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Mouthpart and Digestive Tract Structure in Four Talitrid Amphipods from a Translittoral Series in Tasmania Ð O P Matthew D

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Mouthpart and Digestive Tract Structure in Four Talitrid Amphipods from a Translittoral Series in Tasmania Ð O P Matthew D J. Mar. Biol. Ass. U.K. (2004), 84, 717^726 Printed in the United Kingdom Mouthpart and digestive tract structure in four talitrid amphipods from a translittoral series in Tasmania Ð O P Matthew D. Johnston* , Danielle J. Johnston and Alastair M.M. Richardson *School of Aquaculture, University of Tasmania, Locked Bag 1-370 Launceston, TAS. 7250, Australia. O Department of Fisheries, Western Australian Marine Research Laboratories, GPO Box 20 North Beach, WA. 6020, Australia. P School of Zoology,Ð University of Tasmania, GPO Box 252C Hobart, TAS. 7001, Australia. Corresponding author, e-mail: [email protected] Structural adaptations of the mouthparts and digestive tract of four talitrid amphipods were examined in relation to diet, habitat and phylogeny.The species di¡ered in their habitat relative to the shoreline and also in their diet: a 5-dentate ‘sandrunner’, Talorchestia species II (a mid to low shore intertidal diatom feeder), a 5-dentate sandhopper, Talorchestia marmorata (a strandline kelp feeder); a 4-dentate sandhopper, Talorchestia species I (extreme high shore, feeding on spinifex grasses), and a 4-dentate landhopper, Keratroides vulgaris (forest leaf litter, litter feeding). Gross structural characteristics of the mouthparts were similar among all threeTalorchestia species re£ecting their phylogenetic relatedness. Increased setation and minor structural di¡erences among the Talorchestia species could be attributed to dietary di¡erences, re£ecting the zones across the shoreline that they inhabit. Mouthparts of K. vulgaris were elongate, with markedly di¡erent setation to the Talorchestia species, re£ecting its more distant phylogenetic position and its diet of decaying leaf litter. Digestive tract structure was more conserved among all species due to their phylogenetic relatedness. The gross digestive structure conformed to the general plan exhibited by most gammaridean amphipods. However, an additional pair of lateral pyloric caeca was evident in all species, the function of which is uncertain. INTRODUCTION genus Talorchestia by Morino & Miyamoto (1998) techni- cally excludes the three species used here from the genus, Amphipods inhabit a diverse range of aquatic and terres- but since no other generic name is available we have used trial habitats. They are most abundant and diverse in Talorchestia in this work. Taxonomic work in progress marine and freshwater environments, but they also extend (Richardson, unpublished data) suggests that one of these across intertidal zones to cryptozoic habitats in the leaf species will be placed in a separate genus (see below). litter of forests, woodlands and grassland. Talitrid amphi- Closest to the sea at Fortescue Bay can be found an pods (Amphipoda: Talitridae) are unique among the order undescribed 5-dentate species of sandhopper (Bous¢eld, Amphipoda as they are the only family to have successfully 1984), Ta l o r c h e s t i a species II that emerges onto the wet made the transition onto land, and they are also more sand to forage and feed mainly on surf diatoms. At the generally accepted as a trans-littoral family: having repre- zone of seaweed and kelp deposition at the mean high sentatives at all levels of the intertidal zone, in fully terres- water mark another 5-dentate sandhopper (Bous¢eld, trial habitats and in freshwaters (Richardson & Swain, 1984), Talorchestia marmorata (Haswell), is abundant in and 2000).They are therefore a valuable group for investigating around piles of cast kelp. At the very highest levels on the evolutionary changes in their mouthparts and digestive shore an undescribed 4-dentate sandhopper (Bous¢eld, tract associated with the colonization of land. 1984), Talorchestia species I, emerges on calm dewy The sandy beaches of Tasmania comprise a substantial evenings to forage and feed on high strandline plants. proportion of the coastline, including beaches of various Immediately inland in closed eucalypt forest, Keratroides degrees of exposure, which subside to a range of native vulgaris (Friend), a common talitrid landhopper, feeds vegetation types inland, ranging from dry grasslands to upon decayed forest leaf litter (Morton & Richardson, wet eucalypt forests and temperate rainforest. Shepherd 1984). This ecological series of four talitrid amphipods (1994) described the distribution of three species of sand- represents four stages of increasing terrestrial adaptation, hopper at Fortescue Bay, a moderately exposed sandy but it is important to stress that these particular talitrid beach in south-east Tasmania and detailed their stomach species are not from a single evolutionary lineage, and contents. The taxonomy of the Australian sandhoppers that sandy shores are unlikely to have been the route and beach£eas is poorly known (Bous¢eld, 1982), and no which talitrids used to colonize land (Richardson et al., sandhoppers have been described since Haswell (1885), 1991; Richardson & Swain, 2000). Phylogenetic relation- despite the presence of a diverse fauna (Richardson, ships within the Talitridae are not yet clearly understood, 1996). Two of the three sandhoppers at Fortescue Bay are but the shared possession of a 5-dentate (Bous¢eld, 1984) undescribed, while the other can be referred to as left lacinia mobilis on the mandibles of Talorchestia species Talorchestia marmorata (Haswell). The rede¢nition of the II and T. marmorata suggest that they are more closely Journal of the Marine Biological Association of the United Kingdom (2004) 718 M.D. Johnston et al. Mouthpart and digestive structure of four talitrid amphipods related to each other than toTalorchestia species I. All three 1984) and mercuric bromophenol blue (Chapman, 1975) Talorchestia species are phylogenetically closer to each other to determine the structure of the digestive tract and the than to the landhopper K. vulgaris, since landhoppers are location of proteins, respectively. thought to have arisen from beach£ea-like ancestors, not sandhoppers (Bous¢eld, 1984). RESULTS Among the various challenges for talitrid amphipods as they colonized the intertidal zone and terrestrial forests Structure of the mouthparts was the necessity to alter their diet according to the avail- Position in situ ability of food items in these habitats. The diets of the four At rest, the in situ positions of the mouthparts are talitrid species examined in this study are substantially similar among all species examined. The opening to the di¡erent. Specialized structures of the mouthparts and oesophagus is situated ventrally, and is bounded anteriorly digestive tract of amphipods have commonly been by the upper lip, posteriorly by the lower lip, and laterally explained as adaptations to the physical and chemical by the mandibles. The ¢rst and second maxillae are situ- characteristics of their diet. Although a considerable ated a considerable distance behind the opening of the amount of evidence is available in the amphipod literature oesophagus, and are £exed toward the centre of the to support this link (Agrawal, 1964; Icely & Nott, 1984) mouth. The maxillipeds are positioned behind the second many authors have failed to recognize that morphological maxillae, with both left and right palps completely di¡erences of the mouthparts and digestive tract may also opposed at rest (Figure 1A). be attributed to a species’ phylogenetic history (Keith, 1974). Few studies have provided evidence to separate the Description of setal types in£uences of phylogeny and diet on the mouthparts and In an e¡ort to standardize setal terminology, setal digestive tract (Kunze & Anderson, 1979; Coelho & classi¢cation in this study has been based on that of Rodrigues, 2001a,b). This study will identify structural Watling (1989) as a consistent setal classi¢cation system di¡erences of the mouthparts and digestive tract structure of Amphipoda is lacking. between four species of talitrid amphipod, and interpret these structural di¡erences in terms of their diet, habitat Maxilliped and phylogeny. It will also help to understand the degree The distal margin of the maxilliped inner plate of all to which structures associated with the mouthparts, which species bears 3^7 calci¢ed apical spine teeth. The three are often used in taxonomic and phylogenetic studies, are apical spine teeth of Keratroides vulgaris are the largest of likely to be modi¢ed by diet. the four species, but are blunted distally (Figure 1B). The three apical spine teeth of Talorchestia marmorata and MATERIALS AND METHODS Talorchestia species I are similar in size, however, Talorchestia species II has seven smaller teeth, which form Collection two distinct rows across the distal margin (Figure 1C). Talorchestia species II and T. marmorata (N¼20) were The maxilliped outer plate of all threeTalorchestia species collected using an aspirator at low tide at the lower and is broad and distally rounded, whereas the outer plate of strandline zones of the sandy shore at Binalong Bay on K. vulgaris is narrow, and tapers distally, giving rise to two Tasmania’s east coast, 3^4 hours after sunset. Talorchestia branching elongated simple setae. The outer plate setal species I (N¼20) was hand collected from spinifex arrangement of Talorchestia species I, Talorchestia species II grasses on the fore-dunes at Fortescue Bay on calm dewy and T. marmorata is similar, with both dorsal margins evenings, and Keratroides vulgaris (N¼20) was collected using bearing a single row of short simple setae and simple petal an aspirator, during the day at Lilydale Falls Reserve. setae. The
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