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Feeding capabilities and limitation of herbivorous molluscs: A functional group approach

Article in Marine Biology · July 1982 DOI: 10.1007/BF00409596

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The user has requested enhancement of the downloaded file. Marine Biology68, 299-319 (1982) MARINE BIOLOGY Springer-Verlag 1982

Feeding Capabilities and Limitation of Herbivorous Molluscs: A Functional Group Approach

R. S. Steneck 1,2,, and L. Watling 3

1 Marine Systems Laboratory, Smithsonian Institution; Washington, D.C. 20560, USA 2 Department of Earth and Planetary Sciences, The Johns Hopkins University; Baltimore, Maryland 21218, USA 3 Department of Zoology and Oceanography Program, Darling Center, University of Maine; Walpole, Maine 04573, USA

Abstract group approach suggests various hypotheses concerning algal community structure, plant/ and herbi- The susceptibility of an alga to an herbivorous mollusc vore/herbivore interactions, the relative importance of depends, in part, upon the size and toughness of the plant structural defenses in , and the evolution of special- relative to the feeding ability of the mollusc. In this study, ized grazers. These hypotheses are examined using data algae are subdivided into seven functional groups based from published accounts. on these and other physiological characteristics. Herbivo- rous prosobranchs and are subdivided into four functional groups based on the structure of their feeding apparatus. Distinct patterns in the diets of these molluscs Introduction are evident when feeding data, based on these functional groups, are examined. Most herbivorous mollusc eat The complexity and variability of natural communities algal forms that are either minute (i.e., micro- and fila- often make descriptions, interpretations, and predictions of mentous algae) or very large and expansive (kelp-like or their structure difficult if not impossible. Although each crustose algae). Algae of intermediate size (erect forms 1- species is thought to occupy a unique ecological niche to 10-cm tall) are eaten to a lesser extent, possibly because (Hutchinson, 1957), commonly there are groups of species they are too large to be rasped from the substratum and that utilize certain aspects of the environment in similar too small for most to occupy. Herbivorous ways. That is, there are groups of functionally similar archaeogastropods (excluding ) and mesogastro- species (functional groups) that occupy similar adaptive pods tend to eat filamentous and microscopic algal forms zones (sensu, Stanley, 1979) although they may be geo- predominantly, whereas limpets and chitons feed on large, graphically and evolutionarily distinct. Recognizing such leathery and crustose algae. These dietary differences groupings may release ecologists from the necessity of reflect functional differences in the feeding apparatus of studying individual species in a community in order to these herbivore groups. Radulae of herbivorous mesogas- understand and predict the outcome of interspecific inter- tropods function like rakes and can ingest larger, tougher actions and to interpret patterns in community structure. algae than can radulae of nonlimpet archaeogastropods. Furthermore, functional groups can be recognized in the The latter function more like brooms by sweeping the fossil record, thereby facilitating interpretations of past substratum broadly, but exerting little force. Limpets and community structure. chitons have superior excavating abilities because their Predators (both carnivores and herbivores) are known radulae have: robust buccal muscles surrounding them, a to affect the distribution, abundance, and fitness of their reduced number of points of contact on the substratum, prey. The diets of predators vary, in part, because of dif- and minerally hardened teeth. The feeding apparatus of ferences in their feeding abilities relative to the differential chitons is most versatile since it possesses features found in susceptibilities of their potential prey. In marine com- all herbivorous gastropod functional groups, and thus, it munities, distribution patterns of benthic algae are can sweep and excavate simultaneously. This functional heavily influenced by herbivory (Paine and Vadas, 1969; Paine, 1977; Lubchenco and Menge, 1978; Vance, 1979). In this paper, we examine functional group interactions * Present address: Department of Zoology and Oceanography Program, Darling Center, University of Maine; Walpole, Maine between benthic marine algal prey and their molluscan 04573, USA herbivores. Specifically, we group herbivorous proso-

0025-3162/82/0068/0299/$ 04.20 300 R.S. Steneck and L. Watling: Algal-Herbivore Functional Groups branch gastropods and polyplacophoran () molluscs thus make comparisons with other herbivorous molluscs according to shared characteristics of their feeding ap- difficult. We recognize that Neritacea is placed in a paratus. We will show that these herbivore groups have distinct order from Archaeogastropoda based on several distinct and restricted diets when their algal prey items are anatomical characters (Morton and Yonge, 1964). How- grouped according to shared characteristics of growth form, ever, since their radula is a rhipidoglossan type (Fretter, size, and toughness. 1965; Hickman, 1980a), they will be included with archaeogastropods for the sake of discussion. We chose to examine only herbivore-algal interactions for the sake of Methods uniformity in many physiological and anatomical proper- ties. Thus we have excluded marine angiosperms although The diets of 106 species of herbivorous molluscs (archaeo- in many respects they appear to be similar to the larger gastropod and mesogastropod , and chitons) were leathery macrophytes (discussed below). obtained from a comprehensive literature search com- bined with previously unpublished data (obtained by R. S. Steneck). Only studies based on careful observations, Results experiments, or analyses of gut and fecal contents were used (197 of the 25l references qualified; Appendix 1). The Prey: Functional Groups of Algae Predominant foods (foods consumed in greatest abun- dance) were categorized according to algal functional There is renewed interest in categorizing marine algae into groups (discussed below). Opisthobranch and pulmonate ecologically meaningful groups (Lieberman etal., 1979; herbivores were omitted because less is known of their Littler, 1980; Littler and Littler, 1980; Montgomery, 1980). diets and, in the case of opisthobranchs, they use their The newer approaches differ from one another in detail, feeding apparatus in a fundamentally different way and but they are generally workable improvements over the

FUNCTIONAL GROUP REPRESENTATIVES MORPHOLOGY ANATOMY GRAZING DIFFICULTY cross-section

I MICROALGAE diatoms blue-greens

Cladophoro 2 FILAMENTOUS ALGAE Ectocorpus A crochoetium ij, r o

3 FOLIOSE ALGAE U/va Porphyra I om }00000000o0

Bryo thomn/um 4 CORTICATED MACROPHYTES Chondria "@Icm @ I2~ Aconthophofa

5 LEATHERY MACROPHYTES Lam/nof/o Fucus non-calcareous crust

6 ARTICULATED CALCAREOUS Halimeda ALGAE Corall/na

T CRUSTOSE CORALLINE crustose corallines ALGAE

Fig. 1. Algal functional groups. Each functional group is designated by a number. Grazing difficulty refers to structural toughness (Littler and Littler, 1980). Not shown is the additional difficulty of grazing algal groups 3, 4 and 6 due to the size and shape of most herbivorous molluscs relative to the size and shape of these algae (see text and Fig. 2) R. S. Steneck and L. Watling: Algal-Herbivore Functional Groups 30 l

Table 1. Ontogenetic changes in functional groupings of algae. Each of the representative algae start out as spores which are functionally similar to microalgae (AG l). The numbering across the rows represents the developmental "path" (in functional groups) a juvenile alga takes before reaching maturity (c). Different species within a genus (e.g. Gigartina spp.) can follow different functional group "paths" during development

Algal group when Genus Algal groups during development mature AG1 AG2 AG3 AG4 AG5 AG6 AG7

AG 1 Diatoms c Blue-green c AG 2 Cladophora spp. 1 c Polysiphonia spp. 1 e AG 3 Ulva spp. 1 2 c Porphyra spp? 1 2 c AG 4 Chondrus spp. 1 c 2 Gigartina spp." 1 2 3 c Gigartina spp." 1 2 AG 5 Laminaria spp." 1 2 3 4 c Fucus spp. 1 2 3 4

AG 6 Corallina spp. 1 2 b Bossiella spp. 1 2 b AG 7 Lithothamnium spp. 1 c Clathromorphum spp. 1 c

Heteromorphic genus with an alternate phase in a different functional group (Table 2) b Persists in this functional group indefinitely Mature morphological state

largely ignored "life form" groupings of the past (Oltmann, Trends in size, morphology, anatomy and grazing dif- 1905; Setchell, 1926; Feldmann, 1937; Chapman and ficulty (toughness) of the algal functional groups are Chapman, 1976) which were more phylogenetically and illustrated in Fig. 1. The first group (AG 1) is represented life-history based. Littler and Littler (1980) and Littler by minute, unicellular and filamentous forms, which have (1980) demonstrated that predictable trends in succes- no holdfasts for attachment to the substratum. This group sional status, photosynthetic ability, calorific value, and includes spores and zygotes of other algal groups (Ta- structural toughness were correlated with thalli of certain ble 1). Algal group 2 contains larger algal filaments that morphologies regardless of their phytogenetic affinity-. Our are attached by holdfasts, and commonly have little or no functional groups (Fig. 1) are similar to those of Littler cortication (i.e., single row of cells). Sporelings of many and Littler (1980) except that we emphasize thallus mor- algae are included in this group (Table 1 discussed below). phology, size and toughness. The third group (AG 3) includes thin sheet and tube We propose that algal functional groups be based on morphologies that are only one or two cells thick. These common morphological and anatomical features (Fig. 1). three groups are small and generally lack the structural Functional groups are enumerated and ranked according integrity necessary to support a three-dimensional struc- to their toughness (defined as the ability to resist being ture of any size. Corticated macrophytes (AG 4) are scratched), a characteristic readily apparent to even casual morphologically complex, tend to be wiry, tough and observers. Several other characteristics of these functional ramifying forms, capable of growing erect and filling groups, which are ecologically important parameters, in- three-dimensional space. The thalli of these algae are dif- clude photosynthetic efficiency, thallus longevity, and suc- ferentiated into an outer layer of small, often thick-walled, cessional status. Our groupings are variable depending cells called a cortex (thus the name "corticated") and a upon the part of the thallus (e.g. holdfast, stipe, or frond) central region of larger thin-walled cells called the me- the stage of development (Table 1), or the ploidy level dulla. Leathery macrophytes (AG 5) are more extensively (Table 2) of the alga. Algal group numbers ("AG n", corticated and are morphologically most complex with where n is a number from one to seven corresponding to a thick-walled cells giving them structural strength sufficient functional group; Fig. 1) are used for ease in reference and to become very large (> 100 m long). This group includes are not meant to represent discrete morphological "jumps" the giant kelps and it differs anatomically from the previ- from one algal group to the next. Rather, this scheme is a ous group by having a proportionally thicker cortex continuum with the mid-point in each algM group de- (especially in stipe forming species), greater size, and picted in Fig. 1. Although a few algal species do not fit morphological complexity. The non-calcified crusts in this neatly into this grouping (e.g. saccate forms), most group are not as morphologically complex as the kelps but (> 90%) do. are equally tough to scrape due to the dense packing of 302 R.S. Steneck and L. Watling: Algal-Herbivore Functional Groups

Table 2. Alternate functional groupings expressed for heteromor- SMALLEST OR RANKING IN SIZE LARGEST OR phic algae depending upon the stage in their life cycle. Each pair is U3 LEAST EXPANSIVE MOST EXPANSIVE -J biologically the same species although they frequently are listed as --I different genera I-- 0 Algae grazed off substrata ~A 50- Genus Algal groups l- O Z 02 i~ Herbi...... ~upy algae AG1 AG2 AG3 AG4 AG5 AG6 AG7 O Z 20-

UFOS~Ora "////. spp. (2N) Codiolum ~- I0- spp. (N) O Intermediatesize refuge i.//~~~~ Porphyra spp. (N) o Conchocelis I 2 5 4 6 5 7 spp. (2N) ALGAL FUNCTIONALGROUP NUMBERS Gigartina spp. (N) Fig. 2. The relative importance of each algal group in the diets of herbivorous molluscs (n~ 106 species). The algal groups are ar- Petrocelis ranged according to the size of the plant thallus (structural height spp. (2N) and expansiveness, depicted in Fig. 1) Laminaria spp. (2N) filamentous phase (N) Ralfsia spp. (2N) Scytosiphon spp. (N)

cells in the outer tissue (M. M. Littler, personal com- munication; Steneck, in preparation). Calcareous algae are toughest because the cell walls contain calcium car- bonate. They comprise two algal groups, articulated and encrusting. Articulated calcareous forms (AG 6) are roughly the size and shape of the corticated macrophytes (AG 4) except that they are composed of a series of short calcare- ous segments connected by flexible joints. Crustose coral- line algae, (AG 7) are heavily calcified and grow postrate over substrata. The trend in toughness, described above and depicted in Fig. 1, is supported by the work of Littler and Littler (1980).

The Herbivores: Functional Groups of Molluscs

Many chitons and prosobranch gastropods (excluding neogastropods) are herbivorous. Of the multitude of factors that potentially limit the diets of molluscs, we hypothesize that body size (relative to size of algae), and body plan (e.g. shape of shell, location of mouth relative to foot) are most important in the overall pattern, and that differences in feeding apparatus are important in observed between-group differences.

Constraints of Herbivore Size and Body Plan on Feeding Fig. 3. The rhipidoglossan radula. Upper: nodosa from Ability: An Intermediate Size Refuge for Algae? St. Croix, U.S. Virgin Islands, 60• ; in transmitted fight the trans- lucency of the radula indicates the teeth are soft due to the ab- sence of a mineralized component in the teeth. Lower: F. nodosa Herbivorous molluscs differ from some other herbivores from St. Croix, 70 x, scanning electron micrograph. The small in- (e.g. fishes and crabs) in that most are small, relatively conspicuous central tooth is probably of little use in food gathering R. S. Steneck and L. Watling: Algal-Herbivore Functional Groups 303

slow moving, and due to the position of their mouth they lages. Anatomical characteristics of the feeding apparatus must physically occupy the substratum they graze. This of gastropods and chitons are well known (e.g. Fretter and restricts the range of algal resources a molluscan herbivore Graham, 1962; Graham, 1973; Purchon, 1977). Therefore, can utilize. our discussion will emphasize functionally important dif- An examination of the algal functional groups known ferences, relative to algal diets, in order to demonstrate to be major components of molluscan diets shows the that consistent patterns are evident when plant/herbivore following trend (Fig. 2, Appendix 1).The most commonly interactions are examined at the functional group level. grazed algal groups are either very small (microalgae [AG 1]; and filamentous algae [AG 2]) or very large and (A ) Rhipidoglossan Radulae ("Brooms") expansive forms (leathery macrophytes lAG 5] and crus- rose corallines lAG 7]). Intermediate-sized algae (foliose The rhipidoglossan radula (Fig. 3) is found in all archaeo- [AG 3], corticated macrophytes [AG 4] and articulated gastropods except true limpets (superfamily Patellacea), calcareous algae [AG 6]), usually ranging in size between which have docoglossan radulae (see below). It is struc- one and 10-cm tall, are relatively ungrazed by molluscs turally the most complex prosobranch radula, having (Fig. 2, Branch and Branch, 1980; Underwood and Jerna- numerous teeth per row (Fig. 4A) and a myriad of koff, 1981). The thallus surface area of the intermediate- muscles in the buccal mass (Fretter and Graham, 1962; sized algae may be too small to support most herbivorous Graham, 1973). Most of these muscles make minor adjust- molluscs and too large to be successfully trampled down ments of tension and position of the radula ribbon, a and grazed without risk of dislodgement by waves or process which results in the splaying of the numerous predators. marginal teeth when the radula is protracted (Fig. 4A). The marginal teeth as well as the more massive lateral Constraints of Molluscan Feeding Apparatus on Grazing teeth are very long with relatively narrow bases of attach- Ability: Survival of the Toughest ment compared to their overall length. Thus, during protraction of the radula a small change in the tension The feeding apparatus of molluscan grazers is complex, applied to the radular ribbon results in an exaggerated and includes the radula, buccal muscles, jaws and carti- movement of the distal tips of the teeth. Most food

EFFECTIVE WIDTH NUMBER OF EXCAVATION OF GRAZE STROKE FUNCTIONAL CAPABILITY POINTS Ribbon Width

@

RHIPIDOGLOSSA 4

| TAENIOGLOSSA

DOCOGLOSSA

@

POLYPLACOPHORA

Fig. 4. The radulae of the herbivorous mollusc functional groups. The homologous teeth of each group are labelled as follows: ct, central tooth; It, lateral tooth; mt, marginal teeth 304 R.S. Steneck and [. Wading: Algal-Herbivore Functional Groups

RHI PIDOGLOSSAN GRAZERS herbivores with greater excavating abilities (Steneck, A n= 22 species 1982). Rhipidoglossan grazers are less capable of grazing very tough substrata because none of their teeth are hardened with iron compounds as are those of doco- 2o glossan and polyplacoph0ran radulae (Lowenstam, 1962: Fig. 4 C, D), and their buccal muscles are not very robust. An examination of the diets reported for 22 species of o I 2 3 4 5 6 rhipidoglossan grazers (Appendix 1) revealed a predomi- nance of microalgae and delicate filaments (Fig. 5A). Scattered reports of this herbivore group feeding on

B TAEN IOGLOSSAN GRAZERS leathery macrophytes (AG 5) may indicate feeding on 40 n= 48 species epiphytes, or softer portions of an alga (discussed below), or the ability of very large gastropods (e.g. the 3o spp.) to remove tough cortical cells because of their great size. Hickman (1976) suggested that rhipidoglossan gastro- pods have a wider range of food resources than was o I 2 5 4 5 6 previously suspected. This is true since some are selective deposit feeders (Hickman, 1976) and others are carnivores (Purchon, 1977). Among the herbivores in this group, DOCOGLOSSAN GRAZERS C n= 21 species however, the upper limit of their abilities (in terms of algal toughness) seems fixed. Rhipidoglossan grazers rarely eat 30 leathery macrophytes (AG5, Appendix 1) and none is known to eat crustose corallines (AG 7). This suggests a 20 limit to the latitude of trophic resources available to these gastropods. 0 F///A VIllA I 2 3 4 5 6 7 (B) Taenioglossan Radulae ("Rakes") D POLYPLACOPHORAN 5O GRAZERS 40 n=15 species The taenioglossan radula (Fig. 6) is found in most meso- gastropods (species list in Appendix 1). It has fewer teeth ~ ~o (Fig. 4B) and a less complex musculature than the rhipido- m 20 glossan radula (Fretter and Graham, 1962; Graham, 1973). The reduced number of marginal teeth in taenio- illlll glossan radulae has been accompanied by a loss of 0 I 2 :5 4 5 6 5' ancillary muscles used to adjust radula tension and posi- FUNCTIONAL GROUPS OF MARINE ALGAE tion. Graham (1973) suggested that these differences in Fig. 5. The predominant diets (expressed in terms of algal func- musculature reflect a change from sweeping to scraping or tional groups, see Table 1 and Fig. 1) for the four functional rasping modes of feeding. Therefore less emphasis is put groups of herbivorous molluscs. Data are from a total of 197 refer- on positional adjustments of the radula and more on the ences examined (listed in Appendix 1) force with which the radula is applied to the substratum. In contrast to rhipidoglossan radulae (Fig. 3), in taenio- glossan radulae the central (rachidian) tooth is commonly gathering is accomplished by marginal and lateral teeth used in food gathering (Fig. 6; Fretter and Graham, 1962; while the central tooth is probably less important in Jiich and Boekschoten, 1980). The chitinous teeth of ingestion (Fretter and Graham, 1962). As the radula is taenioglossan radulae, like those of rhipidoglossan radu- retracted, the food is gathered by the inward sweep of the lae, are relatively soft (Fig. 6; Jones etal., 1935; Lowen- widely splayed marginal teeth. This results in wide grazing stare, 1962). strokes (Fig. 4A), with the total number of points con- The dietary range of taenioglossan grazers (Fig. 5 B) tacting the substratum (number of teeth times number of reflects radula modifications characteristic of this group cusps per tooth) during a "bite", for a given row, being (Fig. 4B). The propensity for grazing microalgae and often greater than 500. Because the marginal teeth of this filamentous algae is probably facilitated by the splaying of group are long, the force exerted by each tooth against the the pluricuspid marginal teeth to produce a greater surface substratum cannot be great (Fig. 4A). Graze marks of this area for collecting particles (Fig. 4 B). The inward "raking" herbivore group are rarely seen on leathery macrophytes and possibly cutting of algal filaments occurs as the teeth (AG 5) and never on calcareous algae (AG 7). Whereas converge toward the central axis of the radula during graze marks on those algal groups are common among retraction. The greater force applied to the substratum, R. S. Steneck and L. Watling: Algal-Herbivore Functional Groups 305

Fig. 7. The docoglossan radula. Upper: Acmaea insessa from Cali- fornia, USA, 325 • ; in transmitted light the presence of hardening minerals can be seen as a dark band along the edge of each tooth. Lower: A. pelta from California, USA, scanning electron micro- graph (800 X )

that graze leathery macrophytes (AG 5) frequently leave distinct graze marks (e.g., Fralick et al., 1974). Fig. 6. The taenioglossan radula of Littorina littorea collected in Maine, USA. Upper: transmitted light view, 250x; note absence of hardening minerals. Middle: scanning electron micrograph, (C) Docoglossan Radulae ("Shovels") 200 • vertical view. Lower: scanning electron micrograph, 225 x, view along the radula showing the number of functional points for all teeth; note the prominence of the central or rachidian tooth, The docoglossan radula (Fig. 7), found in all true limpets which, unlike the rhipidoglossan grazers (Fig. 3), most likely (Superfamily Patellacea), is characterized by an extreme comes into contact with the substratum reduction in number of teeth per row (Fig. 4C) and number of muscles in the buccal mass. There are few, if and the robustness of radular teeth in taenioglossans (Figs. any, marginal teeth and the teeth do not splay outwardly 4 B, 6) may explain how they graze a greater proportion of against the substratum as they do with the groups dis- tough leathery macrophytes and articulated cussed above. The lateral and marginal teeth are com- (Fig. 5 B) than do rhipidoglossans. Taenioglossan grazers monly short, stout, have a relatively wide base of attach- 306 R.S. Steneck and L. Watling: Algal-Herbivore Functional Groups merit (Fig. 7; Newell, 1979) and are moved over the sub- stratum in a rasp-like fashion. Graham (1973) noted that hypertrophy of the odontophoral muscles may be neces- sary to provide stability, rigidity and force to the radula during the grazing stroke. These features, augmented by the occurrence of hardening agents (iron and silicate compounds; Fig. 7) on the distal portions of the teeth (to minimize wear), provide for a greater excavating capa- bility on tougher substrata. The excavating abilities of the feeding apparatus ex- tend the grazing capability of limpets to include leathery macrophytes and crustose corallines (Fig. 5 C). Articulated corallines and corticated macrophytes are not eaten, prob- ably because of their size and shape rather than their toughness (Fig. 2, discussed above). Smaller algae may be difficult for limpets to ingest because the specialized adaptations for excavating may restrict their ability to effectively sweep micro and filamentous algae. The teeth on radulae are immobile and often there are spaces between teeth (depicted in Steneck, 1982). This may make limpets poorly suited to graze filamentous and foliose algae (AG 2 and 3). Unless the substratum is excavated, thereby "uprooting" the filaments with the substratum, the filaments may slip between the teeth during grazing. Thus, ingestion of microalgae may result from the limpet scrap- ing the substratum surface, or by excavating the substra- tum on which the microalgae live. Variations in the diet of limpets, relative to radular differences, will be covered in a future paper (Steneck and Watling, in preparation).

(1)) Polyplacophoran Radulae ("Multi-purposed Tool") Fig. 8. The polyplacophoran radula. Upper: Tonicella lineata from Washington, USA, 90x; note that the dominant lateral tooth in each row is completely inpregnated with mineral. Lower: All polyplacophoran (chiton) radulae have 17 teeth per Craspedockiton hernphilli from St. Croix, 90 x, scanning electron row (Figs. 4 D, 8) of which only four appear to be used in micrograph, vertical view; the tricuspid dominant teeth are mineralized, whereas the elongate "spoon-handled" teeth are not grazing. Two teeth ("dominant teeth"; Fretter and Gra- ham, 1962) usually function to excavate substrata. These teeth commonly have three cusps, and are hardened (heavily mineralized with iron and silicate compounds; Lowenstam, 1967). The two slightly spoon-shaped mar- Chitons differ from other herbivorous molluscs with ginal teeth (Fig. 8) are long, relatively soft (unmineralized) radulae that converge during grazing (i.e., rhipidoglossan and lightly sweep the substratum. and taenioglossan) by being superior excavators. Their Although chitons (Polyplacophora) belong to a class excavating abilities are probably due to the reduced different from snails () and diverged early in number of points contacting the substratum (two to six, the evolution of the phylum (Cambrian period; Pojeta and depending upon the number of cusps present, Figs. 4 and Runnegar, 1976), there are several similarities between the 8), and robust buccal muscles (Graham, 1973). The exca- feeding apparatus of the two groups. For example, Gra- vating ability of chitons was demonstrated by Jt~ch and ham (1973) noted that chiton radulae operated like those Boekschoten (1980), who showed that the chiton Lepido- of taenioglossans with the teeth converging toward the chitona sp. penetrates shells as it grazes, whereas Littorina center during grazing. That the dominant teeth of chitons littorea (taenioglossan grazer) only brushes "algal films" scrape the substratum with a force comparable to that of off the shell surfaces. In addition, chitons have been docoglossan (limpet) grazers is evident in the depth of reported to cut pieces of algae (Himmelman and Carefoot, graze marks made in crustose corallines (personal observa- 1975; Boyle, 1977), a capability probably due to the lateral tion). These teeth are followed by the light inward-sweep- teeth converging against one another. The majority of ing action of the marginals that probably pick up loose chiton species with known diets eat crustose corallines debris and algal filaments in a way similar to rhipido- while the rest mostly eat microalgae or leathery macro- glossan and taenioglossan grazers. phytes (Fig. 5 D). R. S. Steneck and L. Watling: Algal-Herbivore Functional Groups 307

Discussion minaria spp. [Fralick et al., 1974] and Fucus spp. [personal observation] respectively), whereas the rhipidoglossan Although exceptions to the patterns described here will grazer, Gibbula umbiIicaIis, is said to feed on algae of the undoubtedly surface (some are discussed below), the same functional groups without leaving marks (Bakker, functional group approach is a promising aid in inter- 1959). The latter grazer may ingest the outer layers of cells preting ecological and evolutionary processes. Specifically, incidentally while feeding on epiphytes (Fretter and Gra- we believe it will be possible to predict the Outcome of ham, 1962) and thus has a minimal effect on the plant. plant/herbivore and herbivore/herbivore interactions at Similarities in diets of functionally different herbivores the functional group level without being bound to a geo- may be due to functional differences within an alga since graphic region, phylogenetic line, geological age or stage not all parts of a plant are functionally equal. For in an alga's life cycle. example, edges of kelp fronds (AG 5) are often thin blades and thus similar to foliose algae (AG 3). Many rhipido- glossan grazers, such as HaIiotis spp., which are said to eat Resolution of Herbivore Functional Groups kelp, do so by eating the detached edge of a drifting Similarities Between Functional Groups foliose portion of the frond (Littler, personal communica- tion). This is functionally quite different (in terms of size, Similarities in diets between herbivore functional groups shape and toughness) from eating the tougher stipe (Vadas, (e.g. taenioglossan and rhipidoglossan grazers, Fig. 5A 1979). Similarly, the crustose holdfasts of some algae such and B) requires a closer examination. We suggest that two as Chondrus spp. (holdfasts=AG 5) and Corallina spp. additional factors be considered. (1) Convergent evolution (holdfast=AG 7) are more grazer-resistant than are the of feeding apparatus may allow different herbivore groups erect portions of those plants (AG 4 and 6 respectively). to utilize similar resources. (2) The resolving power of a Dietary overlap between functional groups could be better literature search on herbivore diets is limited because the evaluated if characteristics that separate functional groups intensity of grazing (ability of an herbivore to remove (i.e., Fig. 1 for algae and Fig. 4 for herbivorous molluscs) algal biomass) on any species of algae is variable depend- were applied to within-functional group variances as well. ing upon the part of the plant eaten, its stage in develop- ment (Table 1), and its ploidy level (stage in its life cycle, Differences within Functional Groups Table 2). We will explore both of these possibilities (dis- cussion of life history differences will be discussed under Dietary range within an herbivore functional group is not plant/herbivore interactions). necessarily linked to the taxonomic affinity of the grazers. Convergences between rhipidoglossan and taenioglos- It is possible for congeneric species to have strikingly dif- san radulae are evident in the striking reductions in the ferent diets. For example, the periwinkles Littorina Iittorea number of marginal and lateral teeth and cusps present in and L. obtusata live sympatrically in the North Atlantic. some rhipidoglossan genera and the increased number of L. littorea grazes microalgae, filamentous and foliose algae those teeth in some taenioglossan genera. The number of (AG t, 2 and 3; Appendix 1), whereas L. obtusata grazes marginal teeth in rhipidoglossans such as Solariella spp. leathery macrophytes (Appendix 1, Bakker, 1959; Fretter and Tegula spp. (depicted in Hickman, 1979, and Fritch- and Graham, 1962; R. S. Steneck, unpublished data). man, 1965, respectively) can be less than half the number These differences in diet may reflect differences in the commonly found in such genera as Fissurella spp. and radula of the two snails. The radula ofL. littorea has more Hemitoma spp. (depicted in Hickman, I980a), The lateral functional points (20) touching the substratum and the teeth may have few or no cusps (e.g., Nerita spp. depicted cusps are more numerous and more pointed than are in Hickman, 1980) thereby reducing the number of points those of the radula of L. obtusata (17 functional points; of contact and thus increasing their excavating abilities depicted in Bandel, 1976). Possibly radula characteristics (Fretter, 1965). helpful in functional interpretations between herbivore Conversely, some taenioglossan grazers such as Rhino- groups will also apply in interpreting functional differ- clavis spp. (depicted in Houbrick, 1978) have very long ences within herbivore functional groups. Thus snails with pluricuspid sweeping marginals and laterals that appear to a greater number of sharply pointed, pluricuspid teeth are be functionally similar to those teeth in rhipidoglossan more likely to be grazers of microalgae and filamentous grazers. algae (AG 1 and 2) whereas herbivores with fewer, blunter Similarities in the diets of functionally different her- teeth and fewer cusps will more likely consume tougher bivores may also be due to significant differences in the algae (AG 5 and 7). intensity of their grazing (i.e. how deeply they graze into the substratum). This is analagous to an aphid and a cow, both of which may eat the same plant, but they do so in Interpreting Ecological Processes functionally different ways, and with very different conse- Herbivore~Herbivore Interactions quences for the plants. Similarly, taenioglossan grazers, such as Lacuna vincta and Littorina obtusata, make deep, Mechanisms that facilitate the coexistence of species have visible marks on the stipes of leathery macrophytes (La- received considerable attention from ecologists as a pos- 308 R.S. Steneck and L. Watling: Algal-Herbivore Functional Groups sible means of explaining the diversity of species in com- Heteromorphic algae (where the haploid and diploid munities. Trophic resources can be an important dimen- phases of an alga's life cycle are different morphologically) sion of a species niche and thus distinct differences be- may survive periods of intensive herbivory by persisting in tween the feeding capabilities and limitations of sympatric a more herbivore-resistant phase of their life cycles (Littler herbivorous molluscs can aid in interpreting how they and Littler, 1980; Lubchenco and Cubit, 1980; Slocum, interact without competitively excluding one another. For 1980). Usually, alternate phases of heteromorphic algae example, a rhipidoglossan grazer, the keyhole limpet, can be assigned to different functional groups (Table 2). Fissurella angusta, lives sympatrically with a docoglossan Structural and morphological characteristics of algae grazer, the true limpet, Acmaea jamaicensis, on coralline have received relatively little attention as defenses against substrata in St. Croix, U.S.V.I. Both were observed to herbivores compared to chemical defenses (see Norris and graze the same areas of crustose corallines, microalgae and Fenical, 1981, for a review of chemical defenses in algae). filamentous algae. Analyses of the gut and fecal contents Algae suspected to possess anti-herbivore chemicals are revealed only diatoms (AG 1) and fine filamentous algae mostly in the larger and tougher algal groups (AG 4, 5 (AG 2, i.e., Herposiphonia spp., Faulkenbergia sp.) in the and 6) (Fenical, 1975; Ogden and Lobel, 1978; O. McCon- gut of F. angusta (3 individuals examined) and coralline nell, personal communication). The largest and toughest of cells (AG 7, Porolithon pachydermum) in the gut of the A. these forms, however, are most commonly eaten by mol- jamaicensis (5 individuals examined). The teeth of F. luscs with greater excavating abilities (i.e., limpets and angusta were severely abraded, cracked and unevenly chitons, Fig. 5). However, Littorina littorea, a taenioglos- worn, whereas the teeth of A. jamaicensis were worn to a san grazer with only a marginal ability to ingest leathery sharp edge. It is even possible that the grazing activity of macrophytes is thought to avoid Fucus sp. because of F. angusta on filamentous algae improves conditions for chemicals found within the thallus (Lubchenco, 1978; the corallines (inferior competitors to filamentous algae Geiselman, 1981). Whereas the radula of this species is [Steneck, 1982]) and thus inadvertently improves the food characteristic of one adapted for grazing microalgae (dis- availability for coralline-grazing limpets. Similar facilita- cussed above), radular differences in L. obtusata enable it tion between molluscan herbivores (i.e., Siphonaria sp. to excavate Fucus sp. apparently unaffected by possible and Cellana sp.) is discussed by Underwood and Jernakoff chemical defenses. Thus, a necessary first step in deter- (1981). mining if a plant's chemical defenses are effective in deterring herbivory, is to establish that the herbivore is physically able to eat the plant. Plant~Herbivore Interactions The functional grouping for any species of algae varies depending upon the part of the plant considered (dis- Trophic Specialization: A Predictable Outcome of the Inter- cussed above), its stage of development or phase in its life section of Plant and Herbivore Functional Groups cycle. Algae that reproduce by spores or gametes begin life, functionally, as minute microalgae (Table 1, AG 1) and Atrophic specialist predominantly eats one, or relatively then, through a variety of "paths", develop into adults of few, species of plant or preferentially. Trophic different functional groups. At each stage, their suscepti- specialization in marine herbivores is more common bility to grazing is crucial to their survival. Littler and among small herbivores of low vagility on larger, longer Littler (1980) demonstrated that Egregia sp. changes func- lived algae (i.e., AG 5 and 7), than it is for any other group tionally from AG 3 to AG 5 during its development and, of marine herbivore (Steneck, 1982). This is because, at the accompanying the morphological changes there are scale perceived by small herbivores, the larger, longer changes in productivity (decreasing per unit weight) and lived algae are a more abundant and predictable source of toughness (increasing). D. Cheney (in preparation) has food for herbivores capable of ingesting them. Among shown that certain algal species have an advantage under gastropods, docoglossan (limpet) grazers are the only grazing pressure from littorinids depending upon whether herbivores capable of eating these algal groups (Fig. 5 C) germinating spores develop directly into filaments (e.g. and coincidentally they also have the greatest number of Fucus sp.) or into crusts (e.g. Chondrus sp.) in the process trophically specialized species (Test, 1945; Graham, 1955; of maturation (Table 1). Juvenile crustose holdfasts of McLean, 1969; Branch, 1975; Black, 1976; Carlton, 1976; Chondrus sp. (AG 5) were shown to be more resistant to Lindberg, 1977; Steneck, 1977, 1982). Many such limpets littorinid (taenioglossan) grazing than were the filamen- spend their entire life on a single algal species. The tous (AG 2) sporelings of Fucus sp. Differential suscepti- evolutionary advantages to species that specialize on any bilities can have a major effect on the algal community that resource are offset by their dependency on it (Levins, develops. For example, Vadas et al. (1977, and in prepa- 1968). Thus, specialized herbivorous molluscs, unlike more ration) demonstrated that the timing of the spring migra- mobile herbivores such as fishes or amphipods, require tion of littorinids in New England affects the algal com- large perennial plants (e.g. kelp, AG 5 and crustose coral- munity that develops, depending on the stage of develop- lines, AG 7) for both food (Fig. 5) and habitat (Fig. 2) ment of the algal recruits relative to the time the littorinids because moving from plant to plant may be costly and arrive. risky (Steneck, 1982). R. S. Steneck and L. Watling: Algal-Herbivore Functional Groups 309

We suggest that the proclivity for trophic specialization Branch, G. M. and M. L. Branch: Competition between Cellana between docoglossan grazers and large, leathery, and tramoserica (Sowerby) (Gastropoda) and Patiriella exigua (Lamarck) (Asteroidea), and their influence on algal standing crustose coralline algae may be a predictable result of stocks. J. exp. mar. Biol. Ecol. 48. 35-49 (1980) interactions between algal groups having the particular Carlton, J. T.: Marine plant limpets of the northeastern Pacific: properties of large size and greater toughness with herbi- patterns of host utilization and comparative plant-limpet vores having characteristics of small size, low mobility and distributions. Western Soc. of Malac. 9, 22 (1976) great excavating abilities in their feeding apparatus. Chapman, V. and D. Chapman: Life forms in the algae. Bot. Mar. 19, 65-74 (1976) Feldman, J.: Recherches sur la vegetation marine de la Mediter- ran+e. La Cote des Albrres. Rev. Algol. i0, 1-339 (1937) Conclusions Fenical, W.: Halogenation in the Rhodophyta: a review. J. Phycol. 11, 245-259 (1975) Fralick, R. A., K. W. Turgeon and A. C. Mathieson: Destruction We offer these examples to demonstrate the utility of a of kelp populations by Lacuna vincta (Montagu). 88, functional group approach in helping to understand the 112-114 (1974) mechanisms behind observed patterns in plant/herbivore Fretter, V.: Functional studies of the anatomy of some neritid interactions between algae and molluscs. Future analyses, prosobranchs. J. Zool, 147, 46-74 (1965) Fretter, V. and A. Graham: British prosobranch , their made specifically within or between functional groups, functional anatomy and ecology, 548 pp. London: Ray Society may elucidate the latitude of functional groups or limits to 1962 the variations possible on a given morphological "theme" Fritchman, H. K.: The radulae of Tegula species from the west (e.g. for variations of rhipidoglossan radulae, see Hickman, coast of North America and suggested intrageneric relation- ships. Veliger 8, 11-15 (1965) 1976, 1977, 1979, 1980a, 1980b). In an evolutionary sense, Geiselman, J.: Ecology of chemical defenses of algae against the this approach can define more clearly the significance of a herbivorous , Littorina littorea, in the New England rocky particular adaptive breakthrough (e.g. the evolution of intertidal community. Proc. 20th Northeast Algal Symposimn gastropods with docoglossan radulae from ancestors with (Abstr.) (198l) rhipidoglossan radulae) in utilizing a new adaptive zone Graham, A.: Molluscan diets. Proc. Malac. Soc., London 33, 144-159 (1955) (e.g. tougher algae, AG 5 and 7) without requiring the Graham, A.: The anatomical basis of function in the buccal mass unlikely discovery of a fossil gastropod containing the food of prosobranch and amphineuran molluscs. J. Zool., Lond. of its last meal 169, 317-348 (1973) Hickman, C. S.: Form, function, and evolution in the archaeogas- tropod radula. Geol. Soc. America (Ab str.) 8, 917-918 (1976) Acknowledgements. We wish to thank R. G. Creese, M. Hickman, C. S.: Adaptive morphology of the trochid gastropod Dethier, D. Duggans, M. E. Hay, C. S. Hickman, R. S. radula. Geol. Soc. America (Abstr.) 11, 84 (1979) Houbrick, J. B. C. Jackson, P. Kat, E. Leigh, S. Lidgard, Hickman, C. S.: Evolution and function of asymmetry in the M. M. Littler, D. Packer, R. T. Paine, S. Palumbi, S. M. archaeogastropod radula. Veliger 23, 189-194 (1980 a) Hiekman, C. S.: Gastropod radulae and the assessment of form in Stanley, G. J. Vermeij for their comments and criticisms of evolutionary paleontology, Paleobiology 6, 276-294 (1980b) various drafts of this manuscript. Funding and facilities for Himmelman, J. H. and T. H. Carefoot: Seasonal changes in this project were provided by a predoctoral fellowship calorific value of three Pacific Coast and their grant from the Smithsonian Institution and by the Ira C. significance to some marine invertebrate herbivores. J. exp. Darling Center of the University of Maine. In particular mar. Biol. Ecol. 18, 139-151 (1975) Houbrick, R. S.: The family Cerithiidae in the Indo-Pacific. In: we wish to thank the people of Computer Services and the Monographs of marine mollusca, No. 1, pp 1-130. Ed. by R. Scanning Electron Microscopy Laboratory at the Smith- T. Abbott. Delaware: American Malacologists, Inc. 1978 sonian for their valuable help and expertise. J. Rosewater Hutchinson, G. E.: Concluding remarks. Cold Spring Harbor and R. S. Houbrick generously provided access to the Syrup. Quant. Biol. 22, 415-427 (1957) Jones, E. I., R. A. McCance and L. R. B. Shackleton: The role of Smithsonian's mollusc collection. Funding for the tropical iron and silica in the structure of the radular teeth of certain research was provided by the Marine Systems Laboratory marine molluscs. J. exp. Biol. 12, 59-64 (1935) of the Smithsonian Institution. Jiich, P. J. W. and G. J. Boeksehoten: Trace fossils and grazing traces produced by Littorina and Lepidochitona, Dutch Wadden Sea. Geologie en Mijnbouw. 59, 33-42 (1980) Levins, R.: Evolution in changing environments, 120 pp. Prince- Literature Cited ton, N J: Princeton Univ. Press 1968 Lieberman, M. D., M. John and D. Lieberman: Ecology of Bakker, K.: Feeding habits and zonation in some intertidal snails. subtidal algae on seasonally devastated cobble substrates off Arch Neer. de Zool. 13, 230-257 (1959) Ghana. Ecology 60, 1151-1161 (1979) Bandel, K.: Studies on from the Atlantic. Veliger 17, Lindberg, D. R.: Marine plant limpets of the northern Pacific: 92-114 (1976) Neogene phylogeny and zoogeography. Western Soc. Malacol. Black, R.: The effects of grazing by the limpet, Acmaea insessa, on 9, 26 (1977) the kelp, Egregia laevigata, in the intertidal zone. Ecology 57, Littler, M M.: Morphological form and photosynthetic perfor- 265-277 (1976) mances of marine macroatgae: test of a functional/form Boyle, P. R.: The physiology and behavior of chitons (Mollusca: hypothesis. Bot. Mar. 22, 161-165 (1980) Polyplacophora). Oceanogr. Mar. Biol. Ann. Rev. 15, 461-609 Littler, M. M. and D. S. Littler: The evolution of thallus form and (1977) survival strategies in benthic marine macroalgae: field and Branch, G. M.: Intraspecific competition in cochlear Born. laboratory tests of a functional form model. Am. Nat. 116, J. Anim. Ecol. 44, 263-282 (1975) 25-44 (1980) 310 R.S. Steneck and L. Watling: Algal-Herbivore Functional Groups

Lowenstam, H. A.: Geothite in radular teeth of recent marine changing scenes in natural sciences, 1776-1976, pp 245-270. gastropods. Science, N.Y. 137, 279-280 (1962) Ed. by Clyde Goulden. Academy of Natural Sciences, Spec. Lowenstam, H. A.: Lepidocrodite and apatite mineral and mag- Pub. 12, 1977 netite teeth of chitons (Polyplacophora). Science, N.Y. 195, Paine, R. T. and R. L. Vadas: The effects of grazing by sea 1372-1375 (1967) urchins, Strongylocentrotus spp. on benthic algal populations. Lubchenco, J.: Plant species diversity in a marine intertidal Limnol. Oceanogr. 14, 710-719 (1969) community: importance of herbivore food preference and Pojeta, J. and B. Runnegar: The paleontology ofrostroconch mol- algal competitive abilities. Am. Nat. 112, 23-29 (1978) luscs and the early history of the phylum Mollusca. Geol. Lubchenco, J. and J. Cubit: Heteromorphic life histories of Surv. Prof. Paper 968, 1-85 (1976) certain marine algae as adaptations to variations in herbivory. Purchon, R.: The biology of the mollusca, 560 pp. Oxford: Perga- Ecology 61, 676-687 (1980) mon 1977 Lubchenco, J. and B. A. Menge: Community development and Setchell, W.: Phytogeographical notes on Tahiti. Part II. Marine persistance in a low rocky intertidal zone. Ecol. Monogr. 48, vegetation Univ. Cal. Publ. Bot. 12, 291-324 (1926) 67-94 (1978) Slocum, C. J.: Differential susceptibility to grazers in two phases McLean, J. H.: Marine shells of southern California. Science of an intertidal alga: advantages of heteromorphic genera- Series 24, Zoology, 104 pp. 1969 tions. J. exp. mar. Biol. Ecol. 46, 99-110 (1980) Montgomery, W. L.: The impact of non-selective grazing by the Stanley, S, M.: Macroevolution, pattern and process, 332 pp. San giant blue damsel fish, Microspathodon dorsalis, on algal com- Francisco: W. H. Freeman 1979 munities in the Gulf of California, Mexico. Bull. mar. Sci. 30, Steneck, R. S.: A crustose coralline-limpet interaction in the Gulf 290-303 (1980) of Maine. J. Phycol. 13, 65 (Abstr.) (1977) Morton, J. E. and C. M. Yonge: Classification and structure of the Steneck, R. S.: A limpet-coralline alga association: adaptations Mollusca. In: Physiology of mollusca Vol. 1, pp, 1-58. Ed. by and defenses between a selective herbivore and its prey. K. M. Wilbur and C. M. Yonge. London: Academic Press 1964 Ecology 63, 507-522 (1982) Newell, R, C.: The biology of intertidal , Third Edition, Test, A. R.: Ecology of California Acmaea. Ecology 26, 395-405 555 pp. Faversham, Kent, England: Marine Ecological Sur- (1945) veys, Lts. 1979 Underwood, A. J. and P. Jernakoff: Effects of interactions be- Norris, S. N. and W. Fenical: Chemical defenses in tropical tween algae and grazing gastropods on the structure of a low- marine algae. In: Atlantic barrier reef ecosystems at Carrie shore intertidal algal community. Oecologia 48, 221-233 Bow Cay, Belize, Scientific Report 1: Structure and com- (1981) munities. Ed. by K. Rtitzler and W. Fenical. Smithsonian Vadas, R. L.: Seaweeds: an overview; ecological and economic Contrib. Mar. Sci. 1981 importance. Experimentia 35, 429-433 (1979) Ogden, J. C. and P. S. Lobel: The role of herbivorous fishes and Vadas, R. L., M. Keser, B. Larson and W. S. Grant: Influence of urchins in coral reef communities. Env. Biol. Fishes 3, 49-63 Littorina littorea on algal zonation. J. Phycol. 13, 84 (Abstr.) (1978) (1977) Oltmann, F.: Morphologie und Biologie der Algen. Jena 1905 Vance, R. R.: Effects of grazing by the sea urchin, Centroste- Paine, R. T.: Controlled manipulations in the marine intertidal phanus coronatus, on prey community composition. Ecology zone, and their contributions to ecological theory. In: The 60, 537-546 (1979)

Appendix 1. A compilation of published studies on the analysis, field observations, and experimental preference diets of herbivorous marine prosobranch gastropods and experiments). CL 2 requires two of the four categories of chitons. Diets are represented in the following two ways: evidence. CL 3 indicates careful field observations (many (1) listed under the category "Predominant Diets" as de- of the older studies). CL 4 indicates questionable assertion scribed in each reference, (2) ranked according to amounts of the molluscs diet (i.e, little, conflicting, or no evidence eaten for each algal group (AG 1 to AG 7) under the presented). CL 5 indicates a mollusc is associated with an category "Dietary Preference Ranking". The certainty level alga, but no evidence was presented regarding its food. of the data are listed under the category "CL", ranging Only CL levels less than or equal to 3 were used in order to from 1 (highest) to 5 (lowest). Specifically, a CL of 1 in- be conservative dicates four categories of evidence (e.g. gut analysis, fecal Rhipidoglossan grazers r.,m Sp. no. Species Predominant diets Dietary preference ranking References

AG1 AG2 AG3 AG4 AG5 AG6 AG7 CL

1 Arene tricarinata Amphiroafragilissima 0 2 0 0 0 1 0 5 Warmke & Almodovar 1963 2 Austroeochlea constricta Diatoms 1 0 0 0 0 0 0 3 Creese & Underwood 1976 3 Calliostoma zizy#hinum "Small algae" 0 1 0 0 0 0 0 3 Fretter & Graham 1962 4 Cantharidus coruscans Durvillea and Macrocystis 0 0 0 2 1 0 0 2 Simpson 1976 O'Q 5 Cantharidus striatus Zostera (epiphytes) 1 0 0 0 0 0 0 5 Bakker 1959 6 Cittariumpiea Microalgae and filaments 1 2 0 0 0 0 0 3 Steneck (pers. obs.) 7 Fissurella angusta Potysiphonia & Her_posiphonia 2 1 0 0 0 0 0 2 Steneck 1982 8 Fissurella barbadensis Lyngbya 1 2 0 0 0 0 0 1 Ward 1966 9 Fissurella crassa Ulva & Enteromorpha 0 0 1 0 0 0 0 2 Brentos 1978 10 Fissurella nodosa Blue greens 1 2 0 0 0 0 0 2 Steneck (unpub. data) 11 Gibbula cineraria "Microscopic epiphytes" 1 2 0 0 0 0 0 3 Bakker 1959 11 Gibbula cineraria "Small algae" 1 1 0 0 0 0 0 3 Fretter & Graham 1962 12 Gibbula pennanti "Microscopic epiphytes" 1 2 0 0 0 0 0 3 Bakker 1959 t~ 13 Gibbula umbilicalis Fucaceae 0 0 0 0 1 0 0 4 Fleure & Gettings 1907 5 13 Gibbula umbilicalis "Small algae" 1 1 0 0 0 0 0 3 Fretter& Graham 1962 14 Haliotis conugata Kelp 0 0 0 0 1 0 0 4 Olsen 1968 15 Haliotis kamtschatkana Chaetoeeros & NavicuIa 1 0 2 3 4 0 0 3 Paul et al. 1977 15 Ha#otis kamtschatkana "Small non-diatomaceous algae" 0 1 0 0 0 0 0 3 Cox 1962 16 Haliotis rugescens Macroeystis 0 0 0 0 1 0 0 4 Olsen 1968 17 Haliotis sorenseni Maeroeystis 0 0 0 0 1 0 0 4 Olsen 1968 18 Haliotis tubereulata Delesseria, Griffithsia & Chondrus 0 1 0 2 0 0 0 4 Graham 1955 18 Haliotis tubereulata Corallina 0 0 0 0 0 1 0 4 Croft 1929 19 Hemotoma octoradiata Microalgae and filamentous algae 1 2 0 0 0 0 0 2 Steneck (unpub. data) 20 Melagraphia aethiops Ulva and CoralIina 0 0 1 0 0 1 0 3 Luckens 1974 20 Melagraphia aethiops Filamentous algae 0 2 0 0 0 0 0 3 Zeldis & Boyden 1979 21 Monodonta Lineam "Ephemerals" 1 1 1 0 0 0 0 3 Bakker 1959 21 Monodonta lineata "Small algae" 1 1 0 0 0 0 0 3 Fretter & Graham 1962 22 Nerita melanotragus "Diatoms and algal filaments" 1 1 0 0 0 0 0 3 Luckens 1974 23 Nerita virginea Oscillatoria 1 0 0 0 0 0 0 3 Sarasua 1944 24 Neritinapeloronta Microalgae 1 0 0 0 0 0 0 3 Bergh 1890 25 Scutus breviculus Ulva 0 0 1 0 0 0 0 2 Owen 1958 26 Tegula brunnea Laminaria and Pterygophora 0 0 0 0 1 0 0 5 McLean t962 26 Tegula montereyi Kelps 0 0 0 0 1 0 0 5 McLean 1962 27 Tegula pulligo Laminaria & Pterygophora 0 0 0 0 1 0 0 5 McLean 1962 28 Theodoxusfluviatilis Filamentous greens 1 2 0 0 0 0 0 3 Ankel 1936 29 Trieolia sp. Sargassum 0 0 0 0 1 0 0 4 Bandel 1974 30 Tricoliapullus Diatom epiphytes 1 0 0 0 0 0 0 3 Ankel 1936 30 Tricolia #ullus Ceramium & Rhodymenia 0 1 1 0 0 0 0 3 Fretter 1955 31 Turbo sp. Filamentous algae 0 1 0 0 0 0 0 3 Tsuda & Randall 1971

t.O t~ Taenioglossan Grazers

Sp. no. Species Predominant diets Dietary preference ranking References

AG1 AG2 AG3 AG4AG5 AG6 AG7 CL

1 A lvania auberiana Dietyota divaricata 0 2 1 0 0 3 0 5 Warmke & Almodovar 1963 2 A lvania crassa Corallina 0 0 0 0 0 1 0 3 Pelseneer 1935 3 A lvania punctura Diatoms & dinoflagellates 1 0 0 0 0 0 0 2 Fretter & Manly 1979 4 Assiminea grayana Diatoms 1 0 0 0 0 0 0 3 Ankel 1936 5 Assiminea succinea Amphiroafragilissima 0 2 0 0 0 1 0 5 Warmke & Almodovar 1963 6 Barleeia rubra Microalgae 1 0 0 0 0 0 0 3 Graham 1955 7 BatiIlaria attramentaria Benthic diatoms 1 0 0 0 0 0 0 2 Whitlatch, Obrebski 1980 8 Batillaria minima Blue green algae 1 0 0 0 0 0 0 3 Garrett 197(I 9 Batillaria zonalis Microalgae 1 0 0 0 0 0 0 3 Driscoll 1972 10 Bithynia tentaculata Filamentous algae 0 l 0 0 0 0 0 3 Fretter & Graham 1962 11 Bittium reticulatum Cystoseira barbata 0 0 0 0 1 0 0 3 Kiseleva 1967 12 Bittium varium Diatoms & filamentous algae 1 1 0 0 0 0 0 3 Bandel 1974 12 Bittium varium Laurencia obtusa 0 2 0 1 0 0 0 5 Warmke & Almodovar 1963 13 Bythinella scholtzi Diatoms 1 O 0 0 0 0 0 3 Fretter & Graham 1962 14 Caecum spp. Diatoms 1 0 0 0 0 0 0 3 G~3tze 1938 15 Caecum antillarum Diatoms and filamentous algae 1 1 0 0 0 0 0 3 Bandel 1974 16 Caecum nitidum Spyridia filamentosa 0 1 0 0 0 0 0 5 Warmke & Almodovar 1963 17 Caecum pulcheIlum Cladophoropsis membranacea 0 1 2 0 0 0 0 5 Warmke & Almodovar 1963 18 Cerithidea californica Benthic diatoms 1 0 2 0 0 0 0 2 Whitlatch, Obrebski 1980 18 Cerithidea californica Microalgae 1 0 0 0 0 0 0 3 Driscoll 1972 19 Cerithidea costata Blue green algae 1 0 0 0 0 0 0 3 Garrett 1970 20 Cerithium variable Centrocerus clavatum 0 1 0 0 0 0 0 5 Warmke & Almodovar 1963 21 Cyclostremiscus ornatus Cladophoropsis membranacea 0 1 0 0 0 2 0 5 Warmke & Almodovar 1963 22 Hydrobia ulvae Ulva 0 0 1 0 0 0 0 3 Ankel 1936 8 ~ 23 Lacuna sp. Fucoid algae 0 0 0 0 1 0 0 3 Morton 1968 24 Lacuna parva Chondrus crispus & Gigartina 0 1 0 1 1 0 0 3 Ankel 1936 25 Lacuna pallidula Fucus serratus 0 0 0 0 1 0 0 5 Gardiner 1929 26 Lacuna vincta Fucus & Laminaria 0 0 0 0 1 0 0 3 Pelseneer 1935 26 Lacuna vincta Laminaria 0 0 0 0 1 0 0 2 Fralick et al. 1974 27 Laevilittorina caliginosa Microalgae and diatoms 1 0 0 0 0 0 0 3 Simpson 1976 28 Littorina cincta Diatoms & Polysiphonia 1 1 0 0 0 0 0 2 Luckens 1964 29 Littorina irrorata Diatoms 1 0 0 0 0 0 0 2 Alexander 1979 0"o > 29 Littorina irrorata Microalgae 1 0 0 0 0 0 0 3 Marples 1966 o~ 30 Littorina littorea Filamentous algae 0 1 2 3 4 0 0 2 Lubchenco 1978 30 Littorina littorea Enteromorpha intestinalis 0 0 1 0 0 0 0 3 Sze 1980 30 Littorina littorea Cladophora & Utvales 0 1 1 0 0 0 0 5 Gardiner 1929 o" 30 Littorina littorea Filamentous and microalgae 1 1 0 0 0 0 0 3 Bakker 1959 30 Littorina littorea Diatoms and blue greens 1 0 0 0 0 0 0 3 Steneck (unpub. data) O 30 Littorina littorea Enteromorpha & sporelings 0 1 1 0 0 0 0 3 Keser 1977 r 30 Littorina littorea Diatoms 1 0 0 0 0 0 0 3 Hylleberg & Christensen 1978 c~ 30 Littorina littorea Juvenile Fucus (filaments) 0 1 0 0 0 0 0 2 Cheney (pers. comm.) 30 Littorina littorea Juvenile Fucus (filaments) 0 1 0 0 0 0 0 3 Lubchenco 1980 31 Littorina neritoides Microalgae 1 0 0 0 0 0 0 3 Sacchi et al. 1977 32 Littorina obtusaZa Fucus serratus 0 0 0 0 1 0 0 2 Young 1975

32 Littorina obtusata Fucus & Ascophyllum 0 0 0 0 1 0 0 l Dongen 1956 32 Littorina obtusata Fucus vesiculosis 0 0 0 0 1 0 0 5 Gardiner 1929 32 Littorina obtusata Fucoid algae 0 0 0 l 0 Morton 1968 32 Littorina obtusata Fucus disticus 0 0 0 1 0 Steneck (unpub. data) 33 Littorina planaxis Microalgae 1 2 0 0 0 Foster 1964 Littorina planaxis 33 Microalgae 1 1 0 0 0 Dahl 1964 ~2 34 Littorina rudis Microalgae 1 1 0 0 0 Bakker 1959 35 Littorina saxatilis Diatoms & blue greens 1 2 3 0 0 Sacchi et al. 1977 36 Littorina scutulata Microalgae 1 2 0 0 0 Foster 1964 36 Littorina scutulata Microalgae 1 1 0 0 0 Dahl 1964 36 Littorina scutulata Diatoms 1 0 0 0 0 Nicotri 1977 ~z 37 Littorina unifaxciata antipoda Diatoms & filamentous algae 1 1 0 0 0 Luckens 1964 38 Macquarella harniltoni "Fronds of " 0 0 0 0 0 Simpson 1976 39 Omalogrya atomus Diatoms & Ulva 1 0 1 0 0 Fretter 1948 40 Pterocera lambis Filamentous reds 0 1 0 0 0 Yonge 1932 41 Pterocera truneata Diatoms & blue greens 1 0 0 0 0 Demond 1957 42 Rissoella caribaea Laurencia t)apillosa 0 2 0 0 0 Warmke & Almodovar 1963 43 Rissoa guerini Codiurn 0 0 0 0 0 Anke[ I936 44 Rissoa ineonspieua Plocamium coccineurn 0 0 0 0 0 Gardiner 1929 45 Rissoa membranacea Epiphytes on Zostera 1 1 0 0 0 Ankel 1936 46 Rissoa parva Corallina 1 1 0 0 0 Pelseneer 1935 46 Rissoa parva Plocamium coccineum 0 0 0 0 0 Gardiner 1929 47 Rissoa splendida Cystoseira barbata 0 0 0 1 0 Kiseleva 1966, 1967 48 Rhissoella diaphrana Delesseria, filamentous & microalgae 1 1 1 0 0 Ankel 1936 49 Rhissoella opulina Filamentous algae 1 1 1 0 0 Ankel 1936 50 Strombus costatus Lyngb/a & Cladophora 1 1 0 0 0 Robertson 1961 51 Strombus gibbus Diatoms & filamentous algae 1 1 0 0 0 Bergh 1895 52 Strombus gigas L yngb/a Cladophora, Hypnea 1 1 0 0 0 Robertson 1961 52 Strombus gigas Diatoms & filamentous algae 1 1 0 0 0 Bergh 1895 53 Strombus raninus L yngbya, Cladophora, Polysiyhonia 1 1 0 0 0 Robertson 1961 54 Strombus troglodTtes Diatoms & filamentous algae 1 1 0 0 0 Haller 1893 55 Skeneoysis planorbis Filamentous algae 1 1 0 0 0 Ankel 1936 56 Terebellum subulatum Diatoms & filamentous algae 1 1 0 0 0 Bergh 1895 57 Viviparus viviparus Microalgae 1 0 0 0 0 Fretter & Graham 1962 58 Zeacumantus subcarinatus Ulva latuca 0 0 1 0 0 McClatchie 1979 Docoglossan grazers

Sp. no. Species Predominant diets Dietary preference ranking References

AG1 AG2 AG3 AG4 AG5 AG6 AG7 CL

1 Acmaea alveus Eel grass 1 0 0 0 1 0 0 5 Jackson 1907 1 Acmaea alveus Zostera marina 0 0 0 0 1 0 0 5 McLean 1966 2 Acmaea antillarum Calcareous algae 0 0 0 0 0 0 1 5 Bandel 1974 3 Acmaea asmi Microalgae on Tegula shells 1 0 0 0 0 0 0 5 Test 1945 3 Acmaea asmi Microalgae on Tegula shells 1 0 0 0 0 0 0 2 Hickman (pets. comm.) 4 Acmaea depicta Zostera 0 0 0 0 1 0 0 5 Test 1945 4 A cmaea depicta Zostera marina 0 0 0 0 1 0 0 5 McLean 1966 5 Acmaea digitalis Diatoms 1 0 0 0 0 0 0 3 Castenholz 1961 5 Acmaea digitalis "Microscopic encrusting algae" 1 0 0 0 0 0 0 3 Haven 1971, 1973 5 A cmaea digitalis Petrocelis 0 0 0 0 1 0 0 3 Slocum 1980 5 A crnaea digitalis Diatoms 1 0 0 0 0 0 0 3 Breen 1972 6 Acmaea insessa Egregia menziesii 0 0 0 0 1 0 0 3 Test 1945 6 A cmaea insessa Egregia menziesii 0 0 0 0 1 0 0 3 Black 1976 6 A cmaea insessa Laminaria 0 0 0 0 1 0 0 3 McLean 1966 6 A cmaea insessa Egregia menziesii 0 0 0 0 1 0 0 2 Bishop & Bishop 1973 6 A cmaea insessa Egregia menziesii 0 0 0 0 1 0 0 3 Yonge 1962 7 A cmaea instabilis Laminaria & Pterygophora 0 0 0 0 1 0 0 5 McLean 1966 7 A cmaea instabilis Lessoniopsis 0 0 0 0 1 0 0 3 Rigg & Miller 1949 7 A cmaea instabiBs A laria 0 0 0 0 1 0 0 3 Carlton 1976 7 Acmaea instabilis Laminaria andersonii 0 0 0 0 1 0 0 3 Yonge 1962 7 A cmaea instabilis Laminaria andersonii 0 0 0 0 1 0 0 3 Test 1945 8 Acmaea limatula Encrusting algae 1 0 0 0 1 0 1 3 Eaton 1968 8 Acmaea limatula Hildenbrandia 0 0 0 0 1 0 0 2 Connor 1975 8 Acmaea Iimatula Petrocelis & Hildenbrandia 0 0 0 0 1 0 0 2 Kitting 1977, 1979 9 Acmaea mitra Microcladia 0 0 0 0 1 0 0 4 Test 1945 9 Acmaea mitra Crustose corallines 0 0 0 0 0 0 1 3 McLean 1962 9 A cmaea mitra Crustose coral[ines 0 0 0 0 0 0 1 3 McLean 1962 m~ 9 Acmaea mitra Crustose corallines 0 0 0 0 0 0 1 3 Kohn (pets. comm.)

9 Acmaea mitra Crustose corallines 0 0 0 0 0 0 1 1 Steneck (unpub. data) ca. 9 A cmaea mitra Crustose corallines 0 0 0 0 0 0 1 2 Kitting 1979 10 Acmaea ochracea Microscopic algae 1 0 0 0 0 0 0 3 Test 1945 11 A cmaea paleacea Eelgrass 0 0 0 0 1 0 0 5 Test 1946 ~z 11 Acmaea paleacea Phyllospadix 0 0 0 0 1 0 0 2 Fishlyn 1976 .o2. 11 A cmaea paleacea UIva 0 0 1 0 0 0 0 3 Horgan 1976 11 Acmaea paleacea Phyllospadix 0 0 0 0 1 0 0 5 McLean 1966 11 Aemaea paleaeea Phyllospadix 0 0 0 2 1 2 0 5 Bishop & Bishop 1973 ~z 11 Acmaea paleaeea Phyllospadix torreyi 0 0 0 0 1 0 0 3 Yonge 1962 =: 12 A cmaea pelta Pelvetia 0 0 0 0 1 0 0 2 Connor 1975 12 Acmaea pelta Petrocelis & Hildenbrandia 0 0 0 0 1 0 0 2 Kitting 1977 O 12 A cmaea pelta Egregia 0 0 0 0 1 0 0 3 Bishop & Bishop 1973 12 A cmaea pelta Kelps 0 0 0 0 1 0 0 3 Test 1945 12 Aemaeapelta Diatoms 1 0 0 0 0 0 0 4 Castenholz 1961 12 Acmaeapelta "Larger, non-encrusting algae" 0 0 0 0 1 0 0 3 Eaton 1968 12 AcmaeapeIta Kelps 0 0 0 0 1 0 0 3 Craig 1968 Nicotri 1977 12 A cmaea pelta Diatoms 1 0 0 0 0 0 0 4 O 12 Acmaeapelta microalgae 1 0 0 0 0 0 0 3 Dethier (unpub. ms.) 13 Acmaeapustulata Calcareous algae 0 0 0 0 0 0 1 2 Bandel 1974 13 A cmaea pustulata Porolithon pachydermum 0 0 0 0 0 0 1 1 Steneck 1982 14 Acmaea rosacea Crustose corallines 0 0 0 0 0 0 1 5 McLean 1966 14 Acmaea rosacea Crustose corallines 0 0 0 0 0 0 1 5 Kozloff 1974 15 A cmaea scabra Encrusting microalgae 1 0 1 0 Haven 1973 16 A emaea scutum Ulva, Iridaea & Enteromorpha 0 1 0 0 Test 1945 16 A emaea scutum Petroeelis & Hildenbrandia 0 0 1 0 Kitting 1977 16 A cmaea scutum Diatoms 1 0 0 0 Castenholz 1961 r.m 16 A emaea scutum Diatoms 1 0 0 0 Nicotri 1977 16 A cmaea scutum Hildenbrandia & Petrocelis 3 0 1 0 Kitting 1979, 1980 (o 17 A emaea strigitella Diatoms 1 0 0 0 Nicotri 1977 17 A cmaea strigitella Microalgae 1 0 0 0 Dethier (unpub. ms.) 18 Aemaea testudinalis "Larger algae" 0 0 1 0 Willcox 1905 18 A emaea testudinalis Crustose corallines 0 0 0 0 Ankel 1936 18 A emaea testudinalis Clathromorphum eircumseriptum 0 0 0 0 Steneck 1977, 1982 19 A emaea trianguIaris Amphiroa tubereulosa 0 0 0 1 Ricketts et al. 1968 19 A cmaea triangularis Amphiroa tuberculosa 0 0 0 1 Test 1945 19 A cmaea triangularis Calliarthron 2 0 0 1 McLean 1962 20 Acmaea virginea Crustose corallines 0 0 0 0 Ankel 1936 20 A cmaea virginea Crustose corallines 0 0 0 0 Clokie & Norton 1974 20 A emaea virginea Cystoseira & Chondrus 0 0 1 0 Gardiner 1929 20 Cellana radiata Chaetomorpha & Enteromorpha 0 1 0 0 Balaparameswara Rao 1975 21 Cellana tramoserica Diatoms & sphores 1 0 0 0 Underwood 1975 O ,7 21 Cellana tramoseriea Microalgae & sporelings 1 0 0 0 Branch & Branch 1980 22 Lottia gigantica Probably blue green algae 1 0 0 0 Stimpson 1970 23 Patelloida alticostata Filamentous algae 1 0 0 0 Black 1977 23 Patelloida alticostata Crustose corallines 0 0 0 0 Creese (pers. comm.) O 23 Patelloida altieostata Crustose corallines 0 0 0 0 Synnot and Wescott 1976 24 eoneinna Diatoms 1 0 0 0 Shabica 1976 ~3 25 Naeella macquarensis Green algae, diatoms & corallines 1 0 0 0 Simpson 1976 26 Nacella polaris Filamentous, microalgae & corallines 2 0 0 0 Walker 1972 27 Patella aspera Lithophyllum 0 0 0 0 Bernard 1960 28 Patella cochlear Lithothamnium 0 0 0 0 Branch 1975 29 Patella compressa Eeklonia maxima 0 0 1 0 Branch 1975, 1971 29 Patella compressa Ecklonia bueeinalis 0 0 1 0 Stephenson 1939 29 Patella compressa Laminaria pallida 0 0 1 0 Koch 1949 30 Patella flexuosa Crustose corallines 0 0 0 0 Vermeij (pers. comm,) 31 Patella longicosta Ralfsia 0 0 1 0 Branch 1975 32 Patella miniata Crustose corallines 0 0 0 0 Branch 1971 33 Patella tabularis Ralfsia 0 0 1 0 Branch 1971 33 Patella tabularis Ralfsia 0 0 1 0 Branch 1975 34 Fucus & Ascophyllum 0 0 1 0 Fretter & Graham 1976 34 Patella vulgata Aseophyllum 0 0 1 0 Fischer-Piette 1948 34 Patella vulgata Gigartina stellata 0 0 1 0 Conway 1946 34 Patella vulgata Fucoids 0 0 1 0 Southward 1964, 1955 34 Patella wdgata Fucus & Aseophyllum 0 0 1 0 Orton 1948 34 Patella vulgata Diatoms & small algae 1 0 0 0 Graham 1932 34 Patella vulgata Corallina & larger algae 0 0 1 1 Davis & Fleure 1903 34 Patella vulgata "Green algae" 0 1 0 0 Moore 1938 34 Patina pellucida Laminaria 0 0 1 0 Graham & Fretter 1947 34 Patina pellucida Laminaria 0 0 1 0 Kain & Svendsen 1969 34 Patina pellucida Laminaria saccharina 0 0 1 0 Gardiner 1929 34 Patina pellucida Laminaria digitata 0 0 1 0 Bakker 1959 34 Patina pellucida Laminaria 0 0 1 0 Warburton 1976 34 Patinapellucida Laminaria sp. 0 0 1 0 Morton 1968 34 Patina pellucida Laminariaceae 0 0 1 0 Vahl 1971 34 Patinapellucida Laminaria saecharina 0 0 1 0 Fisher 1934 34 Patina pellucida Laminaria sp. 0 0 1 0 Steneck (unpub. data) ~e ui 35 Seurria parasitica Lessonia nigrescens 0 0 1 0 Vahl 197 ! 36 Seurria scurria Lessonia nigrescens 0 0 1 0 Marincovich 1973 Polyplacophoran grazers

Sp. no. Species Predominant diets Dietary preference ranking References

AG1 AG2 AG3 AG4 AG5 AG6 AG7 CL

1 Acanthochitona hemphilli Crustose corallines 2 0 0 0 0 0 1 2 Steneck (unpub. data) 2 Acanthochiton rubrolineatus Diatoms 1 0 0 0 0 0 0 2 Arakawa 1963 3 Calothrix & filamentous algae 1 1 1 0 0 0 0 3 Glynn 1970 3 Acanthopleura granulata Porolithonpachydermum 0 0 0 0 0 0 1 2 Steneck (unpub. data) 3 Acanthopleura granulata "Calcareous algae" 0 0 0 0 0 0 1 2 Bandel 1974 4 Ceratozona squalida Microalgae 1 2 0 0 0 0 0 2 Steneck (unpub. data) 5 Chiton tubereulatus Blue greens and filamentous algae 1 1 0 0 0 0 0 3 Glynn 1970 6 Cyanoplax hartwegii Pelvetia 0 0 0 0 1 0 0 2 Connor 1975 6 Cyano#lax hartwegii Pelvetia 0 0 0 0 1 0 0 2 Robb 1975 7 Hemiarthrum setulosum Crustose corallines 0 0 0 0 0 0 1 3 Simpson 1976 8 Ischnoehiton limaciformis "Calcareous algae" 0 0 0 0 0 0 1 3 Bandel 1974 9 Katharina tunicata Diatoms 1 0 0 0 0 0 0 3 Kozlov 1976 9 Katharina tunieata Hedophyllum sessile 0 0 0 0 1 0 0 3 Dayton 1975 10 Lepidochiton einereus Diatoms 1 0 0 0 0 0 0 3 Fretter 1937 11 Mopalia muscosa Gigartina & Endocladia 0 0 0 1 1 0 0 2 Connor 1975 11 Mopalia rnuseosa Corallina, Gelidium & Gigartina 0 0 0 0 1 2 0 2 Boolootian 1964 12 Plaxiphora aurata Crustose corallines 0 0 0 0 0 0 1 2 Simpson 1976 13 Tonicella lineata Crustose corallines 0 0 0 0 0 0 1 3 Demopulos 1975 13 Tonicella lineata Crustose corallines 0 0 0 0 0 0 1 3 Barnes 1972 13 Tonieella lineata Crustose corallines 2 0 0 0 0 0 1 3 Barnes & Gonor 1972 13 Tonicella #neata Epiphytes on corallines 1 1 0 0 0 0 2 3 Kohn (pets. comm.) 14 TonicelIa marmorea Crustose corallines 0 0 0 0 0 0 1 5 Langer 1977 14 Tonicella marmorea Crustose corallines 2 0 0 0 0 0 1 3 Steneck (pets. obs.) 15 Tonicella rubra Crustose corallines 0 0 0 0 0 0 1 5 Langer 1977 15 Tonieella rubra Crustose corallines 2 0 0 0 0 0 1 3 Steneck (pets. obs.) 15 Tonieella rubra Diatoms & microalgae 1 0 0 0 0 0 0 3 Milligan 1916 g~

O~ > cr~

,< O P~ R. S. Steneck and L. Wading: Algal-Herbivore Functional Groups 317

Literature Cited in Appendix Dahl, A. L.: Macroscopic algal foods of Littorina ,planaxis Philippi and Littorina scutulata Gould. Veliger 7, 139-143 Literature cited below does not include references already cited in (1964) the text. Davis, J. A. and H. J. Fleure: Patella. Liverpool Mar. Biol. Comm. Mem. 10, 1-76 (1903) Alexander, S. K.: Diet of the periwinkle Littorina irrorata in Dayton, P. K.: Experimental evaluation of ecological dominance Louisiana salt marsh. GulfRes. Rpt. 6, 293-295 (1979) in a rocky intertidal algal community. Ecol. Monogr. 45, Ankel, W. E.: Die Frabspuren yon Helicion und Littorina und die 137-159 (1975) Funktion der Radula. Verh. d. Dtsch. Zool. Ges. 12, 174-182 Demond, J.: Micronesian reef-associated gastropods. Pacific Sci. (1936) 11, 275-341 (1957) Arakawa, K. Y.: Studies on the molluscan faeces (I). Publ. Seto Demopulos, P. A.: Diet, activity and feeding in Tonicella lineata mar. biol. Lab. 11, 185-208 (1963) (Wood 1815). Veliger 18, 42-46 (1975) Balaparameswara Rao, M.: Some observations on feeding, anat- Dongen, A. Van: The preference of Littorina obtusata for Fuca- omy, histology of the digestive tract and digestive enzymes in ceae. Arch. Neerl. Zool. 11, 373-386 (1956) the limpet Cellana radiata (Born) (Gastropoda: Prosobranchia). Driscoll, A. L.: Structure and function of the alimentary tract of Proc. Malac. Soc. Lond. 41, 309-320 (1975) Battillaria zonaIis and Cerithidea californica, style-bearing Bandel, K.: Fecal pellets of Amphineura and Prosobranchia Mol- mesogastropods. Veliger 14, 375-386 (1972) lusca from the Caribbean coast of Columbia South America. Eaton, C. M.: The activity and food of the file fimpet Acmaea Senckenb. Marit. 6, 1-32 (1974) limatula. Veliger 11, 5-12 (1968) Barnes, J. R. and J. J. Gonor: The larval settling response of the Fischer-Piette, E.: Sur les 616ments de prospGrit6 des Patelles lined chiton Tonicella lineata. Mar. Biol. 20, 259-264 (1973) et sur leur spGcifit~. 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M.: The ecology of Patella Linneaus from the Cape Fretter, V.: Some observations on Tricolia ,pullus (L.) and Mar- Peninsula, South Africa. I. Zonation, movements and feeding. garites helicinus (Fabricius). Proc. Malacol. Soc. Lond. 31, Zoologica Africana. 6, 1-38 (1971) 565-585 (1955) Breen, P. A.: Seasonal migration and population regulation in Fretter, V. and A. Graham: The prosobranch molluscs of Britain Limpet Acmaea (Collisella) digitalis. Veliger 15, 133-141 and Denmark. Part 1. Pleurotomariacea, Fissurellacea and (1972) Patellacea. J. Moll. Stud. Supplement 1, 1-33 (1976) Brentos, M.: Growth in the keyhole limpet Fissurella crassa Fretter, V. and R. Manly: Observations on the biology of some Lamarck in Northern Chile. Veliger 21, 268-273 (1978) sublittoral prosobranchs. J. Moll. Stud. 45, 209-218 (1979) Carlton, J. 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