2003 NORTHEASTERN NATURALIST
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1 2003 NORTHEASTERN NATURALIST 10(1):17 24 EFFECT OF TEMPERATURE ON DEVELOPMENT TIME IN EGG MASSES OF THE INTERTIDAL NUDIBRANCH, DENDRONOTUS FRONDOSUS (ASCANIUS 1774) (OPISTHOBRANCHIA, DENDRONOTACEA) Janet L. Watt 1 and Ronald B. Aiken 1,* ABSTRACT - Dendronotus frondosus (Ascanius 1774) is a common inhabitant of the intertidal zone of the lower Bay of Fundy. This nudibranch experiences great daily fluctuations in physical conditions that affect all aspects of its life cycle. We examined the effect of temperature (5, 11, and 15 C) on the development time of eggs of an intertidal population of this species. Eggs developed more slowly at 5 C than at 11 C and did not develop past the second polar body stage at 15 C. The effect of this difference in development time may be to compress the settlement period to span less time than the oviposition period. INTRODUCTION The effects of temperature on development time have been described for several species of opisthobranch molluscs (Chia 1973, Dehnel and Kong 1979, Eyster 1986, Farfan and Ramirez 1988, Harris et al. 1980, Kress 1975, Lalli and Conover 1973, Morse 1971, Perron and Turner 1977, Strathmann 1987, Thompson , Todd and Havenhand 1985, Williams 1974). In those studies where comparisons were made between development times at different temperatures, there was always a negative correlation between these two parameters (Dehnel and Kong 1979, Farfan and Ramirez 1988, Lalli and Conover 1973, Perron and Turner 1977, Thompson 1966, Todd and Havenhand 1985). Intertidal organisms in the Bay of Fundy are faced with extreme daily fluctuations in several physical factors (see papers in Thomas 1983) that could have profound effects on their survival. These effects can be realized at several points in the life cycle. In this paper we describe temperature effects on the development times of eggs of a nudibranch mollusc Dendronotus frondosus to test the hypothesis. Dendronotus frondosus is a common intertidal inhabitant of the rocky shores of the Bay of Fundy. Its eggs are laid in May and June (Aiken 2003), primarily on rock surfaces that, at low tide, are covered with the knotted wrack Ascophyllum nodosum. In the northeast Pacific, 1 Department of Biology, Mount Allison University, Sackville, New Brunswick, Canada E4L 1G7. * Corresponding author - raiken@mta.ca.
2 18 Northeastern Naturalist Vol. 10, No. 1 D. frondosus lays an egg mass of Type B (Hurst 1967). Such egg masses are characterized by a jelly sheet attached to the substrate and a cylindrical area that contains the egg capsules and is secondarily twisted. Dendronotus frondosus lays an untidy coil (Hurst 1967) that varies in color, although Todd (1981) found that eggs are generally white with some masses displaying yellow and pink eggs. Dendronotus frondosus eggs have been recorded to hatch in 6 days at 14 C (Williams 1974), 7 15 days at 8 11 C (Hurst 1967), 32 days at 10 C (Sisson 2002), and 32 days at 10 C (Thompson 1967). Since there was considerable variation in the recorded hatch times within overlapping ranges of temperature, we decided to compare development times of eggs of this species from the same local population. MATERIALS AND METHODS Specimens of D. frondosus were collected at low tide at Green s Point 16 km south of St. George, New Brunswick (45 04 N, W). Green s Point is at Letite Passage between Passamaquoddy Bay and the Bay of Fundy. We removed animals by hand from rock surfaces throughout May and June. Specimens were placed in plastic buckets containing sea water at ambient temperature and were transported to the Huntsman Marine Science Centre in St. Andrews, N.B. These animals were placed individually in screened polypropylene tubes. The tubes were floated in 57 L plastic aquaria receiving flow-through sea water pumped directly from the ocean. Animals were allowed to acclimate for 24 h before being transferred to the experimental apparatus. The experimental apparatus for each temperature tested consisted of a 10 L glass tank placed inside a larger 57 L plastic aquarium. The larger aquarium served as a water bath and was enclosed in 2.5 cm thick styrofoam insulation. The 10 L glass tank stood on 4 bricks inside the plastic aquarium for exposure to an even flow in the water bath. There were three identical setups, maintained at either 5, 11, or 15 C. The 57 L water baths were maintained at the temperatures of 5 and 15 C with the use of Haake-D1, Fisons (typ ) temperature control units. The tank maintained at 11 C received ambient temperature direct flow seawater that was pumped directly from Passamaquoddy Bay. The experimental temperatures used in this experiment are representative of those to which developing egg masses would be subjected in the field. Temperatures of 5 and 11 C would be typical of mid to late spring (April early May) and early summer (late June), respectively. At our field site, 15 C does not normally occur but has been recorded from the area in the last century (Lotze and Milewski 2002). Light intensity and photoperiod were not controlled and varied with ambient light entering the laboratory windows.
3 2003 J.L. Watt and J.B. Aiken 19 The small glass aquaria were lined (bottom and sides) with precleaned glass microscope slides which served as egg-laying substrates. Sea water depth was similar in each of the three 10 L aquaria and covered the glass slides. Each tank was approximately one-third full. Thermometers in each of the three 10 L glass aquaria monitored temperature daily. An air stone with a Hagen-Elite 802 air pump aerated each of the 10 L aquaria. Salinity ( ) was recorded daily with a temperature compensated refractometer (Bio Marine Inc., Aquafauna). The animals were placed individually in plastic bags that were floated, one per 10 L glass aquarium, for 1 h to acclimate to their respective temperatures before being released to lay eggs. Once an egg mass was laid, the glass slide was inserted into a polypropylene specimen container. The specimen containers had l cm holes on opposite sides covered with Nitex mesh to provide aerated water to the eggs. The containers were assigned an identification number and placed back into their respective aquaria. Observations of developmental sequence and timing were made on each egg mass each hour for the first 12 h after oviposition, every 6 h for the next 72 h, and then once daily until the eggs hatched. Fourteen developmental stages between the 1-cell and hatching stage were identified and monitored (Fig. 1). A Wild Heerbrugg M compound microscope and Wild Heerbrugg Apochromat dissecting microscope were used to make these observations. The longest dimension of 90 newly laid eggs (30 from each temperature) was measured using an ocular micrometer on the Wild Heerbrugg M compound microscope. Cumulative time (min) for development was calculated for each of the 46 egg masses observed. Because not all egg masses were discovered at the time of egg laying, only those found at 1-cell stage were used. The number of egg masses scored was 13, 16, and 17 at 5, 11, and 15 C, respectively. Differences in hatching time were compared for significance with a one-tailed student t-test for unpaired samples (Zar 1984). RESULTS Egg masses of this intertidal population of D. frondosus contain several thousand eggs and have a white and translucent appearance from a thick gelatinous matrix that surrounds the eggs. In the field, they are laid on rock surfaces though they were laid readily on glass microscope slides in the laboratory. The mean diameter of an undeveloped egg was 142 ± 15.8 µm ( X ± SD). All values presented below represent the average development period in days ± SD at each stage for all egg masses at a given temperature regime. Variation in temperature and salinity is shown in Table 1.
4 20 Northeastern Naturalist Vol. 10, No. 1 At 5 C, all 13 egg masses examined had synchronous development with approximately 90% of the several thousand eggs in each mass at the same stage of development at any given time. The mean cumulative time from fertilization to hatching at this temperature was 33.2 ± 6.16 days (Fig. 1). At 11 C ambient temperature, all 16 egg masses monitored showed development and the mean cumulative time to complete development was 19.1 ± 5.7 days (Fig. 1). Statistical analysis of the 5 and 11 C cumulative development data revealed that the time to hatch at 5 C was significantly longer than at 11 C ambient temperature (one-tailed t-test, t = 4.91, df = 15, P < ). At 15 C, the 17 egg masses observed developed a very different pattern from than seen at the lower temperatures. Regular development never proceeded after the second polar body stage and no eggs ever hatched. Within 6 h of being laid, the entire egg mass appeared abnormal from cell divisions that produced either uneven cleavage (1 large cell with 5 or 6 small cells), or intermediate stages (i.e., with 3, 6, or 7 cells). Some eggs exhibited no cleavage, indicating that they were either unfertilized or dead. DISCUSSION There is no shortage of confusion over the taxonomic status of D. frondosus. Animals used in this study correspond to the northern intertidal form of Sisson (2002) or the intertidal ecomorph of Aiken (2003). The identity of animals described as D. frondosus in the Pacific (Hurst 1967, Williams 1974) or Europe (Swennen 1961, Thompson 1967) and their relationship to the species used here await a taxonomic evaluation. Consequently, comparisons between populations in different geographic areas must be treated with some caution. Two of the temperatures at which eggs from intertidal D. frondosus were incubated (5 C and 11 C) could be expected in the field over the reproductive season. The hypothesis that the time taken for development would decrease as temperature increased was indeed observed for these two experimental temperatures. Development of this intertidal population of D. frondosus took longer at 5 C than it did at 11 C, with cumulative averages to hatching of 33.2 and 19.1 days, respectively. As such, this population of D. frondosus conforms with Table 1. Mean temperatures ( C ± SD) and salinities recorded over the duration of egg development for Dendronotus frondosus. Nominal Temperature Recorded Temperature Salinity Range (ûc) (ûc ± SD) ( ) ± ± ±
5 2003 J.L. Watt and J.B. Aiken 21 earlier calculations on egg size and development time (Todd and Doyle 1981). Egg masses at both of these temperatures developed synchronously, with approximately 90% of the eggs in each mass at the same stage at the same time. Therefore, at least 90% of each egg mass was fertilized leaving few empty capsules. In the present study, at 15 C, development ceased at the second polar body. This result is similar to that of Dehnel and Kong (1979) for Cadlina luteomarginata. In their study, development did not proceed beyond the fourth cleavage at 20 C. It must be assumed that the eggs laid by animals from the sampled population of D. frondosus were not adapted to constant immersion at this high water temperature and therefore could not develop. The temperature range of Passamaquoddy Bay during mating, reproduction, and consequent egg laying seasons is from 3 to 12 C (Forgeron 1959). Our observations from the present study and those from published temperature data (Forgeron 1959) indicated that surface temperatures of the sea at this site would rarely reach 15 C. Lotze and Milewski (2002) indicate that this surface temperature was reached only 3 times in the last 100 years. There have been two previously published studies on the time taken to hatching for D. frondosus in North America. Williams (1974) studied veliger development in a California population and found that at 14 C, animals hatched at a mean cumulative time of 6.1 days. These data are markedly different from the results of the present study and show that Hatch Late veliger Active veliger Early veliger Trochophore Gastrula Blastula Fourth Division 5ûC (N = 13) 11ûC (N = 16) 15ûC (N = 17) Third Division Second Division First Division Polar Body 2 Polar Body 1 1-Cell Mean Cumulative Development Time (days ± s.d.) 40 Figure 1. Mean cumulative development time (days ± 1 SD) for eggs of Dendronotus frondosus at 5, 11, and 15 C.
6 22 Northeastern Naturalist Vol. 10, No. 1 eggs from this population developed rapidly at temperatures very close to those at which we observed no development. This again raises the question of whether these are simply differences reflecting adaptation of local populations to local conditions or whether these are separate species. Results presented by Sisson (2002) are directly comparable to those from this study. Sisson s northern intertidal form of D. frondosus is the same animal as studied here. The times taken to hatching are very similar, although eggs from this study were smaller. We did no detailed analysis of the larvae produced from these eggs but they were, based on casual observation, the lecithotrophic veligers described by Sisson (2002). This temperature-dependent rate of development means that eggs laid very early in the season will develop more slowly than those deposited later. The effect of this is to compress the period for veliger release and subsequent settlement to one much shorter than that devoted to egg laying (Todd and Doyle 1981). Since these are lecithotrophic larvae (Sisson 2002), the dispersal period would, presumably, be much less variable and lead to a more proscribed settlement period. This compression of the settlement period allows larvae to take advantage of the year s warmest water (June through October) (Trites and Garret 1983) for post-settlement growth before winter. Further experimentation relating development time with the point in the reproductive season at which eggs were laid would be needed to answer this question. ACKNOWLEDGMENTS We thank C. Carey and D. McClary for help with collection of specimens. Laboratory facilities were provided by the Huntsman Marine Science Centre and we wish to especially thank Mr. Fred Purton for his assistance. J. Stewart read an early draft of the manuscript and substantial improvements were made by three anonymous reviewers. Financial support was provided by a Gates-Kirkland Summer Fellowship to JLW and NSERC Research Grant 2286 to RBA. LITERATURE CITED Aiken, R.B Some aspects of the life history of an intertidal population of the nudibranch, Dendronotus frondosus (Ascanius, 1774) (Opisthobranchia: Dendronotoidea) in the Bay of Fundy. The Veliger 46: Chia, F. S Oviposition, fecundity, and larval development of three sacoglossan opisthobranchs from the Northumberland Coast, England. The Veliger 13: Dehnel, P.A., and D.C. Kong The effect of temperature on developmental rates in the nudibranch Cadlina luteomarginata. Canadian Journal of Zoology 57:
7 2003 J.L. Watt and J.B. Aiken 23 Eyster, L.S The embryonic capsules of nudibranch molluscs: literature review and new studies on albumen and capsule wall ultrastructure. Bulletin of the American Malacological Society 4: Farfan, B.C., and L.F.B. Ramirez Spawning and ontogeny of Bulla gouldiana (Gastropoda: Opisthobranchia: Cephalaspidea). The Veliger 31: Forgeron, F.D Temperature and salinity in the Quoddy Region. International Passamaquoddy Fisheries Board Report to the International Joint Commission. Appendix I, Oceanography. Harris, L.G., M. Powers, and J. Ryan Life history studies of the estuarine nudibranch Tenellia fuscata (Gould 1870). The Veliger 23: Hurst, A The egg masses and veliger of thirty northeast Pacific opisthobranchs. The Veliger 9: Kress, A Observations during embryonic development in the genus Doto (Gastropoda: Opisthobranchia). Journal of the Marine Biological Association of the United Kingdom 55: Lalli, C.M., and R.J. Conover Reproduction and development of Paedoclione doliiformis, and a comparison with Clione limacina (Opisthobranchia: Gymnosomata). Marine Biology 19: Lotze, H.K., and I. Milewski Two hundred years of ecosystem and food web changes in the Quoddy Region, outer Bay of Fundy. Conservation Council of New Brunswick. Fredericton, NB. Canada. 188 pp. Morse, M.P Biology and life history of the nudibranch mollusc Coryphella stimpsoni (Verrill 1879). Biological Bulletin 140: Perron, F.E., and R.D. Turner Development, metamorphosis, and natural history of the nudibranch Doridella obscura Verrill (Corambidae: Opisthobranchia). Journal of Experimental Marine Biology and Ecology 27: Sisson, C.G Dichotomous life history patterns for the nudibranch Dendronotus frondosus (Ascanius 1774) in the Gulf of Maine. The Veliger 45: Strathmann, M.F Opisthobranchia. Pp , In M.F. Strathmann (Ed.). Reproduction and development of marine invertebrates of the northern Pacific coast. University of Washington Press, Seattle, WA. 670 pp. Swennen, C Data on the distribution, reproduction and ecology of the nudibranchiate molluscs occurring in the Netherlands. Netherlands Journal of Sea Research 1/2: Thomas, M.L.H. (Ed) Marine and coastal systems of the Quoddy region, New Brunswick. Canadian Special Publication Fisheries and Aquatic Sciences 64. Ottawa. ON. Canada. 306 pp. Thompson, T.E Studies on the reproduction of Archidoris pseudoargus (Rapp) (Gastropoda Opisthobranchia). Philosophical Transactions of the Royal Society of London (B) 250: Thompson, T.E Direct development in a nudibranch, Cadlina laevis, with a discussion of developmental processes in the Opisthobranchia. Journal of the Marine Biological Association of the United Kingdom 47:1 22. Todd, C.D The ecology of nudibranch molluscs. Oceanography Marine Biology Annual Review 19:
8 24 Northeastern Naturalist Vol. 10, No. 1 Todd, C.D., and R.W. Doyle Reproductive strategies of marine benthic invertebrates: a settlement-timing hypothesis. Marine Ecology Progress Series 4: Todd, C.D., and J.N. Havenhand Preliminary observations on the embryonic and larval development of three dorid nudibranchs. Journal of Molluscan Studies 51: Trites, R.W., and C.J.R. Garrett Physical oceanography of the Quoddy region. Pp. 9 34, In M.L.H. Thomas (Ed.). Marine and Coastal Systems of the Quoddy region, New Brunswick. Canadian Special Publication Fisheries and Aquatic Sciences 64. Ottawa. ON. Canada. 306 pp. Williams, L.G Veliger development in Dendronotus frondosus (Ascanius 1774) (Gastropoda: Nudibranchia). The Veliger 14: Zar, J.H Biostatistical analysis. Prentice-Hall. London, UK.
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