D. Stanwell-Smith and A. Clarke British Antarctic Survey, Cambridge, U.K., CB3 0ET
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1 Acknowledgements: ALE and NJC are Researchers in the Consejo Nacional de Investigaciones Cientificas y Tecnicas (CONICET, Argentina) and the Comisin de Investigaciones Cientificas de la Provincia de Buenos Aires (CIC), respectively. This note is a part of a project granted by CONICET and CIC. REFERENCES 1. ALDRIDGE, D.W., Ecology, 3: ALDRIDGE, D.W., W.D. RUSSELL-HUNTER & D.E. BUCKLEY, 198. Can. J. Zool., 4: BROWN, D.S., Zool. J. Unman Soc, 93: BROWN, K.M. & T.D. RICHARDSON Ve/iger, 35: BROWNE, R.A., Ecology, 59: BUCKLEY, D.E., 198. Biol. J. Linnean Soc. 27: BURKY, A.J., Proc Malac. Soc. Lon., 41: CAZZANIGA, N.J., 199. Veliger, 33: CAZZANIGA, N.J. & A.L. ESTEBENET, Hist. Nat., 4 (22): RESEARCH NOTES CAZZANIGA, N.J. & A.L. ESTEBENET, Comp. Physiol. Ecol, 13 (3): DEMIAN, E.S. & A.M. IBRAHAM, Zool. Soc. Egypt Bull., 24: ESTEBENET, A.L. & N.J. CAZZANIGA, Malac Rev.,25:\-\ ESTEBENET, A.L. & N.J. CAZZANIGA, Apex, 8 (4): FERRER, J.R., G. PERERA & M. YONG, In Proc. 1th Int. Malac. Cong., Tubingen, 1989 (C. Meier-Brook, ed.), 2: HALE, M.C., 194. The ecology and distribution of the introduced snail, Marisa cornuarietis (Ampullariidae) in South Florida. M. Sc. Thesis, University of Miami, 115 pp. Coral Gables, Florida. 1. JOKINEN, E.H., J. GUERETTE & R.W.KORTMANN, Freshwat. Invert. Biol., 1: KEAWJAM, R.S., Malac. Rev., 2: KEAWJAM, R.S. & E.S. UPATHAM, 199. J. Med. Applied Malac, 2: LUM-KONG, A. & J.S. KENNY, J. Moll. Stud., 55: RICHARDSON, T.D. & J.F. SCHEIRING, Veliger, 37: J. Moll. Stud. (1998), 4, The Malacotogical Society of London 1998 The timing of reproduction in the Antarctic limpet Nacella concinna (Strebel, 198) (Patellidae) at Signy Island, in relation to environmental variables '... As the survey of spawning in various phyla of marine invertebrates has disclosed, correlation with temperature change is cited over and over again by investigators, seldom, however, with experimental evidence...' Arthur Giese, 1987' The limpet Nacella concinna (Strebel, 198) is abundant around the Antactic Peninsula and the islands of the Scotia arc, occurring from the intertidal to over 1 m depth. It is a very common species in the nearshore Antarctic environment, with a mean population density at Signy Island of 124 ± 21 m" 2. The distribution and reproductive ecology of N. concinna has been studied at Palmer station, Anvers Island (3 43' S, 4 5' W) 3-4 ; Esperanza Bay on the Antarctic Peninsula (3 18' S, 5 55' W) 5 ; and at Signy Island, South Orkney Islands ( 43' S, 45 3' W) 2 - Nacella concinna is herbivorous, grazing algae and diatoms 4 and is a broadcast spawner with pelagic larvae. The present note describes field observations of spawning behaviour made predominantly between 1987 and 1994, together with experimental work conducted at Signy Island as part of a major study of near shore benthic invertebrate larval ecology. It has long been known from work at Signy 7 that N. D. Stanwell-Smith and A. Clarke British Antarctic Survey, Cambridge, U.K., CB3 ET concinna has a unique spawning behaviour. It is a non-homing limpet which roams freely over a variety of hard and soft substrata 2. In early spring individuals aggregate in temporary stacks of up to 12 individuals. These stacks are usually visible on flat rocks for 7-1 days and consist of an apparently random mix of sexes. Spawning usually occurs in a very narrow timeframe, often on a single day of the year 7 and after spawning the individuals disperse once more. This unusual behaviour would appear to be an adaptation to maximize fertilization success. Spawning aggregation occurs in many molluscs 8, and has also been observed in the deep sea where it reduces sperm dilution which increases fertilisation success'. Previous workers 2-4 have proposed that the proximate environmental cue for spawning in N. concinna is temperature. Picken 2 noted that in the years of his study ( ) spawning occurred about 3 weeks after the seawater temperature rose to -1.4 C, and he proposed this as a general result. Since 1987 regular observations of spawning behaviour have been made by SCUBA divers in Factory Cove, close to the British Antarctic Survey research station in Signy Island. Factory Cove is a sheltered bay of predominantly soft sediment, with patches of cobbles and boulders; it has a dense population Downloaded from by guest on 14 November 218
2 124 RESEARCH NOTES 2 1 T (sediment) 3 CO 4* C W a> Q. I H H- o Q) 1 ( Q) H no seawater data no seawater data 1994 (rocks) Downloaded from by guest on 14 November October November December
3 RESEARCH NOTES 125 Figure 1. The timing of spawning in Nacella concinna in Factory Cove, Signy Island. The kite diagrams show the number of animals in individual stacks, seen on rocks in Factory Cove. The check marks indicate the dates when seawater temperature reached 1.5 C (Tl) and -.5 C (T2). Spawning is indicated by large check mark (S). Note the top kite diagram: N. concinna were observed to stack on soft sediment in 1994 (Plate 1), as discussed in text. Observations by Picken, (12); British Antarctic Survey marine assistants, (B.A.S. unpubl. data); pers. obs., occurred. Winter seawater temperatures in Factory cove are typically -1.9 C and peak summer values are usually between +.3 C and +1.5 C (1, 11). The two temperature thresholds shown on Figure 1 thus mark the start and end of the spring period of rapid temperature change in Factory Cove; once the seawater has reached about -.5 C, further warming is typically slower and more episodic". This occurs consistently each year between October and December, although there is interannual variation in the onset and duration of warming. It is immediately evident from these plots that there is little correspondence between the timing of the spring increase in seawater temperature and the timing of spawning. The one consistent aspect is that spawning is usually after T2. Pearson product moment correlations were calculated between the date of spawning and (i) the timing of the two temperature thresholds, (ii) the start of the summer microplankton chlorophyll (>2 u.m) and Figure 2. A variation in the unique stacking behaviour of Nacella concinna (7) seen on soft sediment at m depth in Factory Cove, Signy Island on 22 November Both sexes were present randomly in the 'ball', and spawning occurred in synchrony. Downloaded from by guest on 14 November 218 of N. concinna2. From 199 to 1983, and then from 1989 to 1994, regular measurements have been made in Factory Cove of a variety of environmental variables. These include seawater temperature, salinity, winter sea-ice duration and thickness, chlorophyll biomass and the major macronutrients (N, P, Si)1". These observations allow a comparison to be made between the timing of spawning and the year to year variation in the timing of key environmental variables that might cue spawning in N. concinna. Figure 1 shows the mean stack size of limpets in Factory Cove, observed during daily dives. Stacks contained 4 to 12 individuals in different years, although in 1994 clumps of up to 35 individuals were observed on soft sediment (Fig. 2). The latter behaviour has not been reported before. As noted previously2-7, the stacks contained both sexes, as evident when spawning occurred. Also shown in Figure 1 are the dates when seawater rose to -1.5 C (Tl) and -.5 C (T2), and when spawning (S)
4 12 RESEARCH NOTES Table 1. Pearson product moment correlations of environmental parameters with spawning date between 1989 and (Other years had incomplete data). : not significant (P >.1). The critical value (P =.5, n = ) is: r =.811. Parameter Pearson correlation coefficient Seawater reaching -1.5 C Seawater reaching -.5 C Microplankton (>2 u.m) bloom threshold (3=5 mg.m 3 ) Nanoplankton (2-2 u.m) bloom threshold (1 mg.m 3 ) Fast-ice breakout from Factory Cove nanoplankton chlorophyll (2-2 p.m) blooms; and (iii) the date of break up of winter fast-ice in Factory Cove (Table 1). Although none were significant at the level P =s.5, correlation between the onset of the microplankton bloom was almost so (r =.754, P s.1). It has been observed that many marine invertebrates cue their spawning with phytoplankton blooms' 3, even when the larvae released are lecithotrophic 14. It is not currently known if N. concinna has feeding larvae although the similar temperate limpet Patella vulgaia releases embryos that develop into planktotrophic veligers 8. Lecithotrophy is believed to be a secondary (derived) feature in larval nutrition, having evolved from planktotrophy 1215 ; this may mean that the response to phytoplankton blooms is retained even in non-feeding larvae. The correlation between spawning and ice breakout was also almost significant, although the date of ice breakout does co-vary with the plankton bloom. This is probably due to the increased light levels following the loss of sea ice, allowing the water-column bloom to build > P >.5.1 > P >.5 Gametes released during the 1994 spawning were collected and fertilised. They were then incubated at 14 temperature steps from -1.9 C to +2.7 C using a thermogradient block 1. These steps were chosen to cover the annual sea temperature range around the Antarctic Peninsula and Sub-antartic islands". Development was assessed by examining larvae under a dissecting microscope every 12 hours, and every 4 hours when hatching and trochophores were imminent. About 5 of the 3 or so embryos growing at each temperature were observed, and cumulative frequency plots were used to determine the time when 5% had reached a particular development stage (Fig. 3). Previous work further South at Palmer station 4 had found trochophores took 193 h to develop at C, whereas in the present study they took only 79 h to reach the same stage; even the cultures at -1.9 C only took 137 h. It is worth noting that the development time to reach trochophore stage increased noticeably below about -1 C. Similar sharp decreases in development rate at very low tempera- Downloaded from by guest on 14 November Temperature ( C) Figure 3. The development of Nacella concinna larvae between -1.9 C and +2.7 C, incubated in a thermogradient block. Data show the time to 5% of larvae reaching blastula (o) and trochophore ( ) stage at different incubation temperatures.
5 tures have been noted in other polar marine invertebrates (Euphausia superba'*, echinoderms ). It would appear that in N. concinna at Signy, summer temperatures between about.5 C and 1.5 C (the normal summer maxima) would result in a broadly similar development time to metamorphosis (between and 7 days to trochophore). Coupled with the lack of correlation between spawning and temperature (Fig. 1, Table 1), this would suggest that reproductive behaviour in N. concinna is fairly insensitive to the normal interannual variation in seawater temperature at Signy Island. The difference in the rate of development at he same temperature between Palmer 4 and Signy Island (this study) would indicate the possibility of some genetic component underlying development rate, although the relationship is in the wrong direction to indicate classical temperature compensation (which would predict faster rates in more southerly populations at any given temperature) 21. To summarize, the data obtained over nine separate years at Signy Island would therefore suggest that reproduction in N. concinna is cued by the spring phytoplankton bloom and not temperature, and that larval development is relatively insensitive to typical summer seawater temperatures. We would like to thank the divers at Signy who recorded their observations of spawning behaviour during , and the marine assistants who made the seawater measurements. REFERENCES 1. GIESE, A.C. & KANATONI, H In: Reproduction of marine invertebrates IX (A.C. Giese & J.S. Pearse, eds), Boxwood Press, California. RESEARCH NOTES PICKEN, G.B J. Exp. Mar. Biol. Ecoi, 42: SHABICA, S.V Antarct. J. U.S., : SHABICA, S.V Ph.D. Thesis, Oregon State Univ. 5. BRETHES, J.-C, FERREYRA, G., VEGA, S. DE LA Polar Biol., 14: WALKER, A.J.M Br. Antarct. Surv. Bull., 28: PICKEN, G.B. & ALLAN, D J. Exp. Mar. Biol. Ecoi, 71: WEBBER, H.H In: Reproduction of marine invertebrates IV (A.C. Giese & J.S. Pearse, eds), Boxwood Press, California. 9. YOUNG, CM., TYLER, P. A., CAMERON, J.L. & RUMRILL, S.G Mar. Biol., 113: CLARKE, A., HOLMES, L.J. & WHITE, M.G Br. Antarct, Surv. Bull., 8: CLARKE, A. & LEAKEY, R.J.G Limnol. Oceanogr., 41: PICKEN, G.B Ph.D. Thesis, Univ. Aberdeen. 13. STARR, M., HIMMELMANN, J.H. & THERRIAULT, J.-C Science, 247: HIMMELMANN, J.H J. Exp. Mar. Biol. Ecoi., 2: REID, D.G Phil. Trans. R. Soc, B 324: STANWELL-SMITH, D. & PECK, L.S., Biol. Bull. (submitted). 17. FOSTER, R.D In: Antarctic ecology II (R.M. Laws, ed.), Academic Press, London. 18. Ross, R.M., QUETIN, L.B. & KIRSCH, E J. Exp. Mar. Biol. Ecoi, 121: PEARSE, J.S Amer. Zooi, 31: HOEGH-GULDBERG, O. & PEARSE, J.S Amer. Zooi, 35: 415^( COSSI, A.R. & BOWLER, K Temperature biology of animals. Chapman & Hall, London. J. Moll. Stud. (1998), 4, The Malacological Society of London 1998 The size and shape of dog-whelks, Nucella lapillus (L.) recolonising a site formerly polluted by tributyltin (TBT) in anti-fouling paint J.H. Crothers Field Studies Council at Neltlecombe Court, Williton, Taunton, Somerset TA4 4HT Watermouth Cove lies on the North Devon coast between Ilfracombe and Combe Martin at 51 13'N 4 4'W (Fig. 1). It is the only natural harbour in the area, apart from Ilfracombe itself, and provides a large number of drying moorings for small boats. The north side of the Cove is the only site along the North Devon/Somerset coast which shows a clear exposure gradation from about Grade 3' in the entrance to Grade 7 further up and, as such, was often visited by groups of students from Nettlecombe Court when studying rocky shore zonation patterns or the variation in dog-whelk (Nucella lapillus) shell shape ratio with exposure 2. Alas, no records were kept (by me) of these student data but I took groups there, on many occasions in the 197s, in order to record L/Ap ratios of 1.47 (indicating exposure grade 7) in the cove itself, grading to 1.32 (exposure grade 3) in the entrance. The insidious decrease in dog-whelk abundance (almost certainly due to tributyltin (TBT) pollution but not recognised as such until the work of Bryan et al., } was published) rendered student visits unprofitable in the 198's. Data collected in established that no breeding N. lapillus remained within the Cove. The shelteredshore form was effectively extinct, and the site was thus available for a study of recolonisation. The use Downloaded from by guest on 14 November 218
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