in the effect of herbivorescommonly observed in experimental studies.Therefore, Buschmann’s experiments suggestdesiccation can modify the model used toexplain algal successional patterns and thatsome physical factors are a causal componentat the community level and not only a factormodulating the biotic interactions.

Commonly, many experimental studiestease apart variation in “herbivoreeffectiveness” (number of plants or biomassremoved per unit time; Lubchenco & Gaines1981) by physical condition of the environment(i.e. temperature, desiccation, etc.).Behavioural performances of herbivores suchas time they spend foraging, or the amplitudeof foraging excursions can be constrained byphysical stress, predators or food supply (e.g.,Jenkins & Hartnoll 2001, Ng & Williams 2006,Escobar & Navarrete 2011). Indeed, speciesinhabiting the mid to high intertidal zones areexposed to high thermal stress, because tidalvariation exposes animals to substrate heating,freezing and/or desiccation (Williams &Morritt 1995, Finke et al. 2007). In the lowintertidal, however, animals are mostlyexposed to wave stress which can dislodge

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both active and resting individuals. Thisphysical gradient may generate a verticalgradient in the effectiveness of herbivores indetermining spatial distribution of algaeabundance and/or composition (seeUnderwood 1980). However, recent studiesdealing with molluscan grazing in the rockyintertidal showed that the effect of herbivorescan not follow a gradient, but instead has apatchy distribution (Díaz & McQuaid 2011). Inthis context, studies conducted in Chileancoasts have shown that a patchy distribution ofresources can resemble the spatial distributionof grazer’ abundance generated by behaviouralescape, or response, to thermally stressfulconditions (e.g., migration, Muñoz et al. 2005,shelter use, Aguilera & Navarrete 2011).

Empirical data shows that the rolesherbivores play in intertidal communitystructure appear to be related to their foragingmodes, behavioural responses to theenvironment and body size. Specifically,“grazers” can free space through feeding onspores and plantlets of macroalgae, thuscalcareous and non-calcareous crusts andbarnacles persist in areas of intense grazing.Therefore, determination of the levels ofredundancy or similarity in the effects of this“sub-set” of species (i.e. grazers) may be ofinterest. In turn, species with either “browser”or “browser/grazer” mode of feeding (i.e.Fissurella, fish), are also capable of consumingadult plants of both ephemeral and corticatedalgae. Taken together, field experimentalstudies suggest that these two “sub-sets” ofintertidal herbivores may have complementaryroles on algae control through differentiation intheir feeding modes as reported for otherinvertebrate species in terrestrial systems (e.g.,spiders, Schmitz 2009). At the population level,however, the effect observed for mostherbivores may be expected to vary inmagnitude modulated by changes in thephysical factors affecting algae growth rate, andboth abundance and composition of herbivores(Nielsen & Navarrete 2004, Wieters 2005).

POSITIVE EFFECTS OF HERBIVORES ON ALGAE

The potential for positive effects of terrestrialgrazers on plant fitness has been discussedextensively in the past (see McNaughton 1986,

Belsky 1987). The traditional view thatherbivores produce negative effects on plantswas challenged by the “Grazing OptimizationHypothesis” (Owen & Wiegert 1976,McNaughton 1986). In a general view, thishypothesis states that primary productivity, oreven plant f itness, is maximised at anintermediate level of herbivory. It couldhappen because plants can compensate oreven over-compensate the effects of herbivoreconsumption at an intermediate level (seeAgrawal 2000 for review). Through dispersingseeds of some palatable plants, herbivores canalso compensate for the damage they exert onit. In this context, spore dispersion and algaetissue survival following herbivoreconsumption has been widely reported inChilean intertidal systems (Santelices 1992).

Algae survival to grazing

Some studies conducted in Chile havereported that sexual and asexual reproductivetissue of some algae can pass alive through thegut of many intertidal invertebrate grazers andfish (apparently not reported in otherlatitudes!). The validity of the phenomenonwas first evaluated by Santelices & Correa(1985) in an assemblage of intertidalmolluscan grazers present in central Chile. Inthis study, on average 56 % of the 27 algalspecies found in the gut content of thesegrazers can survive digestion and are able togrow in cultures started from the faecal pellet.Opportunistic or ephemeral algae species(e.g., ulvoids) had a much greater ability topass alive along the digestive tract ofmolluscan grazers than corticated species(Santelices & Correa 1985, Santelices 1992).

Diverse mechanisms of algae ingested bygrazers have been observed in lab cultures, forexample tissue regeneration or protoplastrelease (see Santelices & Ugarte 1987). InChlorophyta, for example, the protoplasts candevelop flagella and settle in the bottom of theculture vessel originating new talli (seeSantelices 1992). Different algae species canhave different capacities to survive digestion,but the characteristics of the feeding apparatusand enzymatic compounds of grazers can be ofgreat relevance. For example, Santelices(1992) found that only a small proportion ofalgae survive the passage through the


digestive tract of Chiton granosus which havean apparently efficient radular apparatus (seeSteneck & Watling 1982 for molluscs’ radularcharacteristics). In contrast some species oflittorinid snails can stimulate the protoplastrelease more than chitons. Furthermore, thegastric compound characteristics of somespecies of grazers can be of great importanceto spore survival. For example only two of 16species of algae can survive digestion by thefish Sicyases sanguineus; this was attributed tothe efficient action of different enzymaticcompounds (Payá & Santelices 1989).

Other components should also beconsidered to explain algae survival afterdigestion, for example the state of hunger ofthe animals. Clearly if an animal has recentlyeaten many propagules of some item, otherrecently ingested items are more likely tosurvive digestion. But when the animal ishungry few fragment are able to survive. Bothenzymatic mechanisms and physiological stateof herbivores are thus directly involved in thisprocess (Bozinovic & Martinez del Río 1996).

Spore dispersal by herbivores

Dispersion of propagules of algae by grazerscan be considered a positive mutualistic animal-plant interaction in which the animal receivesan energy input from algae consumed, or fromsome parts of it, and the algae gain a potentiallyeffective dispersing mechanism. One exampleof this mechanism is presented in the amphipodHyale media (Buschmann & Santelices 1988).This species tears up the mature cystocarps ofthe red algae Mazzaella laminarioides, releasingthe spores and thus transporting them in theirlegs and body to other sites (see alsoBuschmann & Bravo 1990, Buschmann &Vergara 1993). This mechanism could be ofgreat importance for algal species that haverestrictive dispersal mechanisms (i.e. un-flagellated spores of Rodophytes) and that couldneed this kind of transport to compete withother algae with wide dispersal strategies (seeSantelices & Ugarte 1987, Buschmann & Bravo1990). Despite the documented cases of sporedispersing, no studies have been yet conductedto explore the importance of these mechanismsin plant-plant competitive interactions.

Field and laboratory studies conducted bySantelices & Bobadilla (1996), report an

increase in benthic spore abundance in thepresence of molluscan grazers. Pedal mucus ofthe species Tegula atra and littorinid snailscan differentially trap propagules of the algaeUlva rigida , Mazzaella laminarioides andLessonia nigrescens (Santelices & Bobadilla1996). Because most molluscs lay an inter-individual mucus trails when they move (seeDavies & Hawkins 1998), some herbivorescould facilitate formation of algal patches atmicro-scales (cm) according to their spatialdispersion and scale of movements at foraging.Further studies should consider thismechanism of spatial heterogeneity in algaedistribution in intertidal habitats.

Gardening

Through resting in a fixed site some intertidalgrazers can affect the micro-space (scale of cm)that surrounds these sites increasing theabundance of algae they commonly consume.The area affected by grazing, some centimetresaround the area where grazers rest, isconsidered a “garden” (Branch 1981, Branch etal. 1992) where the algae consumed by theseherbivores (e.g., green algae) persist at higherabundances at micro-scale (cm). Grazers caneliminate competing species of algae thatcolonize the gardens, defend aggressively theseterritories against other grazers precludingoverexploitation, and maintain low consumptionrates (Stimson 1970, Branch et al. 1992,Plaganyi & Branch 2000). Because “gardening”is correlated with systems of poor productivity(Branch et al. 1992), this behaviour drivesherbivores to a specialized diet which reflectsthe degree of adaptation of different species tochanges in the physical and chemicalenvironment where they live.

Although “gardening” is common in othersystems in molluscs, fish and some Polychaeta(Plaganyi & Branch 2000), in Chile only onestudy examines the possibility of gardeningbehaviour and associated territoriality (i.e. inthe grazer Scurria araucana ; Morales &Camus 2005 In: Resúmenes XI CongresoLatinoamericano de Ciencias del Mar,Valparaíso Chile, see also Rojas & Ojeda 2007).Well developed homing behaviour, togetherwith short foraging excursions observed insome species of the scurria genus (i.e. Scurriaplana, S. zebrina, S. viridula; author personal

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observations), could be indicative of thisbehaviour. However, no aggressive responsesassociated with territoriality, nor clear“gardens” have been yet reported in thesespecies.

Other positive effects and compensatorypotential

A potential positive animal-kelp interactionbetween the l impet Scurria scurria andLessonia nigrescens has been suggested in thepast (Santelices 1987). The species S. scurralive inside cavities bored in the proximal partsof the stipes of the kelp L. nigrescens(Santelices et al. 1980). When the stipe islarger and heavy, the grazing effect of S.scurra increases the probability that stipes canbe removed by water drag. Thus, this reducesthe risk for entire plant of L. nigrescens tobecome so heavy to be susceptible todetachment by water drag increasing theirlongevity compared with plants where S.scurra is absent (see Santelices et al. 1980).Therefore, S. scurra appears to have a positiveeffect on populations of L. nigrescens playing a

specific, albeit unique, role which couldrequire a thorough re-examination because norecent information is available dealing withthis specific grazer-kelp interaction.

In general, few studies have been conductedto evaluate the potential compensatory or over-compensatory growth responses of algaeagainst consumption by herbivores. However,compensatory potential has been reported insubtidal systems. For example, a recent studyreports that the subtidal kelp Macrocystispyrifera can compensate for the grazing of theamphipod Peramphithoe femorata (Cerda et al.2009). Through resource allocation to grazedblades, M. pyrifera are able to tolerateintermediate intensity of consumption followingthe main expectation of the “grazingoptimization hypothesis”. Thus, it is of interestto explore the frequency of compensation ofalgae to herbivore’s consumption in intertidalhabitats and also grazing intensity triggeringthis response. It is also of interest to determinewhether positive effects on algae fitness areeither sensitive or entirely independent ofherbivore identity as the optimizationhypothesis suggests.

TABLE 1

Main advances in knowledge about functional roles of herbivores, and future avenues for studiesdealing with their effects on intertidal community structure.

Principales avances en el conocimiento de los roles funcionales de los herbívoros, y direcciones futuras paraestudios centrados en sus efectos sobre la estructura de comunidades intermareales.

Advances since Santelices’ (1987) review

A. Establishment of clear differentiation in functionalroles within dif ferent assemblages (i .e. lowfunctional redundancy).

B. Characterization of herbivores’ contribution duringalgal succession (identity effect).

C. Importance of herbivores’ functional traits;behavioural patterns, body size and feeding modesin their effects on algal communities.

D. A clear potential for omnivory across different taxabroaden their functional roles in intertidalcommunity

E. Importance of physical factors (e.g., nutrientsupply, desiccation) modulating herbivoreeffectiveness and functional effects.

F. Relevance of chemical induction of algal defensesby small herbivores in consumer-resourceinteractions.

Future avenues, studies focused on:

A. Potential for functional compensation amongspecies within assemblages.

B. Factors affecting behavioural strategies (e.g., timespent foraging, home range) of herbivores, andconsequences in spatial distribution of resources.

C. Physiological and behavioural responses ofherbivores to local stress.

D. Feeding plasticity and animal food selection bygeneralist herbivores.

E. Geographic variation in herbivores roles andpotential shifts in their functional structure (e.g.,from redundancy to complementarity).

F. Algal compensation, or even overcompensation,(e.g., in growth, reproduction) after herbivores’attack.

G. Human impact as potential mediator of specificherbivore-algae interactions.


CONCLUDING REMARKS

In general, knowledge about the role ofherbivores in the intertidal community in Chileis still scarce considering the high diversity ofspecies present in the Chilean coasts(Fernández et al . 2000). Nevertheless,enormous advances have been made since thelast review of the topic by Santelices (1987)encouraging future avenues of research on thefunctional roles of herbivores in intertidalcommunities (summarized in Table 1).

A number of studies suggest quantitative aswell as qualitative differences in herbivoreeffects in different latitudes (e.g., temperateversus tropical). This may be related to thethermal tolerances, behavioural responses andchanges in both composition and abundance ofherbivores over geographical scales(Rivadeneira et al . 2002; Rivadeneira &Fernández 2005) (see future avenues Table 1Cand 1E). Since both the growth rate andsurvival of algae are influenced by theinteraction of temperature and herbivores(Rothausler et al. 2005), herbivore-algaeinteractions could vary in a predictive wayacross latitudes (see future avenues Table 1E).

Studies dealing with effects of herbivoreson algae life history, and both algal populationand community dynamics (i.e. succession) areof great interest to understand how changes ofassemblage composition translate intovariation in both food web structure andecosystem functioning. Through consumptionof different primary producers (macroalgaeand microalgae), and through generation ofbare space, herbivores can perform importantfunctional roles at the community level (seemain advances Table 1A and 1D). Likewise,because herbivores are also consumed byother species, including humans, bothindividual functional traits and population-levelinformation are also of great interest tounderstand their impacts on ecosystemprocesses (Schmitz 2008). Whether intertidalherbivores have redundant (= equivalents) orcomplementary roles (e.g., Walker 1992,Naeem 1998, Loreau 2004) on Chileanintertidal communities has been poorlyexplored. Future studies should also focus onthe potential for functional or numericalcompensation among different species andassemblages (Ruesink & Srivastava 2003) (see

future avenues Table 1A). Un-explored effectsof intertidal herbivores like polychaeta andcrustacea, among others, limit predictionsabout true compensation after potentialspecies extinction or regional contractions ofpopulations (see Jaksic 2003, Rivadeneira &Fernández 2005). According to f indingsregarding animal diet and differential impactsthat herbivores exert on intertidalcommunities in Chile (see main advancesTable 1A, 1D), they might not be properlyconsidered as part of a single “functionalgroup” or “functional guild” (Simberloff &Dayan 1991, Díaz & Cabido 2001). Thus, howherbivores are functionally related throughtheir effects on community structure and therole they play on ecosystem functioning couldbe a task for the future of herbivore-algaeinteraction studies in Chilean intertidalcommunities.

ACKOWLEDGEMENTS: I greatly appreciate thecomments and helpful criticism of Bernabé Santelices(CASEB-PUC), Martin Thiel and Bernardo Broitman(CEAZA-UCN) to an early draft of the manuscript.Preliminary ideas of this review were conceived duringmy PhD training; advice from Sergio Navarrete (ECIM-PUC) during this time is greatly appreciated, and alsosupport from the Andrew Mellon Foundation andCONICYT scholarship. I thank all ‘Chango-LAB’ and‘ECIMinianos’ for camaraderie and friendship.Financial support for finishing this manuscript wasprovided by Bernardo Broitman (CEAZA-UCN)through Fondecyt grant # 1090488. Dr. Stuart Jenkins(Bangor-UK) and two anonymous referees greatlyimproved a final version of this manuscript.

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Associate Editor: Álvaro PalmaReceived March 4, 2011; accepted May 12, 2011

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The functional roles of herbivores in the rocky intertidal