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

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Antifouling Adaptations of Caridean Shrimps: Cleaning of the Antennal Flagellum and General Body Grooming Marine Biology 49, 69-82 (1978) MARINE BIOLOGY © by Springcr-Verlag 1978 Antifouling Adaptations of Caridean Shrimps: 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 shrimp 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 animals 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.
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