Download Production of tropical larvaceans in Kingston Harbour, Jamaica: are

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
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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).
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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.
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Received on November 20, 1996; accepted on November 10, 1997
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