Trophic Behaviour and Functional Morphology of the Feeding Appendages of the Laomediid Shrimp Axianassa Australis (Crustacea: De
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J. Mar. Biol. Ass. U. K. 2001), 81,441^454 Printed in the United Kingdom Trophic behaviour and functional morphology of the feeding appendages of the laomediid shrimp Axianassa australis Crustacea: Decapoda: Thalassinidea) Vaª nia Rodrigues Coelho* and Se¨ rgio de Almeida RodriguesO *Departamento de Zoologia, Instituto de Biocieª ncias, Universidade de Sa¬ o Paulo, CP 11461, CEP 05422-970, Sa¬ o Paulo, SP, Brazil. Present address: Columbia University, Biosphere 2 Center, 32540 Biosphere Road, Oracle, AZ, 85623, USA. ODepartamento de Ecologia Geral, Instituto de Biocieª ncias, Universidade de Sa¬ o Paulo, CP 11461, CEP 05422-970, Sa¬ o Paulo, SP, Brazil. *E-mail: [email protected] The trophic behaviour, stomach contents, and morphology of the feeding appendages, with emphasis on setae, of a species of Laomediidae, Axianassa australis Crustacea: Decapoda: Thalassinidea), were investi- gated. This species is a deposit feeder. The 32 described setal types were clustered in four main categories: plumed, serrate, plumodenticulate and simple. By examining the setae and spatial position of the segments of the appendages, it is possible to infer that the main function of the 1st and 2nd pereiopods, the 3rd pair of maxillipeds, as well as the dactylus, propodus, carpus and merus of the 2nd maxilliped, is to brush particles. The ischium, basis and coxa of the 2nd maxilliped appear to be specialized for particle retention. For the remaining mouthparts, brushing is generally the main function of the basal endites, while the coxal endites retain particles. Patterns of morphological adaptations to feeding habits are proposed for the Thalassinidea based on a review of the literature. Setal diversity, ratio of plumodenticulate to serrate setal types and mandible morphology are linked to ecological adaptations to trophic modes. Conversely, the presence and degree of development of the crista dentata appear to be related to phylogenetic heritage rather than to feeding mechanisms. Stomach contents are also indicative of trophic modes used by the species; while the predominance of small particles can indicate either ¢lter or deposit feeding, stomach contents with high quantities of large particles suggest deposit feeding as the exclusive trophic mechanism. INTRODUCTION scarcity of knowledge on the feeding mechanisms of species of this clan. In the present study, the trophic behaviour, stomach Thalassinidean shrimp are commonly found living in contents, and morphology of the feeding appendages, burrows excavated in sandy or muddy substrates in in- with emphasis on setae, of a species of Laomediidae, tertidal and shallow subtidal areas Dworschak, 1987a; Axianassa australis Rodrigues & Shimizu, 1992, are Swinbanks & Luternauer, 1987; Dworschak & Pervesler, analysed. The results are compared with other thalas- 1988; Gri¤s & Chavez, 1988; Lemaitre & Rodrigues, sinidean species Nickell et al., 1998; Stamhuis et al., 1991). Despite the cosmopolitan nature of the group and 1998; Pinn et al., 1999a; Coelho et al., 2000b; Coelho & its abundance in benthic communities, there is a paucity Rodrigues, in press), and patterns of morphological of information on the trophic behaviour of these adaptations to di¡erent feeding strategies are proposed. crustaceans. The few studies available deal mainly with Callianassidae or Upogebiidae species MacGinitie, 1930, 1934; Pohl, 1946; Devine, 1966; Rodrigues, 1966; MATERIALS AND METHODS Dworschak, 1987b; Scott et al., 1988; Nickell & Atkinson, 1995; Coelho et al., 2000a,b; Coelho & Rodrigues, in Specimens of Axianassa australis were collected with a press), while the feeding habits of other families have yabby pump at Praia do Arac° a¨ ,Sa¬ o Sebastia¬ o, SP, Brazil. remained obscure. In contrast, information on thalassini- A map and detailed information on the study site can be dean burrow morphology has accumulated in the litera- found in Dworschak & Rodrigues 1997). The substrate in ture MacGinitie, 1930; Frey & Howard, 1975; Ott et al., which the burrows of A. australis were found consist of 1976; Pemberton et al., 1976; Swinbanks & Murray, 1981; muddy siliciclastic sediments on the surface and Dworschak, 1983, 1987b; Nash et al., 1984; Scott et al., compacted shells at 30^40 cm depth Dworschak & 1988; Atkinson & Nash, 1990; Dworschak & Ott, 1993; Rodrigues, 1997). Nickell & Atkinson, 1995; Ziebis et al., 1996; Astall et al., Live animals were transported to the laboratory and 1997; Dworschak & Rodrigues, 1997; Bird & Poore, 1999; kept in aquaria for feeding behaviour observations from Coelho et al., 2000a), and some models relating trophic September to December 1996. Nine specimens of modes with burrow architecture have been proposed A. australis were placed in aquaria similar to the one Gri¤s & Suchanek, 1991; Nickell & Atkinson, 1995). The described by Rodrigues & Ho« dl, 1990) ¢lled with validity of such models, however, is compromised by the sediment from the collection site. The aquaria were Journal of the Marine Biological Association of the United Kingdom 2001) 442 V.R. Coelho and S. de A. Rodrigues Functional morphology in Axianassa maintained with fresh running seawater pumped from the nearby bay, at ambient temperature. The animals were fed every two days with a mixture of ¢ne sediment and commercial ¢sh food. Five shrimp were ¢xed in 70% alcohol immediately after capture. In the laboratory, these animals were dissected under a light microscope for observations of feeding appendages and stomach contents. The 1st and 2nd pairs of pereiopods and the mouthparts of three individuals were prepared for SEM analysis following the procedures of Felgenhauer 1987). The appendages were also submitted to treatments for removal of mucus, debris and epibionts Felgenhauer, 1987). The material was then critical-point dried, placed on stubs, sputter-coated with gold-palladium and analysed on the SEM Stereoscan 440, Amray 1810, DSM940 Figure 1. View of the general stomach content of Axianassa Zeiss). The stubs examined in the present study are australis. Scale bar: 100 mm. deposited at the National Museum of Natural History, Smithsonian Institution, Washington, DC 12 stubs, USNM 279044). Setal types The mode of articulation of the setal shaft was not Setal classi¢cation always visible due to the amount of di¡erent setal layers. In the majority of the setae where this feature was The setal types were distinguished according to the observed the socket was infracuticular exceptions are classi¢cation system proposed by Farmer 1974). This mentioned in the descriptions).The approximate measure- system is apparently the most appropriate for categorizing ment of the insertion angle of the setule was noted when setae in studies of feeding mechanisms Coelho et al., considered important in description of the setae i.e. in 2000b). The types were clustered in four main categories: distinguishing one setal type from another). Annulations plumed, serrate, plumodenticulate and simple. Descrip- and pores are reported only when conspicuously present. tions are provided for the external morphology of Long setules bear small spines distributed in an each type of setae, in addition to drawings and photos alternating pattern exceptions are mentioned in the illustrating the main characteristics. These types were descriptions). Setal size corresponds to the approximate identi¢ed by a letter representing the major group in maximum length recorded it can be found between which they are included, and a number Factor, 1978). parenthesis, after the description of the setal type). In the The terminology used in the descriptions follows Watling descriptions, some ¢gures may illustrate characteristics 1989). found in several kinds of seta. Although such ¢gures may correspond to a di¡erent setal type than the one described, the feature being illustrated is shared by both setal types. Descriptions of the setae are given below. RESULTS Feeding behaviour Group A: plumed setae Figure 2); setae bearing only setules on shaft. In the aquarium, Axianassa australis was only observed to Type A1. Pappose setae, with setules loosely arranged deposit feed. No suspension feeding, by ¢ltering or resus- Figure 3A) in an irregular pattern around shaft pending particles, was recorded. Tofeed, the shrimp make 600 mm). Type A2. Plumose setae, with two rows of inward lateral movements with the 2nd pair of pereiopods, setules inserted almost opposite one another 1208)on brushing particles from the burrow £oor during this shaft. This type has a supracuticular socket 936 mm) process. These particles are accumulated in front of the Figure 3B). Type A3. Setae with two dense rows of mouthparts, creating a sediment pile that is laterally smooth setules on one side and setules irregularly distrib- supported by the 1st pair of pereiopods. Next, the 3rd uted on other side of shaft 480 mm) Figure 3C).Type A4. pair of maxillipeds brushes the sediment toward the 2nd Setae with short serrate setules irregularly distributed maxillipeds, either by making inward lateral movements along the distal half of shaft 3 mm) Figure 3D. or stretching the appendages forward and then folding them back. The 2nd pair of maxillipeds collects and trans- ports the particles toward the mouth. During the process of particle handling by the 1st maxillipeds and maxillae, a cloud of ¢ne particles is expelled laterally. Stomach contents The stomach content of the specimens was composed of small sediment particles and detritus Figure 1). The size Figure 2. Types of plumed setae found in Axianassa australis range