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Echinodermata): a Behavioral and Morphological Study

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Echinodermata): a Behavioral and Morphological Study Marine Biology (2004) 145: 265–276 DOI 10.1007/s00227-004-1327-5 RESEARCH ARTICLE R. Morgan Æ M. Jangoux Juvenile–adult relationship in the gregarious ophiuroid Ophiothrix fragilis (Echinodermata): a behavioral and morphological study Received: 21 October 2003 / Accepted: 4 February 2004 / Published online: 17 March 2004 Ó Springer-Verlag 2004 Abstract Ophiothrix fragilis forms dense beds in the Juveniles and adults are closely associated with one North Sea–English Channel region, where juveniles are another, and both the morphology and behavior of exclusively found on adults. The aim of this study was to juveniles play an important role in that relationship. see how the behavior and morphology of juveniles could help elucidate the close juvenile–adult relationship found in this species. Juveniles are found on the disk, arms and in the bursae of adult conspecifics, the ones on the disks Introduction being significantly larger. No clear advantage seems to be gained by the juveniles being in the bursae, and their Aggregations in echinoderms are not uncommon. Rep- presence there is most likely due to juvenile movement resentatives from all five classes can form dense aggre- on adults and to and from adults. Hooked spines serve gates from a few hundred to a few thousand individuals as anchory organs during the early life of the juvenile, per square meter (Salsman and Tolbert 1965; Brun 1969; but growth of the arms enhances its anchory capabilities Dana et al. 1972). Such aggregations are either a re- and the hooked spines become secondary in that respect. sponse to environmental stimuli, social behavior or both They regress as ophiuroids become older, to the and can be short- or long-term events. A localized food advantage of the other spines used in suspension feeding. source or the period of reproduction can make a variety Juveniles are attracted to conspecifics, and true gregar- of species aggregate, but these will usually disperse once ious behavior has been observed. The tip of each arm, the food source has been depleted or reproduction has the terminal tentacle, plays a major role in distance taken place (Beach et al. 1975; Vadas et al. 1986; Sloan chemoattraction, with juveniles needing at least one in- and Northway 1982; Young et al. 1992). Long-term tact terminal tentacle to be able to initiate a response. aggregations can, however, be found, with some of the Electron microscope observations of the terminal ten- more impressive ones formed by ophiuroids (Brun 1969; tacle permitted us to recognize two different potential O’Connor et al. 1983; Fujita and Ohta 1989). receptor structures designated sta¨ bchens. The first pos- The brittle-star Ophiothrix fragilis forms dense beds, sesses one long projecting cilia and is mostly present reaching densities of up to 2,000 individuals m)2.Itisa around the base of the terminal tentacle, while the other suspension-feeding species, the individuals of which live has one to five short projecting cilia and is mostly found in hydrodynamically active areas rich in suspended on the tip. No receptors are found on the shaft. material. They would receive a high delivery rate of food Receptors are not associated with secretory structures. that, as Warner (1979) pointed out, is necessary to maintain the high densities at which they live. Social behavior would also be an important factor necessary Communicated by O. Kinne, Oldendorf/Luhe for such crowded populations to exist. Broom (1975) R. Morgan (&) Æ M. Jangoux showed that, in the field, adults are able to recognize Laboratoire de Biologie Marine (CP 160/15), conspecifics once they are in contact with them. Universite´ Libre de Bruxelles, 50 Avenue Franklin Roosevelt, In the North Sea–English Channel region, where the 1050 Brussels, Belgium main recruitment event occurs in September (Davoult E-mail: [email protected] Tel.: +32-2-6502970 et al. 1990), a large number of juveniles are found on the Fax: +32-2-6502796 adults. Juveniles are also found all year round on adults, M. Jangoux although in somewhat lower numbers than during the Laboratoire de Biologie Marine, Universite´ de Mons-Hainaut, main recruitment period (Smith 1940; Warner 1969, 20 Place du Parc, 7000 Mons, Belgium 1971). 266 In the majority of benthic invertebrates, juvenile niles were measured under a dissecting microscope using a micro- mortality is high and the postsettlement/juvenile period meter eyepiece, while calipers were used for the adult measurements. We used the method of Guille (1964) to measure the disk diameter. is an important one, regulating the whole population Results were analyzed by ANOVA at the P<0.05 level. Nonlinear (Gosselin and Qian 1997; Hunt and Scheibling 1997). regression analysis was done using the SYSTAT program. Juveniles were found only on adults in O. fragilis beds, the former being localized either on the arms, disks and/ or in bursae of the latter (Warner 1971; Davoult et al. Juvenile behavior 1990). This last observation has led some authors to believe that young juveniles move into the bursae after To test for juvenile movements within the adult population, five adult individuals deprived of juveniles were placed in an aerated metamorphosis to find shelter and an ample supply of aquarium (17·11·12 cm). Ten juveniles (1–1.5 mm disk diameter) oxygenated seawater (Smith 1940). This would imply a were subsequently deposited on the arms of the adults (two juveniles close relationship between adults and juveniles and, per adult). Every 2 days, for 10 days, the adults were examined supposedly, some adaptive particularities that help under a dissecting microscope, the aquarium was carefully checked and the locations of juveniles were noted. The adults could easily be maintain such a relationship. discriminated by the high polychromacy found in this species, and The aim of this study was to investigate how the the arms, by the presence of regenerating or broken ones. behavior and morphology of juvenile O. fragilis helps To test for any olfactory response in juveniles, a Davenport’s maintain the close juvenile–adult relationship found in Y-system was used (Davenport 1950). Figure 1 illustrates the experimental set-up. Twenty assays (each assay needing one juve- this species. nile with a disk diameter of 1–1.5 mm) were made per test, each assay lasting until the juvenile either made a choice or did not move for 20 min (for the different stimuli used see Table 3). The seawa- ter, sand, oysters and conspecific ophiuroids used for the tests came Materials and methods from the site of the adult population. Ophiocomina nigra came from a mixed Ophiothrix–Ophiocomina population situated in Brittany Specimens of Ophiothrix fragilis (Abildgaard, 1789) were collected (France). During the experiment the flow rate was maintained at ) monthly from January to December 2002 by SCUBA diving at approximately 50 ml.min 1. Wemeldinge (Netherlands), from a population situated on an sandy To evaluate whether the arm tip plays any role in chemorecep- bottom/oyster bed at a depth of 25 m. These were brought back to tion, tests using a Davenport’s Y-system were made with 20 juve- the marine biology laboratory of the Universite´ Libre de Bruxelles niles having intact arm tips or having two, four or five amputated and kept in a closed-circuit aquarium until further manipulations arm tips. Experiments with intact and amputated individuals were were carried out. performed using a single set of 20 juveniles (each juvenile with a disk diameter of 1–1.5 mm). After each amputation, individuals recov- ered for at least 3 h before the next experiment was carried out. Results of the Davenport Y-system tests were analyzed using a Location and biometry of juveniles Yate’s Chi-squared test at the P<0.05 level. After each collection trip, 150 adult individuals were carefully examined under a dissecting microscope for any juveniles present, and the location of the latter noted (either ‘‘apparent’’ on arms or Juvenile morphology disks or ‘‘cryptic’’ in bursae). To check for any juveniles present in the bursae, these were carefully opened up with the help of a scalpel. Juveniles were fixed in Bouin’s fluid in seawater, dehydrated in a The length of the longest arm and the disk diameter of the juveniles graded series of ethanol, critical point dried, mounted on stubs, and of the adults on which they were found were also noted. Juve- coated with gold and observed on a Jeol JSM-6100 scanning Fig. 1 Davenport’s Y-system: aquaria in which different stimuli were placed (A, B) and receptacle in which water was collected (C ). Region 1 was where the juvenile Ophiothrix fragilis were placed at the start of the experiment. Choice between A and B was considered made once the disk of the juvenile was in region 2 (left or right) 267 Table 1 Ophiothrix fragilis. Location and mean disk diameter of The relative lengths of the arms and disks of juveniles juveniles from conspecific adults [s.d. standard deviation; * signif- are shown in Fig. 3. By following a single cohort of icantly different (ANOVA, P<0.05)] juveniles over time (Fig. 3; t1–t3), we could infer that Location on Percent Mean disc growth of the disk relative to the arms was reduced in adult juveniles diameter (s.d.) the early stages of juvenile development. However, be- cause of the low number of individuals in the cohort, ‘‘Apparent’’ juveniles Disc 32 2.78* (1.00) nonlinear regression analysis was carried out using the (n=152) Arm 63 1.91 (1.04) data from all juveniles. Nonlinear regression analysis ‘‘Cryptic’’ juveniles Bursa 5 0.96 (0.25) 2 (n=8) revealed highly significant fitting (R =0.445; F=1,090; P<0.001) of the model Y=r{1)exp[)k(X)xi)]}, with the following estimated parameters: the asymptotic ratio electron microscope.
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