Herbivore-Kelp Interactions in Chilean Subtidal Communities: a Review

Home , Austrocidaris, Lessonia trabeculata, Loxechinus albus, Meyenaster, Puerto Toro, Tegula tridentata

Revista Chilena de Historia Natural 70: 4!-52, I 997 REVIEW Herbivore-kelp interactions in Chilean subtidal communities: a review

Interacciones alga-herbfvoro en comunidades submareales chilenas: una revision

JULIO A. V ASQUEZ1 and ALEJANDRO H. BUSCHMANN2

1 Departamento de Biologia Marina. Facultad de Ciencias del Mar, Universidad Cat61ica del Norte, Cas illa I I 7, Coquimbo-Chile. E-mail: [email protected] 2 Departamento de Acuicultura, Laboratorio de Cultivos Marinos, Universidad de Los Lagos, Casilla 933. Osorno-Chile

ABSTRACT

This paper reviews the literature evidence on the herbivore-kelp interactions along the Chilean coast, basically the role of sea urchins and gastropods in the structure of rocky shallow subtidal marine communities. Due to the morphology of the Chilean coast, we divided our analysis in two large zones. In northern Chile, between 18°- 42° S, the Cordillera de la Costa runs close to the coast generating extremely exposed habitats. In this zone two species of Lessonia are dominant in intertidal and subtidal habitats. Here, the sea urchin Tetrapygus niger is the most abundant grazer producing extensive intertidal and subtidal barren grounds. South of 42" S to Cape Horn, Macrocystis pyrifera forms the most conspicuous kelp association in a fjord zone, where hundreds of islands produce protected habitats. Four species of sea urchins and the gastropod Tegula atra graze on M. pyrifera. However, their effects are spatially and temporaly restricted. The foraging behavior of the principal herbivore. the sea urchin Loxechinus a/bus, is influenced by the degree of wave action, restricting its effect to exposed areas. In very protected areas Tegula atra affects the population dynamics of M. pyrifera.

Key words: Chile, benthic herbivores, kelp. subtidal habitats.

RESUMEN

Este trabajo revisa la literatura de las interacciones alga-herbivoro, especialmente el efecto de erizos y caracoles gastr6podos en la estructura de comunidades submarales someras en !as costas de Chile. Por la morfologia de la costa de Chile. nuestro analisis estádividido en dos grandes zonas. En el norte. entre Ios 18° y Ios 42" S, la Cordillera de la Costa Chile se distribuye muy cerea de la costa, generando habitats extremadamente expuestos. En esta zona dos especies de Lessonia son dominantes en habitats intermareales y submareales someros. Aqui. el erizo negro Tetrapygus niger es el pastoreador más abundante, generando extensos "fondos blanqueados". AI sur de Ios 42" S y hasta el Cabo de Hornos, cientos de islas forman fiordos protegidos del movimiento de agua donde Macrocystis pyrifera es el alga dominante. Cuatro especies de erizos y Tegula spp. son Ios pastoreadores más conspicuos asociados a estas comunidades. Sin embargo, el efecto de su pastoreo está delirnitado espacial y ternporalrnente. La conducta de pastoreo del herbfvoro más abundante, Loxechinus albus, esta restringida a áreas cxpuestas al oleaje. En áreas rnuy protegidas, Tegula atra afecta significativamente la dinarnica poblacional de M. Pyrifera.

Palabras clave: Chile, habitats subrnareales, herbivoros benticos, huirales.

INTRODUCTION dominate in cover and biomass to a depth of 25-30 m in the northern and southern Shallow subtidal rocky-bottom areas in hemispheres (Dawson et al. 1960, Druehl warm and cold temperate seas are domina- 1970, 1978, Kain 1962, 1977, 1979, North ted by large brown algal associations (Da- 1971, Barra1es & Lobban 1975, Velimerov yton 1985). The orders Laminariales and et al. 1977, Choat & Schiel 1982, Villouta Fucales, form extensive kelp forests and & Santelices 1984, Santelices & Ojeda

(Received 23 June I 995: accepted 29 October I 996: managed by F. Patricio Ojeda) 42 VASQUEZ & BUSCHMANN

1984a, I 984b, Schiel & Foster 1986, Ha- The situation described above would be rrold & Pearse 1987, Vasquez 1989, 1991, rather different north to 42°S where Macro- 1992, Camus & Ojeda 1992). These kelp cystis pyrifera (L.) C.Ag. is not the domi- forests provide the habitat for many inver- nant kelp species. Instead areas are domi- tebrates and fishes, and constitute one of nated by Lessonia trabeculata Villouta et the major factors in their distribution and Santelices. In subtidal shallow rocky areas abundance (J ones 197 I, 1972, I 97 3, North of central and northern Chile, Tetrapygus I 971, Duggins 1980, 1981, Santelices & niger (Molina) is the most abundant sea ur- Ojeda 1984 a, b, Vasquez & Castilla I 984, chin (Viviani 1975, Vasquez personal ob- Harrold & Pearse 1987, Vasquez 1993a, servation). The high population density of 1993b). Large brown algae also provide this species impedes the settlement of ma- areas for spawning and larval settlement croalgae propagules and maintains extensi- where exposure to water movement and ve barren areas. As discussed by Vasquez predation is reduced (Ghelardi 1960, Moo- (1989), the ecological impact of T. niger in re 1971, 1972, 1973, Cancino & Santelices areas dominated by subsurface kelp forests 1984, V asquez & Santelices I 984, Ojeda & of L. trabeculata would not appear to be Santelices 1984, Snider I 985). all-or-none (sensu Harrold & Pearse 1987) Kelps appear unique among the world's as reported for some northern hemisphere macrophyte communities because almost kelp communities. T. niger modifies algal the entire plant can be heavily grazed by morphology and produces two morphotypes one type of herbivore: the sea urchin (Da- that are affected differently by bottom sur- yton 1985). Not all species of sea urchin ges. These morphological modifications have this potential but in most temperate have important consequences for the persis- areas at least one species does (Lawrence tence of L. trabeculata populations (V as- 1975). In the northern hemisphere sea ur- quez 1992). chins are among the major grazers structu- This paper reviews the literature on the ring kelp communities in shallow waters ecological role of herbivores associated (see reviews by Lawrence I 975, Schiel & with kelp stands along the Chilean coast. Foster I 986, Harrold & Pearse I 987). On We discuss and compare the evidence from the contrary, the results of several studies northern and southern Chilean kelp com- in southern South America suggests sea ur- munities on the following topics: herbivore chin herbivory is not an important structu- diversity and distribution, predator-herbi- ring factor of these communities. Barrales vore interactions, and relevant biological & Lobban (1975) documented the absence and physical factors in the structure of the- of large and abundant grazing echinoid po- se South American kelp communities. We pulation along the coast of Chubut in Ar- contrast these results with the evidence that gentina. Three species of echinoids occur has emerged from the northern hemisphere in this area, but individuals are too small kelp communities. and not in sufficient number to graze inten- sively (Barrales & Lobban 1975). Likewise, Dayton ( 1985) found kelp forests DIVERSITY AND DISTRIBUTION OF THE where sea urchins do not graze actively. SEA URCHIN AND OTHER HERBIVORES V asquez et al. (1984) found a similar situa- ALONG CHILEAN COAST tion in the kelp forests of Isla Navarino, southern Chile, where algal species are Seven genera with fifteen species of sea apparently regulated by interspecific com- urchin inhabit the Chilean coast (Mortensen petition and substratum availability (Sante- 1952, Larrain 1975). Five of these species lices & Ojeda 1984b). This was confirmed are associated with kelp communities. Te- experimentally by Castilla & Moreno (I 982), trapygus niger (Molina) and Loxechinus al- who artificially increased the densities of four bus (Molina), two sympatric species, are species of echinoids in enclosures in the same associated with Lessonia spp and Macro- kelp forest, and found no effect of the herbi- cystis integrifolia Bory kelp forests in sub- vores on the algal abundance. tidal and intertidal areas between 18° and HERBIVORE-KELP INTERACTIONS IN SUBTIDAL HABITATS 43

42° S (Viviani 1979, Brattstrom & Johan- In the latitudes mentioned above, Tetra- sen 1983, Contreras & Castilla 1987, V as- pygus niger is the most abundant sea urchin quez 1989). L. a/bus is the most conspicuo- associated with L. trabeculata kelp forests us sea urchin in the fjord zone (south to 42° (Vasquez personal observation). Dense po- S), where Macrocystis is the dominant kelp pulations of this sea urchin species impede species (Dayton 1985). Nearby, in the coas- the settlement of macroalgal propagules tal kelp forest at Isla Navarino in the Bea- and maintain extensive barren grounds gle Channel, Loxechinus albus, Arbacia (Vasquez 1993 b). dufresnei (Blainville), Pseudechinus mage- In these communities the abundance, dis- llanicus (Philippi), and Austrocidaris cana- tribution patterns and diets of the most cons- liculata (Agassiz) coexist in areas domina- picuous organisms associated with L. trabe- ted by M. pyrifera (V asquez et al. 1984, culata were studied by Vasquez (1989, Castilla 1985). However, in some southern 1990, 1992, 1993b ). The organisms included Chilean areas, the gastropod Tegula atra were selected because of their direct (ben- (Lesson) seems to be the most important thic herbivores) or indirect (benthic preda- grazer in M. pyrifera beds (Moreno & Su- tors and carnivorous fishes) relationships therland 1982, Buschmann 1992, Busch- with the stability (sensu Dayton et al. 1984) mann 1995). of the L. trabeculata kelp forest in northern Chile (V asquez 1993a, 1993b ). The sea urchin T. niger and the gastropod snail Tegula KELP COMMUNITIES IN NORTHERN tridentata Potiez et Michaud were the ben- AND CENTRAL CHILE thic herbivores considered. The herbivorous fish Aplodactylus punctatus Valenciennes In comparison to the data accummulated in has also been abundantly found in central the northern hemisphere, the southwestern and northen Chile (Caceres et al. 1993, Pacific and particularly the subtidal com- 1994). The sea star Meyenaster gelatinosus munities of central and northern Chile (Me yen) and three carnivorous fishes ( Chei- have received little attention. Some studies lodactylus variegatus Molina, Mugiloides in the south part of Chile (Alveal et al. chilensis Cuvier et Valenciennes, and Semi- 1973, Dayton et al. 1973, Dayton 1974, cossiphus maculatus (Peres) were evaluated Dayton et al. 1977, Dayton 1985, Moreno as the most abundant predators. & Sutherland 1982, Ojeda & Santelices The benthic herbivores, Tetrapygus ni- 1984a, Villouta & Santel ices 1984, 1986, ger and Tegula tridentata, are most the V asquez et al. 1984, V asquez & Cast ilia abundant and frequently found in L. trabe- 1984, Moreno & Jara 1984, Contreras & culata kelp beds at Playa El Prances, nor- Castilla 1987) generally provide accurate thern Chile. T. niger is discontinuously dis- descriptions of the structure of subtidal tributed throughout the kelp bed forming communities dominated by M. pyrifera. patches on stable rocky bottom. The distri- Exceptional are the experimental manipu- butional patterns of this sea urchin are co- lations of sea urchin densities in southern rrelated with the abundance and distribu- Chile (Castilla & Moreno 1982) and the tion fluctuations of Meyenaster gelatinosus exclusion of the canopy of dominant algae (Vasquez 1993b). Large T. niger comprise in Valdivia (Moreno & Sutherland 1982), c.a. 40% of the diet of this sea star. The and in the Beagle Channel (Santelices & average size of T. niger indicates that the Ojeda 1984 a). population at Playa El Prances is mainly In northern and central Chile (18°- 42°S) formed by large individuals. During the Lessonia trabeculata forms extensive subti- study period, sea urchin recruitment was dal kelp beds on rocky bottoms in areas ex- not recorded and it has been shown that re- posed and semiexposed to heavy surge. As gular recruitment may be necessary to this is the type of subtidal habitat most maintain the population densities in the commonly found along this portion of the presence of predators (Kenner 1992). The Chilean coast, this is the most important analysis of gut contents of T. niger shows kelp in this area. that crustose calcareous algae were the 44 VASQUEZ & BUSCHMANN most frequent and abundant food item in to trophic necessities in both hemispheres, the diet (V asquez 1993 b). the evidence suggests that the principal Tetrapygus niger forms high density causes of T. niger grouping in subtidal kelp groups in areas with strong water move- beds of L. trabeculata are the bottom coas- ment (sea bed and coastal currents). The tal currents (Vasquez 1989, 1993b). causes that provoke the formation of sea On the other hand, the causes of the sea urchin fronts have seldom been studied in urchin aggregations in northern Chilean subtidal macroalgae communities (Schiel & waters differ from those in shallow coastal Foster 1986). It has been asserted that the areas in the northern hemisphere. In these front formed mainly by strongylocentrotid environments, strong water movement pro- individuals is the principal factor genera- duces high sea urchin mortalities (Lissner ting the destruction of kelp beds (see re- 1980, 1983). Russo (1977), Cowen et al. view by Harrold & Pearse 1987). Bernstein (1982) and Ebert (1982), have demonstra- et al. (1983) stated that the sea urchin ted that the exposure to intense water mo- fronts are defense mechanisms against pre- vement diminishes the abundance and mo- dators. Nevertheless, Vadas et al. (1986) difies the sea urchin trophic behavior. demonstrated that the results obtained by Furthermore, the wave motion and coastal Bernstein et al. (1983) were the results of currents can limit feeding (Himmelman & their experimental design and that the sea Steel 1971, Mann & Breen 1972, Mann urchin grouping was produced by food con- 1973, Lissner 1980, Choat & Schiel 1982) centration. Harrold & Reed ( 1985) propo- and greatly affect the annual rate of survi- sed that drifting algae constitute an impor- val and the body size of many sea urchin tant food resource and their abundance and species (Ebert 1982). In subtidal kelp beds predictability release the benthic macroal- of L. trabeculata where a high density ofT. gae from grazing pressure. Apparently the niger occurs, the vegetation coverage is strongylocentrotids of the northern hemis- greatly reduced, generating patches domi- phere have morphological adaptations that nated exclusively by crustose calcareous al- allow them to capture and incorporate this gae (Vasquez 1989, 1991). resource in their diet. However, in the Even though the intensity of water mo- southern hemisphere T. niger, the most vement promotes the aggregation of Tetra- abundant sea urchin in rocky subtidal com- pygus niger, in contrast to that documented munities in northern and central Chile, is for other types of sea urchins in the nor- unable to use drift algae as an important thern hemisphere, the acummulative effect food item. V asquez ( 1986) I and Contreras of the phenomenon appears to have similar & Castilla ( 1987) demonstrated that the ecological consequences. Therefore, the re- feet are not efficient in capturing drift al- duction of benthic grazers (due to migra- gae. In this context, this morphological tion or mortality) in subtidal areas, or a de- constrain of the urchins can be compensa- crease in sea urchin grazing abilities due to ted, partly by aggregation. The formation water movement, have significant effects of high density groups of T. niger in zones on hard bottom benthic communities. Thus, with strong bottom currents should increase the effect of water movement (waves and the probability of retaining drifting algal currents) can generate temporal and spatial material among the sea urchin spines. The- grazing refuges analogous to those propo- refore the data presented by V asquez sed by Lubchenco and Gaines (1981) allo- (1989, 1993b) support the results obtained wing the settlement and growth of macroal- by Vadas et al. (1986), relative to the cause gal propagules. of the formation of sea urchin groups. Tegula tridentata was found by Vasquez However, even though groups of sea ur- (1993b) throughout the kelp bed of L. tra- chins appear to respond in a certain degree beculata, associated with stable rocky sea- beds and small rocks on sandy bottom, and the analysis of its size suggests recruitment Vasquez JA ( 1986) Morfologfa de estructuras alimenta- during the entire year in the northern rias como factores en la organizaci6n de comunidades submareales. Biota (Chile) I: I 04. Chilean coast. T. tridentata gut content HERBIVORE-KELP INTERACTIONS IN SUBTIDAL HABITATS 45 analysis shows that this gastropod snail is them to small prey. This is evident for M. an omnivorous organism including many chilensis and C. variegatus, where the prey items in its diet, including algae and maximum sizes of T. niger in their gut con- benthic invertebrates. tents do not exceed a test diameter of 20 The effect of predators upon populations mm. Considering the abundance of carnivo- of herbivores associated with subtidal kelp rous fish the selective predation of these communities of macroalgae (see reviews by organisms on small size prey could explain Schiel & Foster 1986, Harrold & Pearse the absence of small of T. niger in the area 1987) is profusely documented. Sea otters studied (Vasquez 1989, 1993b). (Enhidra lutris), fishes (Semicossiphus pul- Although the analysis of carnivores gut cher, Centrostephanus coronatus), sea star content does not allow inference regarding (Pycnopodia heliantoides, Patiria miniata) the regulation of their prey population, the and lobsters (Homarus americanus, Panuli- results suggest that the herbivore abundan- rus interruptus) have received special atten- ce notably associated with L. trabeculata is tion as natural controls of population densi- affected by the predation of a carnivorous ties and diets of strongylocentrotids in the guild (sensu Root 1967). This hypothesis northern hemisphere. In northern California, differs from that proposed for the subtidal E. lutris is one of the most important preda- kelp beds of the northern hemisphere, whe- tors in the control of the sea urchin densities re just one key predator (sensu Paine 1966, (Estes & Palmisano 1974, Estes 1980, Estes however see Power et al. 1996 for a new et al. 1978, 1981, 1982). In southern Cali- definition) regulates the population density fornia, predation of S. pulcher and C. coro- of its prey items (Lowry and Pearse 1973, natus is also an important factor in the regu- M ann 1977, Estes et al. 1978, 1982, Dug- lation of sea urchin populations gins 1980, Tegner & Dayton 1981, Berns- (Himmelman & Steel1971, Nelson & Vance tein et al. 1982, Tegner & Levin 1983). Ne- 1979, Tegner & Dayton 1981, Cowen 1983). vertheless, the evidence presented by The asteroids P. miniata and P. heliantoides Foster and Schiel (1988) strongly indicates are important in the regulation of echinoids that the concept of the sea otter as a keysto- (Mauzey et al. 1968, Paine & V ad as 1969, ne species is applicable only to a relatively Dayton et al. 1984). In California, P. inte- small number of sites and thus does not rruptus predation produces the greatest constitute a general explanation of kelp effect on the abundance, distribution, size community structure in California. frequency and feeding behavior of various A number of factors have been reported species of Strongylocentrotus (Tegner & to determine the abundance, distribution, Dayton 1981, Tegner & Levin 1983). Howe- physiology and reproduction of benthic ma- ver the abundance of urchins cannot only be rine algae (Schwencke 1971, Santelices affected by predators, as but also by factors 1977, Norton et al. 1982). Among physical affecting recruitment such as larval abun- factors, water motion is of particular im- dance and early post-settlement survival portance in the morphological expression (Watanabe & Harrolld 1991). and distribution of benthic macroalgae The star fish M eyenaster gelatinosus, (Connell 1972, Koehl 1977, 1982, 1984, and the carnivorous fish Mugiloides chilen- Jackson 1977, Menge 1978, Lubchenco & sis, Cheilodactylus variegatus and Semicos- Menge 1978, Druehl 1978, Sousa 1979, syphus maculatus, are the most important 1984, Gerard & Mann 1979, Paine & Levin predators in the community dominated by 1981, Denny et al. 1985). On the other L. trabeculata. All these carnivores include hand, herbivory is the main biological fac- Tetrapygus niger and Tegula tridentata in tor affecting their abundance and distribu- their diets. In this way, these species would tion (see reviews by Lawrence 1975, Lub- have an additional effect on the regulation chenco & Gaines 1981, Gaines & of the main herbivores associated with L. Lubchenco 1982, Schiel & Foster 1986, Jo- trabeculata. M. gelatinosus preys on large hnson & Mann 1988). T. niger, whereas the dimensions of the Despite possible interrelations between oral structures of carnivorous fishes restrict physical and biological factors, the general 46 YASQUEZ & BUSCHMANN trends of the experimental ecological stu- Another seasonal but very important dies, with the exception of those by Veli- factor in the structure of bottom kelp fo- merov and Griffiths (1979), Santelices & rests in northern Chile is the use of L. tra- Ojeda ( 1984 a, 1984b) and Dayton et al. beculata as the substratum for the settle- ( 1984 ), have been to consider them as two ment of elasmobranch fish egg capsules independent forces. In this context, herbi- (Vasquez 1989). This event produces high vory, water motion and spacing between rates of mortality in large plants during plants, have been analyzed as independent summer months. Notwithstanding, this re- structural factors that influence intertidal productive behavior facilitates the settle- macroalgal populations. ment of propagules and the growth of L. Experimental studies conducted in nor- trabeculata through the reduction of intras- thern Chile (Vasquez 1989, 1991, 1993a, pecific interaction with parental plants. 1993b, V asquez & Santelices 1990) reveal that benthic herbivores, sea urchins and gastropod snails modify algal morphology, KELP COMMUNITIES IN SOUTHERN CHILE producing two morphs: plants that grow in the absence of herbivores, with numerous The most conspicuous kelp associations are flexible stipes ("bushy form"), and plants formed by the giant kelp Macrocystis pyri- in the presence of grazers, with one or few fera, whose geographical distribution in the stipes of little flexibility ("arborescent Pacific Ocean includes the west coast of form") in the presence of grazers. Water North America and southern Chile (Neus- motion (bottom surges) generates selective hul 1972). In contrast to the situation in the mortality which affects significatively the north Pacific, few ecological studies have arborescent form. been done in giant kelp forests from On land, plants growing at high densities southern South America. These works has of plants have low rates of growth, repro- been focused on: I) the influence of the sea duction and survivorship compared to plants urchins on the distribution and abundance growing in similar environments but with of M. pyrifera (Dayton 1974, 1975, 1985, low population densities (Harper 1977). In Casti lla & Moreno I 982, V asquez et al. this context, evidence related to marine ma- I 984, Castilla I 985); 2) population dyna- croalgae differs. Schiel & Choat (1980) indi- mics and community structure of M. pyrife- cated that Ecklonia radiata and Sargassum ra (Moreno & Sutherland I 982, Moreno & sinclairii reach a larger size when part of a J ara 1984, Santelices & Ojeda 1984 a b, dense population in semi-exposed environ- Ojeda & Santelices 1984, Dayton 1985) ments. These authors suggested that plant and 3) regulation patterns of sea urchin po- gregariousness decreases the mortality pro- pulations (Dayton et al. 1977, Vasquez & duced by water movement. Black (1977) Castilla 1984, Vasquez et al. 1984, Dayton found that mortality and growth rates of ju- 1985, Castilla I 985). venile Egregia laevigata Setch. are density- In the kelp forests of Isla Navarino, San- dependent, at least during the first three telices & Ojeda (1984 a) tested the effects months of age. Santelices & Ojeda ( 1984b) of three sets of ecological factors on the suggested that distance between adult plants distribution and organization of the M. of Lessonia nigrescens Bory is a critical fac- pyrifera populations: I) the possibility of tor influencing the recruitment of juveniles competitive exclusion of Macrocystis by at intertidal habitats of central Chile. In sub- Lessonia vadosa Searles by removing spe- tidal bottom kelp forests of Lessonia trabe- cimens of L. vadosa at the upper side of the culata in northern Chile, the distance bet- giant kelp forest; 2) the possibility of survi- ween plants (high densities) is a mechanism val of transplanted plants, growth in deeper that favors the persistence of Lessonia, pri- water and adequacy of the substratum; 3) marily reducing herbivory (increasing the the possibility of interspecific interference whiplash effect of the fronds) and secondari- on density and distributional patterns remo- ly reducing the dredging effect of the bottom ving the floating canopy of large Macro- surges (Vasquez 1989, 1992). cystis plants. HERBIVORE-KELP INTERACTIONS IN SUBTIDAL HABITATS 47

Their results indicate that the importan- more frequently under boulders. Loxechin- ce of the factors determining the population us was commonly found on boulders, less structure and distribution patterns of Ma- frequently found in rock crevices or under crocystis differ according to the section of boulders, and never found inside the hol- the bed. They pointed out that the nearsho- dfast of Macrocystis pyrifera. re edge of the belt appears to be set by in- Gut content analysis indicated that terspecific competition with L. vadosa. Ex- Loxechinus had the most diversified diet of perimental results indicated than even benthic algae, Macrocystis being the most though M. pyrifera could recruit under the frequent item. Pseudechinus consumed L. vadosa canopy, densities and growth ra- mainly Macrocystis, whereas Austrocidaris tes are lower than in absence of L. vadosa. and Arbacia contained others frondose ben- If L. vadosa is removed, the Macrocystis thic algae and sessile invertebrates. Arba- belt extended 1 to 2 m further into shallo- cia was particularly notable with over 50% wer water. However, these experimental of the gut content consisting of serpulids data provide no information on which to and barnacles. base an evaluation of the factors restricting If the gut contents obtained for the four L. vadosa to shallower waters. sea urchin species are grouped according to The deepest edge of the M. pyrifera bed their nature, it is possible to distinguish in the Puerto Toro area appears primarily four groups of food: (a) Macrocystis pyrife- set by substratum availability (Santelices & ra fronds, wich are the commonest food; Ojeda 1984). However, during winter, de- (b) other frondose algae (mainly Gigartina creased light intensities and temperatures skottsbergii Setchell et Gardner, Halopteris perhaps limit apical elongation. Field ob- hordacea, Lessonia spp., Epymenia falklan- servation indicated that interspecific com- dica Taylor); (c) calcareous algae (crustose petition between M. pyrifera and Lessonia coralline); and (d) invertebrates (barnacles, flavicans Bory, result from conditions of serpulids, sponges). These four categories, unlimited substratum availability. In the together with the four microhabitats consi- few areas with solid substrata extending dered illustrated the patterns of resource into deeper waters, it would appear that axes utilization. Loxechinus and Arbacia monospecific stands of L. flavicans often overlap greatly in their microhabitat distri- limit the seaward border of M. pyrifera bution. Pseudechinus and Austrocidaris (Santelices & Ojeda 1984). shared a diversity of rather cryptic micro- Four species of sea urchins (Loxechinus habitat such as crevices, under boulders albus, Arbacia dufresnei, Pseudechinus and holdfasts of M. pyrifera. Nevertheless, magellanicus, Austrocidaris canaliculata) even though they had a considerable degree occur in the coastal kelp forest of Macro- of overlap. Austrocidaris was more fre- cystis at Puerto Toro in the Beagle Chan- quently found in crevices and under boul- nel. The distribution patterns and diets of ders while Pseudechinus occurred mostly the four species suggest a clear separation in Macrocystis holdfasts. of the microhabitats used and the diet (Vas- All four species include M. pyrifera quez et al. 1984 ). The localization of the fronds in their diets, with a high degree of sea urchin species was noted in relation to overlap among several pairs of species. Ne- four types of microhabitat: on boulders, in vertheless, Loxechinus, Arbacia and Aus- holdfasts of Macrocystis and under boul- trocidaris consumed other species of algae ders and crevices. The number of observa- (frondose and calcareous) and Arbacia con- tions and the probability of occurrence of sumed mainly invertebrates. Furthermore, each sea urchin species in each of the four according to a related experimental study microhabitat categories showed that Pseu- (Castilla & Moreno 1982) performed in this dechinus and Austrocidaris were found in Macrocystis bed, the fronds of M. pyrifera, the four microhabitat categories but with the principal food item in three of the sea different probabilities. Pseudechinus occu- urchin species, are not a limiting resource. rred more frequently inside the holdfast of Indeed, Castilla & More no ( 1982) determi- M. pyrifera, while Austrocidaris was found ned that L. a/bus, one of the most conspi- 48 VASQUEZ & BUSCHMANN cuous sea urchin in the belt, consumed mann 1992). A new sporophytic cohort of mainly pieces of drifting fronds and had no M. pyrifera recruit during June-July (Bus- significant effect on the recruitment or sur- chmann 1992). In this area the gastropod vival of juvenile Macrocystis. In addition, Tegula atra appears to be the most abun- Santelices & Ojeda (1984a) found that the dant grazer and would seem to explain the recruitment pattern of M. pyrifera is deter- decrease in Macrocystis abundance during mined mainly by the presence of adult ca- the summer (Buschmann 1995). Neverthe- nopy rather than by grazers. less, although this M. pyrifera abundance Based on a broad geographical survey pattern appears to be related to grazing by between 44° and 52°S along southern Chile T. atra, the interactions with environmental and the Argentinian coast, Dayton ( 1985) variables such as nutrient availability and pointed out that the distribution and abun- temperature, that appear to be important in dance of Macrocystis is determined by the northern hemisphere (Tegner & Dayton availability of suitable rocky substratum, 1987), needs to be studied before further the interspecific competition with Lessonia conclusions can be made. vadosa (shallow waters) and with L. flavi- The Loxechinus foraging behavior is in- cans (deeper waters), entanglement with fluenced mainly by the degree of wave sur- drift algae and the heavy settlement of hi- ge and by hunger (Dayton 1985), as in valves on the kelp fronds, degree of expo- Strongylocentrotus spp. ( Harrold & Reed sure to waves, the grazing of the echinoid 1985). As Dayton (1985) indicated, Loxe- L. albus and indirectly, the effects of hu- chinus often restricts its local distribution man fishing of Loxechinus. He documented to areas exposed to severe wave action. The that in many areas between 44° - 52° S, importance of hunger is a well known fac- Macrocystis is overgrazed by L. albus. In tor influencing the behavior of sea urchins other areas L. albus exist in lower densities and, in some cases, the formation of the sea or is absent altogether and does not affect urchin grazing fronts, irrespective of densi- the Macrocystis population, as suggested ty (Lawrence 1975, Harrold & Reed 1985, by Castilla & Moreno (1982), Castilla Harrold & Pearse 1987). With regard to (1985), Santelices & Ojeda (1984 a) and hunger, drift algae are abundant in all areas Vasquez et al. (1984). with large kelp forests (Castilla & Moreno Furthermore, Dayton ( 1985) stated that 1982, Dayton 1985). In these areas Loxe- Loxechinus albus has an important role in chinus was commonly seen but usually was the control of Macrocystis abundance in not very abundant. It is clear that they do wave exposed sites and that its effect on not forage far from the food source (Casti- this kelp decreases as the intensity of the lla & Moreno 1982, Santelices & Ojeda wave action also decreases. This explana- 1984b ). In most protected areas, drift is tion is the basis for the general belief that abundant, and Loxechinus is often rare sea urchins only play a major role in harsh (Vasquez et al. 1984). In most other areas environmental conditions with severe stor- where they are abundant, Loxechinus fora- ms, low nutrients and warm temperatures ges actively (Dayton 1985). (Harrold & Reed 1985). For the above rea- Little evidence relates to the regulation sons, wave protected environments have of the sea urchin population density in long-lived perennial Macrocystis populatio- southern South America. Dayton (1985) ns (North 1971, Rosenthal et al. 197 4, Ge- hypothesized that low larval availability is rard 1976, Kirkwood 1977, Dayton et al. an important factor related to the relatively 1984, Druehl & Wheeler 1986). Some Chi- low abundance of Tierra del Fuego Loxe- lean M. pyrifera populations also have life chinus population. These habitats are in- spans of 2 to 4 years (Santelices & Ojeda fluenced by the circumpolar Westwind 1984, Moreno & Sutherland 1982, Wester- Drift current, and the only source of Loxe- meier & Moller 1990). However, M. pyrife- chinus larvae is from the Cape Horn Archi- ra populations found in the northernmost pelago. Assuming that Loxechinus larvae part of the archipelago region in southern are similar to other echinoids in spending Chile have an annual life cycle (Busch- four or more weeks in the plankton, the HERBIVORE-KELP INTERACTIONS IN SUBTIDAL HABITATS 49

Westwind Drift would carry most of the lar- lied by a guild of predators and not by a vae away, and the only recruitment into the- keystone type species. Also, this review se habitats would come from eddies or areas show that the Macrocystis pyrifera beds in where larvae are trapped (Dayton 1985). the central-southern coast of Chile are not In the northern hemisphere, the abun- controlled by sea urchins in exposed sites dance of sea urchins is often influenced by and the main herbivores are the gastropod predators such as sea otters (Estes & Palmi- Tegula atra in protected sites. sano 1974, Dayton 1975), fishes and/or As has been pointed out by many au- lobsters (Mann 1977, Tegner & Dayton thors (V asquez et al. 1984, Cas till a 1985, 1981, Cowen 1983), crabs (Kitching & Dayton 1985, V asquez 1992), the effects of Ebling 1961, Bernstein et al. 1983), or aste- the herbivores-kelp interaction in southern roids (Mauzey et al. 1968, Paine & Vadas Chile differs from those in the northern he- 1969, Rosenthal & Chess 1972). As Casti- misphere. In the last years, it has been a lla & Moreno (1982) and Castilla (1985) tendency to generalization from the studies indicated, no single, efficient sea urchin done in Macrocystis or in Laminaria. In predator exists in the Macrocystis pyrifera this contex, and due to the importance of kelp communities of southern Chile. Appa- kelp communities in the southern hemis- rently, the most conspicuous predators of phere these strong biological interactions sea urchins are two species of asteroids: must be re-examinated. Meyenaster gelatinosus, which occurred in abundance only north of Golfo de Penas (Dayton 1985), and Cosmasterias lurida ACKNOWLEDGMENTS Philippi, which is the principal predator found in coastal belts of Macrocystis at We thank Drs. Joanna Jones (University of Puerto Toro in southern Chile (V asquez & Liverpool) and John Lawrence (University Castilla 1984, Castilla 1985). However, of South Florida) for critical reading the Loxechinus and the other sea urchin species manuscript, and the support of the Direc- are very rare in the diet of Cosmasterias ci6n de Investigaci6n of Universidad Cat6- lurida (Vasquez & Castilla 1984). lica del Norte and Universidad de Los La- Loxechinus has effective defense beha- gos. This review was partialy included on viors, and Meyenaster only reduces Loxe- the research proposal of FONDECYT N° chinus densities on isolated boulders 5960001 and 1960202 (JA Vasquez). from which the urchins can be stampeded without immediate immigration (Dayton et al. 1977). When the boulders are suffi- LITERATURE CITED ciently isolated and large, this stampe- ding phenomenon can result in Macrocys- ALVEAL K, H ROMO AND J VALENZUELA (1973) Consideraciones ecol6gicas de !as regiones de tis being released from Loxechinus Valparafso y Magallanes. Revista de Biologfa Mari- predation long enough to recruit and sur- na (Chile) 15: 1-29. vive to reproduce. BARRALES HL & JL LOBBAN (1975) The comparative ecology of Macrocystis pyrifera with emphasis on the forest of Chubut, Argentina. Journal of Ecology 63: 657-677. CONCLUDING REMARKS BERNSTEIN BB, SC SCHOETER & KH MANN (1983) Sea urchin (Strongylocentrotus droebachiensis) aggregating behaviour investigated by a subtidal This review indicate that the northern po- multifactorial experiment. Canadian Journal of pulation of Lessonia the sea urchin Tetra- Fishery and Aquatic Science 40: 1975-1986. BLACK R ( 1977) The effects of grazing by the limpet pygus niger is the main grazer producing Acmea insessa, on the kelp Egregia laevigata, in extensive barren grounds, but also the the intertidal zone. Ecology 57: 265-277. effect of the gastropod Tegula tridentata BRATTSTROM H & A JOHANSSEN (1983) Ecological and regional zoogeography of the marine benthic and the fish Aplodactylus punctatus are im- fauna of Chile. Sarsia, 68: 289-339. portant. Water movement can either facili- BUSCHMANN AH ( 1992) Algal communities of a wave- tate or impede the access of benthic grazers protected intertidal rocky shore in southern Chile. In: Seeliger U (Ed.) Coastal Plant Communities of to the plants and this herbivores are contra- Latin America: 91-104. Academic Press, San Diego. 50 V ASQUEZ & BUSCHMANN

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