A 9-year increasing trend in mesozooplankton biomass at the Hawaii Ocean Time-series Station ALOHA
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1 ICES Journal of Marine Science, 61: 457e463 (2004) doi: /j.icesjms A 9-year increasing trend in mesozooplankton biomass at the Hawaii Ocean Time-series Station ALOHA Cecelia C. Sheridan and Michael R. Landry Sheridan, C. C., and Landry, M. R A 9-year increasing trend in mesozooplankton biomass at the Hawaii Ocean Time-series Station ALOHA. e ICES Journal of Marine Science, 61: 457e463. Mesozooplankton biomass in the North Pacific Subtropical Gyre (NPSG), as measured by the Hawaii Ocean Time-series program at Station ALOHA (22.45(N 158(W), increased significantly from 1994 to The changes occurred at a rate of 60 mg DW m ÿ2 yr ÿ1 for night-time collections and 45 mg DW m ÿ2 yr ÿ1 for daytime collections. Principal components analysis indicates that the 9-year trend was driven by an increase in small (e2.0 mm) zooplankton that do not migrate on a diel cycle. This plankton class is known to increase during the summer at Station ALOHA when the water column is most stratified, and a strong summertime response is also apparent within the long-term trend from 1998 through Both long-term and seasonal changes in zooplankton biomass at Station ALOHA can be linked to an enhanced role of nitrogen fixation in ecosystem productivity. Climate forcing from El NiñoeSouthern Oscillation (ENSO) events may have influenced nitrogen fixation, general ecosystem productivity, and thus zooplankton biomass in the NPSG. However, it is difficult to evaluate the effect of climate cycles in this region without the benefit of a longer time-series at Station ALOHA. Because biomass trends in higherlevel consumers like mesozooplankton can have cascading influences on lower levels, understanding the relative roles of bottom-up climate influences and top-down trophic processes will be important in resolving long-term trends in community composition and structure in the subtropical North Pacific Ocean. Ó 2004 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved. Keywords: Central North Pacific, Hawaii Ocean Time-series, nitrogen fixation, subtropical gyre, zooplankton. Accepted 23 March C. C. Sheridan: Department of Oceanography, University of Hawaii, 1000 Pope Road, Honolulu, HI 96822, USA. M. R. Landry: Integrative Oceanography Division, Scripps Institution of Oceanography, La Jolla, CA , USA; tel: ; fax: ; mlandry@ucsd.edu. Correspondence to C. C. Sheridan: tel: ; fax: ; sheridan@hawaii.edu. Introduction In the 1960s and 1970s, the high plankton diversity and relative constancy of rank-order species abundance in the North Pacific Subtropical Gyre (NPSG) were taken to indicate an ecosystem controlled by complex biological interactions rather than physical perturbations in space or time (e.g. Hayward et al., 1983). Consequently, research during this era focused on understanding the internal regulatory processes underlying the existence of a plankton community in its quintessential climax successional state (sensu Clements, 1936; e.g. Hayward and McGowan, 1979; Hayward, 1980; McGowan and Walker, 1985). In recent years, the tenets for applying climax theory to the NPSG have been challenged by systematic, higher frequency observations from satellite and shipboard sampling. These new observations, largely from the 15- year-old Hawaii Ocean Time-series (HOT) program (Karl, 1999), have established that phytoplankton production and standing stock vary on a regular seasonal cycle and irregularly through perturbations associated with Rossby waves, cyclonic eddies, and meandering fronts (e.g. Letelier et al., 2000; Seki et al., 2002; Sakamoto et al., in press). Although the magnitude of biomass change in the NPSG is not on the scale of highly seasonal temperate and polar regions (Longhurst, 1998), it is clear that the system is neither temporally nor spatially uniform (Karl et al., 2002). Identifying long-term trends in the central North Pacific Ocean using the HOT data set has been challenging owing to the relatively few number of observations in this timeseries. Recent compilations of the 15-year record from the /$30 Ó 2004 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.
2 458 C. C. Sheridan and M. R. Landry HOT Station ALOHA (22.45(N 158(W) reveal significant long-term changes in the physical structure of the water column (Lukas, 2001), the strength of the carbon dioxide sink (Dore et al., 2003), and the source of nitrogen for export production (Dore et al., 2002). Comparison of HOT data with older ecosystem studies further suggests that key components of the NPSG plankton community may fluctuate in abundance over longer (decadal) time scales (Karl et al., 2001; Landry et al., 2001). In this study we report the first evidence of long-term change in NPSG mesozooplankton biomass as measured on monthly intervals by the HOT program since We define a linear trend in the 9-year data set and explore the contribution of different zooplankton size fractions to the biomass change using principal components analysis (PCA). Materials and methods Zooplankton samples described in this study were collected each month from Station ALOHA (22.45(N 158(W), a site 100 km north of the island of Oahu in the central North Pacific Ocean (Karl and Lukas, 1996), from 1994 to Mesozooplankton at Station ALOHA are collected using a 1-m 2, 200-mm mesh plankton net towed obliquely through the w160 m euphotic zone ( for details, see Landry et al., 2001). On every cruise, three replicate net tows are conducted during the day (10:00 to 14:00) and three at night (22:00 to 02:00). Plankton from each tow are immediately wet-sieved, and the resulting size fractions (0.2e, e1, 1e2, 2e5, and O5 mm) are frozen in liquid nitrogen. Dry weight biomass for each size fraction is determined after thawing and oven drying (60(C for w5 days). Day dry weights presented for each cruise are the mean of three replicate daytime collections summed over all size fractions. Similarly night dry weights are the mean of three replicate night-time collections summed over all size fractions. The biomass of diel vertical migrators is referred to as migrant and is calculated as night minus day. Temporal trends in night, day, and migrant biomass are explored using linear regression of cruise mean biomass (g DW m ÿ2 ) over time (days). We conduct PCA with v j variables (descriptors) = all day and migrant size fractions (j ¼ 10) and s k samples = all pertinent cruise observations (k ¼ 85). Data entered into the PCA are log-transformed (ln½xþ 1Š) but not standardized before calculation of the covariance matrix. Four cruises where only night collections were taken or with anomalous migrant data were not used. The PCA was conducted using PRS SIRIUS for Windows (v. 1.2B); all other statistics were calculated using SPSS (v ). Results The total biomass of mesozooplankton collected during the night and day at Station ALOHA has increased since 1994 (Figure 1A, B). The increasing trends for night-time and daytime collections (Figure 1) are highly significant (linear regression, p! 0:005). The total biomass of diel vertical migrators (nighteday) did not increase (Figure 1C). Note that anomalous negative migrant numbers were observed when day biomass exceeded night biomass; in 2001 this occurred during a rare bloom of the diatom Hemiaulus hauckii (Figure 1). No temporal trends are observed in the residuals of the regressions (insets, Figure 1). In consideration of the potential effect of the 1998 PDO reversal, when day and night biomass data sets are split into two sub-series, the slope of the initial 4 years (1994e1997; 1:20! 10 ÿ4 gdwm ÿ2 d ÿ1 ) and that of the latter half of the time-series (1999e2002; 2:36! 10 ÿ4 g DW m ÿ2 d ÿ1 ) do not differ significantly from one another (F-test for equality of two slopes, p > 0:05; Sokal and Rohlf, 1995). PCA was used to separate variation in the biomass of day and migrant size fractions into two principal axes (Figures 2 and 3). Cruise scores clearly increase along the first principal axis (Figure 2A; linear regression, r 2 ¼ 0:184, p! 0:005). The first axis scores are separated by a highly negative winter group in 1994e1995 (Group I, Figure 3) and a highly positive summer group in 1998e2002 (Group II, Figure 3). Intra-annual variation in cruise scores along the first axis is highest in the latter half of the time-series, 1998e2002. In contrast, high cruise scores in the summer of 1996 dominate the second principal axis (Group III, Figure 3), with high positive scores also noted for the summer and late spring of 1998 and 1999 (Figure 2). Intraannual variation in cruise scores along the second principal axis is highest in the earlier half of the time-series, 1994e1996. Day and migrant size fractions contributed differently to each PCA axis (Figure 3). Projection of the apices of the variable (descriptor) axes (D X and M X in Figure 3) onto each principal axis indicates the contribution of those variables to the principal axis (Legendre and Legendre, 1998). It is apparent that small, non-migrating (daytime) zooplankton drive ordination of cruise scores along the first principal axis (D e1, Figure 3), whereas migrant zooplankton drive ordination along the second principal axis (M e2, Figure 3). All other descriptors (D 0.2&2e5,M 0.2&5 ) did not contribute significantly to the ordination because these variables fall below the radius of the equilibrium descriptor circle (0.447) along each principal axis (Legendre and Legendre, 1998). Discussion Zooplankton biomass at Station ALOHA has increased significantly over the past 9 years, at a rate of 60 mg DWm ÿ2 yr ÿ1 for night-time collections and 45 mg DW m ÿ2 yr ÿ1 for daytime collections (Figure 1A, B). Expressed as an instantaneous annual rate, the increase in biomass at the HOT Station ALOHA (+5 yr ÿ1 ) is comparable to trends
3 Increasing trend in mesozooplankton biomass at station ALOHA 459 DAY dry weight (g m -2 ) NIGHT dry weight (g m -2 ) A B - - MIGRANT dry weight (g m -2 ) C - * (-0.11) * (-0.32) Figure 1. Mesozooplankton dry weight biomass measured monthly during the Hawaii Ocean Time-series (HOT) program at Station ALOHA (22(45#N 158(W) from 1994 to Mean biomass for plankton collected during the (A) night, (B) day, and (C) the biomass of migrating zooplankton (nighteday) are shown. Linear regressions for each plot (dashed lines) are as follows: (A) night g DW m ÿ2 ¼ 1:62! 10 ÿ4 )d þ 0:458; (B) day g DW m ÿ2 ¼ 1:23! 10 ÿ4 )d þ 0:204; and (C) migrant g DW m ÿ2 ¼ 3:92! 10 ÿ5 )d þ 0:257. Insets are the unstandardized residuals from each regression (g DW m ÿ2 ) vs. time (days). observed in more traditionally dynamic ocean environments. For example, the 80% decline in zooplankton displacement volume in the California Current (Roemmich and McGowan, 1995) from 1970 to 1993 corresponds to an instantaneous rate of ÿ7 yr ÿ1. The first axis from our zooplankton biomass principal components analysis (PCA) reflects the long-term trend in the HOT data (Figure 2A). Examination of the first principal axis reveals that variations in the biomass of small (e2.0 mm), non-migrant zooplankton drive the increasing trend at Station ALOHA (D &D 1, zooplankton Figure 3). Both inter- and intra-annual variations in small zooplankton contribute to the PCA trend, with the largest changes occurring during the summers of 1998e2002 (Figure 2). Landry et al. (2001) previously described a significant summer maxima in small (0.2e2 mm) zooplankton biomass at
4 460 C. C. Sheridan and M. R. Landry 0.4 A 0.3 Axis 2 Scores (23.7%) Axis 1 Scores (33.5%) B Figure 2. Results of the principal components analysis (PCA) of HOT zooplankton biomass. The PCA was run with day and migrant (=nighteday) size-fractionated dry weight biomass. Scores for (A) the first principal axis and (B) the second principal axis are shown. The first axis scores from the HOT zooplankton PCA increase significantly with time (y ¼ 0:000514x ÿ 0:185; r 2 ¼ 0:184). The two PCA axes explained a total of 57.2% (axis 1 ¼ 33:5%; axis 2 ¼ 23:7%) of the total variance in zooplankton biomass at Station ALOHA. Station ALOHA. Although this biomass maxima occur during a season of intense water column stratification (Bingham and Lukas, 1996), the summer is also a time of high primary production due to the introduction of new nutrients from nitrogen-fixing plankton (Dore et al., 2002) and high growth irradiances in the lower euphotic zone (Letelier et al., 2004). As (i) the size classes responsible for seasonal and long-term changes in zooplankton biomass are similar and (ii) a strong summertime response is also apparent within the long-term trend, both the summer and long-term increases in zooplankton biomass at Station ALOHA likely derive from the same source, e.g., the input of nutrients from nitrogen fixation. Considerable biochemical evidence from the HOT program suggests that the contribution of nitrogen fixation to elemental cycling in the North Pacific Subtropical Gyre (NPSG) has increased. For example, inventories of nitrogen have become larger relative to phosphorus (Church et al., 2002; Karl et al., 2003), and di-nitrogen (N 2 )-supported export increased relative to nitrate (NO 3 ÿ )-supported export throughout the late 1990s (Dore et al., 2002). Higher activity of nitrogen-fixing phytoplankton at Station ALOHA could have led to an increase in mesozooplankton biomass through either direct trophic transfer or indirect enhancement of ecosystem productivity. Establishing a direct link between diazotrophs and zooplankton is difficult because abundance data for nitrogen-fixing phytoplankton do not exist. However, the hypothesis of a recent shift in general ecosystem productivity is supported by recent changes in pigment biomarkers (Figure 4; from Karl et al., 2002). Biomarkers diagnostic for cyanobacteria, prymnesiophytes, pelagophytes, and diatoms increased in concentration
5 Increasing trend in mesozooplankton biomass at station ALOHA 461 AXIS M 2 M 1 M M 0.2 III D 5 D x M x CRUISE Scores DAY Loadings MIGRANT Loadings D 0.2 D 1 D -0.1 I II AXIS 1 Figure 3. A correlation biplot of cruise scores and variable (descriptor) loadings from the HOT zooplankton biomass PCA. Apices of the descriptor axes are divided into day (D X ) and migrant (M X ) categories, where X Z the size fraction of each category (i.e. O5 mm, 2e5 mm, 1e2 mm, e1 mm, 0.2e mm). Score extrema are noted by shaded boxes, where Group I Z low axis 1 and 2 scores [winter 1994 and 1995], Group II Z high axis 1 and low axis 2 scores [summer and early fall 1998e2002], and Group III Z high axis 2 scores [summer 1996]. through the late 1990s, although we note that variations in biomarker concentrations (Karl et al., 2002) and in the first principal axis of the zooplankton PCA do not directly covary (compare Figures 2A and 4). Clearly more research is needed to evaluate ecosystem dynamics involving nitrogen fixation, eucaryotic phytoplankton, and mesozooplankton at Station ALOHA. Large-scale climate variations ultimately control the dynamics of ocean ecosystems (McGowan et al., 1998; Chavez et al., 2003), and alteration of NPSG stratification and mixed layer depths by El NiñoeSouthern Oscillation (ENSO) events may have spurred the enhanced ecosystem productivity at Station ALOHA. During the 1991e1995 period of negative Southern Oscillation Index Values (SOI; Troup, 1965), evidence suggests that reduced mixing of the upper water column (Karl et al., 1995) selected for enhanced growth of nitrogen-fixing phytoplankton in the NPSG (Karl, 1999). After 1996, a moderate mixing regime (corresponding to positive SOI values) is thought to have enhanced nitrogen fixation and nitrogen export at Station ALOHA by refueling the ecosystem with phosphate (Dore et al., 2002). Although these associations suggest that changes in zooplankton biomass at Station ALOHA may be linked to ENSO-related fluctuations, our limited observations prior to 1996 make it difficult to determine whether or not the long-term trend is oscillatory in nature. Understanding climate influences at Station ALOHA is further complicated by the 1998 reversal of the Pacific Decadal Oscillation (PDO; Mantua and Hare, 2002). The effect of this low-periodicity (w20 years) climate pattern on NPSG ecosystem dynamics is not well understood, but fluctuations in the PDO typically manifest as step changes M 5 D 2 in multiple ecosystem properties (Ebbesmeyer et al., 1991; Hare and Mantua, 2000). Although plankton seasonality was more pronounced after 1998 (Figure 2), a clear step increase is not apparent in our zooplankton biomass data. Regression residuals from day and night biomass trends do not show a temporal pattern (Figure 1, insets) and regression slopes do not change significantly within the time-series. A plankton response to PDO fluctuations may have been complicated by the effects of the 1997/1998 drought on upper water column salinity and seasonal thermocline stability at Station ALOHA (Lukas, 2001). Further evaluation of PDO influences should be postponed until it is possible to assess effects of the 2003 PDO index reversal ( on plankton seasonality and biomass at ALOHA, if the current trend is maintained. Although future research at the HOT Station ALOHA will continue to explore links between climate-influenced variations in mixing and changes in plankton community structure, top-down processes are also likely to be important in understanding relationships among components of the NPSG ecosystem. For example, the microbial community in the NPSG forms a tightly coupled system, where perturbations at one end of the microbial loop rapidly translate into changes in the biomass of the other components (Calbet and Landry, 1999). Mesozooplankton can exert a measurable grazing impact on O5 mm protists in the microbial loop (Calbet and Landry, 1999), and such trophic impacts, though small, may be sufficient to tip the balance between slow rates of increase or decrease where the mean state of all stocks is a net growth of zero. Because NPSG populations of zooplankton and microbial system dominants such as Prochlorococcus vary on decadal time scales (Karl et al., 2001; Landry et al., 2001; Landry, 2002), the relative roles of top-down trophic processes and bottom-up climate influences should be an important component of future time-series studies in the subtropical North Pacific Ocean. Acknowledgements We are indebted to several individuals, namely Karen Selph, Stephanie Christensen, Rebecca Scheinberg, Scott Nunnery, and Colleen Allen, for their participation in the HOT zooplankton program from 1994 to We also acknowledge the creative vision and perseverance of HOT co-p.i.s Drs Dave Karl, Bob Bidigare, Roger Lukas, Ricardo Letelier, and John Dore. We sincerely thank the large number of individuals who have collected HOT core data over the past 15 years. This article was significantly improved by comments from Bob Bidigare, Skip McKinnell, and two anonymous reviewers. We sincerely thank PICES for providing student travel support to the 2003 International Zooplankton Production Symposium in Gijón, Spain. Our research was funded by NSF grants
6 462 C. C. Sheridan and M. R. Landry A Zeaxanthin '-Hexanoyloxyfucoxanthin 19'-Butanoyloxyfucoxanthin B C D Fucoxanthin Figure 4. Temporal changes in pigment biomarkers at Station ALOHA during 1994e1999. For each datum, pigment inventories were integrated from the surface to 175 m. The pigments are diagnostic for the following phytoplankton groups: (A) cyanobacteria [zeaxanthin], (B) prymnesiophytes [19#-hexanoyloxyfucoxanthin], (C) pelagophytes [19#-butanoyloxyfucoxanthin], and (D) diatoms [ fucoxanthin]. Adapted from Karl et al. (2002). OCE and OCE This paper is SOEST contribution 6381 and U.S. JGOFS contribution References Bingham, F. M., and Lukas, R Seasonal cycles of temperature, salinity, and dissolved oxygen observed in the Hawaii Ocean time-series. Deep-Sea Research II, 43: 199e213. Calbet, A., and Landry, M. R Mesozooplankton influences on the microbial food web: direct and indirect trophic interactions in the oligotrophic open ocean. Limnology and Oceanography, 44: 1370e1380. Chavez, F. P., Ryan, J., Lluch-Cota, S. E., and Niquen, C. M From anchovies to sardines and back: multidecadal change in the Pacific Ocean. Science, 299: 217e221.
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