Downward carbon transport by diel vertical migration of the copepods Metridia pacifica and Metridia okhotensis in the Oyashio region of the western subarctic Pacific Ocean

ARTICLE IN PRESS Deep-Sea Research I 56 (2009) 1777–1791

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Downward carbon transport by diel vertical migration of the copepods Metridia pacifica and Metridia okhotensis in the Oyashio region of the western subarctic Pacific Ocean Kazutaka Takahashi , Akira Kuwata, Hiroya Sugisaki, Kazuhisa Uchikawa, Hiroaki Saito Tohoku National Fisheries Research Institute, 3-27-5 Shinhama-cho, Shiogama 985-0001, Japan

a r t i c l e in fo

abstract

Article history: Received 5 April 2008 Received in revised form 3 April 2009 Accepted 7 May 2009 Available online 14 May 2009

Seasonal change in the downward carbon transport due to respiration and mortality through diel vertical migration (DVM) of the calanoid copepods Metridia pacifica and Metridia okhotensis was estimated in the Oyashio region, western subarctic Pacific during six cruises from June 2001 to June 2002. M. pacifica (C4, C5 and adult females) was an active migratory species throughout the year though its DVM amplitude varied among seasons and stages. The mean distribution depths of adult females during the daytime were positively related with the illumination level in the water column, being shallowest in April and deepest in January. M. okhotensis generally showed lessextensive migrations than M. pacifica. Therefore, together with their lower abundance, this species is considered to be a less-important mechanism of downward transport of carbon except for April when their DVM was more active and descended deeper than M. pacifica, which remained in the upper 150 m even during the daytime. The mean migrating biomass of the two Metridia species was 558 mg C m2 d1 and was high during summer to winter (263–1676 mg C m2 d1) and low during spring (59–63 mg C m2 d1). Total downward flux through DVM fluctuated between 1.0 and 20.0 mg C m2 d1 with an annual mean of 8.0 mg C m2 d1. Contribution of the respiratory flux was greater than the mortality flux and accounted for 64–98% of total migratory flux throughout the year except for January when contribution of both fluxes was equal. Overall the annual carbon transport by DVM of Metridia spp. was estimated as 3.0 g C m2 year1, corresponding to 15% of the annual total POC flux at 150 m at the study site, suggesting that DVM is a significant process for carbon export in the subarctic region as well as that in tropical and subtropical oceanic regions. Since DVM in M. pacifica is more active during the non-bloom season when the gravitational flux of particulate matter is low, this species plays an important role in driving the biological pump in the subarctic Pacific during summer to winter. Crown Copyright & 2009 Published by Elsevier Ltd. All rights reserved.

Keywords: Active flux Mesozooplankton Respiration Mortality Micronekton Predation Myctophids

1. Introduction The Oyashio region is located at the westernmost edge of the western subarctic gyre of the North Pacific.

 Corresponding author. Tel.: +81 22 365 9929; fax: +81 22 367 1250.

E-mail address: [email protected] (K. Takahashi).

Different from the open waters of the subarctic North Pacific, which are recognized as a high-nutrientlow-chlorophyll (HNLC) area, this region exhibits large annual variations in nutrient concentrations and plankton biomass, largely due to the chain-forming diatom bloom in spring (Saito et al., 2002). The primary production by the spring bloom makes this region a strong sink of atmospheric CO2 in spring (Midorikawa et al., 2003),

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resulting in the higher export efficiency estimates of POC (up to 520 mg C m2 d1) from the euphotic zone compared to other areas of the world ocean (Kawakami et al., 2004). The North Pacific Intermediate Water (NPIW) has been shown to be formed in this region and is known as a significant sink of anthropogenic CO2 (Tsunogai et al., 1993). Understanding the biological and physical processes that affect the vertical transport of organic materials, i.e. the ‘‘biological pump’’, in this region is key to determining the role of the North Pacific in the global carbon cycle. Mesozooplankton play a significant role in driving the biological pump. The grazing/defecation process in surface waters to produce sinking fecal pellets is well documented (e.g. Fowler and Knauer, 1986), though the vertical flux of fecal pellets decreases exponentially with depth because of decomposition (Pace et al., 1987). It has been reported that diel and seasonal vertically migrating organisms are also an important pathway in carbon export by consumption of organic matter in the surface waters and metabolizing of the ingested food or the organisms being preyed upon below the mixed layer (Longhurst et al., 1990; Longhurst and Williams, 1992; Dam et al., 1995; Zhang and Dam, 1997; Steinberg et al., 2000). This process has been termed the active flux (Longhurst and Harrison, 1988). In the Oyashio region, ontogenetic seasonal vertical migration by large calanoid copepods is known to function as a significant process in carbon export. According to Kobari et al. (2003), 4.3 g C m2 year1, corresponding to 91.5% of the POC flux at 1000 m depth, is exported through the ontogenetic seasonal vertical migration of three Neocalanus species, which reproduce at depth and do not return to the surface after mating. On the other hand, the role of diel migrants in the biological pump in this region has not been well investigated so far, though this behaviour is commonly seen among various taxa in the mesozooplankton and micronekton in this region (e.g. Hattori, 1989; Sugisaki et al., 1991; Terazaki, 1995; Moku et al., 2000; Yamaguchi and Ikeda, 2000; Nakagawa et al., 2003). The calanoid copepods Metridia spp. form a major group of diel vertical migrants in the mesozooplankton community of the subarctic, subantarctic and polar waters (e.g. Osgood and Frost, 1994; Hays, 1995; Lopez and Huntley, 1995; Atkinson et al., 1996). In the Oyashio region, two species, M. pacifica and M. okhotensis, commonly occur as diel vertical migrants that undergo the diel vertical migration (DVM) across the bottom of euphotic zone and/or permanent pycnocline (Hattori, 1989; Padmavati et al., 2004; Takahashi et al., 2008). They are primarily suspension feeders, preferring microsized (410 mm ESD) phyto- and zooplankton (Batchelder, 1986; Ide et al., 2008) and in turn are preyed on by mesopelagic fishes and cephalopods as their main diet (Pearcy et al., 1979; Gordon et al., 1985; Moku et al., 2000; Uchikawa, unpublished), suggesting that they function as an important link between the surface waters and the mesopelagic zone. Recently, the importance of the active flux through diel vertical migration by M. pacifica also has been shown in the subarctic western gyre in summer (Kobari et al., 2008).

In this study we have attempted to estimate the seasonal change of carbon flux through DVM of Metridia spp. on the year-round basis, particularly due to respiration and mortality by predation of micronektonic fish in order to discuss the functional role of Metridia spp. in the biological pump of the subarctic Pacific Ocean. Our study demonstrates that DVM of Metridia spp. is an important pathway for carbon export in the Oyashio region and that it plays a significant role in driving the biological pump particularly during summer to winter.

2. Materials and methods 2.1. Migrating biomass of Metridia spp. Zooplankton sampling was carried out in the Oyashio region off Cape Erimo, Hokkaido (Fig. 1), during six cruises from June 2001 to June 2002 (Table 1). Additional sampling was also conducted in January and May 2001 at the same site (Stn 29) in order to determine daytime zooplankton distribution with depth. Vertical profiles of temperature and salinity were monitored with a CTD (Sea Bird Electronics), which was equipped with Niskin bottles to collect water samples for chlorophyll a concentration measurements. Details of the oceanographic conditions are given elsewhere (Takahashi et al., 2008). Diel change in the vertical distribution pattern within the upper 500 m of the water column was determined by a midnight/ midday VMPS net (Vertical Multi-layer opening–closing Plankton Sampler; 50 cm  50 cm opening, 330 mm mesh, Terazaki and Tomatsu, 1997) tow in which the following layers were sampled: 0–50, 50–150, 150–300, and 300–500 m. The samples were immediately preserved with 5% buffered formalin seawater, and part of each sample (ca. 1/4–1/2) collected in the 0–50 m layer was

50 48 46 Latitude (ºN)

1778

hio

as

44

Oy A4 A7 A9

42 40

tension

Stn. 31 Stn. 29 Kuroshio Ex 38 140

142

144

146

148

150

152

154

156

Longitude (ºE) Fig. 1. Sampling area and location of the sampling stations. All sampling for Metridia spp. was conducted at Stn 29 (closed circle) except for November 2001 when the sampling was carried out at Stn 31 (open circle). Triangles indicate sampling site for myctophid fish by MOCNESS in order to estimate the predation pressure on Metridia spp. (see text).

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Table 1 Oceanographic characteristics for the 6 cruises. Cruise

WK0106 TR0108 WK0111 WK0201 WK0204 WK0206

Date

28–29 Jun 2001 31 Aug–1 Sep 2001 9–10 Nov 2001 24–25 Jan 2002 14–15 Apr 2002 15–16 Jun 2002

Mean temperature (1C)

MLDa (m)

EZDb (m)

Chl-ac (mg m2)

PPd (mg C m2 d1)

POC flux at 150 me (mg C m2 d1)

0–50 m

50–150 m

150–500 m

8.9 10.7

2.3 2.2

2.6 2.5

13 13

52 32

79 98

592 359

9 52

8.3 1.3 1.1 9.5

4.4 1.4 1.1 3.1

2.3 2.5 2.0 2.3

55 96 30 15

46 49 14 33

85 50 607 90

432 92 2662 456

32 14 186 9

All sampling were conducted at stn 29 (411N, 144.41E), except for November 2001 when the sampling was conducted at stn 31 (41.31N, 144.21E). a Mixed layer depth (Ds of 0.125 kg m3 from surface density). b Euphotic zone depth defined as the 1% depth of surface irradiance (A. Kuwata, unpublished data). c Chlorophyll a standing stock in the water column 0–200 m (A. Kuwata, unpublished data). d Primary production integrated from the surface to the EZD (Yokouchi et al., 2004). e POC flux at 150 m was based on sediment trap data for a trap moored at 1100 m at the same sampling site (Takahashi, unpublished data) and the equation given by Martin et al. (1987).

also filtered on a 200 mm nylon mesh and frozen in a plastic petri dish at 80 1C for measurement of the dry weight. In the shore laboratory, for the genus Metridia, specimens were identified and counted according to stages. Since a preliminary examination revealed that early stages (C1–C3) and adult males of both Metridia species do not show a notable DVM, the migrating biomass and active flux were estimated only for C4, C5 and adult females of both species. Diel migrating biomasses of the Metridia spp. were estimated from the difference between nighttime and daytime averaged biomass (density of copepods  body dry weight) in the upper 150 m. Day/night mean copepod abundance was estimated from 6 hauls of the VMPS (excluding samples collected at dusk and dawn) for each cruise. Dry weight of Metridia spp. in each cruise was measured using specimens sorted from the frozen samples, which were dried at 60 1C over 24 h and weighed with a microbalance (Sartorius ME5). Dry weight was converted into a carbon weight using a factor of 0.467 (Ikeda et al., 2007). 2.2. Estimation of respiratory flux The downward flux of respiratory carbon exported below 150 m by Metridia spp. during the daytime was estimated as the sum of the flux by each developmental stage (C4, C5 and adult females) for all cruises from the following equation: F r ¼ Ld  Ni  RCi, where Fr is the downward flux of respiratory carbon (mg C m2 d1), Ld the length of the daytime (h), Ni the abundance of migrating Metridia spp. at a given stage i across 150 m (number of inds m2 d1). Also RCi ¼ carbon respiration rate of Metridia spp. at a given stage i (mg C ind1 h1) was estimated from its body dry weight (DW, mg ind1) and the mean temperature (T, 1C) between 150 and 500 m (Table 1) with the empirical allometric

relationship of Ikeda et al. (2001): ln RO ¼ 0:399 þ 0:801 ln DW þ 0:069 T, where RO is the oxygen consumption rate (ml O2 ind1 h1). The estimated rates for the species and stages were converted to respiratory carbon equivalents (RC: mgC ind1 h1) as RC ¼ RO  RQ  12/22.4, where RQ (respiratory quotient) is the molar ratio of carbon produced to oxygen utilized, 12 is the atomic weight of carbon and 22.4 is the molar volume of an ideal gas at standard temperature and pressure. We used an RQ of 0.97, assuming a protein-based metabolism (Gnaiger, 1983). 2.3. Estimation of mortality flux Previous studies based on population dynamics models for Metridia pacifica suggested that daily mortality of their copepodite stages ranged between 1% and 3% (Batchelder and Miller, 1989; Sunami and Hirakawa, 2000). In this paper, we assume that 1–2% d1 of the migrating biomass of Metridia spp. resulted in mortality due to predation by myctophid fishes, which are known to prey on the copepods as a main part of their diet (Pearcy et al., 1979; Batchelder, 1985; Gordon et al., 1985; Moku et al., 2000; see also Appendix A), and the proportion of the mortality due to the myctophid fishes that occurs below 150 m was determined using field-collected samples. Accordingly, the mortality flux of a given Metridia species was estimated as the sum of the flux for each developmental stage (C4, C5 and adult females) for all cruises from the following equation: F m ¼ Bi  m  %M deep , where Fm is the downward flux due to mortality (mg C m2 d1), Bi the biomass of migrating Metridia species at a given stage i across 150 m (mg C m2 d1), and M the daily mortality of migrating population that was assumed to be 0.01 or 0.02, which varies depending on the seasonal change in predation pressure by myctophid fishes. In the Oyashio region the biomass of myctohid

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fishes is generally high during autumn–winter and becomes lower from spring to summer (Ikeda et al., 2008, Sugisaki et al., unpublished data), partly because of the southward seasonal migration for spawning of a dominant species, Diaphus theta (Moku et al., 2003). Therefore in this study mortality of 2% d1 is applied to November and January (high predation pressure period), while 1% d1 is used for other months (low predation pressure period). %Mdeep is the proportion of mortality due to myctophid fishes that occurs below 150 m. In this parameter, the mortality at night was taken into account in the mortality flux as well as that during daytime, since ‘‘non-migrating individuals’’, a portion of the population that at any one time remains below 150 m at night, are also dependent on the production at surface waters through irregular DVM (Hays et al., 2001). The period of the non-migrating phase in M. pacifica was suggested to be less than few days (Hays et al., 2001), and we assumed that the fraction of the migrating population remaining below 150 m is constant on a daily basis during each sampling time, so that mortality flux applies to the ‘‘nonmigrating’’ individuals. The proportion %Mdeep is inferred from gut content analysis of the three dominant myctophid fishes in the Oyashio region, D. theta, Stenobrachius leucopsarus and S. nannochir, accounting for 66–88% of the mesopelagic fish in biomass (Ivanov, 1997). Day and night multi-layer samplings from 1000 m to the surface using large-size MOCNESS (4 m2 mouth area, 1/8 inch oval mesh, Wiebe et al., 1985) were conducted at Stns A4, A7 and A9 in the Oyashio region (Fig. 1) during four cruises from May 2003 to July 2004 (Table 2). The range of sampling (0–1000 m) covered the main distribution range of both Metridia species (Batchelder, 1985; Padmavati et al., 2004). The towing speed of the MOCNESS was around 2 knots. Since sampling efficiency of the MOCNESS for myctophid fishes is known to be significantly lower than that of a mid-water trawl, the abundance and biomass of fish were adjusted by using a factor of 10 (Yamamura, 2007). The fish specimens were preserved in 10% buffered formalin immediately after the collection. In the shore laboratory, all the mesopelagic fishes were classified into species, and the gut contents of the three dominant myctophid species were examined under a microscope. Because of the difficulty in identifying

partially digested specimens, all Metridia from the gut larger than ca. 1.4 mm in PL (corresponding to M. pacifica C4) were pooled as Metridia except for obvious adult males. Based on the gut content analysis and density of the myctophid fishes, day/night consumption rates of Metridia spp. by the myctophid fishes per square meter were estimated for surface (0–150 m) and deep (150–1000 m) waters, assuming an egestion time of 8 h except for fishes in the surface waters during summer and autumn when 6 h was used because of the higher water temperature (see Moku et al., 2000). The obtained proportion of mortality of each Metridia species due to predation by myctophid fishes that occurs below 150 m was applied to the calculation for the corresponding month for the estimation of the active flux by Metridia spp. Finally the total active flux was compared with concurrently measured other factors such as primary production (Yokouchi et al., 2004), grazing rate of Metridia spp. at 0–150 m (Takahashi et al., 2008) and POC sinking flux at 150 m (Table 1).

3. Results 3.1. Seasonal variation in the DVM and migrating biomass Adult females and late copepodites (C4 and C5) of M. pacifica showed clear nocturnal occurrence in the surface waters throughout the sampling period (Fig. 2). Generally the distance traveled during DVM increased with growth. Depth of descent during the daytime varied among seasons, being shallowest in April and deepest in January (Fig. 2). The mean distribution depths of adult females during the daytime were positively related to the depth of the euphotic zone (Fig. 3a). The DVM behaviour in M. okhotensis was variable depending on the developmental stages and season, and the depths reached during DVM appeared to decrease with growth. Nocturnal occurrence of adult females in the surface waters was limited to April, and they primarily remained deeper than 300 m in other months (Fig. 4), whereas late copepodites (C4 and C5) appeared in the surface waters more frequently (Fig. 4), though they

Table 2 Summary of the myctophid fish sampling by MOCNESS in the Oyashio region, subarctic Pacific. Cruise/season

Stns

Date

Sampling period

Abundance of fish (inds m2)

Wet weight of fish (g m2)

0–150 m

0–150 m

150–1000 m

150–1000 m

WK0305/spring

A4, A7

9–10 May 2003

Day Night

0.0 1.6

3.4 6.6

0.0 2.8

16.6 42.6

WK0309/autumn

A4, A7

13–17 Sept 2003

Day Night

0.0 8.0

17.8 7.4

0.0 29.1

64.1 26.2

WK0402/winter

A4, A9

17–18 Feb 2004

Day Night

0.0 6.4

12.8 10.4

0.0 4.5

49.7 41.0

WK0407/summer

A4, A9

31 Jul–2 Aug 2004

Day Night

0.0 1.9

3.6 2.6

0.0 4.8

9.1 10.5

The abundance and biomass of fish were adjusted by using a 10% sampling efficiency with the MOCNESS/midwater trawl (Yamamura, 2007).

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Metridia pacifica Jun 2001 0 50

Aug

Nov

Jan 2002

Apr

Jun

F

150 300 Day

Night

500

Depth (m)

0 50

0

5 10 15 20

0 20 40 60 80 100 0 10 20 30 40 50

0

10 20 30 40 0 100 200 300 400 500 0

0 20 40 60 80 100

0

20

0

0

2

40

60

0

20

40

60

80

C5

150 300

500

0 50

20

40

60

20

40

60

4

6

8

10

0

20 40 60 80 100

C4

150 300

500 0

10

20

30

0

50 100 150

0 10 20 30 40 50

0 5 10 15 20 25

0 0.5 1 1.5 2

0

10 20 30 40 50

-3

Abundance (ind m ) Fig. 2. Seasonal and diel change in vertical distribution of C4, C5, and adult females (F) of Metridia pacifica in the Oyashio region. Open and closed bars indicate daytime and nighttime distributions, respectively. X-axis is common for daytime abundance and nighttime abundance.

sometimes showed little evidence of migration (e.g. C4 in June 2001, C5 in November). The distribution depth of adult females and C5 during the daytime also became shallower in April and was positively related to the depth of the euphotic zone (Fig. 3b). Throughout the sampling period, abundance and biomass that migrated across 150 m was higher in M. pacifica than in M. okhotensis except for April (Fig. 5). Mean annual migratory biomass of M. pacifica was 17 times higher than that of M. okhotensis (527 vs. 31 mg C m2 d1). In April, M. okhotensis, however, surpassed M. pacifica in the migrating biomass since almost all M. pacifica remained in the upper 150 m during the daytime (Fig. 2). In total, the migratory biomass of the two Metridia species varied between 58.6 (April) and 1676.4 (August) mg C m2 d1 with an annual mean of 558.2 mg C m2 d1.

3.2. Temporal and spatial variation in predation pressure by myctophid fishes The myctophid predators were relatively abundant from autumn to winter and decreased during spring to summer (Table 2), which is consistent with our assumption of seasonal change in predation intensity

(see Section 2). Predation pressure on Metridia spp. by the myctophid fishes in the upper 150 m varied from 4 (July) to 19 (May) copepod inds m2 d1, while below 150 m it varied from 1 (May) to 13 (February) copepod inds m2 d1 (Fig. 6). In spring (May) almost all mortality by predation occurred in the upper 150 m at night (98%), whereas in winter (February) the proportion of mortality below 150 m was higher than in the upper layer (73% vs. 27%). During summer (July) and autumn (September), the number of preyed-upon Metridia spp. below 150 m at night was almost the same as that in the upper 150 m (Fig. 6).

3.3. Downward transport of carbon due to DVM of Metridia spp. Total downward flux through DVM fluctuated between 1.0 and 20.0 mg C m2 d1 with an annual mean of 8.0 mg C m2 d1 (Table 3). The flux was relatively high from summer to winter and the fluctuation pattern largely corresponded with the migrating biomass of the dominant species, M. pacifica (Table 3). In general the contribution of the respiratory flux was higher than that of the mortality flux and it was estimated to account for 64–98% of the total migratory flux throughout the year

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Metridia pacifica

Metridia okhotensis 0

0

y = 58.58 + 6.623x R = 0.934 y = 89.64 + 6.060x R = 0.820

Mean depth of daytime distribution (m)

y = 59.24 + 5.007x R = 0.900 100

100

200

200

300

300

400

400

Adult females C5 C4

Adult females C5 C4

500

500 20

10

30

40

50

60

10

20

30

40

50

60

Euphotic Zone Depth (m) Fig. 3. Metridia pacifica (a) and M. okhotensis (b). Relationship between the mean depth of the daytime distribution and euphotic zone depth. Euphotic zone depth was defined as the 1% depth of surface irradiance (see Table 1). Additional data from two cruises (January and May 2001) were also included. All regression lines in the figures were statistically significant (Po0.05).

Metridia okhotensis Aug

Jun 2001 0 50

Nov

Jan 2002

Apr

Jun

F

150 Day

Night

No occurrence

300 500

Depth (m)

0 50

0

1

2

0

2

4

0

1

0

2

1

0

10

20

0

5

1 0 15

0 10 20 30 40 50

0

10

20

0

0

1 2

C5

150 300 500

0 50

6

8

0

10

20

30

0

2

4

6

0

2

4

0

1

2

30

C4

150 300 500 0

1

2

0

10

20

30

0

1

2

3

3

2

4

3

4

5

-3

Abundance (ind m ) Fig. 4. Seasonal and diel changes in vertical distribution of C4, C5, and adult females (F) of Metridia okhotensis in the Oyashio region. Open and closed bars indicate the daytime and nighttime distribution, respectively. X-axis is common for daytime abundance and nighttime abundance.

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Metridia pacifica

1783

Metridia okhotensis

2000

300 Nighttime population

1500

Migrating population

-2

-1

Migrating biomass (mgC m d )

250

200

Across 150m depth (Night minus Day) 1000

150

100 500 50

0

0 J

J

A

S

O

N

D

J

F

M

A

M

J

J

J

A

S

O

N

D

J

F

M

A

M

J

Month Fig. 5. Seasonal change in the abundance and biomass of surface migrating population of Metridia pacifica and M. okhotensis in the Oyashio region. Note that the scale of the y-axis is different between the two species.

except for January when contribution of both fluxes was equal. The total migratory flux of Metridia spp. ranged from 2% to 96% of daily grazing on autotrophic carbon and 1–22% of grazing on total POC (Table 3). Moreover, their active flux corresponded to 1–96% of the POC sinking flux at 150 m depth with an annual mean of 36% (Table 3). On an annual total basis, the total migratory flux corresponded to 26% of the total grazing on autotrophic carbon and 8% of the POC grazing on (Table 3).

4. Discussion 4.1. Metridia spp. as diel migrants in the Oyashio region This study showed that M. pacifica is a strong diel vertical migrant across the permanent pycnocline (ca. 150 m) in the Oyashio region throughout the year. As in previous studies (e.g. Zhang and Dam, 1997; Al-Mutairi and Landry, 2001), this study assumed the day/night biomass differences of Metridia spp. in the upper 150 m reflected the true migrating biomass, rather than daytime net avoidance, and that the animals fed only in the surface waters at night and resided below 150 m during the day. Since Metridia spp. including M. pacifica is generally well known as a strong diel migrant in conjunction with nocturnal feeding activity in the surface waters (e.g. Osgood and Frost, 1994; Hays, 1995; Lopez and Huntley, 1995; Atkinson et al., 1996; Takahashi et al., 2008), the assumption is considered appropriate for the estimation of migrating biomass. Moreover, the sampling

error due to spatial variability in distribution was minimized by averaged abundance of triplicate samplings. The amplitude of DVM in M. pacifica was variable depending on the developmental stage and season. We observed that M. pacifica show DVM behaviour from C4 to adult females. Although this phenomenon agrees with the previous study in the Oyashio region (Padmavati et al., 2004), the DVM in C3 individuals was also determined by high-resolution sampling (Batchelder, 1985; Hattori, 1989). Therefore the migrating biomass of M. pacifica in this study might be an underestimation, though contribution of younger individuals to the active flux is considered to be negligible because of their small scale of DVM (o100 m; Hattori, 1989), which was undetectable with our sampling. After they reach C4, DVM activity of the copepods generally becomes more evident and extensive according to their growth, while the amplitude of DVM varied seasonally. For example DVM of M. pacifica occurred largely within the upper 150 m in April, whereas all stages showed obvious migrations of greater than 150 m amplitude in January (Fig. 2) and these variations were closely related to the illumination level in the water column (Fig. 3a). Such plasticity of DVM in Metridia spp. is regarded as a response to reduce the predation risk from visually orienting predators (Hays et al., 1995; Hays, 1995). Moreover, we observed the constant occurrence of nonmigrating individuals, staying at depth at night as previously reported in this species (Hattori, 1989; Hays et al., 2001). Hays et al. (2001) suggested that such individual variability in DVM was influenced by the body condition, with animals with larger lipid stores not needing to risk coming to the surface to feed at night. These data indicate that the migrating biomass (and

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Day Night

Depth (m)

0-150m

150-1000m May 0

5

10

15

Jul. 20

0

5

10

15

20

Depth (m)

0-150m

150-1000m Sep. 0

5

10

15

Feb. 20

0

5

10

15

20

Number of Metridia spp. preyed upon by myctophid fishes (ind m-2 d-1) Fig. 6. Seasonal change of diel and vertical variation of predation pressure on Metridia spp. by three dominant myctophid fishes (D. theta, S. leucopsarus, S. nannochir) in the Oyashio region. Open and closed bars indicate daytime and nighttime predation, respectively.

hence active flux) through DVM in Metridia spp. is variable according to biotic and abiotic factors such as their life cycle, food availability, predation and light intensity. DVM in M. okhotensis was variable according to the stage and season as previously reported in the Oyashio region (Hattori, 1989; Padmavati et al., 2004). Generally their DVM became less active with growth, and females were substantially distributed below the permanent pycnocline except for in April. As this species is known to show extensive DVM in the Okhotsk Sea (Vinogradov and Arashkevich, 1969), high temperature of the surface waters during summer to autumn in the Oyashio region might inhibit their DVM. Consequently, together with their low abundance, they were generally less important as a transporter of active flux in the Oyashio region except for April, when their DVM was relatively active and they descended deeper than M. pacifica, making this species the primary migrant (Table 3).

4.2. Validity of mortality flux estimation For diel vertical migrants, estimates of the mortality flux and its temporal and spatial variability are limited in

the literature and especially field data on mortality rates for copepods in the open ocean are minimal. Zhang and Dam (1997) estimated the mortality flux using the daily weight-specific mortality model suggested by Peterson and Wroblewski (1984). Hidaka et al. (2001) modified the Peterson and Wroblewski equation by considering the habitat temperature and the metabolic and growth parameters of the mesozooplankton. When we applied these models to M. pacifica, mean daily mortality rate ranged between 5% and 14% with a mean of 6–7% (Table 4). We did not adopt these estimations in this study since they are higher than the mortality (1–3% d1) derived from the population dynamics model analysis for different populations of the same species (Batchelder and Miller, 1989; Sunami and Hirakawa, 2000). As an alternative method, we assumed that three species of myctophid fish daily consume 1–2% of the migrating population of Metridia spp. biomass. Although various factors would affect the mortality of copepods, predation has been suggested as the primary cause, accounting for ca. 2/3–3/4 of the total mortality (Hirst and Kiørboe, 2002). In the subarctic Pacific, Mackas and Tsuda (1999) suggested several groups as predators of mesozooplankton, viz. carnivorous zooplankton

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Table 3 Seasonal variation of active transport by the DVM in Metridia spp. (M. pacifica+M. okhotensis) in the Oyashio region, subarctic North Pacific. Sampling date 29 Jun 2001 Migrating biomass across 150 m (mg C m2 d1)

63.3

Annual mean

31 Aug 2001 1676.4

(60.6+2.6) (1589.1+8) Grazing at 0–150 m (mg C m2 d1)a On autotrophic carbon

14 Nov 2001

22 Jan 2002

14 Apr 2002

15 Jun 2002

263.1

472.1

58.6

622.4

(260.0+3.1)

(453.3+18.8)

11.6 gC m2 (7.9+3.7) 35.6 gC m2 (27.4+8.2)

8.6 (6.9+1.7)

8.0 (7.0+1.0)

3.0 gC m2 (2.6+0.4)

1.0 (0.1+0.9)

7.2 (5.6+1.6)

5.7 (4.9+0.8)

2.1 gC m2 (1.8+0.3)

0.0 (0.0+0.0)

1.4 (1.3+0.1)

2.3 (2.1+0.2)

0.9 gC m2 (0.8+0.1)

31.3 4.9 1.9 95.7

44.0 10.8 3.8 35.8

25.9 8.4 1.0 15.0

8.8 (8.8+0.0) 30.6 (30.6+0.0)

10.5 (10.0+0.5) 47.2 (44.9+2.3)

67.4 (27.4+40.0) 131.2 (53.3+77.9)

Total migratory flux (mg C m2 d1)

1.6 (1.5+0.1)

20.0 (17.3+2.7)

4.2 (4.1+0.1)

10.1 (9.5+0.6)

1.0 (0.1+0.9)

Respiratory flux (mg C m2 d1)

1.3 (1.2+0.1)

15.8 (13.7+2.1)

2.7 (2.6+0.1)

5.1 (4.8+0.3)

Mortality flux (mg C m2 d1)

0.3 (0.3+0.0)

4.3 (3.6+0.6)

1.5 (1.5+0.0)

5.0 (4.7+0.3)

44.3 8.5 0.3 18.0

35.8 10.9 5.6 38.5

47.6 13.6 1.0 13.1

96.2 21.4 11.0 70.7

of of of of

grazing on autotrophic carbon grazing on total POC primary productionb POC flux at 150 mc

–

31.8 (21.7+10.1) 97.5 (75.1+22.5)

55.9 (47.6+8.3) 183.1 (156.1+27.1)

% % % %

558.2

(22.2+36.5) (609.8+12.5) (527.5+30.7)

3.7 (3.6+0.1) 19.1 (18.5+0.6)

On total POC

Annual total

1.5 0.8 0.0 0.6

27.6 (26.8+0.8) 175.2 (170.2+5.0)

Mortality flux was estimated assuming 1–2% daily mortality due to predation by myctophid fish (see text). The total migratory biomass and flux are noted with bold type. a Takahashi et al. (2008). b Primary production rates are from Yokouchi et al. (2004). c Calculated based on POC flux at 1100 m estimated by the sediment trap moored at same sampling site (Takahashi, unpublished data) by using the Martin et al. (1987) equation.

Table 4 Comparison of mortality flux in Metridia spp. in the Oyashio region between different methods. Species (dry weight)

M. pacifica (0.006–0.13 mg ind

Method for mortality estimation

Daily mortality (% d1)

Assumed period when mortality flux occurs

1–2

Day and night

6 (5–11)

Modified weightspecific mortality model

Population dynamics model ) Weight-specific mortality model

2.1

0.8

This study

Day

18.9

7.1

7 (5–14)

Day

22.1

8.3

Peterson and Wroblewski (1984) Hidaka et al. (2001)

Population dynamics model Weight-specific mortality model

1–2

Day and night

0.2

0.1

This study

4 (3–6)

Day

1.0

0.4

Modified weightspecific mortality model

4 (2–5)

Day

0.8

0.3

Peterson and Wroblewski (1984) Hidaka et al. (2001)

1

M. okhotensis (0.05–0.58 mg ind1)

Mean mortality flux Annual total mortality References flux (gC m2 d1) (mg C m2 d1)

(e.g. chaetognaths, euphausiids, amphipods, medusae), planktivorous pelagic fish (e.g. salmon, saury, sardine), other top predators such as seabirds and whales, and micronekton (e.g. small squids, mesopelagic fishes, shrimps). Although the predation on mesozooplankton in this region is still not well quantified, existing knowledge at the present time indicates that myctophids are a primary predator of Metridia spp. (Appendix A). Although

mean estimated predation pressure on Metridia spp. by the myctophid fishes in this study, 13 inds m2 d1, only corresponded to 0.03–0.6% of the migrating population of M. pacifica for each sampling, we consider that our assumption is conservative and reasonable given that the estimation of myctophid biomass based on the largesize trawl sampling would be significantly lower than a more realistic value determined by the acoustic method

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Table 5 Comparisons of studies measuring the active flux and its ratio to POC flux at 150 m (Updated from Kobari et al., 2008). Specific active flux also noted. Location

Pacific Ocean Oyashio region Western subarctic gyre (K2) Western subarctic gyre (K2) Eastern equator Eastern equator Central equator Western equator Western equator Western equator ALOHA ALOHA

Migrant

Time of year

Migrating Ta (1C) biomass (mg C m2 d1)

Respiratory flux Mortality flux Total active flux % of POC (mg C m2 d1) (mg C m2 d1) (mg C m2 d1) flux at 150 m

Specific flux (d1)

References

Metridia pacifica Yearand M. okhotensis round Metridia pacifica Aug

2.3

558.2

5.7

2.3

8.0

15

0.014

This study

3.2

144.4

3.5

0.9

4.3

10

0.030

Kobari et al. (2008)

MESO+MACRO

Jul/ Aug

3

30.8

72

0.024

Steinberg et al. (2008)

MESO

13

96.0

4.2

2.9

7.1

18

0.074

MESO

Mar/ Apr Oct

13

155.0

7.3

5.4

12.7

25

0.082

MESO+MACRO

Oct

14

52.8

7.9

–

7.9

4

0.150

MESO+MACRO

Oct

14

47.2

3.8

–

3.8

8

0.081

MESO+MACRO

Feb

296.1

13.2

4

16.8

31

0.057

43

0.008

Zhang and Dam (1997) Zhang and Dam (1997) Rodier and Le Borgne (1997) Rodier and Le Borgne (1997) Hidaka et al. (2001) Hidaka et al. (2001) Al-Mutairi and Landry (2001) Steinberg et al. (2008)

9.3

1280

M-NEKTON

Feb

9.3 2875.6

MESO+MACRO

Yearround Jun/ Jul

9

Sept.

18

MESO+MACRO

Atlantic Ocean NFLUX MESO+MACRO BATS

MESO+MACRO

BATS

MESO

Year- 18 round Mar/ 18 Apr

23.5

–

b

22.8

–

23.8

142.0

3.6

–

3.6

15

0.025

158.0

3.7

4.8c

18

0.030

29

2

–

2

3

0.0690

50.0

1.5

–

2c

8

0.0400

191.0

14.5

–

14.5

34

0.0759

Longhurst et al. (1990) Steinberg et al. (2000) Dam et al. (1995)

–: no data, MESO: mesozooplankton, MACRO: macrozooplankton, M-NEKTON: micronecton (fish, squids, crustaceans). a Temperature of migrant habitat during daytime. b Gut flux is included. c DOC flux is included.

(Gjøsaeter, 1984; Koslow et al., 1997; Yasuma, 2004; Yasuma et al., 2006).

4.3. Role of Metridia spp. in the biological pump in the Oyashio region Mean active flux through DVM in Metridia spp., 8.0 mg C m2 d1, was comparable to those previously reported from subtropical and tropical waters (Table 5). This flux was supported mainly by the high migrant biomass since the export efficiency (specific flux) of Metridia spp. was considerably lower than those in subtropical and tropical waters (Table 5), probably because of the low temperature of their daytime habitat, which effectively lowers their metabolic rates. The low specific flux with high biomass would be a characteristic of the active flux by diel migrants in the subarctic waters (Table 5). Overall the annual carbon transport by DVM in the two species of Metridia was estimated as 3.0 gC m2 year1, corresponding to 1% of the annual primary production and 15% of the annual particulate carbon flux at 150 m at the

study site (Table 3). The relative importance of the active flux, however, varied seasonally between 0.6% and 96% of POC flux at 150 m. The contribution of Metridia spp. in the downward carbon export was higher during the nonblooming season (summer to winter) when near-surface nutrients are more depleted (Limsakul et al., 2002), than in the productive season (spring), and this variation is associated mainly with the spring bloom, which lowers the relative importance of the active flux of Metridia spp. through its high POC flux (Table 1) and its shading effect, which lowers the DVM amplitude (Fig. 3). After the spring bloom, the mesozooplankton biomass reaches its annual peak in the Oyashio region mainly due to the development of interzonal large calanoid copepods such as Neocalanus species and Eucalanus bungii, which subsequently descend to depths, implying that the carbon export by the ontogenetical vertical migration has its peak in summer (Kobari et al., 2003). Consequently, in terms of the biological pump in the Oyashio region, the active flux of Metridia has a complementary role, filling the period when fluxes from POC and other calanoid copepods are low from summer to winter. This indicates that Metridia plays an important role in driving the biological pump in

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Table 6 Comparison of regional difference of mean and maximum abundance of Metridia pacifica in subarctic Pacific. Stage

Area

Adult females

Oyashio region Oyashio region

C5

Western subarctic gyre Alaskan gyre (OSP) Alaskan gyre (OSP) Gulf of Alaska

References

8000

Jan

2002

4800

0–500

This study

15,000

Jul

1997

4400

0–2000

Jun

1991

–

0–200

a

0–2000

Padmavati et al. (2004) Tsuda and Sugisaki (1994) Batchelder (1985)

430

1980 2500

Jun

1987

–

0–80

Dagg (1993)

16,000

Jul

2002

–

0–100

Debob Bay

30,000

Jul

2003

–

0–160

Bering Sea Bering Sea

28,000 7000

Apr May

1994 1980

– –

0–200 0–120

Bering Sea

1700

May

1979

–

0–100

Hopcroft et al. (2005) Halsband-Lenk (2005) Kang et al. (2006) Vidal and Smith (1986) Dagg et al. (1982)

45,000 17,000

Aug Jul

2002 12,900 1997 7707

0–500 0–2000

700

Jun

1991

0–200

Nov

1980 8500a

0–2000

This study Padmavati et al. (2003) Tsuda and Sugisaki (1994) Batchelder (1985)

Jun

1984

–

0–80

Dagg (1993)

27,000

Jul

2003

–

0–160

Bering Sea

10,500

May

1979

–

0–100

Halsband-Lenk (2005) Dagg et al. (1982)

Oyashio region

10,000

Jun

1997

3511

0–2000

Oyashio region Western subarctic gyre Alaskan gyre (OSP) Bering Sea

15,000 680

Aug Jun

2002 1991

5300 –

0–500 0–200

26,000

Jan

1981 6100a

Western subarctic gyre Alaskan gyre (OSP) Alaskan gyre (OSP) Debob Bay

Adults+C5 Gulf of Alaska C5+C4 Bering Sea

a

Year Annual mean abundance Water column (ind m2) sampled (m)

Nov

Oyashio region Oyashio region

C4

Month of maximum abundance

Maximum abundance (ind m2)

10,000 2000

28,000 4400

–

0–2000

Padmavati et al. (2003) This study Tsuda and Sugisaki (1994) Batchelder (1985)

10,500

May

1979

–

0–100

Dagg et al. (1982)

27,000 20,000

May May

1987 1980

– –

0–250 0–120

Incze et al. (1997) Vidal and Smith (1986)

Calculated from Figs. 6–8 and Table 2 in Batchelder (1985).

open waters of the subarctic North Pacific, which is known as an high-nutrient low-chlorophyll (HNLC) area, lacking an apparent diatom bloom (Banse and English, 1999). The consistent occurrence of M. pacifica with high abundance throughout the subarctic Pacific supports our inference (Table 6). Kobari et al. (2008) also reported that the active flux through DVM by M. pacifica accounted for 6–44% of POC flux in an open water station (K2) in the western subarctic gyre in August. This study indicates that DVM by Metridia spp. is a significant process in carbon export in the subarctic region in addition to ontogenetic migration by interzonal copepods such as Neocalanus spp. (Kobari et al., 2003). Even though our estimation of the active flux was made using data for only the two species of Metridia, it is comparable with those by the whole mesozooplankton community in tropical and subtropical oceanic regions (Table 5), suggesting that the significance of the active flux

by DVM in the subarctic region is much higher than our estimation because of the occurrence of other active diel migrants such as euphausiids, amphipods, chaetognaths, etc. (Steinberg et al., 2008). Together with other processes in the active flux such as DOM excretion (Steinberg et al., 2000) and gut flux (Schnetzer and Steinberg, 2002), further estimation of the active flux by entire mesozooplankton and micronekton community is necessary to reveal the extent of the biogeochemical cycle in the subarctic Pacific. Acknowledgements We wish to acknowledge the captains and crew of the research vessels Wakataka-maru and Torishima and all participants of the cruises for their cooperation at sea. We also thank A. Izumi and Y. Akama for their assistance of laboratory work, K. Hidaka for his help in the

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calculation of mesozooplankton mortality, M. Moku for the information of gut clearance rate of myctophid fish, and A. Yasuma for the estimation of myctophid biomass. A part of this research was supported by grants of the DEEP from the Fisheries Agency of Japan and by grant-in-Aid for Young Scientists (A), 2007, 18688011-

0001from the Ministry of Education, Science, Sports and Culture to KT. Appendix A See Table A1.

Table A1 Examples of studies for gut content analysis of planktivores in the subarctic Pacific including adjacent seas. Potential predator

Species of predator

Dominant prey

Study area

References

Japan Sea

Terazaki (1993)

NW Pacific

Terazaki (1995)

Euphausiids

Sagitta elegans Eukrhonia hamata Euphausia pacifica

Neocalanus spp., Paracalanus parvus, Conchoecia pseudodiscophora Pseudocalanus spp., Metridia pacifica, Neocalanus flemingeri Oithona similis, Metridia pacifica Oncaea spp. Oncaea similis, Metridia pacifica Diatoms, flagellates, copepod nauplii

Sullivan (1980) Sullivan (1980) Nakagawa et al. (2003)

Amphipods

Themisto japonica

Appendicularians, Copepods, Fish larvae

Themisto japonica

Copepods, Chaetognaths, Amphipods

Alaskan gyre Alaskan gyre Oyashio region Oyashio region Oyashio region Oyashio region

Carnivorous zooplankton Chaetognaths Sagitta elegans Sagitta elegans

Ctenophores

Bolinopsis infundibulum Neocalanus cristatus, Aetideidae copepods

Planktivorous pelagic fish and other top predator Chum salmon Oncorhynchus keta Themisto japonica, Clione limacina, Thysanoessa longipes Sockeye salmon Oncorhynchus nerka Themisto japonica, Thysanoessa longipes, Neocalanus cristatus Pink salmon Oncorhynchus Themisto japonica, Clione limacina, Neocalanus criatstus gorbuscha Fareast sardine Sardinops melanostictus Neocalanus plumchrus, Oithona similis, Pseudocalanus sp. Sardinops melanostictus Neocalanus spp. Pseudocalanus minutus Pacific saury

Cololabis saira

Euphaisia pacifica, Neocalanus spp.

Cololabis saira

Neocalanus plumchrus

Cololabis saira

Neocalanus plumchrus, Neocalanus cristatus, Euphausia paficica Euphausia pacifica, Copopods, Amphipods

Yamashita et al. (1985) Sugisaki et al. (1990) Toyokawa et al. (2003)

NW Pacific NW Pacific

Takeuchi (1972) Takeuchi (1972)

NW Pacific

Takeuchi (1972)

Oyashio region Oyashio region Oyashio region Oyashio region Oyashio region Oyashio region Oyashio region

Yoshida (1987) Iizuka (1987) Sugisaki and Kurita (2004) Taka et al. (1982) Odate (1977)

Chub mackerel

Scomber japonicus

Walleye pollock

Theragra chalcogramma Neocalanus cristatus, Euphausia paficica

Fin whales Sei whales

Balaenoptera physalus Balaenoptera borealis

Euphausia pacifica, Tysanoessa spp. Neocalanus criatatus Neocalanus crtatatus, Neocalanus plumchrus, Calanus pacificus

North Pacific Kawamura (1982) North Pacific Kawamura (1982)

Diaphus thetaa

Euphausuia pacifica, Metridia pacifica, Neocalanus spp.

Oyashio region NW Pacific

Moku et al. (2000)

Oyashio region Oyashio region Off Oregon

Gordon et al. (1985)

NW Pacific

Furuhashi (1987) Gordon et al. (1985)

Metridia pacifica, Neocalanus spp. Eupahsiids

Oyashio region Bering Sea

Neocalanus cristatus, Neocalanus spp., Pleuromamma scutullata Neocalanus plumchrus, Eucalanus bungii, Metridia pacifica

Oyashio region Bering Sea

Moku et al. (2000)

Mesopelagic micronekton Myctophid fishes

Diaphus theta

a

Diaphus theta

a

Stenobrachius leucopsarusa Stenobrachius leucopsarusa Stenobrachius leucopsarusa Stenobrachius leucopsarusa Stenobrachius leucopsarusa Stenobrachius nannochira Stenobrachius nannochira

Metridia pacifica, Neocalanus plumchrus, Neocalanus cristatus Metridia okhotensis, Metridia pacifica, Metridia sp. Metridia pacifica, Neocalanus spp. Eupahsuia pacifica, Parathenmisto japonica, Metridia pacifica Neocalanus criatstus, Metridia pacifica, Neocalanus plumchrus Metridia okhotensis, Eupahsiids, Pleuromamma sp.

Iizuka (1987) Yamamura et al. (2002)

Furuhashi (1987)

Moku et al. (2000) Pearcy et al. (1979)

Tanimata et al. (2008)

Furuhashi and Shimazaki (1989)

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Table A1 (continued ) Potential predator

Gonostomatid fishes

Sternoptychid fishes Squids

Shrimps

Species of predator

Dominant prey

Study area

References

Stenobrachius nannochira Protomyctophum tompsoni Protomyctophum tompsoni Lampanyctus jordani

Pleuromamma sp., Ostracods, Gaidius variabilis

Oyashio region NW Pacific

Gordon et al. (1985)

Oyashio region Oyashio region Oyashio region NW Pacific NW Pacific NW Pacific

Gordon et al. (1985)

Oyashio region Oyashio region Oyashio region Oyashio region Oyashio region Oyashio region

Uchikawa et al., 2002

Metridia pacifica, Neocalanus plumchrus, Neocalanus cristatus Copepods, Mysids

Lampanyctus jordani

Eupahsuia pacifica, Decapod crustaceans, Neocalanus cristatus Thysanoessa sp., Euphausia pacifica

Tarletonbeania taylori Tarletonbeania taylori Symbolophorus calforniensis Notoscopelus japonicus

Neocalanus plumchrus, Amphipoda, Metridia pacifica Neocalanus criatstus, Themisto spp., Candacia colombiae Metridia pacifica, Neocalanus plumchrus, Neocalanus cristatus Eupahsuia pacifica

Gonostoma gracile

Pleuromamma spp, Ostracods, Amphipods

Gonostoma gracile

Euphausiids, Ostracods, Unidentified copepods

Cyclothone atraria

Pleuromamma sp. Gaidius sp., Ostracods

Cyclothone pseudopallida Maurolicus japonicus

Gaidius variabilis, Gaidius sp., Ostracods Euphausia pacifica, Chaetognaths, Calaunus pacificus

Berryteuthis anonychus Berryteuthis magister Watasenia scintillans

Neocalanus cristatus, Sagitta elegans, Amphipods Calanus sp., Amphipods Metridia paficica

Gonatus madokai Gonatopsis japonicus

Chaetognaths Amphioids

Sergestes similis Bentheogennema borealis Hymenodora frontalis

Scyphomesuda, Scyphomesuda, Euphcausiids) Scyphomesuda, Euphcausiids) Scyphomesuda, Euphcausiids) Scyphomesuda, Euphcausiids)

Notostomus japonicus Systellaspis braueri

Furuhashi (1987)

Uchikawa et al. (2008) Gordon et al. (1985) Furuhashi (1987) Kawamura and Fujii (1988) Kawamura and Fujii (1988)

Uchikawa et al. (2001a) Gordon et al. (1985) Gordon et al. (1985) Gordon et al. (1985) Uchikawa et al. (2001b)

NE Pacific NW Pacific Oyashio region NW Pacific Japan Sea

Uchikawa et al. (2004) Okutani et al. (1988) Uchikawa, unpublished data Okutani et al. (1988) Okutani et al. (1988)

Copepods, Chaetograths Large crustaceans (Decapods, Mysids,

Off Oregon Off Oregon

Nishida et al. (1988) Nishida et al. (1988)

Large crustaceans (Decapods, Mysids,

Off Oregon

Nishida et al. (1988)

Large crustaceans (Decapods, Mysids,

Off Oregon

Nishida et al. (1988)

Large crustaceans (Decapods, Mysids,

Off Oregon

Nishida et al. (1988)

Metridia spp., which used in this study as a mediator of the active flux, are noted in bold type. a Species used for mortality flux estimation in this study.

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