Survey
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
Journal of Plankton Research Vol.20 no3 pp.557-569, 1998 Production of tropical larvaceans in Kingston Harbour, Jamaica: are we ignoring an important secondary producer? Russell R.Hopcroft1 and John C.Roff Department of Zoology, University ofGuelph, Guelph, Ontario NIG 2W1, Canada 1 Present address: Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, CA 95039-0628, USA Abstract. The larvacean community was observed during an 18 month period at the mouth of eutrophic Kingston Harbour, Jamaica. During this period, larvaceans averaged 3607 m~3 with a biomass of 2.2 mg ash-free dry weight m~3 (32.6 mg AFDW nr 2 ) in a community dominated by Oikopleura longicauda. There were no relationships between larvacean biomass and any size fraction of chlorophyll, suggesting that other factors must normally regulate larvacean communities. The evidence indicates that this regulation is by predation. Annual production by larvaceans was 586 kJ nr 2 year 1 (29.3 g AFDW nr 2 year 1 ); production of houses could represent an added 300-600 kJ nr 2 year 1 . While copepod biomass was 10 times higher than that of the larvaceans during the same period, copepod growth rates were only one-third those of larvaceans. Thus, larvacean annual production is at least 30% that of the copepods, due to their rapid growth rates, and at least 50% that of the copepods when house production is considered. The contribution of larvaceans to plankton production has been underappreciated historically when only their biomass is considered. Introduction Copepods have generally been considered the most important metazoan secondary producers in pelagic marine ecosystems, both in terms of abundance and biomass (e.g. Raymont, 1983). Only recently has much numerical attention been paid to other groups, such as the salps and larvaceans, that are also common components of these communities (King et al., 1980; Alldredge, 1981, 1984; Deibel, 1985). These gelatinous taxa have proven more difficult to quantify due to temporal and spatial heterogeneity (e.g. Seki, 1973; Paffenhofer and Lee, 1983; Uye and Ichino, 1995; Nakamura et al, 1997) in combination with generally inappropriate sampling techniques (but see Paffenhofer, 1983). Larvaceans can contribute significantly to planktonic biomass (see previous references; Hopkins, 1977; Clarke and Roff, 1990; Roff et al., 1990; Hopcroft and Roff, 1995) and their growth rates are typically much greater than those of copepods at the same temperature (Hopcroft and Roff, 1995; Uye and Ichino, 1995; Hopcroft et al, 1998a). Production by larvaceans could therefore be significant in comparison to that of the copepods, even though their biomass may be lower, because their higher growth rates may compensate for a lower biomass. Here we present estimates of the abundance, biomass and production of larvaceans in a tropical neritic ecosystem, where growth rates of zooplankton will be at their temperature-dependent maxima. Tropical waters are, in general, poorly studied, but the planktonic marine communities surrounding Jamaica have been the focus of extensive study over the past decade (Roff et al, 1990; Webber and Roff, 1996; Webber et al, 1996; Hopcroft et al, 1998b). This study represents © Oxford University Press 557 R.R.Hopcroft and J.CRoff the second part of a detailed comparison of annual larvacean production at sites along a trophic continuum from oligotrophic offshore waters through mesotrophic coastal waters (Clarke and Roff, 1990; Roff et al, 1990) to eutrophic Kingston Harbour. Method The study site was located in the outer region of Kingston Harbour (see Figure 1 in Hopcroft et al, 1998a) in an area with a relatively constant depth of 15 m. Depths inside the harbour do not generally exceed 15 m, and average between 5 and 10 m. Previous studies have indicated the eutrophic nature of this region of the harbour (Wade etal., 1972; Webber etal., 1992). Temperature and salinity vary little annually, generally ranging from 27 to 30°C, and from 34 to 36%o, respectively. Some depression of these parameters is possible after extremely heavy rains due to the outflow from Hunt's Bay, a shallow embayment that receives the harbour's only river (Webber et al, 1992). Plankton samples were collected fortnightly between July 1992 and December 1993. Zooplankton collections were taken using 64 and 200 urn mesh plankton nets of 0.5 m mouth diameter (modified, WP2 pattern). Each net was hauled vertically from 12 m depth to the surface at -0.3 m s"1. Duplicate samples were killed immediately in 2% formalin, and later preserved in 10% formalin. Concurrent collections for phytoplankton were taken by replicate Niskin bottle casts at 1, 5 and 10 m; 2 1 from each cast were filtered serially through 20 um Nitex, GF/D (nominal pore size ~2 um) and GF/F (-0.4 um) filters under low pressure to determine size-fractionated chlorophyll (net-, nano- and picoplankton, respectively), using fluorometric techniques [see Hopcroft and Roff (1990) for further details]. Light attenuation was determined for most occasions using a Licor quantum sensor. Larvaceans from 64 um net samples on each date were identified with the aid of Buckman and Kapp (1975), then enumerated and measured using the ZoopBiom software and digitizing system of Roff and Hopcroft (1986). Sample aliquots were obtained using the beaker split method (Van Guelpen et al, 1982), with up to 120 individuals of a given taxon measured; increasingly larger aliquots were examined for less abundant species when they were common. Flowmeters were employed inside and outside of the plankton nets, and the average filtration efficiency of 45% was used to estimate abundance; similar values for filtration efficiency have been obtained previously for these nets (Chisholm and Roff, 1990a). Biomass, expressed as ash-free dry weight (AFDW), was calculated for each individual based on trunk (lower lip to back of trunk) length-weight regressions from Hopcroft et al. (1998a). To estimate shrinkage after preservation, freshly collected killed individuals were measured five times, repositioning after each measurement. After 4 months in 10% formalin, the same individuals were remeasured five times. The before and after preservation trunk lengths were analysed by species, using an ANOVA with individuals considered as blocks. Growth rates were taken from Hopcroft et al (1998a), with rates pooled by 558 Production of tropical larvaceans in Kingston Harbour family (i.e. Oikopleuridae, Fritillaridae). With few exceptions, growth rates of Fritillaridae were only available from nearby Lime Cay, but we limited our use of data to rates obtained in experiments where chlorophyll concentrations, produced by nutrient enhancement, were within the range observed in Kingston Harbour. Similarly, because growth rates estimated by our techniques may be sensitive to extremely high concentrations of total zooplankton (Hopcroft and Roff, 1995; Hopcroft etal, 1998a), data were also restricted to those observations when larvacean biomass was within the range normally encountered in the harbour. Thus restricted, there was no significant difference between species within families (f-test, P > 0.05). The mean daily specific growth rates employed for this study were: 2.49 ± 0.14 day-1 (n = 21, range = 1.2-3.3) for the Oikopleuridae and 2.03 ± 0.07 day 1 {n = 35, range = 1.5-2.8) for the Fritillaridae. Estimates of annual production were obtained by the instantaneous growth rate method, with daily production calculated as the product of an individual's biomass and the instantaneous growth rate (Pr = B X g; see Hopcroft et ai, 1998a). Daily production was averaged over the entire sampling period, assuming an energy density of 20 kJ g"1 AFDW calculated from the biochemical composition of Thaliaceae (Madin etal., 1981). Results Phytoplankton community The phytoplankton community was distinctly layered in its biomass, as indicated by chlorophyll a and phaeopigment concentrations (Figure 1). Chlorophyll was 1 m A ill /uii o « J J A S O N D J F M A M J J A S O N D J J A S O N D J F M A M J J A S O N O 1992 1993 1992 1993 Fig. 1. Seasonal and vertical variations in chlorophyll a and phaeopigment concentrations in outer Kingston Harbour. Accumulative concentration in picoplankton (•), pico + nanoplankton (O) and total (A). 559 RJUlopcroft and J.CRoff highest (mean 1.98 mg nr 3 ) and most variable (CV = 73%) in the surface waters,, with concentration and variability decreasing with depth (mean 1.21 mg nr 3 , CV = 56% at 5 m; mean 0.96 mg nr 3 , CV = 54% at 10 m). At all depths, nanoplankton dominated the community, contributing 70% of the chlorophyll at the surface and less at depth (59% at 5 m; 47% at 10 m). The picoplankton was the least variable size fraction, either within or among depths, while the netplankton was the most variable. Weighting for depth (i.e. 1,5 and 10 m samples were taken as representative of 0-2.5, 2.5-7.5 and 7.5-15 m, respectively), chlorophyll a concentration averaged 1.19 mg nr 3 (17.9 mg nr 2 ), with 15,59 and 26% contributed by the net-, nano- and picoplankton, respectively. Phaeopigments were less variable than chlorophyll a, with the relative contribution by phaeopigments increasing with depth. Weighting for depth, phaeopigment averaged 0.60 mg nr 3 —50% that of chlorophyll a—indicating an environment dominated by actively growing rather than detrital pigments. The depth of the euphotic zone (1 % surface irradiance) generally exceeded the station's depth, averaging 21.7 m (range 15.5-32 m). Larvacean community A total of seven larvacean species were identified in Kingston Harbour over the 34 sampling occasions. Mean larvacean abundance was 3607 nr 3 (range 0-16 910) or 54 100 nr 2 and mean biomass was 2.2 mg AFDW nr 3 (range 0-10.3) or 32.6 mg AFDW nr 2 . With the exception of one date when larvaceans were virtually absent, there was a range of values of -1-1.5 orders of magnitude in both these estimates (Figure 2). Oikopleura longicauda dominated the larvacean community, both in terms of abundance (79%) and biomass (87%; Table I). Appendicularia sicula, Fritillaria borealis sargassi and Oikopleura dioica each made comparable but variable contributions to the larvacean community biomass, occasionally even dominating the biomass (Figure 3). Although often observed, F.haplostoma, F.pellucida and O.fusiformis were relatively unimportant in terms of abundance or biomass. All data were adjusted for shrinkage on preservation, which although minimal (averaging 3.4% of live trunk length), was nonetheless significant for the three species examined: O.longicauda (n = 16, P < 0.0001), O.dioica (n = 6,P< 0.0001) and A.sicula (n = 6,P = 0.0064). The size-frequency distributions of larvaceans were concentrated between 100 and 600 um trunk length (Figure 4). The few scattered occurrences of individuals larger than 800 um were contributed by F.haplostoma. Microcosm experiments (Hopcroft et aL, 1998a) suggested that some juveniles may pass through a 64 um screen, particularly for the smallest species A.sicula; however, in terms of biomass, such losses are probably insignificant. We could determine no meaningful relationships between concurrent chlorophyll estimates in any size fraction (singly or combined) and larvacean biomass. No relationships were found between copepod biomass (by genus or combined) and larvacean biomass, although none of the four peaks of larvacean biomass occurred during times of high copepod biomass (data from Hopcroft et aL, 1998b). 560 Production of tropical larvaceans in Kingston Harbour JJASONDJ FMAMJJASOND 1992 1993 Fig. 2. Seasonal abundance, biomass and production of the larvacean community from outer Kingston Harbour. Production by the larvacean community averaged 107 J m~3 day 1 (5.4 mg AFDW nr 3 day 1 ) or 586 kJ nr 2 year 1 (29.3 g AFDW m"2 year 1 ). The annual pattern of productivity was similar to that of biomass (Figure 2), with production overwhelmingly dominated by O.longicauda. Discussion Control of population abundances The lack of any significant temporal relationship between larvaceans and chlorophyll at the harbour station suggests that phytoplankton is generally not the factor modulating their biomass or production. This is consistent with the observation that a maximum of only 24% of the variation in growth rate can be explained in terms of chlorophyll (Hopcroft et al, 1998a). The phytoplankton 561 R.R.Hopcroft and J.CRoff 100 J A S O N D J F M A M J J A S O N 1992 1993 Fig. 3. Seasonal contributions of each species to total larvacean community biomass in outer Kingston Harbour. Table L Relative contribution of the dominant larvacean species at Kingston Harbour station averaged over the sampling period from July 1992 to December 1993 Species Oikopleuridae Oikopleura dioica Oikopleura fusiformis Oikopleura longicauda Fritillaridae Appendicularia sicula Fritillaria borealis sargassi Fritillaria haplostoma Fritillaria pellucida Abundance Biomass 6.8 1.0 78.9 3.9 0.6 87.1 8.0 5.1 0.2 2.7 5.2 0.4 - community is locally influenced by winds (Hopcroft and Roff, 1990) and rainfall (Webber et al., 1992), which affect the layering and circulation of the outer harbour, but these influences will be captured in the range of chlorophyll data in our monitoring studies. We have argued (Hopcroft et al, 1998a) that larvacean instantaneous growth rates are probably not controlled by resources or competition within the range of chlorophyll and larvacean population densities normally encountered off Jamaica. In the outer harbour, the zooplankton community itself is only directly influenced by physical factors (winds, rainfall) under 562 Production of tropical larvaceans in Kingston Harbour 1000 OQ 0.00001 0 200 400 600 800 1000 1200 1400 1600 1800 Trunk Length (um) Fig. 4. Mean size spectra of larvaceans from outer Kingston Harbour based on (A) abundance and (B) biomass. extreme conditions (Webber et al, 1992). Thus, if the larvacean community is not normally strongly influenced by resources or physical factors, then it is presumably regulated by its predators. The harbour is dominated by small individuals and species of larvaceans. An inverse relationship between trunk length and temperature has been observed for O.dioica (Uye and Ichino, 1995). This same inverse relationship between body size and temperature apparently extends across the Larvacea (and the Copepoda), resulting in these populations being smaller than their temperate counterparts. The skewed size distributions of larvaceans observed in our study have also been observed in Japanese waters (Uye and Ichino, 1995). Such skewed distributions suggest that survivorship is a function of animal size. Although sizeselective competitive interactions with other nanoplankton feeders could be 563 RJUiopcroft and J.C.Roff advanced as a mechanism for long-term reduction in size frequency, such arguments are tenuous and difficult to support. We suggest that the most probable reason for small organism size here is intensive predatory control of larvacean populations throughout their life cycle, but particularly so for larger individuals. Further evidence for the significance of predatory control comes from our microcosm experiments (Hopcroft et al, 1998a). In our microcosms, at natural phytoplankton concentrations (with and without nutrient addition), larvacean populations exploded when their predators (e.g. larger copepods, cnidarians, chaetognaths, fish larvae) were excluded by the pre-screening process, reaching levels of abundance and biomass well in excess of those observed naturally. In two separate harbour microcosm experiments, larvacean populations feeding on natural concentrations of phytoplankton increased to abundances exceeding 500 000 nr 3 . Under natural conditions, in the presence of their normal complement of predators, such explosive population increases do not occur. We therefore deduce that in tropical larvacean communities, where adequate resources appear to be generally available to maintain high growth, where population biomass is low compared to other herbivores, and where major changes in abundance are infrequent, predation must generally be the major regulatory mechanism of populations. Application of growth rates We have previously argued that the growth rates of larvaceans (and salps) may make them the fastest-growing metazoans on the planet, and that they exceed the growth of the copepods by a factor of 10 or more (Hopcroft and Roff, 1995). This position was advanced from the perspective of their potential production, but the production of larvaceans in natural waters seldom reaches that observed in our experiments (but see Seki, 1973; Nakamura et al., 1997). For this reason, it is important to consider the appropriate method for expressing growth and calculating production. In planktonic animals, growth is expressed either in terms of the daily specific rate (G) or the instantaneous rate (g), where G = e« - 1 and g = ln(W,/WQ)/t. For the individual that survives a time interval, both G and g can be appropriately used to predict its final weight accurately, knowing its initial weight. However, at the population level, this equivalence only applies when individuals all survive in the absence of predation (and competition). The assumption is often made that planktonic populations and their biomass (B) are in steady state, with all production instantaneously removed by grazing. In this case, production (Pr) is appropriately calculated as Pr = gB, rather than by Pr = GB (i.e. by growth increment summation), because G describes the accumulation (compounding) of biomass during the production interval (e.g. Downing and Rigler, 1984). Discrepancies between G and g are most pronounced when g is large. For organisms with high growth rates, calculations using g will underestimate production if biomass is accumulating at maximal rates (i.e. no losses) and calculations using G will overestimate production if biomass is in steady state. In reality, zooplankton populations constantly shift between steady state and biomass accumulation or 564 Production of tropical larvaceans in Kingston Harbour reduction. From a broader perspective, which growth rate is used is functionally unimportant in temperate and polar ecosystems, because there, for most groups of organisms, g is low and close to G. In tropical ecosystems, where growth rates are generally higher and zooplankton biomass may approach a steady state, the use of the appropriate growth rate becomes important. The larvaceans represent an extreme example of discrepancies between values of g and G; our average g = 2.49 for the Oikopleuridae is equivalent to G = 11.1, an ~4 fold difference in magnitude. While we often observe larvacean production in microcosms that is most correctly predicted by Pr = BG (i.e. considerable biomass accumulates, and mortality is approximately zero; see Hopcroft and Roff, 1995), this is seldom the case in the natural environment where production is more likely to be appropriately estimated by Pr = gB. However, if feeding activity by predatory groups on larvaceans is diel, then biomass of larvaceans could accrue during the daylight period, when predatory pressure is low, only to be cropped overnight when predatory activity is higher. In such a case, despite the population appearing to be in 'steady state' from day to day, g could provide substantial underestimates of larvacean production on a daily basis. Unfortunately, such high-resolution data are seldom collected, and would be difficult to demonstrate unless the same parcel of water could be repeatedly sampled (i.e. as in a mesocosm study). Production of the larvacean community When attention has been paid to the entire zooplankton community, larvaceans are frequently cited as the 'herbivores' next in importance following the copepods (e.g. Hopkins, 1977). Our results clearly indicate that, in terms of production, larvaceans make significant contributions in comparison to the copepod community. The planktonic communities of Kingston Harbour and surrounding areas have been studied in four waves of activity and, despite the use of relatively coarse (200-288 um) nets in many of these studies, larvaceans have represented -5-20% of the observed copepod abundance (Moore, 1967; Grahame, 1976; Moore and Sander, 1979; Lindo, 1991; Webber et al, 1996). Similar proportionate contributions have been noted in Puerto Rican waters (Youngbluth, 1976, 1980; Yoshioka et al., 1985). Unfortunately, whereas copepod biomass is often quantified, the same is not true for the larvaceans. Studies in which the biomasses of both the copepods and larvaceans are concurrently estimated are rare. Fortunately, estimates of the copepod community are available concurrently with larvaceans for the outer harbour. Copepod biomass averages 22.1 mg AFDW m~3, instantaneous growth rates average -0.71 day 1 and an annual production of 1679 kJ m~2 has been estimated (Hopcroft et al., 1998b). Thus, while the average larvacean biomass of 2.2 mg AFDW m~2 is only 10% of the copepod community average, because larvacean growth rates are some 3-3.5 times higher than those of the copepods, annual larvacean production is 586 kJ m~2 year*1, -35% that of the copepods. The difference between copepod and larvacean production is further reduced if we account for the production of filtering structures ('houses'), that are discarded and re-secreted frequently. The carbon 565 RJLHopcroft and J.CRoff content of newly secreted houses has been estimated as 23 ± 13% of body carbon for O.vanhoeffeni (Deibel, 1986) with a comparable estimate of 10-20% of AFDW for O.rufencens (Alldredge, 1976, 1977). Because these houses are predominantly composed of mucopolysaccharides, their calorific value will be low (-4.3 calories g"1 = 18.1 kJ g"1). The rate of house production is of greater uncertainty. Although Fenaux (1985) determined a linear relationship between house production time and temperature, which would suggest 15 houses per day at the 28°C typical for our study, he suggested caution in extrapolating this relationship outside of his 13-23°C range. At 15 houses per day, this would be equivalent to a daily production of between 150 and 300% of the biomass, equivalent to an additional 55-110 J nr 3 day 1 or 300-600 kJ nr 2 year 1 . This yields a total larvacean production estimate of 886-1186 kJ nr 2 year 1 , which is 53-71% that of the copepods. At nearby mesotrophic Lime Cay, the abundance, biomass and production of the entire planktonic community have been previously quantified employing sampling protocols identical to this study (Chisholm and Roff, 1990a,b; Clarke and Roff, 1990; Hopcroft and Roff, 1990; Roff et ai, 1990). Clarke and Roff (1990) found annual abundance and biomass means for larvaceans of 440 nr 3 and 0.37 mg AFDW m~3, respectively, and employed upper and lower estimates of growth rates of 1.6-3.8 day 1 , to estimate an annual production of 132-323 kJ nr 2 plus 84-168 kJ m~2 year 1 as house production. Annual copepod production for Lime Cay over this same period was 688 kJ nr 2 year"1 (Chisholm and Roff, 1990a). Taking Clarke and Roff's (1990) lower growth rate estimates as the most conservative, then larvacean production at Lime Cay also represents 32% of the copepod production. Simultaneous estimates of larvacean and copepod biomass are available from relatively few other locations. In Tampa Bay, Florida, O.dioica numbers averaged 3800 nr"3 throughout the bay, with an average biomass of 1.85 mg nr 3 equivalent to 7% of the copepod biomass (Hopkins, 1977). The larvacean contribution to biomass would have been higher if other more stenohaline species, restricted to the outer bay, had been included in his estimates. A detailed study in temperate inlet waters of the Inland Sea of Japan (Uye and Ichino, 1995) found extremely variable numbers of larvaceans with a mean annual abundance of 978 nr 2 , but with abundances of -20 000 nr 3 common from May through June. They found an average annual biomass of 1.69 mg C m~3 and estimated an annual production of 953 mg C m"3 (-357 kJ nv 2 year"1) not including house production. Concurrent data on the copepod community indicate an average biomass of 39.1 mg C m~3 and an annual production of 2500 mg C m~3 (Liang and Uye, 1996; Liang et ai, 1996; S.Uye, unpublished data) or -1170 kJ nr 2 year 1 . It would therefore appear that, even in temperate ecosystems, larvacean production is 35-40% of the copepod production if house production (-50-100) kJ m"2 year"1 is considered. During 'blooms', larvacean production can even rival that of the copepods (Nakamura et ai, 1997). Although additional abundance estimates of larvaceans are available in several other studies, they have not been summarized here because their biomass, growth rates and production cannot yet be put into perspective compared to the copepods. 566 Production of tropical larvaceans in Kingston Harbour Hopcroft et al. (1998b) noted that the annual copepod production in outer Kingston Harbour exceeded many 'productive' temperate systems such as the North Sea (1260 kJ nr 2 year 1 ; Roff et al, 1988), the Scotian Shelf (988 kJ nr 2 year 1 ; McLaren et al, 1988) and Passamaquoddy Bay (800-850 kJ nr 2 year"1; Middlebrook and Roff, 1986). When the combined production of copepods and larvaceans is considered, the 'secondary' productivity of the outer harbour becomes an impressive 2265 kJ nr 2 year"1 (not including house production of 300-600 nr"2 year"1). Based on both phytoplankton and zooplankton abundances (M.K.Webber and D.F.Webber, personal communication), even higher production occurs deeper in Kingston Harbour and Hunts Bay. Yet Kingston Harbour is not simply an anomalous tropical case; data from eutrophic Kaneohe Bay (Newbury and Bartholomew, 1976) suggest that copepod production there could exceed 2800 kJ m~2 year"1. While larvaceans were also implicated as important herbivores in the Kaneohe Bay study (Hirota and Szyper, 1976), their biomass and production were not quantified; however, a later study determined an average larvacean abundance of 3180 m~3 (46 100 m~2; Taguchi, 1982). We have demonstrated that production by larvaceans is disproportionate in comparison to their biomass due to their high growth rates. Clearly, the importance of zooplankton groups locally or globally can no longer be assessed simply in terms of their relative abundance or biomass, but must be assessed in terms of production. Similarly, although total zooplankton biomass in tropical systems is lower than in temperate ones, these differences are substantially offset by higher growth rates. Thus, rates of secondary production in tropical neritic zooplankton have often been greatly underestimated, not only for the larvaceans, but for the copepods as well. Far from being oceanic deserts, or areas of low productivity, tropical pelagic environments can have productivities comparable to, or exceeding, those in temperate regions. Accordingly, they deserve greater research attention than they currently receive. Acknowledgements We thank M.Greenfield, D.Steele and J.Woodley of the University of the West Indies for access to facilities; D.Lombard, G.Persad, K.Rose, J.Whitt, F.Yee Sang and the staff of Port Royal Marine Lab for field assistance; D.F.Webber and M.K.Webber for logistical support; and D.Lombard and C.Clarke-Hopcroft for laboratory support. This work was supported by an NSERC operating grant to J.C.R. and an OGS award to R.R.H. References Alldredge,A.L. (1976) Field behaviour and adaptive strategies of appendicularians (Chordata: Tunicata). Mar. Bioi, 38,29-39. Alldredge,A. (1977) House morphology and mechanisms of feeding in the Oikopleuridae (Tunicata, Appendicularia). /. Zooi, 181,175-188. Alldredge,A. (1981) The impact of appendicularian grazing on natural food concentrations in situ. Limnol. Oceanogr, 26, 247-257. Alldredge^A.L. (1984) The quantitative significance of gelatinous zooplankton as pelagic consumers. 567 RJUlopcroft and J.CRoff In FashanvMJ.R. (ed.), Rows of Energy and Materials in Marine Ecosystems. Plenum, New York, pp. 407-433. Buckmann.A. and Kappji. (1975) Taxonomic characters used for the distinction of species of Appendicularia. Mitt Hamburg ZooL Mus. Inst, 72,201-228. ChisholmJL.A. and RoffJ.C. (1990a) Abundances, growth rates, and production of tropical neritic copepods off Kingston, Jamaica. Mar. BioL, 106,79-89. Chisholm^L.A. and RoffJ.C. (1990b) Size-weight relationships and biomass of tropical neritic copepods off Kingston, Jamaica. Mar. BioL, 106,71-77. Clarke.C. and RoffJ.C. (1990) Abundance and biomass of herbivorous zooplankton off Kingston, Jamaica, with estimates of their annual production. Estuarine Coastal Shelf Sci., 31,423-437. DeibelJD. (1985) Blooms of the pelagic tunicate, Dolioletta gegenbauri: Are they associated with Gulf Stream frontal eddies? / Mar. Res., 43,211-236. DeibelJD. (1986) Feeding mechanism and house of the appendicularian Oikopleura vanhoeffeni. Mar. BioL, 93,429-436. DowningJ.A. and Rigler,F.H. (1984) A Manual on Methods for the Assessment of Secondary Productivity in Fresh Waters. Blackwell Scientific, London, p. 501. FenauxJR. (1985) Rhythm of secretion of oikopleurid's houses. Bull. Mar. Sci, 37,498-503. GrahameJ. (1976) Zooplankton of a tropical harbour: The numbers, composition, and response to physical factors of zooplankton in Kingston Harbour, Jamaica. / Exp. Mar. BioL EcoL, 25,219-237. HirotaJ. and SzyperJ.P. (1976) Standing stocks of zooplankton size-classes and trophic levels in Kaneohe bay, Oahu, Hawaiian Islands. Pac. Set, 30, 341-361. Hopcroft,R.R. and RoffJ.C. (1990) Phytoplankton size-fractions in a tropical neritic ecosystem near Kingston, Jamaica. J. Plankton Res., 12,1069-1088. Hopcroft^R-R. and RoffJ.C. (1995) Zooplankton growth rates: extraordinary production by the larvacean Oikopleura dioica in tropical waters. /. Plankton Res., 17,205-220. Hopcroft,R.R., RoffJ.C. and Bouman,H.A. (1998a) Zooplankton growth rates: the larvaceans Appendicularia, Fritillaria and Oikopleura in tropical waters. /. Plankton Res., 20,539-555. HopcroftJR.R., RoffJ.C. and Lombard.D. (1998b) Production of tropical copepods in the nearshore waters off Kingston, Jamaica: the importance of small species. Mar. BioL, in press. Hopkins,T.L. (1977) Zooplankton distribution in surface waters of Tampa Bay, Florida. BulL Mar. Set, 27,467-478. King.K.R., HollibaughJ.T. and Azam,F. (1980) Predator-prey interactions between the larvacean Oikopleura dioica and bacterioplankton in enclosed water columns. Mar. BioL, 56, 49-57. Liang,D. and Uye.S. (1996) Population dynamics and production of the planktonic copepods in a eutrophic inlet of the Inland Sea of Japan. II. Acartia omorii. Mar. BioL, 125,109-117. Liang.D., Uye,S. and Onbe'.T. (1996) Population dynamics and production of the planktonic copepods in a eutrophic inlet of the Inland Sea of Japan. I. Centropages abdominalis. Mar. BioL, 124,527-536. Lindo.M.K. (1991) The effect of Kingston Harbour outflow on the zooplankton populations of Hellshire, south-east coast, Jamaica. Estuarine Coastal Shelf Sci., 32, 597-608. Madin,L.P., Cetta.C.M. and McAlister.V.L. (1981) Elemental and biochemical composition of salps (Tunicata: Thaliacea). Mar. BioL, Si, 217-226. McLarenJ.A., TrembIay,M.J., Corkett.CJ. and RoffJ.C. (1989) Copepod production on the Scotian Shelf based on life-history analyses and laboratory rearings. Can. J. Fish. Aquat. Sci., 46,560-583. Middlebrook.K. and RoffJ.C. (1986) Comparison of methods for estimating annual productivity of the copepods Acartia hudsonica and Eurytemora herdmani in Passamaquoddy Bay, New Brunswick. Can. J. Fish. Aquat. ScL, 43,656-664. Moore,E. and Sander JF. (1979) A comparative study of zooplankton from oceanic, shelf, and harbour waters of Jamaica. Biotropica, 11,196-206. Moore,E.A. (1967) A study of surface zooplankton in the Caribbean Sea off Jamaica. PhD Thesis, McGill University, Montreal, p. 138. Nakamura.Y., Suzuki.K., Suzuki.S. and HiromiJ. (1997) Production of Oikopleura dioica (Appendicularia) following a picoplankton 'bloom' in a eutrophic coastal area. J. Plankton Res., 17, 113-124. Newbury.T.K. and Bartholomew,E.F. (1976) Secondary production of microcopepods in the southern, eutrophic basin of Kaneohe Bay, Oahu, Hawaiian Islands. Pac. ScL, 30, 373-384. Paffenh6fer,G.-A. (1983) Vertical zooplankton distribution on the northeastern Florida shelf and its relation to temperature and food abundance. /. Plankton Res., 5,15-33. Paffenhofer,G.-A. and Lee.T.N. (1987) Development and persistence of patches of Thaliacea. In Payne,A.I.L., GullandJ.A. and BrinkJCH. (eds), The Benguela and Comparable Ecosystems. S. Afr. J. Mar. ScL, 5, 305-318. 568 Production of tropical larvaceans in Kingston Harbour Raymont J.E.G. (1983) Plankton and Productivity in the Oceans. Part 2. The Zooplankton. Permagon Press, Toronto. RoffJ.C. and Hopcroft,R.R. (1986) High precision microcomputer based measuring system for ecological research. Can. J. Fish. Aquat. ScL, 43,2044-2048. RoffJ.C., Middlebrook,K. and Evans,F. (1988) Long-term variability in North Sea zooplankton off the Northumberland Coast: Productivity of small copepods and analysis of trophic interactions. / Mar. BioL Assoc UK, 68,143-164. RoffJ.C., Hopcroft,R.R., Clarke.C, Chisholm,L.A., Lynn,D.H. and Gilron.G.L. (1990) Structure and energy flow in a tropical neritic planktonic community off Kingston, Jamaica. In Barnes,M. and Gibson,R.N. (eds), Trophic Relationships in the Marine Environment- Proceedings of the 24th European Marine Biology Symposium. Aberdeen University Press, Aberdeen, pp. 266-280. Seki,H. (1973) Red tide of Oikopleura in Saanich Inlet. La Mer, 11,153-158. Taguchi.S. (1982) Seasonal study of fecal pellets and discarded houses of Appendicularia in a subtropical inlet, Kaneohe Bay, Hawaii. Estuarine Coastal Shelf Sci., 14,545-555. Uye.S. and Ichino,S. (1995) Seasonal variations in abundance, size composition, biomass and production rate of Oikopleura dioica (Fol) (Tunicata: Appendicularia) in a temperate eutrophic inlet. / Exp. Mar. BioL EcoL, 189,1-11. Van GuelpenJL, Markle JD.F. and Duggan,D J. (1982) An evaluation of accuracy, precision, and speed of several zooplankton subsampling techniques. /. Cons. Int. Explor. Mer, 40,226-236. Wade.B.A., Antonio.L. and MohonJR. (1972) Increasing organic pollution in Kingston Harbour, Jamaica. Mar. Pollut. Bull., 3,106-110. Webber,D.F. and RoffJ.C. (1996) Influence of Kingston Harbor on the phytoplankton community of the nearshore Hellshire coast, Southeast Jamaica. Bull Mar. Sci., 59,245-258. Webber J3.F., Webber,M.K. and RofU.C. (1992) Effects of flood waters on the planktonic community of the Hellshire coast, southeast Jamaica. Biotropica, 24, 362-374. Webber,M.K., RoffJ.C, Chisholm,L.A. and Clarke.C. (1996) Zooplankton distributions and community structure in an area of the south coast shelf of Jamaica. Bull. Mar. Sci, 59,259-270. Yoshioka,P.M., Owen.G.P. and Pesante,D. (1985) Spatial and temporal variations in Caribbean zooplankton near Puerto Rico. /. Plankton Res., 7,733-751. Youngbluth,MJ. (1976) Zooplankton populations in a polluted tropical embayment. Estuarine Coastal Mar. ScL, 4,481-196. Youngbluth.M.J. (1980) Daily, seasonal, and annual fluctuations among zooplankton populations in an unpolluted tropical embayment. Estuarine Coastal Mar. ScL, 10, 265-287. Received on November 20, 1996; accepted on November 10, 1997 569