Feeding Capabilities and Limitation of Herbivorous Molluscs: a Functional Group Approach
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See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/226058212 Feeding capabilities and limitation of herbivorous molluscs: A functional group approach Article in Marine Biology · July 1982 DOI: 10.1007/BF00409596 CITATIONS READS 535 1,123 2 authors, including: Les Watling University of Hawaiʻi at Mānoa 184 PUBLICATIONS 5,046 CITATIONS SEE PROFILE All content following this page was uploaded by Les Watling on 18 August 2014. 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/herbivore 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 algae, 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 chitons 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 species 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 herbivores to occupy. Herbivorous ways. That is, there are groups of functionally similar archaeogastropods (excluding limpets) 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 (chiton) 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 snails, 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