Marine Biology 49, 69-82 (1978) MARINE BIOLOGY © by Springcr-Verlag 1978

Antifouling Adaptations of Caridean : Cleaning of the Antennal Flagellum and General Body Grooming

R.T Bauer

Biological Sciences Department, California Polytechnic State University; San Luis Obispo, California, USA

Abstract Structural specializations of chelipeds used by caridean in two kinds of grooming activity are described. In general body grooming, the chelipeds, and in some species, the last walking legs, nip, pick or brush material from the exoskele- ton. When the cleaning chelipeds are the second pair, the carpal segment is multi- segmented, increasing distal flexibility which aids in grooming. Tufts of compound setae and setal "chela locks" are characteristic of cleaning chelae. In represen­ tatives from 13 of 15 caridean families surveyed, brushes of serrate setae surround the carpal-propodal joint of the first cheliped. This setal structure is used in the specific task of cleaning the chemotactile antennal flagellum. Cleaning brushes on the last walking legs of some species are involved in general body cleaning. Ex­ periments on Heptacarpus pictus showed that when the cleaning chelipeds were ablated, body parts became fouled with epizoites and particulate debris in experimental shrimps, while control shrimps showed little fouling. Suggestions on the adaptive role of general body cleaning in these natant are discussed. A survey of cleaning characters in representatives from 15 caridean families suggest that such characters are rather constant within a family. A possible correlation between the taxonomic success of a family and the degree of development of general body clean­ ing is suggested.

Introduction Materials and Methods Caridean shrimps, important faunal com­ A list of the caridean species observed ponents of many marine habitats, can be is presented in Table 1. General methods frequently observed cleaning the body of observation have been given in Bauer with the third maxillipeds, chelipeds (1977). The effects of ablating the and last walking legs. The cleaning be­ cleaning chelipeds were observed in havior of Pandalus danae has been de­ Heptacarpus pictus. Experimental shrimp had scribed (Bauer, 1975), as has antennular the second chelipeds removed, while con­ cleaning (Bauer, 1977), gill cleaning trols had the first walking leg (never and embryo care (Bauer, in press) in involved in grooming) ablated. Shrimps caridean shrimps. All studies have in­ were placed in 4 to 5 1 plastic buckets dicated that cleaning behavior prevents covered with many 2 to 3 mm holes fouling of the body by epizooites and through which seawater could circulate. particulate debris. The present report These cages were hung in running unfil- continues my studies on caridean clean­ tered seawater. Attached to the cases, ing, and focuses on grooming done with as settling plates for fouling organisms, the chelipeds and walking legs. Special were standard microscope slides and 50 x attention is given to cleaning of the 70 mm rectangles of asbestos board. antennal flagellum and the general body Experiments were conducted in 1974, surfaces. The purpose of this report is from 8-2 5 February (25 shrimp in each to describe the functional morphology of treatment) and from July 22 - August 1 these cleaning behaviors and to report (20 shrimp, each treatment). Gravid fe­ experiments on the adaptive value of males carrying early embryos were used general body grooming. to prevent interruption of the experi-

0025-3162/78/0049/0069/302.80 70 R.T. Bauer: Cleaning Behavior in Shrimp

Table 1. Occurrence of antennal and general body cleaning behaviors in caridean species observed alive. X: Behavior observed,- I: behavior inferred from morphology; -: behavior neither observed nor inferred

Species Antennal cleaning General body General body with carpal- c:leanin g by cleaning by propodal brush a pair of last of Cheliped I chelipeds walki ng leg

Hippolytidae Heptacarpus pictus X X X (Stimpson) H. stylus X X X (Stimpson) H. paludicola X X X (Holmes) H. palpator I I I (Owen) H. taylori I (Stimpson) I I H. brevirostris (Dana) X X I Lysmata californica x x X (Stimpson)

Pandalidae

Pandalus danae X X X P. platyceros X I 1 Brandt P. hypsinotus I I I Brandt P. montaqui tridens X I I (Rathbun) Pandalopsis dispar X I I (Rathbun) ' Crangonidae

Crangon nigxicauda (Stimpson) Paracrangon echinata (Dana)

Alpheidae Alpheus sp. (San Diego) Alpheus sp. (Gulf of California) Betaeus macginitieae X X B. harfordi Hart I I

Palaemonidae

Palaemon ritteri X

ment by molting — these individuals do lies, based on behavioral observation, not molt until after hatching of embryos morphology of appendages and the litera­ (Bauer, 1976a). When, in periodic checks, ture, was conducted (Table 2). Those hatching was observed in some females, species in which only preserved material the experiment was terminated. After was examined were judged to possess a preservation, various parts of the exo- particular cleaning behavior if the skeleton were examined by light micro­ appendage in question had the same struc­ scopy for fouling. ture or processes as homologous limbs A survey of the cleaning morphology used in cleaning by species observed of representatives from caridean fami­ behaviorally. R.T. Bauer: Cleaning Behavior in Shrimp 71

Results cleaning chelipeds, which also func­ tioned in food searching and handling. Morphology of Cleaning Chelipeds In the hippolytids, alpheids, and pandalids studied, the cleaning (second) In caridean species observed preening chelipeds possessed a multiarticulated the body, one of the two pairs of cheli­ carpal segment (Fig. 1). The carpus is peds characteristic of carideans was in­ subdivided into a variable number of volved in grooming. Chelipeds used in segments which articulate with one an­ preening are usually the more slender other, increasing the flexibility of the of the two pairs, bearing dense tufts limb. These chelipeds are amazingly mo­ of serrate or multiscaled setae on the bile, with the carpus capable of being chelae (Fig. 1). For example, in the twisted into a variety of "s"-shaped hippolytids Heptacarpus spp. and Lysmata and circular configurations during califomica, the second chelipeds preen grooming. Subdivision of the second the body, while the first pair are cheliped carpus is a character of taxo- heavier, used in macerating food. Simi­ nomic importance in the Caridea (Holthu- larly, in Alpheus spp. and Betaeus spp. , is, 1955), being constant within each the second chelipeds are for preening, of the following families: Hippolytidae, while the first are much larger, func­ Alpheidae, Pandalidae, Ogyrididae, Pro- tioning in agonistic behavior and prey cessidae, and Glyphocrangonidae. Sub­ capture. Moreover, the first pereiopods division of the carpus occurs only in of Crangon spp. are subchelate, used in the second chelipeds of carideans, not prey capture, while the second are the first. slender preening chelipeds in c. nigricav- Palaemon ritteri is the only species da. In contrast, the first chelipeds of observed in which the first chelipeds Palaemon ritteri are the grooming limbs, were used for grooming, and as indicated while the second pair are robust, used above, the carpus is entire. Wickler and in agonistic behavior and food capture. Siebt (1970) reported that another cari­ In pandalids observed, the second cheli­ dean, Hymenocera picta (Gnathophyllidae) , peds were used for grooming, but the used its first chelipeds in grooming, first pair are small and slender, with and the first cheliped carpus is entire vestigial chelae, used in food search in this family. An atyid species, Cari- (Bauer, 1975). In all species observed, dina nilotica, uses both the first and preening was never the sole function of second chelipeds in cleaning the body

Fig. 1. (A) Heptacarpus pictus; (B) Betaeus macginitieae; (C) Alpheus sp. Cleaning chelipeds with a multisegmented carpus (bracketed). Scale bars = 1.0 mm 72 R.T. Bauer: Cleaning Behavior in Shrimp

Table 2. Distribution of antennal and general body cleaning behaviors in representatives of caridean families. P: Present; A: absent. D: Direct behavioral observation; M: behavior inferred from limb morphology; L: from the literature

Family Antennal General body General body Source of grooming by grooming by grooming by information carpal-propodal chelipeds last walking leg brush of Cheliped 1 (1) (2) (3)

Hippolytidae Heptacarpus spp. Lysmata califor- nica Hippolyte spp. (Chelipeds 2) (but cleaning brush 1-3: D, M Spirontocaris spp. absent in Hippo­ Caridion gordoni lyte californien- (Bate) sis)

Alpheldae Alpheus spp. 1-3: D, M Betaeus spp. {done by third (Chelipeds 2) raaxillipeds)

Crangonidae p or A (Chelipeds 2 in spp Crangon spp; Paracrangon Crangon 1-3: D, M echinata these limbs ab­ ! sent- in P. echinata)

Glyphocrangonidae Glyphocrangon spp. 1-3: M (Chelipeds 2)

Rhynchocinetidae Rhynchocinetes sp. P(?) 1-3: N (Chelipeds 1 and/or 2)

Neraatocarcinidae Nematocarcinus 1-3: M ensifer Smith (Chelipeds 1+2)

Oplophoridae A can tii eph yra sp. P(?) 1-3: M (Chelipeds 1+2)

(Fryer, 1960), and, in atyids, there is chelipeds. Cleaning by both pair of never carpal subdivision of chelipeds. chelipeds in atyid shrimp has been re­ From the information gathered here on ported above, and neither pair have sub­ carpal subdivision, two generalizations divided segments. Similarly, the non- can reasonably be made: (1) when the caridean shrimps Gennadas sp. (Penaeidea) carpus of the second cheliped is sub­ and stenopus sp. (Stenopodidea) groom divided, that limb is a cleaning limb, with more than one pair (personal ob­ (2) when the first chelipeds or first servation) , and multiarticulation of and second chelipeds are used in groom­ cheliped segments is also lacking. ing, neither cheliped carpus will be An exception to these generalizations subdivided. has been found in Crangon nigricauda (Cran­ It may be that when more than one gonidae) in which the second cheliped pair of chelipeds are used in preening, is used in grooming, but unlike other there is no selective pressure for car­ carideans using the same appendage, the pal subdivision, i.e., most areas can carpus of the limb is not subdivided. be groomed by one or the other pair of In this species, a much greater mobility R.T. Bauer: Cleaning Behavior in Shrimp 73

Table 2 (continued)

Family Antennal General body General body Source of grooming by grooming by grooming by information carpal-propoda chelipeds last walking leg brush of Cheliped 1 (1) (2) (3)

Atyidae Caridina nilotica 1: M; 2+3: M,L (Roux) (Fryer, 1960)

Pandalidae Pandalus spp. Pandalopsis spp. 1-3: D, M

Stylodactylidae Stylodactylus sp. 1-3: M

Palaemonidae Palaemon spp. 1: D, H; 2: D,M,L Palaemonetes spp. (in Palaemoniinae) (Schone, 1961); 3: Palaemonid spp. (Chelipeds 1) A D,M,L (illustrations Pontoniid spp. (in Pontoniinae) and species descrip­ tions in Holthuisi 1951, 1952) Gnathophyllidae Gnathophyllimi ameri- 1-3: M canum Guerin (Chelipeds 1) Hymenocera ele- 1: M: 2: M, L gans Heller (Chelipeds 1) (Wickler and Seibt, H. picta Dana 1970); 3: H

Processidae

Processa spp. A 1+3: Mj 2: M, L (one or both (illustrations in Chelipeds 2) Manning and Chace, 1971)

Procarididae Procaris hawaiana 1-3: M Holthuis (no chelipeds)

Pasiphaeidae Pasxphaea emargx- 1-3: M nata Rathbun (possibly by Pereiopod 4) is found in the basal segments of the compound setae at the tip (see Fig. 15 grooming chelipeds than in other cari- in Bauer, 1976b). deans examined. Flexibility of the coxa- Table 2 summarizes the mode of cheli- basal and basi-ischial joints, as well ped grooming for representatives of 15 as that of the articulation of the coxa caridean families. In the Glyphocrangoni- to the sternum, is much higher than in dae and Processidae, the generalization carideans such as Heptacarpus spp., Panda lus that the second chelipeds are grooming spp. , Palaemon spp. and Glyphocrangon sp. limbs is made by inference from other examined. Apparently, the distal flexi­ families where the second cheliped car­ bility given by carpal subdivision to pus is subdivided and which have been the second chelipeds of other species observed in use as grooming limbs. In using them in grooming is replaced in families such as the Pasiphaeidae, the C nigricauda by basal flexibility. Other­ doubt cast on cheliped cleaning was wise, the second chelipeds of this spe­ based on the observation that neither cies are like other grooming chelipeds, pair of chelipeds has a similar struc­ i.e., long and slender, with tufts of ture to known cleaning chelipeds, i.e., 74 R.T. Bauer: Cleaning Behavior in Shrimp the limbs examined possessed a form simply arches over the carpal-propodal appearing to be of little use in groom­ joint (Procaris hawaiana, Crangon spp.) These ing of the kind described in the present setae are in a "V"-shaped configuration study (see "General Body Grooming", be­ in Palaemon ritteri, Pandalus danae, and Hepta­ low) . carpus pictus. Propodal brushes are made A common feature of caridean cleaning of serrate setae set in rows parallel chelae is the presence of interdigitat- to the long axis of the segment and ing stout setae (pegs, spines of other directed inferiorly. This brush is lo­ authors) on the zips of chelal fingers cated on the medio-inferior side of the (chela lock; Bauer, 1975). Thompson proximal end of the propodus. Setae in (1965, 1966) has discussed the distribu­ both carpal and propodal groups bear tion of this character in caridean double rows of tooth setules, typical groups. Scanning electron microscopy of setae involved in cleaning. has shown that a stout seta on the im­ Morphological investigation of first movable (propodal) finger of the chela chelipeds of shrimps not observed be- fits between two similar setae on the haviorally revealed that in 13 of 15 movable (dactylar) finger (Bauer, 1975; families examined, antennal cleaning see Fig. 17 in Bauer, 1976b). Chela brushes are present and similar in form locks have been found in oplophorids, and location to those described above Eugonatonotus spp., hippolytids (Thompson, (Table 2). Only the Alpheidae and Atyi- 1966) and pandalids (Chace and Manning, dae lack these brushes, and the alpheids 1972) . Heptacarpus pictus has chela locks groom the antennal flagellum with a dif­ on both pair of chelae (see Fig. 17 a-c ferent appendage (see "Antennal Cleaning", in Bauer, 1976b). Chela locks may be a below). Results of this survey indicate feature allowing the chelae to pick up that presence or absence of an antennal and grasp small objects, which could be cleaning brush on the first cheliped is an important factor in the shrimp's abil­ a constant character within a caridean ity to nip and pick at the exoskeleton family. during grooming. Exact opposition of cutting or crushing keels along the in­ ner edges of the fingers may be effected by chela locks. Grooming Brush of the Last Walking Leg Other carideans appear to have simi­ Distal segments of the walking legs of lar adaptations for proper opposition shrimps examined are similar in shape of the fingers. In the Rhynchocinetes sp. and setation, except that there are se­ examined, the tips of the fingers of tal brushes on the distal end of the both pair of chelae have several spinous propodal segment of the last leg in Hepta­ setae which intermesh on closure of the carpus spp., Lysmata californica, Palaemon rit­ chela. Palaemon ritteri has setae subequal teri, Pandalus spp., Alpheus spp., Betaeus in size and subterminal in position spp. (but not Crangon spp.) This brush is which appear to serve a similar function composed of varying numbers of rows of (see Fig. 17 in Bauer, 1976b). serrate or multiscaled setae similar to setae on the third maxillipeds used in grooming (see Figs. 4 and 5 in Bauer Antennal Cleaning Brushes of the First Cheliped 1977; Fig. 24 in Bauer, 1976b). Pandalus danae has three well developed brushes Setal brushes on the first chelipeds of on the propodal segment, dorsolateral, Heptacarpus spp., Lysmata californica, Palaemon ventrolateral and ventromedial in posi­ ritteri, Pandalus danae, Crangon nigricauda and tion (Plates 6-8 in Bauer, 1975). other carideans perform the very specif­ In other carideans (Table 2), pres­ ic task of grooming the flagellum of the ence or absence of a propodal brush on second antenna (Tables 1 and 2). Clean­ the last leg seems to be a family char­ ing brushes used in antennal grooming acteristic (or at least characteristic were always located on either side of for the majority of species within a the carpal-propodal joint of Pereiopod 1 family). For example, all hippolytids [Figs. 2, 3; and see Plate 3 in Bauer, examined (except Hippolyte californiensis) 1975, and scanning electron microscope have the brush. Within the Palaemonidae, (SEM) Figs. 20, 21 in Bauer, 1976b]. The all the Palaemoniinae (except Leander spp.) first cheliped may vary in size, struc­ and Euryrhynchiinae have the brush, ture and function in these different whereas the pontoniids do not (based on shrimps but, whatever these differences, figures and species descriptions in the antennal cleaning brush is similar Holthuis, 1951, 1952). Crangon spp. and in form and location, with motor pat­ Paracrangon echinata (Crangonidae) dc not terns involved in its use being alike. have this grooming brush, and examina­ Sometimes, a group or row of serrate tion of figures and species descriptions setae located distally on the carpus from many sources indicate its absence R.T. Bauer: Cleaning Behavior in Shrimp 75

Fig. 2. (A) Palaemon ritteri; (B) Crangon nigromaculata. First chelipeds with carpal-propodal setal brushes (arrowed) used in cleaning antennal flagellum. Cp: carpus; Pd: propodus. Scale bars = l.Omm

// A

Fig. 3. (A) Procaris hawiana; (B) Heptacarpus pictus. First chelipeds with carpal-propodal brushes (arrowed). Cp: carpus; Pd: propodus. Scale bars = 1.0 mm 76 R.T. Bauer: Cleaning Behavior in Shrimp

Fig. 4. (A) Heptacarpus pictus; (B) Palaemon ritteri; (C) Lysmata californica. Cleaning of antennal flagellum by the first cheliped (arrowed); see text for further explanation. Scale bars = 5.0 mm

in the related Glyphocrangonidae. Repre­ lipeds around the flagellum when lowered sentatives of several families examined and "scrub" it with rubbing movements. do not appear to possess this brush (Ta­ Although it would appear that more thor­ ble 2) . ough cleaning could be done with the Atyid shrimps are the only carideans third maxillipeds, cleaning of the fla­ examined in which the grooming brush of gellum with the first cheliped is a Pereiopod 5 is on the dactylar rather quick, efficient movement. than propodal segment. In atyids, the The alpheid shrimps (Alpheus spp., Be- flexor margin of the dactylus is bor­ taeus spp.) observed extensively groom dered by stout serrate setae, with the the antennal flagellum not with the setal comb being used for grooming in first chelipeds, but use the third maxil­ Caridina spp. (Fryer, 1960). Bouvier's lipeds only. Absence of the carpal-pro­ figures in his 1925 monograph on atyids podal brushes of the first chelipeds was show the position of the dactylar comb noted earlier. The first chelipeds of to be constant within the family. these shrimps are large, strong and im­ portant in agonistic behavior (e.g. No­ lan and Salmon, 1970; and own personal observation). These limbs appear to be Antennal Cleaning too cumbersome to clean the antennal Rotation of the antennal flagellum for­ flagellae with their carpal-propodal ward is the first indication it will be joints, and the concomitant setal groups cleaned. In all species observed, the are absent (Fig. 5). A similar condition carpal-propodal joint of the first cheli­ (third maxilliped grooming of antennal ped flexes around the base of the flagel­ flagellae) has been observed in the lum (Fig. 4A), and is then depressed, atyid xiphocaris elongatus (G. Rryer, per­ sliding the setal brushes around the sonal communication) . joint along the length of the flagellum (Fig. 4B), cleaning it. The character­ istic loop formed in the flagellum as it General Body Grooming is returned dorsally easily identifies this behavior (Fig. 4C). Occasionally, General body grooming can be defined to Heptacarpus pictus, Palaemon ritteri and Panda- include all preening activities exclu­ lus danae will clamp the third maxil- sive of the following: brushing of re- R.T. Bauer: Cleaning Behavior in Shrimp 77

I 1

Fig. 5. (A) Alpheus sp; (B) Betaeus macginitieae. First chelipeds,- arrows indicate locations where setal brushes used in antennal cleaning are found in other shrimps. Cp: carpus; Pd: propodus. Scale bars = 2.0 mm Fig. 6. (A) Heptacarpus pictus; (B) Palaemon rit­ teri. General body grooming; (A) second cheliped nipping at antennal scale (arrowed); (B) first chelipeds brushing the eye (arrowed). Scale bars = spiratory surfaces by the chelipeds; all 2.0 mm cleaning by third maxillipeds and anten­ nal flagellum cleaning by the first chelipeds. General body grooming encom­ passes all nipping and picking at body parts by the cleaning chelipeds and the gers. The latter behavior occurs partic­ brushing movements of the last walking ularly if the region cleaned has an in­ legs. tricate topography. Cleaning chelipeds Cleaning chelipeds and last walking of Heptacarpus picuts, Palaemon ritteri and legs share the task of general body Alpheus spp. can clean all the cephaelo- cleaning. For example, in Heptacarpus thoracic area. Ventral abdominal areas, pictus and Palaemon ritteri, the chelipeds e.g. pleopods, abdominal pleurae etc., clean most of the body, with the last are preened by the chelipeds as well. legs making comparatively fewer and less Certain postures of the body and complicated movements toward the ab­ cleaning limbs are characteristic of domen and pleopods. On the other hand, general body grooming. When some ventral the last legs of Pandalus danae play a much area is being preened, the chelipeds greater role in cleaning than in the reach back with a "U" shape (Fig. 7A). above mentioned species (Bauer, 1975). In Heptacarpus pictus, the abdomen is Cleaning movements of the chelipeds flexed beneath the body so that cheli­ are similar in all species observed peds can reach ventral abdominal areas. (Figs. 6, 7). Chelae move rapidly over After cleaning of pleopods, the shrimp the area being groomed, with picking, rids them of dislodged debris by fanning tugging and snapping by the chelal fin- them. Palaemon ritteri is the most acrobat- 78 R.T. Bauer: Cleaning Behavior in Shrimp

Fig. 7. Palaemon ritteri. General body grooming. Pig. 8. Palaemon ritteri. General body grooming (A) first chelipeds cleaning the pleopods (ar­ by setal brushes on last walking leg. (A) last rowed) ; (B) second cheliped holding a walking abdominal segment being groomed (arrowed), note leg (arrowed) while leg is being cleaned by also grooming of carapace by the cleaning cheli­ first chelipeds and third maxillipeds (light peds; (B) tail fan being groomed (arrowed). arrows). Scale bars = 5.0 mm Scale bars = 5.0 ram

ic of the shrimp observed in grooming. Experimental Resuxts The body rests on the tip of the flexed tail posteriorly and on the tips of the Cleaning chelipeds were removed from a extended legs anteriorly (Fig. 7A). P. group of Heptacarpus pictus (experimer.tals) / ritteri also has the distinctive habit of as well as a control group (non-grooming holding one of the walking legs with the leg ablated), with both groups being ex­ second cheliped while the cleaning cheli­ posed to fouling in cages. After termina­ peds (and third maxilliped) groom the leg tion of the experiment, non-molted ex­ (Fig. 7B) . H. pictus, when cleaning the tail perimental shrimps qualitatively showed fan, will hold its leading edge in place fouling of the exoskeleton; control with the first chelipeds while preening shrimps did not. Macroscopically, most the area with the cleaning chelipeds. areas cleaned by the chelipeds, partic­ ularly setose areas, were fouled by Grooming of the abdomen with the se- particulate debris in experimentals. tal brush on the last walking leg in­ Smooth areas (e.g. the carapace) did not volves a variety of scratching and rub­ accumulate debris. The underside of the bing movements (Fig. 8) which have been thorax, the bases of the legs, edge of described in detail for Pandalus danae the gill covers, and the pleopods had (Bauer, 1975). noticeable accumulation of material. R.T, Bauer: Cleaning Behavior in Shrimp 79

skeleton of fouled shrimps, i.e., Leuco­ thrix sp., other bacteria, diatoms, cili­ 40 ates.

Discussion 130 Antennal Cleaning .Expenmen I oContro! Representatives of most caridean fami­ §20 lies groom the long antennal flagellum ft N=12 • 12 12 10 with carpal-propodal brushes on the first cheliped; in two families, the third maxillipeds were used. Antennal flagellae are long multisegmented struc­ In |„ tures waved about by the shrimp and are i * 0 probably important sites of tactile and carapace rostrum leg carapace rostruL m Kleg taste reception (Barber, 1961). Although February July no experimental work has been performed, Treatment fouling of non-groomed antennules of shrimp (Bauer, 1975; Bauer, 1977) indi­ Pig. 9. Heptacarpus pictus. Fouling of body cates that frequent grooming of a sen­ parts by vorticellid ciliates in control and sory appendage prevents its fouling. It experimental shrimps in ablation of cleaning is probable that frequent cleaning of cheliped experiments. X, 95% confidence limits the antennal flagellum prevents fouling given which might interfere with chemo- and mechanoreception. In 13 of 15 families examined, a mechanism, the carpal-propodal brush of the first cheliped, has been developed to clean the antennal flagellum in a Microscopic examination of body parts quick movement. Both the brush and the showed that in experimentals a wide movement used are very similar to that variety of micro-fouling organisms were used by ants in grooming their flagel- attached. These organisms were much like liform antennae (Wilson, 1971). In ants, those found on fouled antennules (Bauer, a curved brush on the fore tarsus of the 1977), fouled gills and fouled embryos first leg is used. As the foreleg and (Bauer, in press) in other experiments the antenna of ants are not homologous with Heptacarpus pictus. Much of the foul­ to the first cheliped and antennal fla­ ing was by Leucothrix sp. , a long-chained gellum (respectively) of shrimp, the bacterium widespread in marine habitats foreleg brush and the behavior are clear­ (Johnson etal., '971; Sieburth, 19751. ly convergent to cheliped brushing of Several kinds of diatoms, other algal the antennal flagellum by shrimp. This cells, and stalked ciliates were at­ convergence in insects may be indicative tached to fouled areas. A hypotrichous of high adaptive value in the structure ciliate was common in debris accumula­ and function of the carpal-propodal tions. A variety of coccoid and bacil- brush of Cheliped 1 in carideans. liform bacteria coated fouled regions (see Bauer, 1977, for SEM illustrations of fouling organisms). General Body Grooming To quantify epizoic settlement, an Caridean shrimp engage in extended easily counted vorticellid ciliate was bouts of cleaning in which the preening used as an indicator of fouling. Certain chelipeds nip and pick at various parts body parts normally cleaned by the of the cephalothorax, abdomen and append­ chelipeds (Fig. 9) were removed from ages. Members of most caridean families control and experimental shrimps, and appear to use one pair of chelipeds for vorticellid counts were taken. Since all general body grooming, but, in addition, shrimps were approximately the same size, some have a setal brush on the last simple counts, rather than vorticellid walking leg which is also used in this density, which would involve difficult behavior. In ablation experiments with measurements of exoskeleton area, were Heptacarpus pictus in this report and Panda- used. Fig. 9 gives the results from the lus danae (Bauer, 1975), the areas normal­ two experiments, showing that in all ly groomed by cleaning limbs became cases experimental shrimps showed signif­ fouled with microbial growth and partic­ icantly higher fouling than controls. ulate debris when not groomed. These ex­ Settling plates attached to the cages periments show that general body groom­ containing shrimps exhibited qualitative­ ing prevents fouling of the exoskeleton ly similar fouling to that on the exo­ by sediment, detritus and epizoic growth. 80 R.T. Bauer: Cleaning Behavior in Shrimp

In a study on antennular preening in keel. Well developed abdominal muscula­ carideans (Bauer, 1977), the detrimental ture powers the backward swimming pro­ effects of fouling were strongly sug­ duced by the paddle-like tail fan. Epi­ gested by damage to olfactory setae on zoic fouling could reduce the efficiency ungroomed antennules of Heptacarpus pictus. and control of both this backward or In the same species, individuals pre­ rapid forward swimming by producing ad­ vented by ablation from gill brushing ditional drag on the body and/or reduc­ suffered clogged and fouled gills which ing mobility between body joints. resulted, in some cases, in death (Bauer, Additional indications that epizoic in press); in the same study, embryos fouling is a selective pressure acting which were not cleaned by the female on swimming animals can be found by look­ suffered heavy fouling and significant ing for presence or absence of anti- mortality. In the case of general body fouling mechanisms in other marine ani­ grooming, however, the deleterious ef­ mals. Pickwell (1971) has remarked on fects of fouling, if any, are not so the low incidence of fouling on the pe­ strongly suggested. For example, it is lagic sea snake Pelamis platurus (L.) . hard to see now the relatively light Heavy epizoic fouling only occasionally fouling of the carapace or abdominal occurs on this reptile, and it is ob­ pleurae could decrease a shrimp's viously incapable of the self-cleaning chances of survival or reproductive of limbed animals. Pickwell notes that success. Experiments designed with more the knotting of the body unique to F. extended fouling periods might elucidate platurus and its high frequency of molt­ this question. Although the frequent ing, unparalleled for a snake, are mech­ molting of caridean shrimp does remove anisms evolved, in part, in response to all fouling, there might be periods in fouling pressure. Other sea snakes in­ the life cycle of some species when habit the bottom, and they do not exhib­ molting rate is low enough to permit it these mechanisms, apparently because extensive fouling (e.g. when females of their frequent contact with hard ob­ are carrying embryos). Glynn (1970) has jects on the sea floor. By rubbing the indicated that heavy algal fouling of body against hard substrates, prevention sphaeromatid isopods may even inhibit of fouling (and aid in skin shedding, molting. the other function of knotting in P. The hard exoskeleton of shrimp (and platarus) can be achieved. all ) is periodically inter­ Scales of fish are protected by a rupted by areas of articulation, so that secreted mucous which makes them gener­ movement can take place between the seg­ ally unsuitable for attachment of in­ ments and joints thus formed. Anything vertebrate larvae. However, the barnacle preventing movement between segments Conchoderma virgatum can attach directly to will interfere with locomotory and feed­ fish in some cases (Beckett, 1968; Ba- ing movements of appendages and postural lakrishnan, 1969), although most individ­ changes of the body. One function of gen­ uals settle on ectoparasites (e.g. cope- eral body cleaning may be to prevent pods) of the fish, rather than on their fouling from building up on articular scales. Since the finned fishes have regions. Glynn (1970), considering ex­ little ability to clean themselves, ex­ perimentally fouled isopods, thought it cept for rubbing against some substrate, likely that fouled individuals starved the task is performed in many cases by from epizoic interference with their other fish or decapod cleaner shrimp, feeding movements. It is also possible which feed on the ectoparasites or that a very heavy buildup of fouling foulers. Thus, cleaning symbioses are organisms could prevent entry into nar­ important to marine fishes (Feder, 1966), row hiding places or interfere with lo­ while they seem to be absent from deca­ comotion simply by weighing the pod shrimp, which can clean themselves. down. Grooming behavior may have bestowed In caridean shrimps, especially, an adaptive advantage on the decapod fouling may interfere with swimming. The (natantian) shrimps which might account, body design of carideans and other na- in part, for their extensive radiation tantian decapods consists of a set of (2000 species) relative to peracarid adaptations for swimming, particularly (mysid) shrimp (400 species) and euphau- the backward swimming of the escape re­ siid shrimp (100 species). The decapod sponse. Partial streamlining seems to caridoid shrimp occupy a much greater be accomplished by the subcylindrical diversity of habitats and modes of life and generally smooth cephalothorax. Flat­ than these other malacostracan caridoid tened antennal scales serve as horizon­ shrimps. tal rudders for control during the es­ Within the Caridea, there may be a cape response, while the long, laterally positive correlation between the number compressed rostrum acts as a stabilizing of pairs of general grooming limbs char- R.T. Bauer: Cleaning Behavior in Shrimp 81 acteristic of a family and its taxonomic - Antifouling adaptations of caridean shrimp: diversity. Those families which have by grooming morphology and behavior, 289 pp. far the greatest diversity in terms of Ph.D. Dissertation, university of California numbers of genera and species, tend to at San Diego 1976b have highly developed general body groom­ - Antifouling adaptations of marine shrimp ing, indicated by the presence of two (Crustacea: : Caridea): functional pairs of general grooming limbs (cheli- morphology and adaptive significance of peds and last walking legs) (Pandalidae, antennular preening by the third raaxillipeds. Hippolytidae, Alpheidae, Palaemonidae: Mar. Biol. 40, 261-276 (1977) Palaemoninae, Atyidae). Results from - Antifouling adaptations of marine shrimp: this study have given no indication of (Decapoda: Caridea): gill cleaning mechanisms general grooming specializations in the and grooming of brooded embryos. J. Linn. Soc. primitive family Procarididae, nor in (Zool.) (In press) the families Stylodactylidae and Pasi- Beckett, H.S.: New record of the barnacle Con- phaeidae — these families have few coderma virgatum in the northwest Atlantic. genera and species. An intermediate J. Fish. Res. Bd Can. 25, 2707-2710 (1968) group, in which at least one pair of Bouvier, E.L.: Recherches sur la morphologie, general cleaning limbs has been indi­ les variations, et la distribution geogra- cated in representatives studied, con­ phique des Crevetes de la familie des Atyides. sists of the Crangonidae, Glyphocrangoni- Encycl. ent. (Ser. A) 4, 1-370 (1925) dae, Oplophoridae, Rynchocinetidae, Nema- Chace, F.A. and R.B. Manning: Two new caridean tocarcinidae, Gnathophyllidae, Processi- shrimps, one representing a new family, from dae, and Palaemonidae: Pontoniinae. marine pools on Ascension Island (Crustacea: In general, families which show the Decapoda: Natantia). Smithson. Contr. Zool. greatest diversification are active epi- 131, 1-18 (1972) benthic forms abundant in nearshore ma­ Feder, H.M.: Cleaning symbiosis in the marine rine, estuarine, and, in the case of environment, in: Symbiosis, Vol. 1. pp 327- atyids, freshwater environments where 380. Ed. by S.M. Henry. New York: Academic fouling pressures tend to be high. Press 1966 Groups in which general body cleaning is Fryer, G.: The feeding mechanism of some atyid best developed may have been able to prawns of the genus Caridina. Trans. R. Soc. resist the deleterious effects of foul­ Edinb. 64, 217-244 (1960) ing, and have beer, free to diversify in these habitats. Glynn, P.W.: Growth of algal epiphytes on a tropical marine isopod. J. exp. mar. Biol. Ecol. 5, 88-93 (1970) Acknowledgements. 1 would like to extend my deep gratitude to all those faculty, staff and Holthuis, L.B.: A general revision of the students at the Scripps Institution of Oceanog­ Palaemonidae (Crustacea: Decapoda: Natantia) raphy, who helped me in so many ways during mi- of the Americas. I. The subfamily Euryrhyn- study of shrimp cleaning behavior. I would like chiinae and Pontoniinae. Occ. Pap. Allan to thank L. Ritchie, Ors. A. Pleminger and R. Hancock Fdn 11, 1-332 (1951) Hessler for their valuable aid; my special - A general revision of the Palaemonidae (Crus­ thanks to Dr. W. Newman for his long-enduring tacea: Decapoda: Natantia) of the Americas. support and assistance in many forms during the II. The subfamily Palaemoninae. Occ. Pap. course of the work. Allan Hancock Fdn 12, 1-396 (1952) - The recent genera of the caridean and steno- podidean shrimps (class Crustacea, order Decapoda, super-section Natantia) with keys Literature Cited for their determination. Zool. Verh., Leiden 26, 1-157 (1955) Balakrishnan, K.P.: Observations on the occur­ Johnson, P.N., J. McN. Seiburth, A. Sastry, C.R. rence of Conchoderma virgatum (Spengler) Arnold and M.S. Doty: Leucothrix mucor in­ (Cirripedia) on Diodon hystrix Linnaeus festation of benthic Crustacea, fish eggs, (Pisces). Crustaceana 16, 101-103 (1969) and tropical algae. Limnol. Oceanogr. 16, Barber, S.B.: Chemoreception and thermoreception. 962-969 (1971) In: The physiology of Crustacea. Vol. II. Sense organs, integration, and behavior, pp Manning, R.B. and F.A. Chace, Jr.: Shrimps of 109-131. Ed. by T.E. Waterman. New York: the family Processidae from the northwestern Academic Press 1961 Atlantic Ocean (Crustacea: Decapoda: Caridea). Bauer, R.T.: Grooming behaviour and morphology Smithson. Contr. Zool. 89, 1-41 (1971) of the caridean shrimp Pandalus danae Stimp- Nolan, B.A. and M. Salmon: The behavior and son (Decapoda: Natantia: Pandalidae). J. Linn. ecology of snapping shrimp (Crustacea: Alpheus Soc. (Zool.) 56, 45-71 (1975) heterochelis and Alpheus normani). Forma Mating behavior and spermatophore transfer in Functio 4, 289-335 (1970) the shrimp Heptacaxpus pictus (Stimpson) Pickwell, G.V.: Knotting and coiling behavior (Decapoda: Caridea: Hippolytidae). J. nat. in the pelagic sea snake Pelamis platurus Hist. 10, 415-440 (1976a) (LJ. Copeia 71, 348-350 (1971) 82 R.T. Bauer: Cleaning Behavior in Shrimp

Schone, H.: Complex behavior. In: The physiology Wickler, W. und U. Seibt: Das Verhalten von of Crustacea, Vol. II. pp 465-52o, Ed. by Hgmenocera picta Dana, einer Seesterne fres- T.H. Waterman. New York: Academic Press 1961 senden Garnele (Decapoda: Natantia: Gnatho- Sieburth, J. McN.: Microbial seascapes, 200 pp. phyllidae). Z. Tierpsychol. 27, 352-36B (1970) Baltimore: University Park Press 1975 Wilson, E.O.: The insect societies, 548 pp. Thompson, J.R.: Comment on phylogeny of section Cambridge: Belknap Press 1971 Caridea (Decapoda: Natantia) and the phylo- genetic importance of the Oplophoroidea. Proc. Symp. Crustacea (Mar. biol. Ass. India) 1, 314-326 (1965) Raymond T. Bauer - The caridean family Bresiliidae (Decapoda: Biological Sciences Department Natantia). A revision and a discussion of its California Polytechnic State University validity and affinities. Crustaceana 11, 129- San Luis Obispo, California 93407 140 (1966) USA

Date of final manuscript acceptance: July 21, 1978. Communicated by N.D. Holland, La Jolla