Hydrobiologia 375/376: 101-111, 1998, S. Baden, L. Pihl, R. Rosenberg, 1.-0. Stromberg, I. Svane & P. Tiselius (eds), Recruitment, Colonization and Physical-Chemical Forcing in Marine Biological Systems. © 1998 Kluwer Academic Publishers.
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Do barnacle larvae respond to multiple settlement cues over a range of spatial scales? 1. M. Hills 1,2,*,**, J. C. Thomason2 , 1. L. Milligan 3 & M. Richardson4 University Marine Biological Station, Millport, Isle of Cumbrae, Ayrshire, KA28 OEG, UK Dept. of Marine Science and Coastal Management, University of Newcastle Newcastle upon Tyne, Tyne & Wear, NE17RU, UK 3 Gatty Marine Laboratory, University of St. Andrews, St Andrews, Fife, KY16 8LB, UK 4 Harrogate Grammar School, Arthur's Avenue, Harrogate, N. Yorkshire, HG2 ODZ * Corresponding author: e-mail:
[email protected] ** Present address: Dept. of Marine Science and Coastal Management, University of Newcastle upon Tyne, Newcastle upon Tyne, Tyne & Wear, NEl 7RU, UK 1
2
Key words: Settlement, cue, barnacle, scale, Semibalanus balanoides
Abstract
Numerous physical and biological factors have been identified which affect the probability of larvae settling on hard substrata. The spatial scale at which these factors operate ranges from km's to sub-mm's. The wide variety of cues that barnacle larvae respond to coupled with the subtleties of cue response to factors like surface roughness, suggests that larvae are fastidious in their choice of settlement sites and thus, (i) settlement is not rapid and, (ii) larvae carry out search behaviour to sample settlement cues. An experimental frame with settlement pits untreated or with either barnacle settlement factor, or cyprid settlement factor, or a squashed cyprid larvae were exposed for a duration of 10 minutes during the Semibalanus balanoides settlement season in the Clyde Sea, UK. A total of 102 of the 240 pits were settled within the 10 minutes. More settlement occurred in the chemically treated pits than the untreated pits suggesting that settlement can be both selective and rapid. Video-photography was carried out in the laboratory of the tracks of S. balanoides cyprids prior to settlement in pits. With untreated pits little search behaviour was identified, cyprids tended to encounter the pit and then settle. Pits treated with squashed cyprid showed a chemical cue-mediated behaviour with cyprids tending to slow down and carryout antennular crawling in the vicinity of the pit. The mean time from entering a 40 x 40 mm window around the pit and settlement was 24.9 s (n =11, SE =5.4). Within the last 1.25 s prior to settlement, cyprids settling in untreated pits moved faster than cyprids settling in CL treated pits (P < 0.01), with a 4 times difference between the mean speeds These data suggest that settlement can be rapid and the pre-settlement track does not necessarily display search behaviour.
Introduction
The settlement stage of sessile marine invertebrate larvae has consequences for subsequent survival and reproductive success (e.g. Connell, 1985; Walters & Wethey, 1996). Such is the importance of this critical stage of the life-cycle that considerable work has been carried out to determine the factors that affect larval settlement. Numerous factors have been identified which affect the probability, both in a positive
and a negative way, of larvae settling on hard substrata. Those factors that affect settlement cover a wide range of scales fromkm's to sub-mm's (e.g. Raimondi, 1990; Le Toumeux & Bourget, 1988). At a large spatial scale the factors tend to be related to differential larval supply due to oceanic and tidal features (e.g. Raimondi, 1990; Pineda, 1994; Hills & Thomason, 1996; Noda & Nakao, 1996), whereas at smaller scales the factors tend to be related to physical, chemical
102 and biological characteristics of the substratum (e.g. Chabot & Bourget, 1988; Raimondi, 1990; Keough & Raimondi, 1996; Holmes et al. 1997). Some of the factors that have been shown to affect settlement of barnacles are summarised in Table 1. These factors that have been shown to affect settlement have been arranged in approximate order of decreasing spatial scale over which they act, from lan's to < mm's. At approximately the m spatial scale there is a change from factors affecting larval supply i.e. bringing the larval to the vicinity of the settlement substrata, to those factors affecting the probability of settlement of a individual larvae in the vicinity of the surface. The change in generic processes affecting settlement rate over spatial scales have been summarised by, for example, Bourget (1988), Pineda (1994) and Hills & Thomason (1996). In the field, substratum roughness has been shown to be the dominant influence on settlement density for the balanomorph barnacle Semibalanus balanoides (Wethey 1984, though see Holmes et al., 1997). Using settlement panels constructed from the same polyester resin but with different size components creating the substratum roughness, Hills & Thomason (1998a) have shown that higher settlement densities were found on surfaces with fine «0.5 mm) and medium (
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Figure 1. The number of pits settled treated with a squashed cyprid, cyprid settlement factor (CSF), barnacle settlement factor (BSF) and no chemical treatment, by cyprids after exposure of the frame for 10 minutes in April, 1996 (X 2 = 13.05, P < O.oI, df =3).
cyprids move from the edge of the video window to a central settlement pit.
Results Settlement in response to chemical cues
A total of 102 of the 240 pits were settled within the 10 minutes of the duration of the experiment. Chi-squared analysis was used to determine if the number of pits settled between each treatment was random i.e. treatment had no effect on settlement. The chi-squared analysis showed that the number of pits settled by treatment was different to random (P- 20
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Figure 2. The tracks of the cyprid prior to settlement in the pits (marked with an X) within the 40 x 40 mm video window; each point represents 0.25 of a second. Treatment of pits: a-c, no chemical treatment; d-f squashed cyprid treatment. The shaded points in Figure 2e represent periods when the cyprid was stationary (light shading =stationary for 0.25-1 s; heavy shading> 1 s).
108 have been shown to increase cyprid settlement density compared to control surfaces (e.g. BSF: Larman & Gabbot, 1975; antennular secretion: Clare et aI., 1994) and to change behaviour (Rittschof et aI., 1984). Chemical cues emanating from adult conspecifics can play an important role as a cue for barnacle settlement in the field (Miron et aI., 1996). In the experiment presented above BSF, CSF and CL all showed a significant positive effect on settlement by the end of the experiment compared to untreated pits. It was not clear whether the attraction caused by CSF and CL was due to presence of the antennular pheromone of the cyprid, or to one or more other chemicals found in the body of the cyprid. However, these results confirm the presence of a cyprid cyprid interaction and suggest that the attractive effect was similar to BSF. Settlement occurred in nearly half of the pits within the 10 minute duration experiment described above. This suggests that settlement can be rapid « 10 min). Presumably, in response to certain cues, the larvae can either carry out the three stage settlement behaviour (Le Tourneux & Bourget, 1988) rapidly, or miss out part of the behaviour, and the stronger the cue becomes the more rapid or more limited the settlement behaviour becomes. Such rapid settlement behaviour would seem to negate the possibility of fastidious searching behaviour. In light of the turbulence around the frame due to relatively rough sea conditions occurring during this experiment and the limited swimming ability of cyprids, attachment to the pit would have to occur rapidly as Lewis (1978) has suggested. If settlement was not rapid then local turbulence might limit any further attachment and would remove the cyprid from the vicinity. Keppel Pier, where this experiment took place, has a mean current speed of between 0.08 and 0.18 ms- 1 in a predominantly unidirectional flow (Moore & Wong, 1995). Changes in numbers of attached larvae in the field have commonly been considered in the range of a number of hours to days, and data are described at scales such as tidally (e.g. Hills & Thomason, 1996), nightly (e.g. Holmes et aI., 1997), daily (e.g. Pineda, 1994 and Bertness et al., 1996), or, periodically (e.g. Minchinton & Scheibling, 1991). However, this study has shown that attachment in the field can be rapid and selective and that for some field experiments, particularly in relation to water soluble chemical cues, short experimental durations could be appropriate. In addition, short experimental durations limit confounding changes in surface characteristics which can occur
rapidly « 24 hrs; Rittschof et al., 1984), limit the consequences of gregarious settlement at higher settlement densities (Hui & Moyse, 1987; Miron et al., 1996) and permit settlement, rather than recruitment (settlement+ post-settlement mortality), to be quantified. Settlement behaviour prior to settlement
The reason for the low settlement in the BSF treated pits ("" 7%) was not clear, as the literature (e.g. Larman & Gabbot, 1975; Gabbot & Larman, 1987) and the field experiment carried out described above suggest that BSF can promote settlement. However, Rittschof et al. (1984) found that BSF had no effect on the settlement of older cultured B. amphitrite cyprids, though, this was due to high settlement in experiments with and without BSF, rather than low settlement in both. The reasons for the low attractiveness of BSF remain unclear. The video trial was carried out to determine the behaviour in the cm - scale vicinity of the pit. Although this spatial scale includes the "" 1 mm scale of the close exploration behaviour and the
