southern Japan Sea, were estimated based on their biomass and population .... experiments; therefore, extra energy associated with feeding ('specific dynamic.
Journal of Plankton Research Vol.21 no.2 pp.299–308, 1999
Production, metabolism and production/biomass (P/B) ratio of Themisto japonica (Crustacea: Amphipoda) in Toyama Bay, southern Japan Sea Tsutomu Ikeda and Naonobu Shiga Biological Oceanography Laboratory, Faculty of Fisheries, Hokkaido University, 3-1-1 Minatomachi, Hakodate 041, Japan Abstract. The production and metabolism of the amphipod Themisto japonica in Toyama Bay, southern Japan Sea, were estimated based on their biomass and population structure data collected from every 2-week samplings from 1 February 1990 through 30 January 1991 (363 days). Over the sampling period, the mean biomass (B) was 370 mg C m–2. Production (P) was calculated as the sum of somatic (Pg) and molt (Pe) production (P = Pg + Pe), and metabolism (M) as the sum of routine metabolism (Mrtn) and diel vertical migration (Mdvm). Integrating over the entire sampling period, Pg and Pe were 1934 and 176 mg C m–2, respectively, and Mrtn and Mdvm were 4100 and 1778 mg C m–2, respectively. Mean daily P/B and Pg/B ratios were 0.016 and 0.014, respectively, and mean Pg/M and P/M ratios were 0.33 and 0.36, respectively. Assuming assimilation efficiency of 0.904, ingestion was computed as 8837 mg C m–2 per 363 days. For the daily maintenance of growth and metabolism, the T.japonica population needs to ingest an amount of prey which equates to 6.6% of their biomass, or 30% of possible total production of their prey animals (copepods and small euphausiids) in Toyama Bay.
Introduction The hyperiid amphipod Themisto japonica is distributed in the Okhotsk Sea, Japan Sea, western subarctic Pacific and southern Kuriles (Bowman, 1960). In the southern Japan Sea, T.japonica is the most abundant pelagic amphipod and ranks second to fourth in the total net zooplankton biomass (Ikeda et al., 1992). As a typical carnivore, T.japonica preys on various other zooplankton species (largely copepods and small euphausiids) and is preyed upon by masu salmon (Oncorhynchus masou), pink salmon (Oncorhynchus gorbuscha), the common squid (Todarodes pacificus), Alaska pollack (Theragra chalcogramma) and Atka mackerel (Pleurogrammus azonus) (cf. Ikeda et al., 1992). Thus, T.japonica is a vital link between secondary production and production of animals at higher trophic levels in the southern Japan Sea. Despite its importance in trophodynamics, no information is presently available about the quantitative production processes of the T.japonica population in the field. The early life cycle of Themisto amphipods is characterized by the hatching of juveniles and their first two moltings within the female’s marsupium (Sheader, 1977; Ikeda, 1990). Then the juveniles are released into ambient water. Ikeda et al. (1992) investigated the population structure of T.japonica in Toyama Bay over a 1 year period and found that its reproduction continued throughout the year. According to their results, the minimum and maximum maturity sizes of T.japonica are 6 and 12 mm for males, and 9 and 17 mm for females. However, the growth pattern was difficult to analyze from field population structure data because of overlapping cohorts due to the continuous reproduction mode of this species. As an alternative approach, Ikeda (1990) determined the growth rate of T.japonica © Oxford University Press
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based on the data of intermolt period and molt increment as a function of temperature of laboratory-reared specimens. Further, Ikeda (1991) combined data of growth, metabolism (= oxygen consumption), molting and fecundity of this species, and established lifetime budgets of assimilated carbon for T.japonica. In this study, information gained from field survey and laboratory experiments on T.japonica is integrated to calculate production (somatic and molts), metabolism (routine and diel vertical migration) and the production:biomass (P:B) ratio of the population of this amphipod in Toyama Bay. Method Population data Numerical abundance and body length distribution of T.japonica were estimated from a series of vertical hauls (500 m to the surface) at an interval of 2 weeks over one full year (24 dates, February 1990 through January 1991) at an offshore station (37°009N, 137°149E) in Toyama Bay. In these data, the body length (BL; the maximum distance between the tip of the head and the distal end of the uropods of the straightened body) was divided into 1 mm increments (16 size classes over the entire range of 1–17 mm BL, covering juveniles just released from the female’s marsupium to mature adults). Details of these results and environmental data (temperature, salinity, total net zooplankton biomass) collected concurrently may be found in Ikeda et al. (1992). Body allometry/carbon content The relationships between BL (mm) and dry weight (DW; mg) and wet weight (WW; mg) for T.japonica have been established as DW = 0.0049 BL2.957 and WW = 0.0304 BL2.832 (Ikeda, 1990). DW carbon contents of T.japonica are 36.15% for 10 mg DW specimens, with no appreciable differences between males and females. The carbon content of dried molts is 23.70% (Ikeda, 1991). Diel vertical migration/habitat temperature Except for early juveniles (1–3 mm), which stay at or near the surface both day and night, older juveniles and adults of T.japonica migrate over an extensive vertical distance each day. The vertical range of the migration varies seasonally from 150 (September) to 400 m (June) for the Toyama Bay population (Ikeda et al., 1992; T.Ikeda, unpublished data) with an annual mean of 250 m. The range of habitat temperature encountered by vertically migrating T.japonica varies seasonally, from 1 to 2°C during the daytime and from 5 to 16°C during nighttime (Ikeda et al., 1992), and estimated daily mean temperature is 6.4°C over the year. Ikeda (1992) reared T.japonica in the laboratory under a fluctuating temperature regime (1–15°C, with an integrated daily mean of 8°C) and at constant temperature (8°C) as a control. Comparison of T.japonica reared in these two thermal regimes revealed no significant effect of thermal modes on the 300
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daily growth and metabolism (= oxygen consumption) of this animal. Thus, daily integrated temperature is a good estimator of habitat temperature for vertically migrating T.japonica. In the present calculation, the integrated habitat temperature of T.japonica was chosen as 15°C for 1–3 mm specimens and 6.4°C for >3 mm specimens. Results Biomass Biomass of T.japonica expressed in carbon units (B; mg C m–3) increased gradually from the beginning of the year, forming several peaks in spring through summer (1.30 mg C m–3 in May, 2.18 mg C m–3 in August and 2.24 mg C m–3 in September), then decreased toward the end of the year (Figure 1), with an integrated mean B over the entire study period (363 days) of 0.739 mg C m–3 or 370 mg C m–2 (Table I). Somatic production Somatic production of T.japonica at a given sampling date was computed as the sum of growth increments of 16 size classes multiplied by the abundance of each s N (CW size class: Pg =i ∑ i i + 1 – CWi)/Di, where Pg is the daily somatic production =1 (mg C m–3 day–1), CWi and CWi + 1 are the weights (mg C) at the beginning and end of the size interval, Di is the developmental time (days) from CWi to CWi + 1, Ni is the abundance (number m–3) of each size class, and s is 16. The BL data were
Fig. 1. Changes with season in daily somatic production (Pg), molt production (Pe), routine metabolism (Mrtn) and diel vertical migration metabolism (Mdvm) (all mg C m–3 day–1) and biomass (B, mg C m–3) of the T.japonica population in Toyama Bay, southern Japan Sea.
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Table I. Summary of a 363 day carbon budget for the T.japonica population in Toyama Bay (1 February 1990 through 30 January 1991). Data are expressed m–3 and m–2; the former was multiplied by 500 for the latter mg C m–3 Mean biomass (B)
mg C m–2
0.739
Production (P = Pg + Pe) 4.221 Somatic (Pg) 3.868 Molt (Pe) 0.353 Metabolism (M = Mrtn + Mdvm) 11.755 Routine (Mrtn) 8.199 Diel vertical migration (Mdvm) 3.556 Assimilation (A = P + M) 15.976 Ingestion (I = A/0.904) 17.673 Ratios P/B Pg/B P/M Pg/M
370 (% of A) (26.4) (24.2) (2.2) (73.6) (51.3) (22.3)
2110 1934 176 5878 4100 1778 7988 8837 = = = =
5.71 5.23 0.359 0.329
converted to dry weight (DW) using the allometric equation, then to C units using C content percentages for each BL class mentioned above. Di was estimated from cumulative developmental time (t; days) as a function of BL and temperature (T, °C) using the modified growth equation of Ikeda (1990) for T.japonica: t = (1.033 – e–0.0426BL)/(0.0246eb), where b = 2.3023(–0.4503 – 10–0.0267T – 0.0366). Pg thus calculated varied greatly with season, from 0.003 (January) to 0.029 mg C m–3 day–1 (August, cf. Figure 1), with an integrated Pg over the entire study period (363 days) of 3.868 mg C m–3 or 1934 mg C m–2 (Table I). Molt production s
The production of molts was given by the equation: Pe = i ∑ (MDWi 3 Ni 3 a/Di), =1 where Pe is the molt production (mg C m–3 day–1), MDWi is the geometric mean DW [= (DWi + 1 3 DWi)0.5] of each size-class, Ni is the abundance of each size class, a is the percent loss in body DW per molting (6.8%; Ikeda, 1991), multiplied by the carbon content of molts (23.7% of DW; Ikeda, 1991) and Di is the intermolt period (IP; days) estimated from the modified equation of Ikeda (1990) as a function of BL and temperature (T; °C) (IP = 10b + 0.0709BL, where b = 100.0366 – 0.0267T) and BL versus DW allometry mentioned above. Pe ranged from 0.0003 (January) to 0.0023 (August) mg C m–3 day–1, with an integrated Pe over the entire study period of 0.353 mg C m–3 or 176 mg C m–2 (Table I). Metabolism The metabolism M (mg C m–3 day–1) was partitioned into two components: routine metabolism (Mrtn) and diel vertical migration metabolism (Mdvm). Mrtn was calculated from oxygen consumption rates (R; µl O2 individual–1 h–1) determined by 302
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placing specimens in the standard cell (7.9 ml capacity) fitted with a YSI oxygen electrode to monitor the change in oxygen content in the cell (Ikeda, 1991). The specimens used for Ikeda’s (1991) study were those collected 4–20 h prior to the experiments; therefore, extra energy associated with feeding (‘specific dynamic action’, cf. Kiørboe et al., 1985) is assumed to be included in his oxygen consumption data. R is a function of the size (DW; mg) of specimens and temperature (T; °C): R = DW0.788 3 100.05355T – 0.2316 (modified from Ikeda, 1991). Mdvm is the amount of oxygen consumed for diel vertical migration (R9; µl O2 individual–1 km–1), which was calculated from the equation of net cost of transport as a function of weight (mg WW) of animals established for pelagic crustaceans (‘multiplepaddle’ propulsive system as compared with the ‘undulatory’ propulsion system of fishes): R9 = 9.02WW0.72 (Torres, 1984; the original equation based on energy unit was modified using oxycalorific equivalent 1 cal = 208.33 µl O2). R9 is independent of temperature in theory (cf. Morris et al., 1990) and is 0.5R9 for T.japonica (>3 mm) migrating 250 m daily (i.e. 0.5 km for round trip). In calculating R or R9, DW or WW of specimens was representeds by the geometric mean DW or WW (Ri 3 Ni) and Mdvm = 0.5 3 10–3 g ofs each size class. Thus, Mrtn = 24 3 10–3 g i ∑ =1 ∑ (R9i 3 Ni), where 24 is to convert hourly rate to daily rate, 10–3 is to convert i=1 micrograms to milligrams, and g (= 0.97 3 12/22.4) is to convert oxygen units to carbon units assuming protein metabolism (RQ = 0.97; Gnaiger, 1983). Both Mrtn and Mdvm thus calculated were the highest in the summer season, and the seasonal range was from 0.005 to 0.063 mg C m–3 day–1 for the former and from 0.003 to 0.025 mg C m–3 day–1 for the latter (Figure 1). Integrated values over the entire study period (363 days) were 8.119 mg C m–3 or 4100 mg C m–2 for Mrtn, and 3.556 mg C m–3 or 1778 mg C m–2 for Mdvm (Table I). Assimilation and ingestion Carbon assimilated by T.japonica (A; mg C m–3 day–1) is defined as A = P + M = Pg + Pe + Mrtn + Mdvm, assuming no leakage of soluble organic matter. The amount of ingested carbon (I; mg C m–3 day–1) was computed adopting an assimilation efficiency value of 90.4% determined on a bentho-pelagic amphipod Calliopius laeviusculus by Dagg (1976), i.e. I = A/0.904. A ranged from 0.008 to 0.087 mg C m–3 day–1, and I from 0.012 to 0.117 mg C –3 m day–1. Integrated A and I values over the entire study period (363 days) were 15.98 and 17.67 mg C m–3, or 7988 and 8837 mg C m–2, respectively (Table I). Ratios between parameters (Pg /B, P/B, Pg /M, P/M, B/N) The ranges of seasonal variations were 0.011–0.026 for somatic production to biomass (Pg/B) ratios, 0.011–0.028 for total production to biomass (P/B) ratios, 0.28–0.44 for somatic production to metabolism (Pg/M) ratios and 0.31–0.48 for total production to metabolism (P/M) ratios. Since the seasonal trends of P/B and P/M ratios were similar to those of Pg/B and Pg/M ratios, respectively, only the latter two ratios are shown in Figure 2. A population (= size) structure index B/N 303
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(mg C individual–1) fluctuated irregularly from 0.174 to 1.867 (Figure 2). From Figure 2, it is seen that the seasonal patterns of Pg/B and Pg/M ratios paralleled each other. The seasonal pattern of the B/N ratios was entirely different from those of Pg/B or Pg/M ratios, and it changed in an opposite fashion to the latter two ratios. Discussion Despite the widespread distribution of hyperiid amphipods over the world ocean (Shih, 1982), there is no information about the production of this group of zooplankton. The only related information presently available is a production estimate for total planktonic gammarid amphipods (not species, but as a group) on Georges Bank by Avery et al. (1996). However, Avery et al.’s (1996) data are not directly comparable to the present results since the P/B ratio they used is of benthic gammarids in the same region. On the bases of similar habitat (marine), ecology (planktonic) and trophic type (carnivore), but disregarding phylogenetic differences, the present estimates of production and Pg/B ratio of T.japonica are compared with the chaetognaths Sagitta elegans and Sagitta hispida (Sameoto, 1973; Reeve and Baker, 1975), and the ctenophores Pleurobrachia bachai and Mnemiopsis maccradyii (Hirota, 1974; Reeve and Baker, 1975) in Table II. Somatic production (Pg) and Pg/B were used instead of total production (P) and P/B for the basis of comparison since daily production of non-crustacean carnivorous zooplankters in Table II represents somatic production (Pg) only. Whereas daily production of T.japonica (5.33 mg C m–2 day–1) is the greatest among these carnivorous zooplankers, its daily Pg/B
Fig. 2. Changes with season in somatic production to biomass (Pg/B; day–1) ratios, somatic production to metabolism (Pg/M) ratios and a population size structure index (B/N; mg C individual–1) of the T.japonica population in Toyama Bay.
304
aCalculated
12.5–20
2.0 1.37
Toyama Bay
6–15
26a
0.5–14
26a
Temperature (ºC)
1.06
0.30
0.157
Maximum size (mg C)
South Florida inshore water La Jolla Bight
South Florida inshore water Nova Scotia water
Habitat
from annual or near annual data.
Sagitta elegans Ctenophores Mnemiopsis mccradyii Pleurobrachia bachiai Amphipods Themisto japonica
Chaetognaths Sagitta hispida
Animal group/species
0.21 (mean) 0.20a 0.014a
0.74a 5.33a
0.006a
0.55a 0.50–1.01
0.31 (mean)
Daily Pg:B
2.00–4.80
Daily Pg (mg C m–2)
Table II. Daily somatic production (Pg) and daily production/biomass ratios (Pg/B) of carnivorous zooplankton
This study
Hirota (1974)
Reeve and Baker (1975)
Sameoto (1973)
Reeve and Baker (1975)
Source
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ratio (0.016) is modest, falling within the wide range of the Pg/B values of other carnivorous zooplankters (0.006–0.31). The P/B ratio (often equivalent to the Pg/B ratio, as noted above) is an appropriate basis for comparing the production potential of various invertebrates, and is largely a function of their sizes (cf. Banse and Mosher, 1980), i.e. the greater the sizes, the lower the P/B ratios. The population size structure index (B/N) used in the present study is not an accurate measure of mean body size of T.japonica unless the size distribution is proved to be the normal. Nevertheless, lower Pg/B ratios associated with larger B/N are seen in this study (Figure 2). Because of the lack of appropriate information, the effect of habitat temperature on the P/B ratio has not been evaluated, but recent results of extremely higher P/B ratios on tropical marine copepods (cf. Webber and Roff, 1995) suggest that habitat temperature is an additional factor affecting the P/B ratios of marine zooplankton. From this view, higher Pg/B ratios seen in S.hispida and Mnemiopsis maccradyii than that of T.japonica may be explained partly by higher habitat temperature and/or their smaller body sizes. Despite a smaller size than that of T.japonica, the lower Pg/B ratio of S.elegans may be a result of the pronounced effect of their lower habitat temperature. Banse and Mosher (1980) noted that the phylogeny of aquatic and terrestrial invertebrates had little effect on the broad relationship between P/B ratio and body size. McLaren et al. (1989) calculated Pg/B ratios of 10 copepod species from Emerald Bank, Scotian Shelf, where the thermal regime is roughly similar to that of Toyama Bay. Among the 10 copepods they studied, Calanus hyperboreus is of special interest because this copepod has an adult body size (2.7 mg DW) similar to that of T.japonica studied here (mid adult size: 3.7 mg DW; cf. Ikeda, 1991). The daily Pg/B ratio of C.hyperboreus is 0.020 (calculated from the annual Pg/B = 7), which is near our estimate of 0.014 for T.japonica. Because C.hyperboreus and T.japonica are a typical herbivore and a typical carnivore, respectively, trophic type appears to have little or no effect on the Pg/B ratios in zooplankton. All these results together suggest that the production potential of T.japonica, as judged by Pg/B ratios, does not differ appreciably from those of other zooplankters if differences in body size and/or habitat temperature are taken into account. Metabolism accounted for the greatest portion (73.6%; Table I) of carbon assimilated by T.japonica. In contrast to terrestrial and aquatic benthic invertebrates, field comparisons between population metabolism and population production are extremely scarce for marine zooplankton (Humphreys, 1979; Banse and Mosher, 1980). As the only data available, Sameoto (1973) estimated field population metabolism and production of the chaetognath S.elegans in Bedford Basin, Nova Scotia, assuming that the extra metabolism for undefined activity of wild specimens equals twice the metabolism determined on captive specimens in the laboratory (wild metabolism = laboratory-determined metabolism 3 2). This correction factor of 32 for estimating metabolism of wild specimens is empirical, derived from studies of fish energetics (cf. Winberg, 1956). In this light, application of the relationship between energy cost for locomotion and body mass established by Torres (1984) is an alternative method providing a logical basis for estimating extra metabolism of wild zooplankton. The present 306
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results suggest that the extra metabolism (Mdvm) needed for the diel vertical migration of T.japonica is 30.30 that of captive specimens (Mrtn), which is much less than 32. Despite these methodological differences, field population metabolism/production ratios (Pg/M) yielded for S.elegans (0.25) by Sameoto (1973) and T.japonica (0.33) in this study are quite close to each other. Lasker (1966) noted that molt production by the euphausiid Euphausia pacifica amounted to 300 mg C m–2 year–1 in the northern North Pacific, and is an important source of oceanic detritus. Molt production by T.japonica in Toyama Bay was calculated as 177 mg C m–2 year–1 (176 3 365/363), which is the same order of magnitude as that of E.pacifica in the northern North Pacific. Comparison of carbon budgets of assimilated carbon in E.pacifica (Lasker, 1966) and T.japonica (this study) revealed that the fraction invested to molt production was greater in the former (15.3%) than the latter (2.2%). Production of larger molts may be one possible cause for greater partition of assimilated carbon to molt production in E.pacifica. However, the size of a single molt, as assessed by the loss in body carbon at each molting, is similar between E.pacifica (4.1%, calculated from Lasker’s data) and T.japonica [4.4%, calculated from Ikeda’s (1991) data]. Alternatively, higher molting frequency of E.pacifica than T.japonica may be the case. From intermolt periods expressed as a function of body size (BL) and temperature for E.pacifica (Iguchi and Ikeda, 1995) and T.japonica (this study), intermolt periods of specimens with similar body size (BL = 10 mm) and at the same temperature (6.4°C) are predicted as 7.9 days for the former and 27.7 days for the latter. Thus, E. pacifica can produce 3.5 molts, while T.japonica casts one molt (although molt increment in terms of body length of the former is 0.6 times the latter), indicating that this dissimilar molting frequency is the major cause which led to different partition of assimilated carbon to molt production in these two crustaceans. To maintain somatic growth, molting and metabolism, the population of T.japonica in Toyama Bay needs to ingest prey animals of 8886 mg C m–2 per year (8837 3 365/363). Comparing this to the annual mean population biomass of 371 mg C m–2 (370 3 365/363), the mean daily food requirement of the population is estimated as 6.5% of their biomass. In Toyama Bay, the major prey animals of T.japonica are copepods and young euphausiids (E.pacifica, body length
