Grazing by the Intertidal Gastropod Melampus Coffeus Greatly Increases Mangrove Leaf Litter Degradation Rates

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Grazing by the Intertidal Gastropod Melampus Coffeus Greatly Increases Mangrove Leaf Litter Degradation Rates MARINE ECOLOGY PROGRESS SERIES Vol. 296: 209–218, 2005 Published July 12 Mar Ecol Prog Ser Grazing by the intertidal gastropod Melampus coffeus greatly increases mangrove leaf litter degradation rates C. Edward Proffitt*, Donna J. Devlin Florida Atlantic University, c/o Harbor Branch Oceanographic Institution, 5600 US 1 North, Fort Pierce, Florida 34946, USA ABSTRACT: Melampus coffeus, a pulmonate gastropod, forages for mangrove leaf litter at low tide and climbs tree trunks to avoid inundation during high tide. Unlike many grazers, these snails can assimilate mangrove leaf material. At Boca Ceiga Bay, Florida, densities of adult snails were high (>100 snails m–2) throughout a 130 m wide intertidal zone. A mark–recapture study indicated that over the course of 1 mo 48.6 ± 6.1% of snails returned to their initial tree during high tides, while those that did relocate moved 6.66 ± 0.60 m and were recorded from 33 new trees at high tide. A field experiment comparing tethered leaves with small and large litter bags showed that snail grazing greatly increased the rate of red (Rhizophora mangle) and black (Avicennia germinans) leaf litter breakdown. Grazing by M. coffeus resulted in 90% weight loss in <4 wk (A. germinans) and 7 wk (R. mangle), compared to slower breakdown in litter bags (12 to 26 wk, A. germinans; >26 wk, R. man- gle). Another experiment showed greater leaf litter accumulation on the forest floor in plots where M. coffeus was excluded. The decomposition coefficient (k) was 10× greater when M. coffeus grazing was allowed than k for any studies that enclosed leaves in litterbags. During our experiment, M. cof- feus consumed an estimated 40.5% of mangrove leaf fall, and 19.8% of leaf litter was exported as particulate or dissolved material. This M. coffeus population can produce an estimated 3 × 106 larvae m–2 yr–1, which suggests that the larval pathway is an important conduit of mangrove leaf resources to the estuarine food web. KEY WORDS: Mangrove · Detritivore · Decomposition · Rhizophora mangle · Avicennia germinans Resale or republication not permitted without written consent of the publisher INTRODUCTION invertebrates might account for a large fraction of leaf breakdown in Florida. This important animal–plant Despite considerable study, the linkages between interaction was missed by earlier studies of decomposi- mangrove forest detritus and adjacent estuarine water tion that excluded M. coffeus and other large inverte- ecosystems are inadequately understood (Odum & brate grazers by studying litter enclosed within mesh Heald 1972, Fell & Master 1973, Snedaker & Lugo bags (Heald 1969, 1971, Lugo & Snedaker 1974, Twil- 1973, Cundell et al. 1979, Twilley et al. 1986, Boto ley et al. 1986). Laboratory studies by Mook (1986) 1992, Holmer & Olsen 2002). Proffitt et al. (1993) showed that M. coffeus could assimilate large fractions reported that grazing by the intertidal gastropod of fresh (79%) and senescent (56%) R. mangle leaves. Melampus coffeus L. (Pulmonata: Ellobiidae) in both McKee & Faulkner (2000) found high rates of grazing field and laboratory trials caused very high rates of by M. coffeus on mangrove leaf litter in both natural breakdown of Rhizophora mangle, Avicennia germi- and restored forests in SW Florida. nans and Laguncularia racemosa leaves. They also Where Melampus coffeus has an abundant and per- found differences among mangrove species and with sistent population in mangrove forests, a substantial different degrees of leaf senescence (Proffitt et al. fraction of mangrove leaf productivity can pass 1993) and were the first to suggest that grazing by through a snail-mediated pathway to the estuary as *Email: [email protected] © Inter-Research 2005 · www.int-res.com 210 Mar Ecol Prog Ser 296: 209–218, 2005 snail biomass, larvae, and feces (Mook 1986, Proffitt et is an active grazer when the forest floor is exposed at al. 1993). Thus, M. coffeus functions as more than just low tide. It escapes being covered by water at high a shredder snail (sensu Newell 1965, Fenchel 1969, tide by climbing tree trunks, prop roots, taller 1970, Newell & Barlocher 1993, Barlocher & Newell seedlings, and various emergent debris. The timing of 1994). Clearly, differences in type of pathway and the this behavioral rhythm was maintained a number of rates of litter degradation in mangrove forests may days when snails were brought in to the lab and kept affect predictions about the proportion of mangrove without any tidal flux (authors’ pers. obs.). productivity that is re-cycled within the forest relative Litterfall occurs in seasonal and species specific pat- to that exported. The objectives of the present study terns mainly as yellow senescent leaves, although were to further quantify the rates of M. coffeus grazing substantial numbers of green leaves fall episodically on Rhizophora mangle and Avicennia germinans leaf during storms (authors’ pers. obs.). The rates of grazing litter; to couple this with measurements of leaf litter fall of Melampus coffeus vary by species and by degree of and standing crop in order to estimate the rate of this senescence of the leaves (Proffitt et al. 1993). Thus, the grazing pathway per unit forest area; and to assess M. proportion of litter entering the system as green versus coffeus population densities over time and across the yellow leaves, the proportion of leaves that exist on the intertidal zone. ground long enough to become brown, and the rates of Melampus coffeus is abundant in many mangrove breakdown of each leaf group all contribute to the forests on both coasts of Florida (authors’ pers. obs.) nature and pattern of coupling of mangrove forests to and is present and sometimes abundant elsewhere in adjacent open-water systems and should be consid- the Caribbean (Golley 1960, Heard 1982). In Tampa ered in models of decomposition and nutrient cycling. Bay, M. coffeus and M. bidatentus co-occur, although We report here on a 26 wk field experiment of man- the latter is more generally found in salt marshes grove leaf breakdown in which mangrove leaves were (Mook 1973). Other studies have indicated the impor- either tethered and thus exposed to Melampus coffeus tance of M. coffeus in leaf breakdown in SW Florida grazing, enclosed in individual small bags, or enclosed (McKee & Faulkner 2000) and have suggested that the with a group of leaves in larger mesh bags that snail may affect seedling distribution in mangrove excluded M. coffeus. We also conducted a caging forests by consuming Avicennia germinans (Smith et study in which litter and snails were removed from one al. 1989). Also, other invertebrates can play significant group and litter but not snails from the other and the roles in mangrove leaf litter breakdown (Poovachira- accumulation of leaf litter over 1 mo was tracked. The non et al. 1986). Crabs have been frequently reported hypothesis tested in the first experiment was that to relocate leaf litter from the forest floor to their bur- leaves enclosed within bags would receive less grazing rows in the Indo-Pacific (Macnae 1967, Van der Valk & and therefore degrade less rapidly than tethered Attwill 1984, Leh & Sasekumar 1985, Robertson 1986, leaves exposed to M. coffeus. The hypothesis evalu- Lee 1989, Robertson et al. 1992). The crabs then con- ated in the second associated experiment was that sume the leaves after allowing some time for microbial litter would accumulate more rapidly on sections of the growth. When leaves are buried under sediment with- forest floor that were fenced to eliminate grazing by M. out crab intervention, decomposition is much slower coffeus. We also collected litterfall during the caging (Holmer & Olsen 2002). Twilley et al. (1997) reported experiment and measured standing crop of litter in the that crabs were important in the removal of litter in forest over a 1.5 yr period. Data on mangrove forest some seasons in Ecuador. structure and M. coffeus population densities were Many ellobiid gastropods have a specialized gizzard also gathered. Grazing rates measured in the litterbag and stomach system that allows a high efficiency of experiment and snail density data were applied to the assimilation of plant matter consumed (Morton 1955). data on litterfall and standing crop in order to estimate Some molluscs also tend to have a diverse complement overall amounts of leaf degradation due to M. coffeus. of digestive enzymes, often including cellulases (Ma- The rate of snail movements around the forest were son 1974). However the digestive enzymes of Melam- determined in a mark–recapture study to provide pus coffeus have not been studied. M. coffeus prefer- information on snail movement and foraging behavior. entially aggregates to green leaves over yellow and brown ones (Proffitt et al. 1993, present study field observations). However, M. coffeus apparently MATERIALS AND METHODS requires more time to break through the tough outer cuticle of green leaves. Consequently, there is a lag Forest structure, litter standing crop, and litterfall. time before grazing effects are evident, whereas on The study was conducted in Boca Ciega Bay, part of yellow and brown leaves, grazing effects are seen the Tampa Bay estuary system, in the mixed species within hours of exposure (Proffitt et al. 1993). This snail mangrove forest at War Veterans Park, Pinellas Proffitt & Devlin: Gastropod grazing and leaf litter degradation 211 County, Florida (Fig. 1). Densities of canopy trees, their heights and diameters at breast height (DBH, mea- sured at about 1.3 m above ground) were determined in 3 × 3 m plots, at stations situated every 10 m along a 130 m long transect extending from shore (0 m) to the upland edge (130 m). Leaf litter standing crop was collected at stations located 10, 50, and 120 m from shore in 5 replicate 30× 30 cm quadrats 4 times over a year in 1993.
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