Bipolar disorder comorbid with alcohol use disorder: focus on neurocognitive correlates.

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) Vaªnia Rodrigues Coelho* and Se¨rgio de Almeida RodriguesO *Departamento de Zoologia, Instituto de Biocieªncias, 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. O Departamento de Ecologia Geral, Instituto de Biocieªncias, 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 investigated. 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 Thalassinidean shrimp are commonly found living in burrows excavated in sandy or muddy substrates in intertidal and shallow subtidal areas (Dworschak, 1987a; Swinbanks & Luternauer, 1987; Dworschak & Pervesler, 1988; Gri¤s & Chavez, 1988; Lemaitre & Rodrigues, 1991). Despite the cosmopolitan nature of the group and its abundance in benthic communities, there is a paucity of information on the trophic behaviour of these crustaceans. The few studies available deal mainly with Callianassidae or Upogebiidae species (MacGinitie, 1930, 1934; Pohl, 1946; Devine, 1966; Rodrigues, 1966; Dworschak, 1987b; Scott et al., 1988; Nickell & Atkinson, 1995; Coelho et al., 2000a,b; Coelho & Rodrigues, in press), while the feeding habits of other families have remained obscure. In contrast, information on thalassinidean burrow morphology has accumulated in the literature (MacGinitie, 1930; Frey & Howard, 1975; Ott et al., 1976; Pemberton et al., 1976; Swinbanks & Murray, 1981; Dworschak, 1983, 1987b; Nash et al., 1984; Scott et al., 1988; Atkinson & Nash, 1990; Dworschak & Ott, 1993; Nickell & Atkinson, 1995; Ziebis et al., 1996; Astall et al., 1997; Dworschak & Rodrigues, 1997; Bird & Poore, 1999; Coelho et al., 2000a), and some models relating trophic modes with burrow architecture have been proposed (Gri¤s & Suchanek, 1991; Nickell & Atkinson, 1995). The validity of such models, however, is compromised by the Journal of the Marine Biological Association of the United Kingdom (2001)

scarcity of knowledge on the feeding mechanisms of species of this clan. In the present study, the trophic behaviour, stomach contents, and morphology of the feeding appendages, with emphasis on setae, of a species of Laomediidae, Axianassa australis Rodrigues & Shimizu, 1992, are analysed. The results are compared with other thalassinidean species (Nickell et al., 1998; Stamhuis et al., 1998; Pinn et al., 1999a; Coelho et al., 2000b; Coelho & Rodrigues, in press), and patterns of morphological adaptations to di¡erent feeding strategies are proposed.

MATERIALS AND METHODS Specimens of Axianassa australis were collected with a yabby pump at Praia do Arac°a¨, Sa¬o Sebastia¬o, SP, Brazil. A map and detailed information on the study site can be found in Dworschak & Rodrigues (1997). The substrate in which the burrows of A. australis were found consist of muddy siliciclastic sediments on the surface and compacted shells at 30^40 cm depth (Dworschak & Rodrigues, 1997). Live animals were transported to the laboratory and kept in aquaria for feeding behaviour observations from September to December 1996. Nine specimens of A. australis were placed in aquaria (similar to the one described by Rodrigues & Ho«dl, 1990) ¢lled with sediment from the collection site. The aquaria were

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 Zeiss). The stubs examined in the present study are deposited at the National Museum of Natural History, Smithsonian Institution, Washington, DC (12 stubs, USNM 279044). Setal classi¢cation

The setal types were distinguished according to the classi¢cation system proposed by Farmer (1974). This system is apparently the most appropriate for categorizing setae in studies of feeding mechanisms (Coelho et al., 2000b). The types were clustered in four main categories: plumed, serrate, plumodenticulate and simple. Descriptions are provided for the external morphology of each type of setae, in addition to drawings and photos illustrating the main characteristics. These types were identi¢ed by a letter representing the major group in which they are included, and a number (Factor, 1978). The terminology used in the descriptions follows Watling (1989).

RESULTS Feeding behaviour

In the aquarium, Axianassa australis was only observed to deposit feed. No suspension feeding, by ¢ltering or resuspending particles, was recorded. To feed, the shrimp make inward lateral movements with the 2nd pair of pereiopods, brushing particles from the burrow £oor during this process. These particles are accumulated in front of the mouthparts, creating a sediment pile that is laterally supported by the 1st pair of pereiopods. Next, the 3rd pair of maxillipeds brushes the sediment toward the 2nd maxillipeds, either by making inward lateral movements or stretching the appendages forward and then folding them back. The 2nd pair of maxillipeds collects and transports 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.

Figure 1. View of the general stomach content of Axianassa australis. Scale bar: 100 mm.

Setal types

The mode of articulation of the setal shaft was not always visible due to the amount of di¡erent setal layers. In the majority of the setae where this feature was observed the socket was infracuticular (exceptions are mentioned in the descriptions). The approximate measurement of the insertion angle of the setule was noted when considered important in description of the setae (i.e. in distinguishing one setal type from another). Annulations and pores are reported only when conspicuously present. Long setules bear small spines distributed in an alternating pattern (exceptions are mentioned in the descriptions). Setal size corresponds to the approximate maximum length recorded (it can be found between parenthesis, after the description of the setal type). In the descriptions, some ¢gures may illustrate characteristics 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. Group A: plumed setae (Figure 2); setae bearing only setules on shaft.

Type A1. Pappose setae, with setules loosely arranged (Figure 3A) in an irregular pattern around shaft (600 mm). Type A2. Plumose setae, with two rows of setules inserted almost opposite one another (1208) on shaft. This type has a supracuticular socket (936 mm) (Figure 3B). Type A3. Setae with two dense rows of smooth setules on one side and setules irregularly distributed on other side of shaft (480 mm) (Figure 3C). Type A4. Setae with short serrate setules irregularly distributed along the distal half of shaft (3 mm) Figure 3D.

Stomach contents

The stomach content of the specimens was composed of small sediment particles and detritus (Figure 1). The size range of the particles was from 1 to 220 mm. Journal of the Marine Biological Association of the United Kingdom (2001)

Figure 2. Types of plumed setae found in Axianassa australis (setae in lateral view). R, row(s).

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 on shaft.

Type B1. Setae with two rows of denticles on distal half of shaft (1.7 mm) (Figure 3E). Type B2. Setae with two rows of denticles on one side and one row of denticles on other side of middle one-third of shaft. Distal one-third of shaft bearing only two rows of denticles. This type has an annulus in the proximal one-third region of shaft (640 mm) (Figure 3F). Type B3. Setae with a thick shaft bearing two rows of denticles on the distal two-thirds of shaft (350 mm). Type B4. Setae bearing two rows of denticles on one side and two rows of denticles on other side of shaft. This type has an annulus in the proximal region of shaft (82 mm). Type B5. Setae with one row of triangularshaped denticles distally and two rows of smaller denticles proximally, on distal half of shaft. Tip is curved (262 mm) (Figure 5A). Type B6. Setae with two rows of denticles on one side and two rows of small denticles on other side of third-quarter of shaft. Distal quarter of shaft with only two rows of denticles (658 mm) (Figure 5B). Type B7. Setae with two rows of small denticles on proximal onethird, two rows of denticles on one side and four rows of small denticles on other side of middle one-third and two

Journal of the Marine Biological Association of the United Kingdom (2001)

rows of denticles on distal one-third of shaft (600 mm). Type B8. Setae with two rows of small denticles on proximal half and two rows of denticles on distal half of shaft (1.4 mm) (Figure 5C). Type B9. Setae with many rows of small denticles on tip of shaft. This type appears to have a sub-apical pore (176 mm) (Figure 5D,E). Type B10. Setae with many rows of tiny denticles along the shaft (1.3 mm) (Figure 5F). Type B11. Setae bearing two rows of denticles, strong and curved proximally and smaller near tip, on distal half of shaft (75 mm) (Figure 6A&E). Type B12. Similar to B11, but with eight rows of small denticles on other side of distal half of shaft. Near tip with two rows of denticles only. Shaft has an annulus in its middle region (180 mm) (Figure 6B,C). Type B13. Setae with 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 with two rows of smaller denticles (90 mm) (Figure 6D,E). Type B14. Setae with a conicalshaped shaft bearing two rows of denticles. Shaft has an annulus in its proximal region (55 mm) (Figure 6F). Type B15. Similar to B14 but with one row of wide denticles. This type has an apical pore. Shaft has annulus in its proximal region (59 mm) (Figure 7A,B).

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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) two rows of small denticles on proximal half of a seta of type B8; (D) rows of small denticles on tip of shaft of a seta of type B9; (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 two rows of denticles (160 mm). Type C8. Similar to C7, but


Figure 4. Types of serrate setae found in Axianassa australis (setae in lateral view). R, row(s).


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 with setules loosely arranged around proximal half of shaft in an irregular pattern. The third-quarter of shaft with two rows of denticles. Curved tip with many rows of small denticles (293 mm). Type C10. Setae with setules loosely arranged around proximal one-third of shaft. The distal two-thirds bearing two rows of denticles. Curved tip with many rows of small denticles (267 mm) (Figure 9A). Group D: simple setae (Figure 10); setae bearing no setules or denticles on shaft.

Type D1. Setae with a smooth straight shaft (280 mm). Type D2. Setae with a smooth shaft presenting a structure similar to a sucking disk on tip (200 mm) (Figure 9B,C). Type D3. Setae with a smooth, slightly curved, conicalshaped shaft. This type has an annulus in the proximal one-third region of shaft (90 mm) (Figure 9D). Description of appendages

The ¢rst and second pereiopods and the mouthparts are the appendages directly involved in the feeding behaviour of A. australis. The morphology of these appendages, with emphasis on setal distribution, is described below. In descriptions of the pereiopods the Journal of the Marine Biological Association of the United Kingdom (2001)

terms medial and lateral refer to surfaces directed toward and away from the median line of the body, respectively. For the mouthparts, the terms inner and outer describe features directed toward and away from the mouth, respectively; medial and lateral correspond to the surfaces toward and away from the median line of the body (Factor, 1978). Usually surfaces directed toward the midline of the body have setae curved toward the mouth, dense setal clustering, and many layers of setae, as in upogebiids and callianassids (Coelho et al., 2000b; Coelho & Rodrigues, in press). Each layer consists of a set of only one type of seta, and may or may not be followed by other layers of di¡erent setal types. When a sequence of layers is mentioned in the descriptions, the ¢rst is the most external one. Density of setae on the appendages is illustrated in Figures 11^15. Second pereiopods (Figures 11 & 15)

Second pereiopods slender, bearing serrate setae. Ischium with setae of type B6 on ventral margin. Merus with setae of type B1 on ventral margin, and of type B8 on medial and lateral surfaces. Carpus and propodus with setae of type B1 on ventral edge, B8 on medial and lateral surfaces, and B10 on dorsal margin. Dactylus bearing setae of type B1 and a row of spines on ventral

446



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) two rows of denticles on distal half of shaft of setae of type C8, the tip of the shaft is curved.

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)

Figure 8. Types of plumodenticulate setae found in Axianassa australis (setae in lateral view). R, row(s). Journal of the Marine Biological Association of the United Kingdom (2001)

Third maxillipeds bearing serrate setae. Endopod ¢vesegmented, 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 medial margin to lower inner surface, lateral edge with setae of type B2. Carpus bearing setae of types B8 and


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. Setal distribution and density on 3rd and 2nd maxillipeds 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: 2 mm.

Figure 11. Setal distribution and density on 2nd and 1st pereiopods of Axianassa australis. Drawings modi¢ed from Rodrigues & Shimizu (1992). Setal density represented by following symbols: &, dense; and *, sparse. L, layer. Scale bar: 2 mm. Journal of the Marine Biological Association of the United Kingdom (2001)

B11 on medial margin to inner surface. Propodus with four setal layers, types B8, B13, B11, B1, on medial edge to inner surface. Dactylus with setae of type B1 on medial margin to lower inner surface and on lateral edge (sparse on this edge).

448



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 and 2nd maxilla 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: 1 mm.

Second maxillipeds (Figure 12)

Endopod ¢ve-segmented, exopod with segmented £agellum, epipod and podobranch. Coxa and basis fused. Coxa, basis and ischium bearing two layers of setae, types C4 and A1, from lower outer surface, through medial margin to lower inner surface. Merus with two layers of setae, types B7 and C5, on medial margin to lower inner surface, and serrate setae, type B2, on distal part of lateral edge. Carpus with plumodenticulate setae, type C7, on distal part of medial margin through inner surface to distal part of lateral edge. Propodus with serrate setae, type B8 on medial margin and distal part of outer surface, and type B1 on lateral edge. Dactylus with serrate setae, type B8 on lateral and medial margins, outer surface and distal part of inner surface, and type B3 on tip. Endopod with two layers of setae, types C1 and A2, on medial margin, and serrate setae, type B1 on distal part of lateral edge. Flagellum segmented, with plumed setae, type A1, on distal part.

First maxillipeds (Figure 13)

Coxal and basal endites prominent, endopod elongate, exopod with segmented £agellum. Coxal endite with three layers of setae C4, A1 and C4, from outer surface, through medial margin to upper inner surface. Basal


endite with four layers of setae, types C1, C10, B5 and B1, from outer surface, through medial margin to upper inner surface, and plumodenticulate setae, type C1, on tip. Endopod with plumodenticulate setae, type C4, on medial and lateral edges, tip with plumed setae, type A2. Exopod with plumodenticulate setae, type C4, on medial margin, and plumed setae, type A2, on tip of £agellum and lateral edge. Second maxillae (Figures 13 & 15)

Coxal and basal endites bilobed, endopod slender and scaphognathite (exopod) large. Proximal lobe of coxal endite with two layers of setae, types C6 and A1, on proximal one-third and plumodenticulate setae, types C6 and C1, on distal two-thirds of lower outer surface, through medial margin to upper inner surface. Distal lobe of coxal endite with plumodenticulate setae, type C7, from lower outer surface to medial margin. Proximal lobe of basal endite with four layers of setae, types C7, C9, D1, C7, from lower outer surface to medial edge. Distal lobe of basal endite with plumodenticulate setae, type C7, on distal part, and four layers of setae, types C7, C9, D2, B1, on the remainder of lower outer surface to medial margin. Endopod with plumodenticulate setae, type C1, on medial and lateral margins. Scaphognathite with plumed setae, type A2 on lateral margin and type A4 on ventral edge.

First maxillae (Figure 14)

Coxal and basal endites unilobed, endopod slender and subdivided. Coxal endite with two layers of setae, types C7


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 plumodenticulate setae, type C1, on tip. Basal endite with plumodenticulate setae, type C4, on medial and lateral 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 plumodenticulate setae, type C4, on distal one-¢fth of upper outer surface to tip. Endopod with plumodenticulate setae, type C7, on distalmost area of proximal segment. Mandible (Figures 14 &15)

Palp three-segmented, incisor process with strong teeth and molar process with row of tubercles. Palp bearing plumodenticulate setae, type C4, on outer surface of proximal segment, and type C1, on outer and inner surfaces of median segment. Distal segment with setae of type C1 on proximal one-¢fth, type C8 on second-¢fth, three layers, types C8, C3 and C2, on third and fourth-¢fth, and three layers, types C8, C3 and D3, on distal one-¢fth of upper outer surface to lateral margin.

Labrum and paragnaths

Labrum triangular-shaped, located in the upper part of the mouth. The paragnaths comprise two rounded


lobes, not very setose, present on the initial part of the oesophagus. The setae present on the paragnaths were not analysed.

DISCUSSION Previous studies on feeding mechanisms of thalassinideans have focused primarily on callianassids and upogebiids (MacGinitie, 1930, 1934; Pohl, 1946; Devine, 1966; Rodrigues, 1966; Dworschak, 1987b; Scott et al., 1988; Nickell & Atkinson, 1995; Coelho et al., 2000a,b; Coelho & Rodrigues, in press). There is information on the trophic behaviour of only one other species of Laomediidae, Jaxea nocturna Nardo (Nickell & Atkinson, 1995). The latter species is a deposit feeder, as Axianassa australis. However, unlike A. australis, the deposit feeding mechanism of J. nocturna involves resuspension of particles (Nickell & Atkinson, 1995). Jaxea nocturna uses the 2nd pereiopods to resuspend the sediment, the 3rd pair of maxillipeds collects the particles in suspension and transfer them to the 2nd pair of maxillipeds. Nickell & Atkinson (1995) occasionally observed the 3rd maxillipeds to collect sediment directly from the burrow £oor as well. In A. australis the sediment is accumulated by the 2nd

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

Serrate

Retention

Brushing and retention Sealing

Production of a water £ow

Serrate Serrate Serrate, plumodenticulate Serrate, plumodenticulate Serrate, plumodenticulate, simple, Serrate, plumodenticulate, simple Plumodenticulate, simple Plumodenticulate, plumed Plumodenticulate, plumed Plumodenticulate, plumed Plumodenticulate, plumed Plumodenticulate Plumodenticulate Plumodenticulate Plumodenticulate, plumed Plumodenticulate, plumed Plumodenticulate Plumodenticulate Plumodenticulate Plumodenticulate Plumed Plumed 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 Setal category Plumed (%) Serrate (%) Plumodenticulate (%) Simple (%) Total (%)

Callianassidae

Laomediidae

Upogebia omissaa

Pomatogebia operculataa

Callichirus majorb

Sergio mirimb

Axianassa australisc

14 (37) 9 (24) 15 (39) ^ 38 (100)

12 (39) 4 (13) 15 (48) ^ 31 (100)

5 (10) 10 (19) 35 (67) 2 (4) 52 (100)

3 (8) 5 (13) 30 (77) 1 (2) 39 (100)

4 (13) 15 (47) 10 (31) 3 (9) 32 (100)

a

, Coelho et al. (2000b); b, Coelho & Rodrigues (in press); c, present study.

pereiopods in front of the 3rd maxillipeds, which brush the particles toward the 2nd maxillipeds. The stomach content of A. australis suggests that this species does not feed on plant matter, consistent with the fact that no sea grasses or macroalgae have been found near or inside its burrows (Dworschak & Rodrigues, 1997). Although alpheid shrimp are known to live associated with A. australis (Dworschak & Coelho, 1999), there are no records of animal fragments in the stomach Journal of the Marine Biological Association of the United Kingdom (2001)

content of the latter species, suggesting that carnivory or scavenging are not among its trophic mechanisms. Conversely, we cannot be sure A. australis does not use other feeding behaviours since only one type of food was o¡ered to the specimens in aquaria. The main function of the appendages have been described for some species of thalassinidean shrimp through direct observation or inferred from morphological di¡erences (Nickell et al., 1998; Stamhuis et al., 1998;

Functional morphology in Axianassa V.R. Coelho and S. de A. Rodrigues Coelho et al., 2000b; Coelho & Rodrigues, in press). One of the most conspicuous features of the appendages is the presence of setae. The general setal morphology indicates some mechanical functions, and the prevalence of a major setal category may denote the principal role played by the appendage during the feeding process. Plumed setae are adapted to retain particles, seal areas between appendages or promote a water £ow. Serrate setae are specialized in brushing or abrading particles. Plumodenticulate setae may combine the functions of plumed and serrate setae, while simple setae appear to be adapted to brush particles (review in Coelho et al., 2000b; Coelho & Rodrigues, in press). The main functions of the feeding appendages of A. australis, based on the spatial position of the appendage segments and the predominance of major setal categories, are summarized in Table 1. Our data suggests that in A. australis the 1st and 2nd pereiopods, the 3rd pair of maxillipeds, as well as the dactylus, propodus, carpus and merus of the 2nd maxilliped, are adapted to brush particles. The ischium, coxa and basis of the 2nd maxilliped appear to be specialized in particle retention. For the remaining mouthparts, brushing is generally the main function of the basal endites, while the coxal endites retain particles. In other thalassinideans, most of the appendage segments in which the principal function seems to be to retain particles, have a concave shape (Coelho & Rodrigues, in press; Coelho et al., 2000b). In A. australis the concave shape also occurs in appendage segments that are apparently more adapted to brush particles, suggesting that some sediment retention could be occurring as well. The 1st and 2nd pereiopods of species of callianassids and upogebiids have dense layers of predominantly plumed or plumodenticulate setae (Nickell et al., 1998; Coelho et al., 2000b; Coelho & Rodrigues, in press). These appendages form a `setal net' where particles in suspension can be retained for feeding purposes (MacGinitie, 1930, 1934; Devine, 1966; Rodrigues, 1966; Dworschak, 1987b; Scott et al., 1988; Nickell & Atkinson, 1995; Coelho et al., 2000a,b; Coelho & Rodrigues, in press). The laomediid J. nocturna also have plumed and plumodenticulate setae on the 1st and 2nd pereiopods, however because of their low setal density these appendages are not well-adapted to hold particles (Nickell et al., 1998). In A. australis the ¢rst two pairs of pereiopods have only serrate setae, being specialized to brush particles but not to retain sediment. The limitations imposed by the setal characteristics of the 1st and 2nd pairs of pereiopods of these two laomediid species could account for the fact that neither are capable of ¢lter feeding. Yet, as previously mentioned, resuspension feeding has been observed in J. nocturna (Nickell & Atkinson, 1995). During this behaviour, the 3rd pair of maxillipeds collects the material resuspended by the 2nd pair of pereiopods. The endopod of the 3rd maxilliped of the latter species has mainly pappose, plumodenticulate and serrate setae (Nickell et al., 1998), di¡ering from A. australis, which has only serrate setae on the endopod of this appendage. Because of the setal morphology of its 3rd maxillipeds it is unlikely that A. australis could feed on suspended particles as J. nocturna (agreeing with our behavioural Journal of the Marine Biological Association of the United Kingdom (2001)

451

observations, since no resuspension of particles was observed in aquaria). The brushes of serrate setae found on the inner surface of the carpus and propodus of the 3rd maxillipeds appear to have an important function in the antennal grooming (Bauer, 1981, 1989; Nickell et al., 1998). The 3rd maxilliped of A. australis has a developed crista dentata that could aid in gathering sediment (during the process of brushing sediment by making inward lateral movements, see Results, Feeding behaviour). Kunze & Anderson (1979) observed a relationship between the degree of macrophagy and the development of the crista dentata in hermit crabs. This does not appear to be true for A. australis, since there are no records of macrophagy for this species. Among the thalassinidean species that feed on deposited particles, some have a developed crista dentata, e.g. J. nocturna, Callianassa subterranea (Montagu), while others do not, e.g. Callichirus major (Say), Sergio mirim (Rodrigues), Upogebia omissa Gomes Correªa, Upogebia stellata (Montagu), Pomatogebia operculata (Schmitt) (Nickell & Atkinson, 1995; Nickell et al., 1998; Stamhuis et al., 1998; Coelho et al., 2000b; Coelho & Rodrigues, in press), supporting Nickell et al.'s (1998) suggestion that this characteristic is more likely related to a phylogenetic heritage than to adaptations to di¡erent feeding mechanisms in the Thalassinidea. The conical serrate setae found on the basal endites of the 1st maxilla (as observed in other thalassinideans, Nickell et al., 1998; Stamhuis et al., 1998; Coelho et al., 2000b; Coelho & Rodrigues, in press) and the strong incisor and molar processes of the mandible seem to be specializations to triturate particles. The setae of the coxal endites of the 1st maxilla of A. australis are long enough to reach inside the mouth, as in upogebiids (Coelho et al., 2000b), and may transport food particles directly into the oesophagus. The mandibular palps and paragnaths could also aid in transporting particles into the mouth. A cloud of particles was observed being expelled by the mouthparts during feeding in A. australis. This phenomenon suggests that a selective process is occurring and the rejected particles are being carried away by a water £ow. This current is likely produced by the £agella of the 2nd and 1st maxillipeds, the exopod of the 1st maxilliped and the scaphognathite of the 2nd maxilla. Mechanisms of particle selection have been observed or suggested for many other crustaceans (Nicol, 1932; Thomas, 1970; Kunze & Anderson, 1979; Schembri, 1982; Alexander & Hindley, 1985; Coelho et al., 2000b; Coelho & Rodrigues, in press). Adaptations to feeding habits inThalassinidea

Nickell et al. (1998) analysed the setal morphology of three thalassinidean species, and concluded that dense amounts of pappose, plumose and plumodenticulate setae are adaptations to ¢lter feeding; higher amounts of denticulate, serrate and cuspidate setae, are specializations to ¢lter and deposit feeding; and larger quantities of serrate and cuspidate setal types are related to deposit feeding. It is di¤cult to compare the present study to Nickell et al. (1998) because the setal classi¢cation system used was di¡erent. Nonetheless, by comparing the data on feeding

452



mechanism and setal morphology of A. australis with other species to which the same setal classi¢cation system was used (Coelho et al., 2000b; Coelho & Rodrigues, in press), we were able to delineate some trends in Thalassinidea. Axianassa australis has mainly serrate setal types, it di¡ers from Callianassidae species which have predominantly plumodenticulate setal types (Coelho & Rodrigues, in press), and Upogebiidae species with mainly plumed and plumodenticulate setal types (Coelho et al., 2000b). Considering the diversity of feeding habits found in callianassids and upogebiids (MacGinitie, 1930, 1934; Pohl, 1946; Devine, 1966; Rodrigues, 1966; Dworschak, 1987b; Scott et al., 1988; Nickell & Atkinson, 1995; Coelho et al., 2000a,b; Coelho & Rodrigues, in press), these di¡erences in prevalence of major setal categories are apparently more related to the morphological characteristics of each family than to ecological specializations to trophic modes. Conversely, when the setal types and feeding mechanisms are analysed for di¡erent species of a same family, some patterns emerge for the thalassinideans. Comparing the amount of setal types found for thalassinidean species (Table 2), we observe that generalist species (e.g. U. omissa, C. major) have higher diversity of setal types than species in the same family which are more specialized feeders (e.g. P. operculata, S. mirim). Pinn et al. (1999a) reached a similar conclusion using a di¡erent setal classi¢cation system for other species of this group. In species within a family, with similar stomach content and mandible morphology, the relatively higher number of serrate setal types seems to indicate a more prominent deposit feeding behaviour (Coelho et al., 2000b). This tendency of higher amounts of serrate setae in species that deposit feed was also suggested by Nickell et al. (1998). However, in species belonging to a same family, the ones with a stronger mandible and higher amount of large particles in the stomach (likely denoting a gastric mill better adapted to grind particles) may have deposit feeding as a more important trophic mode and still bear proportionally less serrate setal types (Coelho & Rodrigues, in press). 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 suspension are usually smaller) than non-suspension feeders that feed directly on the sediment (Coelho & Rodrigues, in press). This necessity to select small particles prior to ingestion could be linked to a lesser ability of the mandible in masticating food. Apparently, species that are mainly suspension feeders have a delicate incisor process (e.g. C. major, P. operculata, U. omissa, U. pusilla, U. stellata, J. nocturna) ( Rodrigues, 1966; Dworschak, 1987b; Nickell & Atkinson, 1995; Nickell et al., 1998; Pinn et al., 1999a; Coelho et al., 2000b; Coelho & Rodrigues, in press). While species that are primarily non-suspension feeders tend to have a strong incisor process (e.g. S. mirim, C. subterranea, A. australis) (Rodrigues, 1966; Nickell & Atkinson, 1995; Nickell et al., 1998; Coelho & Rodrigues, in press). Yet some species, such as C. subterranea, may also have a marked tendency to deposit feed by resuspending particles (Stamhuis et al., 1998). Journal of the Marine Biological Association of the United Kingdom (2001)

Buchanan (1963) describes Calocaris macandreae Bell as a non-selective deposit feeder with well-developed incisor and molar processes, and gastric mill, but does not provide detailed descriptions or illustrations of the mandible or stomach. Pinn et al. (1999a) describe and illustrate, by scanning electron microscope photographs, an apparently smooth incisor process for this species (except for C. macandreae, all species mentioned above have a toothed incisor process). According to CalderonPerez (1981) and Pinn et al. (1998, 1999a), C. macandreae seems to be primarily a deposit feeder, but may also be able to suspension feed and, based on stomach contents, can be carnivorous (the only thalassinidean species currently known to be so). Due to the unique feeding habit of this species inside the Thalassinidea, further investigations on the trophic behaviour would be particularly important to elucidate the role of the mandible during the feeding process of this and other Calocarididae species. Stomach contents with mainly small particles, e.g. C. major, P. operculata, U. omissa, A. australis (Coelho et al., 2000b; Coelho & Rodrigues, in press), appears to indicate either ¢lter or deposit feeding. Conversely, the predominance of larger particles, e.g. S. mirim (Coelho & Rodrigues, in press), suggests deposit feeding as the exclusive trophic mode. Foregut morphology seems to denote di¡erences in diet (Schaefer, 1970; Powell, 1974; Ngoc-Ho, 1984; Pinn et al., 1999b), thus this anatomical feature may also be an indicator of the trophic mode used by the species. Morphology of the feeding appendages re£ects di¡erent trophic mechanisms in the Thalassinidea, and may be used to predict feeding modes for species of this group (Coelho & Rodrigues, in press). However, various morphological features rather than isolated anatomical characteristics should be considered when inferring the possible trophic behaviours of the species. Since most information on feeding mechanisms comes from studies on Callianassidae and Upogebiidae species, inferences on the trophic behaviour of species in other families based on morphological characteristics should be viewed with caution.

We would like to acknowledge the comments of Richard Brusca and two anonymous referees on a preliminary version of this manuscript. Our thanks to Walter Brown and Susann Braden, National Museum of Natural History, Smithsonian Institution, Washington DC, and Eªnio Mattos, University of Sa¬o Paulo, for their assistance with the SEM analysis. We are also grateful to the sta¡ of the Centro de Biologia Marinha (CEBIMar ^USP) for their help during ¢eld work. V.R.C. was ¢nancially supported by Fundac°a¬o de Amparo a© Pesquisa do Estado de Sa¬o Paulo (PhD grant, Process 96/04446-6).

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