Trophic Behaviour and Functional Morphology of the Feeding Appendages of the Laomediid Shrimp Axianassa Australis (Crustacea: De

Home , Callianassa subterranea, Callianassidae, Upogebia africana, Upogebiidae

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 of the particles was from 1 to 220 mm. setaeinlateralview).R,rows).

Journal of the Marine Biological Association of the United Kingdom 2001) Functional morphology in Axianassa V.R. Coelho and S. de A. Rodrigues 443

Figure 3. Setal types found in Axianassa australis. A) Setules loosely arranged in irregular pattern around proximal half of shaft of a seta of type C1; B) two rows of setules inserted almost opposite one another 1208) on shaft of a seta of type A2; C) two dense rows of smooth setules on one side and setules irregularly distributed on other side of shaft of a seta of type A3; D), serrate setules irregularly distributed on distal half of shaft of a seta of type A4; E) two rows of denticles on distal half of shaft of a seta of type B1; F) two rows of denticles on one side and one row of denticles on other side of middle one-third of shaft of a seta of type B2.

Group B: serrate setae Figure 4); setae bearing only denticles rows of denticles on distal one-third of shaft 600 mm). on shaft. Type B8. Setae with two rows of small denticles on prox- Type B1. Setae with two rows of denticles on distal half imal half and two rows of denticles on distal half of shaft of shaft 1.7 mm) Figure 3E). Type B2. Setae with two 1.4 mm) Figure 5C). Type B9. Setae with many rows of rows of denticles on one side and one row of denticles on small denticles on tip of shaft. This type appears to have a other side of middle one-third of shaft. Distal one-third of sub-apical pore 176 mm) Figure 5D,E). Type B10. Setae shaft bearing only two rows of denticles. This type has an with many rows of tiny denticles along the shaft 1.3 mm) annulus in the proximal one-third region of shaft Figure 5F).Type B11. Setae bearing two rows of denticles, 640 mm) Figure 3F). Type B3. Setae with a thick shaft strong and curved proximally and smaller near tip, on bearing two rows of denticles on the distal two-thirds of distal half of shaft 75 mm) Figure 6A&E). Type B12. shaft 350 mm). Type B4. Setae bearing two rows of denti- Similar to B11, but with eight rows of small denticles on cles on one side and two rows of denticles on other side of other side of distal half of shaft. Near tip with two rows of shaft. This type has an annulus in the proximal region of denticles only. Shaft has an annulus in its middle region shaft 82 mm). Type B5. Setae with one row of triangular- 180 mm) Figure 6B,C). Type B13. Setae with two rows of shaped denticles distally and two rows of smaller denticles strong curved denticles on distal half of shaft. Near tip the proximally, on distal half of shaft. Tip is curved 262 mm) shaft rami¢es in two branches curved upwards and Figure 5A). Type B6. Setae with two rows of denticles on tapering to tip. Tip with two rows of smaller denticles one side and two rows of small denticles on other side of 90 mm) Figure 6D,E). Type B14. Setae with a conical- third-quarter of shaft. Distal quarter of shaft with only shaped shaft bearing two rows of denticles. Shaft has an two rows of denticles 658 mm) Figure 5B). Type B7. annulus in its proximal region 55 mm) Figure 6F). Type Setae with two rows of small denticles on proximal one- B15. Similar to B14 but with one row of wide denticles. This third, two rows of denticles on one side and four rows of type has an apical pore. Shaft has annulus in its proximal small denticles on other side of middle one-third and two region 59 mm) Figure 7A,B).

Journal of the Marine Biological Association of the United Kingdom 2001) 444 V.R. Coelho and S. de A. Rodrigues Functional morphology in Axianassa

Figure 5. Setal types found in Axianassa australis cont.). A) Triangular-shaped denticles on distal part of shaft of setae of type B5; B) two rows of denticles on one side and two rows of small denticles on other side of third-quarter of shaft of a seta of type B6; C) tworowsofsmalldenticlesonproximalhalfofasetaoftypeB8;D)rowsofsmalldenticlesontipofshaftofasetaoftypeB9;E) detail arrow) of sub-apical pore ?) of a seta of type B9; F) rows of tiny denticles on shaft of a seta of type B10.

Group C: plumodenticulate setae Figure 8); setae bearing setules and denticles on shaft. Type C1. Setae with setules loosely arranged around shaft in an irregular pattern. Tip bearing two rows of denticles 260 mm) Figures 3A & 7C). Type C2. Setae with setules densely inserted at an angle of approximately 40 degrees. Tip with two rows of denticles 65 mm) Figure 7D). Type C3. Setae with setules densely inserted at an angle of approximately 408 on proximal two-thirds of shaft. The distal one-third with two rows of denticles. Tip is curved 62 mm). Type C4. Setae with setules loosely arranged around proximal two-thirds of shaft in an irregular pattern. The distal one-third with two rows of denticles 193 mm). Type C5. Setae with two rows of short setules on proximal two-thirds of shaft. The distal one-third with two rows of denticles 650 mm).Type C6. Setae with setules loosely arranged around proximal half of shaft. The distal half with two rows of denticles on one side and one row of setules on other side of shaft 246 mm) Figure 7E). Type C7. Setae with setules loosely arranged around proximal half of shaft in an irregular pattern. The distal half with Figure 4. Types of serrate setae found in Axianassa australis two rows of denticles 160 mm).TypeC8. Similar to C7, but setaeinlateralview).R,rows).

Journal of the Marine Biological Association of the United Kingdom 2001) Functional morphology in Axianassa V.R. Coelho and S. de A. Rodrigues 445

Figure 6. Setal types found in Axianassa australis cont.). A) Two rows of denticles, strong and curved proximally and smaller near tip, on distal half of shaft of a seta of type B11; B) two rows of strong and curved denticles on one side, and rows of small denticles on the other side of distal half of shaft of setae of type B12, near tip with only two rows of denticles; C) detail of the eight rows of small denticles present on distal half of shaft of a seta of type B12; D) setae of type B13, these setae have two rows of strong curved denticles on distal half of shaft, near tip the shaft rami¢es in two branches curved upwards and tapering to tip, tip has two rows of smaller denticles; E) seta of type B13, on left side, and of type B11, on right side of picture; F) setae of type B14, these setae have a conical-shaped shaft bearing two rows of denticles, the shaft has an annulus in its proximal region. with a curved tip 67 mm) Figure 7F). Type C9. Setae terms medial and lateral refer to surfaces directed with setules loosely arranged around proximal half of toward and away from the median line of the body, shaft in an irregular pattern. The third-quarter of shaft respectively. For the mouthparts, the terms inner and with two rows of denticles. Curved tip with many rows of outer describe features directed toward and away from small denticles 293 mm). Type C10. Setae with setules the mouth, respectively; medial and lateral correspond to loosely arranged around proximal one-third of shaft. The the surfaces toward and away from the median line of the distal two-thirds bearing two rows of denticles. Curved tip body Factor, 1978). Usually surfaces directed toward the with many rows of small denticles 267 mm) Figure 9A). midline of the body have setae curved toward the mouth, dense setal clustering, and many layers of setae, as in Group D: simple setae Figure 10); setae bearing no setules or upogebiids and callianassids Coelho et al., 2000b; denticles on shaft. Coelho & Rodrigues, in press). Each layer consists of a Type D1. Setae with a smooth straight shaft 280 mm). set of only one type of seta, and may or may not be Type D2. Setae with a smooth shaft presenting a structure followed by other layers of di¡erent setal types. When a similar to a sucking disk on tip 200 mm) Figure 9B,C). sequence of layers is mentioned in the descriptions, the Type D3. Setae with a smooth, slightly curved, conical- ¢rst is the most external one. Density of setae on the shaped shaft. This type has an annulus in the proximal appendages is illustrated in Figures 11^15. one-third region of shaft 90 mm) Figure 9D). Second pereiopods Figures 11 & 15) Second pereiopods slender, bearing serrate setae. Description of appendages Ischium with setae of type B6 on ventral margin. Merus The ¢rst and second pereiopods and the mouthparts with setae of type B1 on ventral margin, and of type B8 are the appendages directly involved in the feeding on medial and lateral surfaces. Carpus and propodus behaviour of A. australis. The morphology of these with setae of type B1 on ventral edge, B8 on medial and appendages, with emphasis on setal distribution, is lateral surfaces, and B10 on dorsal margin. Dactylus described below. In descriptions of the pereiopods the bearing setae of type B1 and a row of spines on ventral

Journal of the Marine Biological Association of the United Kingdom 2001) 446 V.R. Coelho and S. de A. Rodrigues Functional morphology in Axianassa

Figure 7. Setal types found in Axianassa australis cont.). A) Setae of type B15, these setae have a conical-shaped shaft bearing one row of wide denticles, the shaft has an annulus in its proximal region; B) arrow indicates apical pore in a seta of type B15; C) two rows of denticles on tip of the shaft of a seta of type C1; D) setules densely inserted at an angle of approximately 408 on shaft of setae of type C2; E) two rows of denticles on one side and one row of setules on other side of distal half of a shaft of a seta of type C6;F)tworowsofdenticlesondistalhalfofshaftofsetaeoftypeC8,thetipoftheshaftiscurved.

margin, setae of type B8 on medial and lateral surfaces, setae of type B9, B8 and B10, respectively on proximal, median and distal surface of dorsal margin.

First pereiopods Figure 11) First pereiopods robust, bearing serrate setae. Ischium with setae of type B7 and three or more spines on ventral edge. Merus with setae of type B7 on ventral margin. Carpus and propodus with setae of type B7 on ventral edge and of type B10 on dorsal margin. Fixed ¢nger and dactylus with row of spines on prehensile edges, and setae of type B10 on lateral surface, dorsal edge, medial surface and ventral margin.

Third maxillipeds Figures 12 & 15) Third maxillipeds bearing serrate setae. Endopod ¢ve- segmented, podobranch, no exopod. Basis with one or two spines on lateral surface. Ischium with crista dentata with 14 strong teeth on inner surface, bearing setae of type B6 from medial margin to lower inner surface, and of type B2 on lateral edge. Merus with setae of type B6 on proximal half and two setal layers, types B12 and B1, on distal half of Figure 8. Types of plumodenticulate setae found in Axianassa medial margin to lower inner surface, lateral edge with australis setae in lateral view). R, rows). setae of type B2. Carpus bearing setae of types B8 and

Journal of the Marine Biological Association of the United Kingdom 2001) Functional morphology in Axianassa V.R. Coelho and S. de A. Rodrigues 447

Figure 9. Setal types found in Axianassa australis cont.). A) detail of curved tip with many rows of small denticles on shaft of a seta of type C10; B) smooth shaft with a structure similar to a sucking disk on tip of setae of type D2; C) detail of tip of shaft of a seta of type D2; D) smooth, slightly curved, conical-shaped shaft of a seta of type D3.

Figure 10. Types of simple setae found in Axianassa australis.

Figure 12. Setaldistributionanddensityon3rdand2nd maxillipeds of Axianassa australis.Drawingsmodi¢edfrom Rodrigues & Shimizu 1992). Setal density represented by following symbols: &,verydense;&,dense;and*, sparse. L, layer. Scale bar: 2 mm.

Figure 11. Setal distribution and density on 2nd and 1st B11on medial margin to inner surface. Propodus with four pereiopods of Axianassa australis. Drawings modi¢ed from setal layers, types B8, B13, B11, B1, on medial edge to inner Rodrigues & Shimizu 1992). Setal density represented by surface. Dactylus with setae of type B1 on medial margin following symbols: &,dense;and*,sparse.L,layer. to lower inner surface and on lateral edge sparse on this Scale bar: 2 mm. edge).

Journal of the Marine Biological Association of the United Kingdom 2001) 448 V.R. Coelho and S. de A. Rodrigues Functional morphology in Axianassa

Figure 14. Setal distribution and density on 1st maxilla and mandible of Axianassa australis. Drawings modi¢ed from Rodrigues & Shimizu 1992). Setal density represented by following symbols: &, very dense; &,dense;and*,sparse.L, layer. Scale bar: 0.5 mm.

Figure 13. Setal distribution and density on 1st maxilliped endite with four layers of setae, types C1, C10, B5 and B1, and 2nd maxilla of Axianassa australis.Drawingsmodi¢edfrom from outer surface, through medial margin to upper inner Rodrigues & Shimizu 1992). Setal density represented by surface, and plumodenticulate setae, type C1, on tip. following symbols: &, very dense; &,dense;and*, sparse. L, Endopod with plumodenticulate setae, type C4, on layer. Scale bar: 1 mm. medial and lateral edges, tip with plumed setae, type A2. Exopod with plumodenticulate setae, type C4, on medial Second maxillipeds Figure 12) margin, and plumed setae, type A2, on tip of £agellum Endopod ¢ve-segmented, exopod with segmented and lateral edge. £agellum, epipod and podobranch. Coxa and basis fused. Coxa, basis and ischium bearing two layers of setae, types Second maxillae Figures 13 & 15) C4 and A1, from lower outer surface, through medial Coxal and basal endites bilobed, endopod slender and margin to lower inner surface. Merus with two layers of scaphognathite exopod) large. Proximal lobe of coxal setae, types B7 and C5, on medial margin to lower inner endite with two layers of setae, types C6 and A1, on prox- surface, and serrate setae, type B2, on distal part of lateral imal one-third and plumodenticulate setae, types C6 and edge. Carpus with plumodenticulate setae, type C7, on C1, on distal two-thirds of lower outer surface, through distal part of medial margin through inner surface to medial margin to upper inner surface. Distal lobe of distal part of lateral edge. Propodus with serrate setae, coxal endite with plumodenticulate setae, type C7, from type B8 on medial margin and distal part of outer lower outer surface to medial margin. Proximal lobe of surface, and type B1 on lateral edge. Dactylus with serrate basal endite with four layers of setae, types C7, C9, D1, setae, type B8 on lateral and medial margins, outer C7, from lower outer surface to medial edge. Distal lobe surface and distal part of inner surface, and type B3 on of basal endite with plumodenticulate setae, type C7, tip. Endopod with two layers of setae, types C1 and A2, on distal part, and four layers of setae, types C7, C9, on medial margin, and serrate setae, type B1 on distal D2, B1, on the remainder of lower outer surface to part of lateral edge. Flagellum segmented, with plumed medial margin. Endopod with plumodenticulate setae, setae, type A1, on distal part. type C1, on medial and lateral margins. Scaphognathite with plumed setae, type A2 on lateral margin and type First maxillipeds Figure 13) A4 on ventral edge. Coxal and basal endites prominent, endopod elongate, exopod with segmented £agellum. Coxal endite with First maxillae Figure 14) three layers of setae C4, A1 and C4, from outer surface, Coxal and basal endites unilobed, endopod slender and through medial margin to upper inner surface. Basal subdivided. Coxal endite with two layers of setae, types C7

Journal of the Marine Biological Association of the United Kingdom 2001) Functional morphology in Axianassa V.R. Coelho and S. de A. Rodrigues 449

Figure 15. Axianassa australis. A) Sparse s) and dense d) setae on the second pereiopod; B) detail of the row of spines on ventral margin of the dactylus of the second pereiopod; C) crista dentata on inner surface of ischium of third maxilliped; D) sparse s), dense d) and very dense vd) setae on the second maxilla; E) outerl view of mandible; F) inner view of mandible showing molar process. and A3, from upper outer surface to medial margin, and lobes, not very setose, present on the initial part of the plumodenticulate setae, type C1, on tip. Basal endite with oesophagus. The setae present on the paragnaths were plumodenticulate setae, type C4, on medial and lateral not analysed. margins, simple setae, type D3, on distal part of medial edge, and with serrate setae, types B4, B14, B15, B2, on proximal three-¢fths, type B3, on fourth-¢fth, and plumo- DISCUSSION denticulate setae, type C4, on distal one-¢fth of upper Previous studies on feeding mechanisms of thalas- outer surface to tip. Endopod with plumodenticulate sinideans have focused primarily on callianassids and setae, type C7, on distalmost area of proximal segment. upogebiids MacGinitie, 1930, 1934; Pohl, 1946; Devine, 1966; Rodrigues, 1966; Dworschak, 1987b; Scott et al., Mandible Figures 14 &15) 1988; Nickell & Atkinson, 1995; Coelho et al., 2000a,b; Palp three-segmented, incisor process with strong teeth Coelho & Rodrigues, in press). There is information on and molar process with row of tubercles. Palp bearing the trophic behaviour of only one other species of plumodenticulate setae, type C4, on outer surface of prox- Laomediidae, Jaxea nocturna Nardo Nickell & Atkinson, imal segment, and type C1, on outer and inner surfaces of 1995). The latter species is a deposit feeder, as Axianassa median segment. Distal segment with setae of type C1 on australis. However, unlike A. australis, the deposit feeding proximal one-¢fth, type C8 on second-¢fth, three layers, mechanism of J. nocturna involves resuspension of particles types C8, C3 and C2, on third and fourth-¢fth, and three Nickell & Atkinson, 1995). Jaxea nocturna uses the 2nd layers, types C8, C3 and D3, on distal one-¢fth of upper pereiopods to resuspend the sediment, the 3rd pair of outer surface to lateral margin. maxillipeds collects the particles in suspension and transfer them to the 2nd pair of maxillipeds. Nickell & Labrum and paragnaths Atkinson 1995) occasionally observed the 3rd maxillipeds Labrum triangular-shaped, located in the upper part to collect sediment directly from the burrow £oor as well. of the mouth. The paragnaths comprise two rounded In A. australis the sediment is accumulated by the 2nd

Journal of the Marine Biological Association of the United Kingdom 2001) 450 V.R. Coelho and S. de A. Rodrigues Functional morphology in Axianassa

Table 1. Main functions proposed for the feeding appendages of Axianassa australis, according to the spatial position of the appendage segments and the predominance of major setal categories.

Function Appendage segment Major setal category

Brushing Dactylus, propodus, carpusa,b,c,merus*,a,c and ischium*,a Serrate of 2nd pereiopod Dactylus, ¢xed ¢ngera,b,c,d, propodus, carpusa,b,merus* Serrate and ischium*,a of 1st pereiopod Dactyluse,f, propodus, carpuse,g, merus* and ischiume,f Serrate of 3rd maxilliped Dactyluse,f,g,h, propoduse,f, carpuse,f,g,merus*,e of 2nd Serrate, plumodenticulate maxilliped Basal endites* of 1st maxillipede,h Serrate, plumodenticulate Basal endites* of 2nd maxillae Serrate, plumodenticulate, simple, Basal endites* of 1st maxillai Serrate, plumodenticulate, simple Distal segment of mandibular palpf Plumodenticulate, simple Retention Ischium, coxa and basis of 2nd maxillipede Plumodenticulate, plumed Coxal endites of 1st maxillipede,h Plumodenticulate, plumed Proximal lobe of coxal endite* of 2nd maxillae Plumodenticulate, plumed Coxalendites*of1stmaxillae Plumodenticulate, plumed Brushing and retention Endopod of 1st maxillipede Plumodenticulate Distal lobe of coxal endite* of 2nd maxillae Plumodenticulate Basal endite* of 1st maxillae Plumodenticulate Sealing Endopod of 2nd maxillipede Plumodenticulate, plumed Endopod of 1st maxillipedf Plumodenticulate, plumed Exopod of 1st maxillipede Plumodenticulate Endopod of 2nd maxillae,f Plumodenticulate Basal endite* of 1st maxillaf Plumodenticulate Proximalh and mediang,h segment of mandibular palp Plumodenticulate Production of a water £ow Flagellum of 2nd maxillipedi Plumed Exopodf and £agellumi of 1st maxilliped Plumed Scaphognathitef Plumed

*, parts of appendages with a concave shape; a, ventral margin; b, dorsal margin; c, medial surface; d, lateral surface; e, medial margin; f, lateral margin; g, inner surface; h, outer surface; i,tip.

Table 2. Comparison among the setal types found in Upogebia omissa, Pomatogebia operculata, Callichirus major, Sergio mirim and Axianassa australis.

Species

Upogebiidae Callianassidae Laomediidae

Setal category Upogebia omissaa Pomatogebia operculataa Callichirus majorb Sergio mirimb Axianassa australisc

Plumed %) 14 37) 12 39) 5 10) 3 8) 4 13) Serrate %) 9 24) 4 13) 10 19) 5 13) 15 47) Plumodenticulate %) 15 39) 15 48) 35 67) 30 77) 10 31) Simple %) ^^2 4) 1 2) 3 9) Total %) 38 100) 31 100) 52 100) 39 100) 32 100) a, Coelho et al. 2000b); b, Coelho & Rodrigues in press); c, present study. pereiopods in front of the 3rd maxillipeds, which brush content of the latter species, suggesting that carnivory or the particles toward the 2nd maxillipeds. scavenging are not among its trophic mechanisms. The stomach content of A. australis suggests that this Conversely, we cannot be sure A. australis does not use species does not feed on plant matter, consistent with the other feeding behaviours since only one type of food was fact that no sea grasses or macroalgae have been found o¡ered to the specimens in aquaria. near or inside its burrows Dworschak & Rodrigues, The main function of the appendages have been 1997). Although alpheid shrimp are known to live described for some species of thalassinidean shrimp associated with A. australis Dworschak & Coelho, 1999), through direct observation or inferred from morphological there are no records of animal fragments in the stomach di¡erences Nickell et al., 1998; Stamhuis et al., 1998;

Journal of the Marine Biological Association of the United Kingdom 2001) Functional morphology in Axianassa V.R. Coelho and S. de A. Rodrigues 451

Coelho et al., 2000b; Coelho & Rodrigues, in press). One observations, since no resuspension of particles was of the most conspicuous features of the appendages is the observed in aquaria). presence of setae. The general setal morphology indicates The brushes of serrate setae found on the inner surface some mechanical functions, and the prevalence of a major of the carpus and propodus of the 3rd maxillipeds appear setal category may denote the principal role played by the to have an important function in the antennal grooming appendage during the feeding process. Plumed setae are Bauer, 1981, 1989; Nickell et al., 1998). The 3rd maxil- adapted to retain particles, seal areas between appendages liped of A. australis has a developed crista dentata that or promote a water £ow. Serrate setae are specialized in could aid in gathering sediment during the process of brushing or abrading particles. Plumodenticulate setae brushing sediment by making inward lateral movements, may combine the functions of plumed and serrate setae, see Results, Feeding behaviour). Kunze & Anderson 1979) while simple setae appear to be adapted to brush particles observed a relationship between the degree of macro- review in Coelho et al., 2000b; Coelho & Rodrigues, in phagy and the development of the crista dentata in press). hermit crabs. This does not appear to be true for The main functions of the feeding appendages of A. australis, since there are no records of macrophagy for A. australis, based on the spatial position of the appendage this species. Among the thalassinidean species that feed segments and the predominance of major setal categories, on deposited particles, some have a developed crista are summarized in Table 1. Our data suggests that in dentata, e.g. J. nocturna, Callianassa subterranea Montagu), A. australis the 1st and 2nd pereiopods, the 3rd pair of while others do not, e.g. Callichirus major Say), Sergio mirim maxillipeds, as well as the dactylus, propodus, carpus Rodrigues), Upogebia omissa Gomes Correª a, Upogebia stellata and merus of the 2nd maxilliped, are adapted to brush Montagu), Pomatogebia operculata Schmitt) Nickell & particles. The ischium, coxa and basis of the 2nd Atkinson, 1995; Nickell et al., 1998; Stamhuis et al., 1998; maxilliped appear to be specialized in particle retention. Coelho et al., 2000b; Coelho & Rodrigues, in press), For the remaining mouthparts, brushing is generally the supporting Nickell et al.'s 1998) suggestion that this main function of the basal endites, while the coxal endites characteristic is more likely related to a phylogenetic retain particles. heritage than to adaptations to di¡erent feeding mechan- In other thalassinideans, most of the appendage isms in the Thalassinidea. segments in which the principal function seems to be to The conical serrate setae found on the basal endites of retain particles, have a concave shape Coelho & the 1st maxilla as observed in other thalassinideans, Rodrigues, in press; Coelho et al., 2000b). In A. australis Nickell et al., 1998; Stamhuis et al., 1998; Coelho et al., the concave shape also occurs in appendage segments 2000b; Coelho & Rodrigues, in press) and the strong that are apparently more adapted to brush particles, incisor and molar processes of the mandible seem to be suggesting that some sediment retention could be occur- specializations to triturate particles. The setae of the ring as well. coxal endites of the 1st maxilla of A. australis are long The 1st and 2nd pereiopods of species of callianassids enough to reach inside the mouth, as in upogebiids and upogebiids have dense layers of predominantly Coelho et al., 2000b), and may transport food particles plumed or plumodenticulate setae Nickell et al., 1998; directly into the oesophagus. The mandibular palps and Coelho et al., 2000b; Coelho & Rodrigues, in press). paragnaths could also aid in transporting particles into These appendages form a `setal net' where particles in the mouth. suspension can be retained for feeding purposes A cloud of particles was observed being expelled by the MacGinitie, 1930, 1934; Devine, 1966; Rodrigues, 1966; mouthparts during feeding in A. australis. This phenom- Dworschak, 1987b; Scott et al., 1988; Nickell & Atkinson, enon suggests that a selective process is occurring and the 1995; Coelho et al., 2000a,b; Coelho & Rodrigues, in rejected particles are being carried away by a water £ow. press). The laomediid J. nocturna also have plumed and This current is likely produced by the £agella of the 2nd plumodenticulate setae on the 1st and 2nd pereiopods, and 1st maxillipeds, the exopod of the 1st maxilliped and however because of their low setal density these appendages the scaphognathite of the 2nd maxilla. Mechanisms of are not well-adapted to hold particles Nickell et al., 1998). particle selection have been observed or suggested for In A. australis the ¢rst two pairs of pereiopods have only many other crustaceans Nicol, 1932; Thomas, 1970; serrate setae, being specialized to brush particles but not Kunze & Anderson, 1979; Schembri, 1982; Alexander & to retain sediment. The limitations imposed by the setal Hindley,1985; Coelho et al., 2000b; Coelho & Rodrigues, characteristics of the 1st and 2nd pairs of pereiopods of in press). these two laomediid species could account for the fact that neither are capable of ¢lter feeding. Yet, as previously mentioned, resuspension feeding has Adaptations to feeding habits inThalassinidea been observed in J. nocturna Nickell & Atkinson, 1995). Nickell et al. 1998) analysed the setal morphology of During this behaviour, the 3rd pair of maxillipeds collects three thalassinidean species, and concluded that dense the material resuspended by the 2nd pair of pereiopods. amounts of pappose, plumose and plumodenticulate setae The endopod of the 3rd maxilliped of the latter species are adaptations to ¢lter feeding; higher amounts of denti- has mainly pappose, plumodenticulate and serrate setae culate, serrate and cuspidate setae, are specializations to Nickell et al., 1998), di¡ering from A. australis,whichhas ¢lter and deposit feeding; and larger quantities of serrate only serrate setae on the endopod of this appendage. and cuspidate setal types are related to deposit feeding. It Because of the setal morphology of its 3rd maxillipeds is di¤cult to compare the present study to Nickell et al. it is unlikely that A. australis could feed on suspended 1998) because the setal classi¢cation system used was particles as J. nocturna agreeing with our behavioural di¡erent. Nonetheless, by comparing the data on feeding

Journal of the Marine Biological Association of the United Kingdom 2001) 452 V.R. Coelho and S. de A. Rodrigues Functional morphology in Axianassa mechanism and setal morphology of A. australis with other Buchanan 1963) describes Calocaris macandreae Bell as a species to which the same setal classi¢cation system was non-selective deposit feeder with well-developed incisor used Coelho et al., 2000b; Coelho & Rodrigues, in and molar processes, and gastric mill, but does not press), we were able to delineate some trends in Thalas- provide detailed descriptions or illustrations of the sinidea. mandible or stomach. Pinn et al. 1999a) describe and Axianassa australis has mainly serrate setal types, it illustrate, by scanning electron microscope photographs, di¡ers from Callianassidae species which have predomi- an apparently smooth incisor process for this species nantly plumodenticulate setal types Coelho & Rodrigues, except for C. macandreae, all species mentioned above in press), and Upogebiidae species with mainly plumed have a toothed incisor process). According to Calderon- and plumodenticulate setal types Coelho et al., 2000b). Perez 1981) and Pinn et al. 1998, 1999a), C. macandreae Considering the diversity of feeding habits found in seems to be primarily a deposit feeder, but may also be callianassids and upogebiids MacGinitie, 1930, 1934; able to suspension feed and, based on stomach contents, Pohl, 1946; Devine, 1966; Rodrigues, 1966; Dworschak, can be carnivorous the only thalassinidean species 1987b; Scott et al., 1988; Nickell & Atkinson, 1995; currently known to be so). Due to the unique feeding Coelho et al., 2000a,b; Coelho & Rodrigues, in press), habit of this species inside the Thalassinidea, further these di¡erences in prevalence of major setal categories investigations on the trophic behaviour would be particu- are apparently more related to the morphological charac- larly important to elucidate the role of the mandible teristics of each family than to ecological specializations to during the feeding process of this and other Calocarididae trophic modes. Conversely, when the setal types and species. feeding mechanisms are analysed for di¡erent species of a Stomach contents with mainly small particles, e.g. same family, some patterns emerge for the thalassinideans. C. major, P. operculata, U. o m i ss a, A. australis Coelho et al., Comparing the amount of setal types found for 2000b; Coelho & Rodrigues, in press), appears to indi- thalassinidean species Table 2), we observe that generalist cate either ¢lter or deposit feeding. Conversely, the species e.g. U. omissa, C. major) have higher diversity of predominance of larger particles, e.g. S. mirim Coelho & setal types than species in the same family which are Rodrigues, in press), suggests deposit feeding as the exclu- more specialized feeders e.g. P. operculata, S. mirim). Pinn sive trophic mode. Foregut morphology seems to denote et al. 1999a) reached a similar conclusion using a di¡erences in diet Schaefer, 1970; Powell, 1974; Ngoc-Ho, di¡erent setal classi¢cation system for other species of this 1984; Pinn et al., 1999b), thus this anatomical feature may group. also be an indicator of the trophic mode used by the In species within a family, with similar stomach content species. and mandible morphology, the relatively higher number of Morphology of the feeding appendages re£ects di¡erent serrate setal types seems to indicate a more prominent trophic mechanisms in the Thalassinidea, and may be deposit feeding behaviour Coelho et al., 2000b). This used to predict feeding modes for species of this group tendency of higher amounts of serrate setae in species that Coelho & Rodrigues, in press). However, various deposit feed was also suggested by Nickell et al. 1998). morphological features rather than isolated anatomical However, in species belonging to a same family, the ones characteristics should be considered when inferring the with a stronger mandible and higher amount of large possible trophic behaviours of the species. Since most particles in the stomach likely denoting a gastric mill information on feeding mechanisms comes from studies better adapted to grind particles) may have deposit on Callianassidae and Upogebiidae species, inferences on feeding as a more important trophic mode and still the trophic behaviour of species in other families based on bear proportionally less serrate setal types Coelho & morphological characteristics should be viewed with Rodrigues, in press). caution. The mandible morphology in thalassinideans also seems to be correlated to feeding habits. Filter feeders and deposit feeders that resuspend particles appear to have increased requirement to select particles since particles in suspen- We would like to acknowledge the comments of Richard sion are usually smaller) than non-suspension feeders that Brusca and two anonymous referees on a preliminary version of feed directly on the sediment Coelho & Rodrigues, in this manuscript. Our thanks to Walter Brown and Susann Braden, National Museum of Natural History, Smithsonian press). This necessity to select small particles prior to Institution, Washington DC, and Eª nio Mattos, University of ingestion could be linked to a lesser ability of the mandible Sa¬ o Paulo, for their assistance with the SEM analysis. We are in masticating food. Apparently, species that are mainly also grateful to the sta¡ of the Centro de Biologia Marinha suspension feeders have a delicate incisor process e.g. CEBIMar^USP) for their help during ¢eld work. V.R.C. was C. major, P. operculata, U. omissa, U. p u s i ll a , U. stellata, ¢nancially supported by Fundac° a¬ o de Amparo a© Pesquisa do J. nocturna) Rodrigues, 1966; Dworschak, 1987b; Nickell Estado de Sa¬ o Paulo PhD grant, Process 96/04446-6). & Atkinson, 1995; Nickell et al., 1998; Pinn et al., 1999a; Coelho et al., 2000b; Coelho & Rodrigues, in press). REFERENCES While species that are primarily non-suspension feeders tend to have a strong incisor process e.g. S. mirim, Alexander, C.G.H. & Hindley, J.P.R., 1985. The mechanism of food ingestion by the banana prawn, Penaeus merguiensis. C. subterranea, A. australis) Rodrigues, 1966; Nickell & Marine Behaviour and Physiology, 12,33^46. 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Journal of the Marine Biological Association of the United Kingdom 2001)