FAU Institutional Repository
Total Page：16
File Type：pdf, Size：1020Kb
FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. Notice: © 1996 Marine Biological Association of the United Kingdom. This manuscript is an author version with the final publication available and may be cited as: Young, C.M., Tyler, P. A., & Gage, J. D. (1996). Vertical distribution correlates with pressure tolerances of early embryos in the deep-sea asteroid Plutonaster bifrons. Journal of the Marine Biological Association of the United Kingdom, 76(3), 749-757. http://dx.doi.org/10.1017/S002531540003143X ~ <\":J \Q J. mar. bioi. Ass. UX (1996), 76,749-757 749 Printed in Great Britain VERTICAL DISTRIBUTION CORRELATES WITH PRESSURE TOLERANCES OF EARLY EMBRYOS IN THE DEEP-SEA ASTEROID PLUTONASTER BIFRONS CRAIG M. YOUNG*, PAUL A. TYLERt AND JOHN D. GAGE+ "Division of Marine Science, Harbor Branch Oceanographic Institution, 5600 US Highway 1 N, Fort Pierce, Florida 34946, USA. 'Department of Oceanography, The University, Southampton, S09 5NH. lDunstaffnage Marine Research Laboratory, Scottish Association for Marine Science, PO Box 3, Oban, Argyll, PA34 4AD The astropectinid asteroid Pluionaster bifrons (Wyville Thomson) occurs on the conti nental slope of the north-east Atlantic between 1000 and 2500 m depths. As in most deep sea animals, the factors limiting bathymetric distribution of this species are unknown. Eggs were fertilized in vitro and incubated through the early embryonic cleavage stages at pressures that correspond to depths from 0 to 3000 m. The highest percentage of normal development occurred near the peak of the species distribution (2000 m), and virtually no normal development occurred at a pressure corresponding to 3000 m depth. Develop mental rate was retarded at pressures higher and lower than those found near 2000 m. These experiments indicate that embryonic pressure tolerances could determine both the upper and lower bathymetric limits of distribution for this species. INTRODUCTION Distributional limits of deep-sea animals have been attributed to various physical and biological factors such as temperature (LeDanois, 1948; Carney et al., 1983), pres sure (Somero et al., 1983), substratum characteristics (Haedrich et al., 1975), or water masses (Gage, 1986; Rowe & Menzies, 1969), but virtually all evidence to date has been correlative and there have been few attempts to test any of the proposed hypotheses experimentally. Many authors have assumed that control of distribution occurs in the larval stages (Rowe & Menzies, 1969: Cutler, 1975). In a thorough but necessarily speculative review of the factors controlling bathymetric distributions, Carney et al. (1983) issued an appeal for experimentation and predicted that further understanding of deep-sea distributions will likely come only as we are able to test the causes. One of the most consistently documented bathymetric patterns in the world ocean is an abrupt increase in the number of species appearing on the slope at between 1000 and 1400 m depth (Gage, 1986; Haedrich et al., 1975, 1980; Mills, 1972; Menzies et al., 1973). Some workers have suggested that this faunal change lies at a natural boundary that marks the beginning of the bathyal zone (Menzies et al., 1973). Secondary increases in appearance and disappearance of species occur at various depths, depending on the taxon underconsideration. For example, Vinogadova (1962) showed that many inverte brate phyla undergo a major faunal transition at -3000 m. 750 CRAIG M. YOUNG, PAUL A. TYLER AND JOHN D. GAGE The hydrostatic pressures found at abyssal depths cause death or adverse sub-lethal effects in both adults and embryos of most shallow-water marine invertebrates (re viewed by Hugel, 1972; Vemberg & Vemberg, 1972). Likewise, many adult deep-sea organisms, including bacteria, protozoans, metazoan invertebrates, and fishes, are barophilic, requiring high pressures to undergo normal physiological functions (e.g. Turley et al., 1993; Yayanos, 1978, 1981a; Yayanos et al., 1981b; Jannasch & Wirsen, 1983; Childress & Somero, 1979). The physiological basis for barophilia involves pressure induced volume changes within cells, organelles, and molecules (Somero et al., 1983; Somero, 1992a,b). In a series of detailed studies on cellular effects of high pressure, embryos of the sea urchin Arbacia punctulata developed abnormally at high pressures (Marsland, 1938, 1970; Zimmermann & Marsland, 1964). Such pressure effects are exacerbated by the low temperatures present in the abyssal zone (Marsland, 1950). We have recently demonstrated barophilia in embryos of Echinus affinis, a regular sea urchin living at a depth of -2000 m in the North Atlantic (Young & Tyler, 1993). This finding is significant from an ecological standpoint because the lower pressure limit tolerated by embryos of E. affinis correlates well with the upper limit of bathymetric distribution. However, the potential role of pressure in setting the lower limit of this or any other deep-sea species has not been investigated. We have investigated the poten tial role of pressure in regulating the lower distribution of ten littoral and bathyal echinoids from tropical seas (Young et al., 1996), and five additional littoral echinoids from the coasts of France and Britain (Young & Tyler, unpublished data). Every shallow-waterspecies thathas been tested to date (including those reviewed by Marsland, 1970) is able to withstand pressures much greater than those found near the lowerlimits of their vertical ranges. Here we provide preliminary data on the pressure physiology of developing em bryos of the lowerbathyal sea star Plutonaster bifrons, which is only the second barophilic invertebrate species whose embryoshavebeen reared in vitro. Plutonasier bifrons spawns small (120 urn) eggs which are of a size that would be expected to produce planktotrophic larvae (Tyler & Pain, 1982). It has a discrete but extended reproductive period ranging from early January to April. This reproductive season would place larvae in the water column just prior to the spring phytoplankton bloom, which varies in timing by as much as six weeks each year (Rice et al., 1986), but which usually begins in early May. The postlarval development has been described by Sibuet & Cherbonnier (1972). Adults feed on a variety of benthic invertebrates, including protobranch bivalves and other asteroids, as well as on carrion (Tyler et al., 1993, 1994). Analysis of gut contents and pyloric caeca weights indicates that feeding activity and nutrient storage vary season ally and out of phase with the gametogenic cycle (Tyler et al., 1993, 1994). Plutonaster bifrons occurs on the continental slope from the Faeroe Channel to South Africa (Clark & Downey, 1992). Its bathymetric range in the Rockall Trough region of the north-east Atlantic is from 1000 to 2500 m (Gage, 1986; Gage et al., 1983) but the species has been reported as shallow as 630 m and as deep as 2965 m elsewhere (Clark & Downey, 1992). The data we report here show an approximate correlation between pressure tolerances of the cleaving embryos and adult bathymetric range, suggesting the possibility that both the lower and upper limits of this slope species may be determined by pressure physiology in early life-history stages. ,GE PRESSURE TOLERANCES OF ASTEROID EMBRYOS 751 MATERIALS AND METHODS ~rsesub-lethal ~rtebrates (re- Plutonaster bifrons (Figure lA) were collected by Agassiz Trawl from a depth of 2200 dult deep-sea m on 10 March 1993 at Station M (Gage et al., 1983) on the Hebridean Slope off northern :l.dfishes, are Scotland. Unctions (e.g. Wirsen, 1983; lIves preSSure ro et al., 1983; ugh pressure, Lighpressures Ie effects are md,1950). , a regular sea ~r,1993). This Jressure limit f bathymetric limit of this or ted the poten- t and bathyal )ral echinoids data). Every lby Marsland, .elower limits veloping ern- md barophilic 'ifrons spawns lanktotrophic eriod ranging e in the water timing by as in early May. )972). Adults res and other Figure 1. (A) Adult Plutonaster bifrons collected from the Hebridean Slope. (B) Newly fertilized ovum contents and of Plutonaster bifrons surrounded by spermatozoa: fu, female nucleus and mn, male pronucleus are ,vary season- visible in the cytoplasm. (C) Late 2-cell embryo initiating second cleavage incubated at 200 atm. (D) Irregular 2-cell embryo incubated at 1 atm. (E) Normal4-cell embryo from 200 atm culture. Scale bar applies to B-F. F, typical embryo incubated at 300 atm pressure that has undergone several irregular nnel to South cleavages. ugh region of 1983) but the Ovaries were dissected from two females and suspended in cold (4°C) sea-water. At where (Clark the time of dissection, many oocytes already appeared to be mature (no germinal ltion between vesicles were visible). Testes were removed from a single male and macerated in cold e, suggesting sea-water. Sperm became very active immediately upon dilution and were used to ~cies may be inseminate eggs teased from the ovaries within a few minutes thereafter. In a subse- 752 CRAIG M. YOUNG, PAUL A. TYLER AND JOHN D. GAGE quent trawl, we found a female with a gonad containing numerous primary oocytes. Incubation in a sea-water solution of I-Methyladenine for 12 h resulted in germinal vesicle breakdown of ~20% of the eggs. However, no viable sperm were available by this time, so additional cultures were not obtained and the experiments could not be repeated a second time. We cleaned much of the gonad debris from cultures by passing the embryos through various grades of nitex screen. Nevertheless, because gametes were obtained by dissec tion and maceration, only a small fraction of each culture consisted of mature eggs that were fertilized successfully. The total percentage of full-sized eggs undergoing cleav age (including both normal and irregular cleavages) ranged from 19·35 to 33·75% (mean: 24·32%; SO ±4·84; N==12) in the various cultures. As cleavage was the only sure indication that any given egg was mature enough to develop, all subsequent analyses involve only eggs that underwent at least one normal or abnormal division.