Relationship between physical and biological processes at an upwelling front off Peru, 15°S

I)ccp-Sca Research. Vol. 32, No. II, pp. 13(11 to 1315. 1985. Printed ill (;real nrilain.

(119P-~41149/85$3(M1 + (I.(~t ~D 1985 Pcrganlon Prc:~s lad.

Relationship between physical and biological processes at an upwelling front off Peru, 15°S A. T. DI-N(;I.I.~R* (Received 11) October 1981 ; in revised form 23 March 1985; accepted 25 March 1985) Abstract---Continuous sampling of temperature, fluorescence and nutrients was performed as part of the JOINT II expedition of the Coastal Upwclling Ecosystcm Analysis program. A 5(81 squarc kilometer region off the coast of Peru at 15°S was survcycd on 8 nights over a 4-week pcriod in May and June 1976. In this region, a surface thermal front is repeatedly obscrvcd, tempcrature increasing as much as I°C per horizontal kilometer. The surface mixed layer shoals as the front is approached from offshore. A maximum in fluorescence corresponds to maxima in productivity and biomass, and is consistently displaced on the order of a kilometer to the warm water side of the thermal front. The intensity of the displaced fluorescence maximum is positively correlated with the sharpness of the surface temperature gradient at the front. The suggested mechanisms for this feature are a combination of growth facilitated by ammonium as a nitrogen source and of distribution of the phototropic Gymnodinium splendens during night-timc sampling throughout the shoaling mixed layer.

INTRODUCTION

OCEANIC upwelling often is studied in terms of both physical dynamics and biological response. The coastal area of Peru has been the site of a number of such studies due to an extensive historical record of upwelling events. GUNTHER(1936a,b) first reported a temperature minimum, a surface signature of active upwelling, near Cabo Nazca (approximately 15°S latitude). Later temperature surveys by Instituto del Mar del Peru (GuILLEN and FLORES, 1965) located a plume-like upwelling feature in the surface layer. Similar surface plumes were found at the same location by expeditions in 1966 (RYTHER et al., 1971), 1969 (WALSH et al., 1971; KELLYand WHITLEDGE, 1975), 1976 and 1977 (HuYER et al., 1978; WHITLEDGEet al., 1980). Upweiling in the Cabo Nazca area can be related to constant features and to variable forcing phenomena. The tendency for upwelling is linked to the local bathymetry and coastal topography (ARTHUR, 1965; MOOERSand ALLEN, 1973; HURLBURT,1974; O'BRIEN et al., 1977). The variable intensity of upwelling is affected by a combination of local winds and coastal trapped waves (STUART, 1981; BRINKet al., 1980; ALLEN, 1980; JONESet al., 1980a) that fluctuate on time scales of days. Upwelling, as manifested by surface temperature, fluctuates on the same times scales. While biological variables and nutrients depend strongly on the physical dynamics, it has proven difficult to specify the precise relation between the biological and chemical variables and the physical upwelling manifestations. RYTJmRet al. (1971), following a * Scripps Institution of Oceanography, A-008, University of California, San Diego, La Jolla, CA 92093, U.S.A. Present address: University of California, Berkeley, CA 94720, U.S.A. 1301

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A.T. DENGLER

drogue set within the surface thermal plume, and BEERS et al. (1971), tracking a chlorophyll patch by means of underway sampling, found evolution and dissipation of patches on scales of days and kilometers, but did not evaluate the degree to which the biological variations were due to physical changes in upwelling over the same scales. The Pisco expedition in 1969 (WALSH et al., 1971; KELLEYand CRUZADO, 1973) used continuous underway sampling to obtain quasisynoptic maps of temperature, chlorophyll level and nutrient concentration. Considerable variation was observed in both the extent of the upwelling feature as indicated by temperature and in the absolute location of nutrient and phytoplankton foci. Although there appears to be a relationship between the thermal patterns at the surface and the distributions of the biological parameters, the relationship cannot be described in detail because only average conditions over large areas are reported. To characterize this relationship, it is necessary to obtain finer resolution in both space and time. Such resolution is available in the data set collected during the JOINT II expedition of the Coastal Upwelling Ecosystems Analysis (CUEA) program. In this paper, I use this data set to address two questions: What is the relationship between the physical measurement of temperature and the biological variables of chlorophyll fluorescence and nutrients? How does this relationship vary over time scales comparable to those of the major variations in local winds and of coastal trapped waves?

SAMPLING AND METttODS

Background The data used here were collected on legs II and III of cruise 108 of the R.V. Thomas G. Thompson during the JOINT II expedition of the C U E A program. The expedition was conducted to the coastal regions of Peru during April, May and June 1976, so as to coincide with the austral-winter upwelling season. Certain conditions in the Peruvian upwelling region during the 1976 expedition appear to have been anomalous. Throughout the 1976 expedition upwelling manifested aguaje conditions (CoDISPOTIet al., 1976; DUGDALEet al., 1977). Aguaje is a colloquial term denoting seasons of intense plankton blooms, red tides, and apparently associated sea bird die-offs and decrease in fishery productivity. Aguaje appears distinct from, but not exclusive of, El Nifio, the occasional incursion of warm water from the north, and occurs no more often than major El Nifio, perhaps on the scale of once in 20 years (Du6DALE et al., 1977). Anomalous conditions characteristic of aguaje are observed in winds, currents, plankton and nutrients. Wind direction appeared normal in 1976, but wind intensity was distinctly high. Coastal winds generally are from the southeast, primarily tangential to the coast with a smaller offshore component (ZuTAet al., 1978). In 1969, BURTet al. (1973) found mean values for surface winds north of Nazca to be 4.6 m s-l. In measurements made in the 1960s ZUTA and GUILLEN(1970) found mean values of 4.8 m s-~. By contrast, winds in the period from 13 May to 7 June, preceding and overlapping the collection of data used here, averaged close to 7.5 m s-i (STUARTetal., 1976; JONESet al., 1980b). The surface manifestations of the currents in 1976 were different from those previously observed. During the period of strong winds noted above, the usual plume structure of isobars at the surface developed into a banded structure with isobars parallel to the coast, as is characteristic of upwelling off Oregon and Northwest Africa (JONESet al., 1980).

Physical and biologicalprocessesat an upwellingfront off Peru

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The composition of the phytoplankton community in 1976 differed from the composition found in previous studies. The Pisco and Piquero 1969 expeditions found the phytoplankton community dominated by diatoms (BLAsCO, 1971 ; BEERSet al., 1971). Only a few scattered stations sampled on the Pisco expedition showed large numbers of the dinoflagellate Gymnodinium splendens. In contrast, the 1976 JOINT II expedition found an extensive bloom of G. splendens which stretched from the Galapagos Islands south to the study area (DuGDALE et al., 1977; D. BLASCO, personal communication). The anomalous bloom persisted throughout the 1976 portion of the expedition (JONES, 1978). An analysis of nutrient distributions in the region was made in the 1976 study. JONES (1978) determined that nitrogen was a limiting nutrient. Calculated phytoplankton uptake accounted for the decrease of nitrate in the surface water between the times of upwelling and of mixing and advection offshore out of the study region. Silicate and phosphate concentrations were always above levels which would limit diatom or dinoflagellate growth. In contrast to the expectations for previous years, silicate was of less importance in influencing the species composition of the phytoplankton, as dinoflagellates rather than diatoms were the major component of the phytoplankton. Data collection

Sampling was designed to measure variations on time scales of days to weeks, and space scales of several kilometers to tens of kilometers. Portions of the underway sampling had sufficient resolution to allow examination down to kilometer scales. There were no physical measurements to evaluate the physical forcing functions of local winds or coastal trapped waves during legs II or. III of the Thomas G. Thompson cruise, although such measurements are available from a period of investigation in the immediately preceding months (BRINKet al.. 1980). The expedition sampled for both horizontal and vertical patterns. Horizontal patterns were investigated by continuous underway sampling of surface waters. The ship followed a zig-zag cruise track over the study area (Fig. 1). Vertical patterns were examined by bottle and CTD casts (FRIEBERTSHAUSERet al., 1977). Casts were made along a single onshoreoffshore line in the same area as the horizontal surveys. Sampling was performed at night, and sampling of only one type was performed on a given night. Over a 30-day period in May and June 1976, horizontal zig-zag cruise tracks were run on 8 nights (Table 1), generally alternating with vertical casts on 6 nights. Underway measurements were made on water pumped continuously from a port 3 m below the surface. Water entered a sea chest, where temperature was measured, and passed through autoanalyzers for measurements of nitrate, nitrite, ammonium, phosphate and silicate. Water also was pumped through a fluorometer for measurement of phytoplankton fluorescence. Signals from these instruments were digitized at 1-min intervals and stored on magnetic tape. For a ship speed of 15 km h -~ (8 kn), this time interval converts to a 250-m sample spacing. Detailed descriptions of the techniques are given in LORENZEN(1966), ARMSTRONGet al. (1967), WALSttet al. (1971) and KELLEYet al. (1975). Vertical casts were made at approximately 5-kin intervals along a line perpendicular to the coast, providing a coarsely sampled vertical section through the study area. These casts sampled much the same suite of parameters as the horizontal sampling. Temperature and salinity were measured at 2-m vertical intervals on CTD casts, and these data were used to calculate density. From the bottle casts, samples were assayed for the variables measured in underway sampling and for oxygen (CoDISPOTI et al., 1976). Primary productivity, by

1304

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Fig. 1, Map of 1976 C U E A study region off Peru. Dotted line is the cruise track for underway sampling, 24 May 1976. Vertical casts were made along the line labeled the "C-line", Contours of temperature was sampled during the 24 May 1976 survey. Contour intcrval is 0.2°C.

JOINT II expedition, May and June Table 1. Continuous underway surveys of surface water characteristics, 1976: Allsurveys areat 15o S, 75.5 o W

Survey No.

Start date (1976)

Start time GMT

Stop date (1976)

Stop time GMT

Number of onshore-offshore transects

71 72 91 92 93 121 122 13l

24 May 24 May 02 June 03 June 04 June 19 June 20 June 24 June

(N)55 1801 0305 0437 0234 1820 0500 0427

24 May 25 May 02 June 03 June 04 June 19 June 20 June 24 June

1438 1003 1607 1625 0829 2335 1016 1(105

10 8 6 6 4 4 4 4

I'hysical and biological processes ~ll an upwelling front off I'e,u

] 305

uptake of HC-bicarbonate over 2-h incubations (STEEMAN-NIELSEN, 1952; HUNTSMAN, 1974), was measured at selected stations (CoDISPOTI et al., 1976). Because salinity was not measured in the horizontal underway surveys, density can not be calculated directly. From CTD casts, the correlation between temperature and density at 4-m depth for any single line of casts is never <0.997 (95% confidence limits on r, 0.990 < r < 0.999). The correlation for all lines of casts grouped together is 0.992 (0.985 < r < 0.995). Therefore, at the surface, temperature can serve reasonably as an indicator of density.

Data analysis The manifestation of the upwelling feature as a banded structure parallel to the coast, and the zig-zag pattern of cruise tracks allow a detailed analysis of the frontal pattern. Each transect is corrected for speed and direction relative to the frontal feature, as determined from spatial plots of the original underway data, and then resampled at 250-m intervals normal to the front. The set of realizations for a night make up an ensemble. Ensembles of realizations are averaged to obtain an ensemble mean trend. To ensure that sampled time series for different variables are synchronous, time series are aligned so that maximum cross-correlation occurs at zero lag. There is a risk of longshore trend contribution to the measured onshore-offshore trend owing to the direction of ship movement while sampling. Mean surface current during this cruise was estimated to be 15 cm s-~ (13 km day-a) to the north (J. VAN LEER, personal communication with B. JONES, 1978). Elapsed time for a single traverse of 20 to 25 km is 1.5 to 2 h. The component of ship motion parallel to the coast is southward, opposite to the currents. The effect of the current thus both increases the independence of transects (realizations) (due to greater effective separation) and increases the longshore component of motion to around 10% of the offshore component. To evaluate the magnitude of the potential bias from longshore contamination, onshore transects are separated from offshore transects for the first night of sampling. Longshore bias in the ensemble mean trends is thus visualized by comparing the onshore and offshore mean trends. A precise analysis is precluded by differences in heading, speed and spacing of sampled points for different onshore and offshore transects. By inspection (Fig. 2a), differences between ensemble mean onshore and ensemble mean offshore trends are negligible when compared to differences within each ensemble trend. There does not appcar to bc a serious contamination of mean onshore-offshore trend by longshore trend. RESULTS AND D I S C U S S I O N

Inspection of the ensemble mean signals indicates the existence of a relationship between physical and biological processes in the upwelling area (Fig. 2). Cold highnutrient water occupied the onshore limit, adjacent to a steep thermal gradient. A region of high fluorescence occurred in the neighborhood of the steep thermal gradient. Further offshore, the temperature gradient decreased and fluorescence increased gently. The generally accepted picture for physical processes in the upwelling region is supported by correlations between ensemble mean trends for different variables (Table 2). The strong negative correlations between temperature and phosphate, silicate, and nitrate are the expected result when cold nutrient-rich water is upweiled onshore and subsequently is mixed with warmer, nutrient-poorer water from offshore.

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A.T. DENGLER

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1307

Physical and biological processes at an upwelling front off Peru

Table 2. Correlations between selected variables measured in the continuous underway surveys. Correlations are from the mean onshore-offshore signal derived from all transects in each underway survey except for transects from survey 71 which were divided into those directed onshore and those directed offshore

Survey

Mean* fluorescence (FI)

Temp: FI

Temp: PO4

Temp: SIO4

Temp: NO3

Temp: NO:

Temp: NH4

FI: NO~

7It 7H: 72 91 92 93 121 122 131

11.6 11.3 12.1 3.3 3.8 3.9 7.7 8.3 12.3

-0.45 -0.72 -0.04 -(I.16 +0.51 +0.64 +0.41 +0.13 +0.95

--0.96 -0.98 -0.98 -0.55 -0.50 -0.99 -0.82 -0.99 -0.99

-0.97 -0.98 -0.99 -0.40 -0.85 -0.99 -0.41 -

-0.90 -0.88 4).96 -0.29 -0.68 -0.99 -0.45 -0.99 -0.99

-0.77 -0.49 -0.95 +0.71 ÷0.84 +0.51 -0.81 -0.98 -0.98

+0.72 +0.79 -0.52 +0.87 -0.90 -0.92 +0.64 +0.19 -0.28

-0.06-0.14 +0.38 -0.07 -(I.15 -0.04 +0.51-0.27 +0.33-0.84 -0.65 -0.04 -0.86 -0.97 -0.04 -0.29 - 0 . ) 4 -0.95

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NO2: NO~

-0.71 +0.94 -0.92 +0.83 -0.57 +0.98 --0.44-0.73 -0.52-(I.71 -4).54 -(I.51 -0.21 -0.04 -4).69 +0.96 -0.43 +0.98

* Arbitrary units. t Five transects commencing onshore and proceeding offshore. Five transects commencing offshore and proceeding onshore.

The differing relationships between fluorescence and different nitrogen species support the relative nitrogen source preferences observed in laboratory and field populations of phytoplankton. Ammonium consistently exhibits a strong negative correlation with fluorescence and variable correlation with temperature. Indeed, when temperature is negatively correlated with fluorescence, fluorescence is strongly negatively correlated with ammonium, and has no significant negative correlations with other nutrients. In laboratory studies, ammonium has been recognized as the preferred nitrogen source (LuDwIG, 1938; GRANTet al., 1967; EPPLEYet al., 1969; EPPLEYand ROGERS, 1970; MCCARTHYand EPPLEY, 1972; GOLDMANand PEAVEY, 1979). Field studies corroborate this preference (MAcISAAC a n d DUGDALE, 1969, 1972; GOERINGetal., 1970; MCCARTHY, 1972; MCCARTHY et al., 1977; EPPLEYetal., 1979; BLASCOand CONWAY,1982). Nitrate, which is more related to physical mixing and is more abundant than ammonium, shows stronger correlations with temperature and weaker correlations with fluorescence. When the mean fluorescence is low, the correlation between nitrate and nitrite is low; when mean fluorescence is high, the nitrate-nitrite correlation is high. Previous investigations have shown that when nitrate is present in abundance, nitrite can be produced and excreted by phytoplankton (VACCARO and RYTHER, 1960; CARLUCCIet al., 1970; KIEFERet al., 1976). Where levels of nitrate are high and phytoplankton are sufficiently abundant, nitrite excretion by phytoplankton will cause the nitrite distribution to assume a parallel structure to the nitrate distribution (Fig. 2a). Where phytoplankton are sparse, excretion will be insufficient to cause the nitrite to be coherent with the nitrate (Fig. 2b). Fluorescence-temperature relationship The simple hypothesis, that the observed fluorescence distribution is the result of physical mixing coupled with spatially uniform growth of phytoplankton, can be tested. If levels of phytoplankton abundance are due to this mixing and uniform growth, and if temperature is conservative, then a linear relationship between fluorescence and temperature would be exhibited (BOYLEet al., 1974). This is not the case. The fluorescencetemperature relationship departs from the linear and is concave downward at the fluorescence maximum near the density front (Fig. 3).

1308

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Fig. 3. Plots of fluorescence, nitrogen, and phosphorous vs temperature from the ensemble mean trends for the night of 25 May 1976. A line connects adjacent samples. Cold temperatures occur in the inshore samples, warm temperatures in the offshore samples. Shaded temperature, in the neighborhood of 17.0°C corresponds to the thermal front. The linear relationship that would exist if mixing were the causal mechanism is shown by the dashed line.

Three mechanisms could generate the observed temperature-fluorescence relationship. First is advection of water with elevated fluorescence into the proximity of the density front. Second is nonconservative loss of heat, therefore lowering of temperature at the fluorescence maximum. Third is in sit, addition or augmentation of fluorescence by growth, physiological adjustment or physical concentration of phytoplankton at the fluorescence maximum. Some combination of these mechanisms must be operating and the likelihood of each can be examined. Two observations argue against the existence of a special process that advects water with high phytoplankton levels to the proximity of the thermal front. The first is the reproducibility of the result. The increase in fluorescence appears in every available set of transects. The advection would therefore have to be extremely specific and finely tuned. The second is that water in which high levels of fluorescence are observed has physical characteristics (temperature and density) intermediate between the water on either side. Water with these physical characteristics is not observed elsewhere within the study region. It does not appear that advection is responsible for the peak observed in fluorescence.

Physical and biological processes at an upwclling front off Peru

1309

The second mechanism, loss of heat, appears a priori, unlikely. Heat will be added to the surface water both by insolation and conduction. The surface water temperature is lower than the air temperature, so heat exchange between sea surface and air will add heat to the surface water (ZUTAet al., 1978). Insolation will add heat at the sea surface. The amount of heat added will be proportional to time at the surface (BRINK et al., 1980). Evaporation and radiant heat losses should be proportional to the sea surface temperature and arc thus unlikely to generate the observed feature. Additional upwelling of colder water represents a conservative mixing process. Local loss of heat appears improbable as the cause of the observed fluorescence-temperature relationship. The third mechanism, an in situ increase in fluorescence, appears most probable, because the alternative mechanisms appear unlikely, and because there are no a priori

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1310

A, T. DENGLER

observational reasons to disqualify this mechanism. The processes which can result in an increase in fluorescence are therefore examined. In situ increase in fluorescence could be due either to an increase in the intensity of fluorescence of chlorophyll or to an increase in the amount of chlorophyll. KIEFER(1973) warned that fluorescence can be inversely related to the productivity of fluorescing cells. If low productivity were the cause of the increase in fluorescence, measured productivity would be lower near the front than away from the front. The actual observation is the reverse (Fig. 4). As observed in the vertical sections, peaks in fluorescence near the front coincide with peaks in total productivity. Consequently peaks in fluorescence indicate peaks in the chlorophyll distribution. Therefore the concavity in the fluorescencetemperature relationship is the result of a nonuniform increase in chlorophyll. Spatial structure The fluorescence feature can be specifically related to the physical frontal feature. The horizontal gradient of surface temperature perpendicular to the frontal feature is selected as a measure of local frontal intensity. A 4-point running average is applied to minimize the impact of noise in the analysis. When the mean trend of temperature gradient is compared to the mean trend of flourescence, a fluorescence maximum is displaced consistently to the warm water (offshore) side of the maximum temperature gradient. The displacement is on the order of 1 km (Table 3). The spatial displacement between maxima is evident in every case where maxima exist in both temperature gradient and fluorescence. The existence of a displacement leads to the question of how the displaced features are related. The fluorescence maximum appears to be a feature associated with the front. The question arises as to whether the magnitude of the fluorescence is more strongly related to surface conditions at the front or to surface conditions at its own location displaced from the front. The question may be tested with a correlation analysis of the anomalies in fluorescence and temperature gradient at the positions of the respective maxima. The analysis (Table 3) confirms the importance of the spatial displacement between the maxima of temperature gradient and fluorescence. Where a maximum in fluorescence exists, the correlation between the anomalies in temperature gradient and fluorescence at Table 3.

Survey 71 72A 72B 91 92 93 121 122 131

Comparisons between the location of the maximum temperature gradient and the location of the maximum fluorescence Displacement distance (km) 0.75 1.25 1.50 1.25 0.75 0.75 0.75 0.75

r~*

r2t

0.02 0.06 0.95 I).68 0.61 0.09 0.89 0.02 0.51 0.10 0.91 0.13 0.95 0.04 0.97 0.17 No fluorescence maximum

Probability (P)~: NS 0.9999 0.9950 0.9999 0.9100 0.9750 0.9950 0.9950

* r I = correlation between AT at AT maximum and fluorescence at fluorescence maximum. t r 2 = correlation between ATat fluorescence maximum and fluorescence at fluorescence maximum. 1: P = probability that r~ > r2, one-tailed test against normal distribution. NS = not significant.

Physical and biologicalprocessesat an upwellingfront off Pcru

1311

their respective maxima is significantly greater than the correlation between both at the position of the flourescence maximum. Restated, fluorescence is more strongly correlated with physical conditions (as indicated by horizontal temperature gradient) immediately at the front than with physical conditions at its own position. The sign of the correlation is positive; when the temperature gradient is steepest, the fluorescence is greatest. Examination of mechanisms As a mechanism to produce the observed fluorescence temperature relationship, I suggest higher productivity at the upwelling front due to the availability of ammonium as a nitrogen source. Maximum productivity (per unit chlorophyll) occurs in the neighborhood of the surface thermal front, on the onshore side of the chlorophyll maximum (Fig. 4). JONES(1978), examining data for this same cruise, observed that phytoplankton assimilation numbers (uptake of carbon per unit carbon) often were positively correlated with nitrate concentration of up to 20 lag-at. 1-l. These concentrations were well above the 1 lag-at. 1-1 found limiting in laboratory studies (EPPLEYand TttOMAS,1969; EPPLEYet al., 1969). The implication is either that nitrate concentration is positively correlated with a growth-inducing quality or negatively correlated with a growth-inhibiting quality. Ammonium concentration is high in the upwelled waters (Fig. 2b) and decreases across the surface front. Levels of ammonium are lowered to levels where preference of ammonium is weakened (MCCARTHYet al., 1977). Proportions of other nutrients (nitrate, phosphate and silicate) are lowered less, and remain well above limiting levels. BARBERet al. (1971) found that an initial lack of organic chelates could inhibit growth in nutrient-rich upwelled water. MACISAACet al. (1985) found a time lag in the physiological shift to increased nutrient uptake rates when the upwelled phytoplankton population initially experienced surface light levels. JONES' (1978) observations indicate that any initial inhibiting period was already past for the majority of data analysed in this paper. However, physiological delay or lack of chelators could be expected to limit growth in the restricted region onshore of the thermal front. Ammonium concentration, as the nutrient with the most significant variations, is suggested to be constraining the productivity per unit chlorophyll on the offshore side of the thermal front. Two additional mechanisms are possible, although I consider them less likely. The first is a relationship between the surface manifestation of fluorescence and the vertical distribution of fluorescence which is different at different distances from the upwelling front. There is not, however, a clear mechanism to induce the necessary differences. The second is turbulent diffusion that varies with distance from the upwelling front. Systematic differences in turbulent diffusion probably exist across the front, but to explain the observed feature, in the absence of inhomogeneous growth rates, the intensity of turbulent diffusion on the offshore side of the front would have to vary inversely with the steepness of the surface thermal gradient at the front. A different mechanism can account for the correlation between the temperature gradient and fluorescence maximum. Throughout the cruise, phytoplankton populations were dominated by the dinoflagellate Gymnodinium splendens (D. BLASCO, personal communication). Sampling was performed at night. CULLENand HORRIGAN(1981) have observed that G. splendens was found concentrated at the surface during the light period in nutrient-rich conditions and more dispersed throughout the mixed layer during the dark period. The mixed layer becomes shallower as the surface thermal front is approached from offshore (Fig. 4a). If the depth of thc mixed layer near the front varies with the

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A.T. DENGLER

sharpness of the gradient at the surface, then the phytoplankton will be dispersed into a water column of proportional thickness. The migratory behavior of G. splendens also may result in concentration of total nutrients, including those contained in phytoplankton. During the day, vertically migrating phytoplankton will not be removed from the mixed layer by mixing at the bottom of the layer. Vertical mixing at the top of the thermocline will provide conservative mixing of dissolved nutrients. Mixing of total nutrients will be nonconservative. Herbivores have the ability to bias this effect, as they can consume phytoplankton, excrete nutrients, and export nutrients, but herbivores were not examined in this study. Without considering the effects of herbivores, I conclude that mixing at the top of the thermocline will lead to local additions of total nutrients to the surface water. Variations in concentration of total nutrients at different locations in the surface layer can be examined by plotting total nutrients vs temperature (Fig. 3). If there is conservative horizontal mixing between water at two locations, then there will be a linear relationship between temperature and total nutrients (either total nitrogen or total phosphorous) at all intermediate points. If there is addition or removal of nutrients, then there will be curvature of the line connecting the boundary points and the intermediate points (DENGLER, 1973; BOYLEet al., 1974). Relative magnitude of addition at any point will be proportional to the curvature at that point (the second derivative with respect to temperature). Assumptions in this analysis include the appropriateness of the boundary points, the continuity of the intermediate region, and the conservative nature of the temperature. Nutrients in phytoplankton were not measured directly, therefore chlorophyll is converted to phytoplankton nitrogen or phosphorous, using conversion factors of (100 _+ 40) lag-Chl/~tg-at.-nitrogen and (23 _+ 6) lag-Chl/lag-at.-phosphorous (STRICKLAND, 1960). The region of highest fluorescence is often a region of downward concavity (positive second derivative with respect to temperature) indicating addition of nutrients. Two mechanisms are suggested which could produce the necessary differential vertical mixing at the thermocline. Both mechanisms are dependent upon the observation that, as the front is approached from offshore, water depth and the thermocline become shallower. The first is internal waves of sufficiently great amplitude in the thermocline which shoal when reaching shallow depths. Shoaling could result in vertical mixing from instability due to shear at the top of the thermocline (KAMYKOWSKI,1974, 1976). The second is wind-driven mixing having a greater effect in mixing at the top of the thermocline when the thermocline is shallower. Both of these mechanisms are testable, but not with the present data. CONCLUSION

A fluorescence maximum displaced to the offshore side of the surface thermal front occurs throughout the available surveys, over a wide range of temperatures and fluorescence levels. The fluorescence maximum results from enhanced phytoplankton growth. The recurrence of the fluorescence-temperature relationship is consistent with the hypothesis that the same mechanisms contribute to the relationship a range of upwelling conditions. Although the intensity of upwelling and the intensity of response may vary, the nature of the response appears constant. lnhomogeneous horizontal growth, maintained over a scale of 1 km, is the probable mechanism producing the observed features. Phytoplankton growth is inhibited in freshly

Physical and biological processes at an upwelling front off Peru

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upwelled water by lack of chelators, as described by BARI3ERet al. (1971). Once the upwelled phytoplankton population experiences surface light levels and shifts-up its nutrient uptake rates (MACISAACet al., 1985), availability of ammonium initially present at high concentrations (1 I.tg-at. 1-I) facilitates growth, lnhomogeneous rates of horizontal turbulent diffusion might augment the effects of differential growth. It should be noted that all of the proposed mechanisms for producing the observed fluorescence peak, whether mixing and diffusion, aggregation or growth, involve horizontally inhomogeneous rates over kilometer scales. Several refinements can be suggested for future investigations of biological processes at physical fronts. To examine the nature of the biological response, the neighborhood of the physical front should be sampled down to scales of tens of meters in horizontal underway surveys, and rate measurements should be made on growth, predation and vertical and horizontal mixing. To examine the dependence of the biological response upon the physical forcing functions, synoptic measurements of both physical and biological parameters should be made over numerous fronts at numerous times. Periodic twodimensional observations provided by satellites have promise for this application. Acknowledgements--I would like to thank D. Goodman, M. M. Mullin, G. N. Somero, M. C. Hendershott, and G. D. Lange for comments and discussions throughout this work. J. J. Simpson, S. G. Horrigan, D. Garbasz, and anonymous reviewers helped with critical readings of the manuscript. I would also like to thank the Coastal Upwelling Ecosystem Analysis program, and J. C. Kelley and R. T. Barber for making their data available. The physical and nutrient data collection was supported by NSF Grant OCE76-01309 to J. C. Kelley and the fluorescence and productivity data collection was supported by OCE75-23722 to R. T. Barber. Finally, my gratitude to J. Carleton-Walker and M. Krup for drafting the figures, and D. Osborn and J. Edgar for typing the manuscript.

REFERENCES ALLENJ. S. (1980) Coastal upwelling: relation between observations and theory. Abstract, I DOE International Symposium on Coastal Upwelling, 4-8 February 1980. ARMSTRONGF. A. J., C. R. STEARNSand J. D. H. STRICKLAND(1967) The measurement of upweUing and subsequent biological processes by means of the Technicon Autoanalyzer and associated equipment. DeepSea Research, 14, 381-389. ARTHURR. A. (1965) On the calculation of vertical motion in Eastern Boundary Currents from determination of horizontal motion. Journal of Geophysical Research, 70, 2799-2803. BARBERR. T., R. C. DUGDALE,J. J. MACISAACand R. L. SMITH(1971) Variations in phytoplankton growth associated with the source and conditioning of upwelled water, lnvestigacion Pesquera, 35, 171-193. BEERSJ. R., M. B. STEVENSON,R. W. EPPLEYand E. R. BROOKS(1971) Plankton populations and upwelling off the coast of Peru, June 1969. Fishery Bulletin, 69,859-876. BLASCOD. (1971 ) Composition and distribution of phytoplankton in the region of upwelling off the coast of Peru. investigacion Pesquera. 35, 61-112. BLASCOD. and H. L. CONWAY(1982) Effect of ammonium on the regulation of nitrate assimilation in natural phytoplankton populations. Journal of Experimental Marine Biology and Ecology, 61,157-168. BOYLEE., R. COLLIER,A. T. DENGLER,J. M. EDMOND,A. C. NG and R. F. STALLARD(1974) On the chemical mass-balance in estuaries. Geochimica et Cosmochirnica Acta, 38, 1719-1728. BRINK K. H., B. H. JONES, J. C. VAN LEER, C. N. K. MOOERS, D. W. STUART, M. R. STEVENSON,R. C. DUGDALEand G. W. HEBURN(1980) Physical and biological structure and variability in an upwelling centcr off Peru near 15°S during March, 1977. In: Coastal upwelling, F. A. RICltARDS, editor. American Geophysical Union, Washington, D.C., pp. 473-495. BURT W. V., D. B. ENFIELD, R. L. SMITtl and H. CREW(1973) The surface wind over an upwelling area near Pisco, Peru. Boundary-Layer Meteorology, 3, 385-391. CARLUCCIA. F., E. O. HARTWlGand P. M. BOWES(1970) Biological production of nitrite in seawater. Marine Biology, 7, 161-166.

1314

A . T . DENGLER

CODISPOTIL. A., D. D. BISHOPand M. A. FRIEBERTSHAUSER(1976) JOINT II R.V. Thomas G. Thompson Cruise 108, bottle data April-June 1976. C U E A Data Report 35,370 pp. CULLENJ. J. and S. G. HORRIGAN(1981) Effects of nitrate on the diurnal vertical migration, carbon to nitrogen ratio, and photosynthetic capacity of the dinoflagellate Gymnodinium splendens. Marine Biology, 62, 81-89. DENGLERA. T. (1973) Silicates and diatoms in New England estuaries. MSc Thesis, Massachusetts Institute of Technology, 89 pp. DUGDALER. C., J. J. GOERING, R. T. BARBER, R. C. SMITHand T. T. PACKARD(1977) Denitrification and hydrogen sulfide in the Peru upwelling region during 1976. Deep-Sea Research, 24,601-608. EPPLEYR. W. and W. H. THOMAS(1969) Comparison of hal f-saturation constants for growth and nitrate uptake of marine phytoplankton. Journal of Phycology, 5,375-379. EPPLEY R. W. and J. N. ROGERS (1970) Inorganic nitrogen assimilation of Ditylum brightwelli, a marinc plankton diatom. Journal of Phycology, 6,344-351. EPPLEY R. W., J. N. ROGERSand J. J. MCCARTHY(1969) Half-saturation constants for uptake of nitrate and ammonium by marine phytoplankton. Limnology and Oceanography, 14,912-920. EPPLEY R. W., E. H. RENGER, W. G. HARRISONand J. J. CULLEN(1979) Ammonium distribution in southern California coastal waters and its role in the growth of phytoplankton. Limnology and Oceanography, 24, 495-509. FRIEBERTSHAUSERM. A., D. D. BlsHoPand L. A. CODISPOTI(1977) Joint !I R.V. Thomas G. Thompson Cruise 108, Legs II and III, CTD Measurements off the Coast of Peru near Cabo Nazca, May-June 1976. CUEA Data Report 40, 246 pp, GOERING J. J., D. D. WALTERand R. M. NAUMAN(1970) Nitrogen uptake by phytoplankton in the discontinuity layer of the eastern subtropical Pacific Ocean. Limnology and Oceanography, 15,789-796. GOLDMAN J. C. and D. G. PEAVEY (1979) Steady-state growth and chemical composition of the marine chlorophyte Dunaliella tertiolecta in nitrogen-limited continuous cultures. Applied and Environmental

Microbiology, 38,894-901. GRANT B. R., J. MADGWICKand G. DAL PONT (1967) Growth of Cylindrotheca closterium var. California (Mereschk.). Reiman and Lewin on nitrate, ammonium, and urea. Australian Journal of Marine and Freshwater Research, 18, 129-136. GUILLEN O. and L. A. FLORES(1965) Exploracion de la region maritima Mancora, Callao, Arica, Crucero. Instituto del Mar del Peru, pp. 1-38. GUNTHER E. R. (1936a) A report on oceanographic investigations in the Peru Coastal Current. Discovery Reports, 13, 107-276. GUNTHER E. R. (1936b) Variations in the behavior of the Peru coastal current with a historical introduction. Journal of the Royal Geographic Society, 88, 37-61. HUNTSMANS. A. (1974) An evaluation of optimal conditions for determination of primary productivity. CUEA Newsletter, 13, 8-10. HURLBURTH. E. (1974) The influence of coastline geometry and bottom topography on the eastern ocean circulation. CUEA Technical Report 21,103 pp. HUYER A., W. E. GILBERT, R. SCHRAMand D. BARSTOW(1978) CTD observations off the coast of Peru, R.V. Melville 4 March-22 May 1977, R.V. Columbus Iselin 5 April-19 May 1977. CUEA Data Report 55, 409 pp. JONES B. H. (1978) A spatial analysis of the autotrophic response to abiotic forcing in three upwclling ecosystems: Oregon, northwest Africa and Peru. CUEA Technical Report 37,263 pp. JONES B. H., K. BRINKand D. BLASCO(1980a) Biological conscqucnccs of coastal trappcd waves in the Peru upwelling system at 15°S. IDOL International Symposium on Coastal Upwclling, 4-8 February 1980. JONESB. H., J. VAN LEER, C. N. K. MOOERSand G. HEBURN(1980b) Observations of non-plume condition in the Peru upwelling region at 15°S. IDOL International Symposium on Coastal Upwelling, 4-8 February 1980. KAMYKOWSKID. (1974) Possible interactions bctwecn phytoplankton and scmidiurnal intcrnal tide. Journal of Marine Research, 32, 67-89. KAMYKOWSKI D. (1976) Possible interactions bctwecn phmkton and scmidiurnal internal tidcs. II. Dccp thermocline and trophic effects. Journal of Marine Research, 34,494-509. KELLr~VJ. C. and A. CRUZADO(1973) Fluctuations and interrelationships among nutricnt concentrations and phytoplankton density in the Western Mediterranean, winter 1970. Thalassia Jugoslavica, 9, 25-31. KELLEY J. C. and T. E. WHITLEDGE(1975) An atlas of sea surface maps of temperature, nutrients, and chlorophyll from Peru, March and April 1969. CUEA Technical Report 9, 82 pp. KELLEY J. C., T. E. WttlTLEDGE and R. C. DUGDALE(1975) Results of sca surfacc mapping in thc Pcru upwelling system. Limnology and Oceanography, 20,784-794. KII-FERD. m. (1973) Chorophyll a fluorescence in marine centric diatoms: responses of chloroplasts to light and nutrient stress. Marine Biology, 23, 39-46.

Physical and biological processes at an upwelling front off Peru

1315

KIEFER D. A., R. J. OLSON and O. HOLM-HANSEN(1976) Another look at the nitrite and chlorophyll maxima in the central North Pacific. Deep-Sea Research, 23, 1199-1208. LORENZEN C. J. (1966) A method for the continuous measurements of in vivo chlorophyll concentration. DeepSea Research, 13,223-227. LUDWIG C. A. (1938) The availability of different forms of nitrogen to a green alga (Chlorella). American

Journal of Botany, 25,448-458. MACISAACJ. J. and R. C. DUGDALE(1969) The kinetics of nitrate and ammonia uptake by natural populations of marine phytoplankton. Deep-Sea Research, 16, 45-57. MACISAACJ. J, and R. C. DUGDALE(1972) Interaction of light and inorganic nitrogen in controlling nitrogen uptake in the sea. Deep-Sea Research, 19, 209-232. MACISAACJ. J., R. C. DUGDALE, R. T. BARBER, D. BLASCO and T. T. PA(?KARD(1985) Primary production cycle in an upwelling center. Deep-Sea Research, 32, 503-529. MCCARTHY J. J. (1972) The uptake of urea by natural populations of marine phytoplankton. Limnology and Oceanography, 17,738-748. MCCARTItY J. J. and R. W. EPPLEY (1972) A comparison of chemical, isotopic, and enzymatic methods for measuring nitrogen assimilation of marine phytoplankton. Limnology and Oceanography, 17, 371-382. MCCARTtlY J. J., W. R. TAYLORand J. L. TAFq'(1977) Nitrogenous nutrition of the plankton in the Chesapeake Bay. 1. Nutrient availability and phytoplankton preferences. Limnology and Oceanography, 22,996-101 I. MOOERS C. N. K. and J. S. ALLEN (1973) Final report of the CUEA summer 1973 Thcoretical Workshop. CUEA Tcchnical Rcport 12, 52 pp. ()'BRII-N J. J., R. M. N. CI,ANCY, A. T. CI,ARKI-, M. CRH'ON, R. EI.SIH:,RRY,T. GAMMliI,RUI), M. MA('VEAN, L. P. ROV:Dand J. D. TIIOMI'SON(1977) Upwelling in the occan: two and three dimensional modcls of uppcr ocean dynamics and variability. In: Modelling and prediction of the upper layers of the ocean, E. B. KRAUS, editor, Pergamon Press, Oxford, pp. 178-228. PARSONS T. R., R . J . LEBRASSUER and J. D. FULTON (1967) Some observations on the dependencc of zooplankton grazing on the cell sizc and conccntration of phytoplankton blooms. Journal of the Oceanographical Society of Japan, 23, 10-17. RYrlII-R J. H., D. W. MENZEI,, E. M. ttURt,I~URr, C. J. LORENZI-Nand N. CORWlN (1971)The production and utilization of organic matter in the Peru coastal current. Investigacion Pesquera, 35, 43--59. STEI-MAN-NIELSEN E. (1952) The use of radioactive carbon (C j'*) for measuring organic production in the sea. Journal du Conseil. Conseil International pour I'Exploration de la Met, 18, 117-140. STRICKLANDJ. D. H. (1960) Measuring the production of marine phytoplankton. Fisheries Research Board of Canada Bulletin, 122, 1-172. STUARTn . W. (1981) Sea-surface temperatures and winds during JOINT It: Part II. Temporal fluctuations, in: Coastal upwelling, F. A. RICItARDS, editor, American Geophysical Union, Washington, D.C. pp. 32-38. STUART D. W.. M. A. SPETSERISand M. M. NANNY (1976) Meteorological data JOINT It: March, April, May 1976, CUEA Data Report 34. VACCAROR. F. and J. H. RYTHER(1960) Marine phytoplankton and the distribution of nitrite in the sea. Journal du Conseil, Conseil International pour I'Exploration de la Met, 25, 2616271. WAI,SII J. J., J. C. KELLEY, R. C. DUGI)ALEand t3. W. FROST(1971) Gross features of the Peruvian upwclling system with special reference to possible dicl variation, lnvestigacion Pesquera, 35, 25-42. WHITLEDGE T. E., J. C. KELLEY and M. A. FRIEBERTSIIAUSER(198(1) Hydrography and underway mapping. R.V. Melville Leg 3, April 1977. CUEA Data Report 64, 220 pp. ZUTA S. and O. GUILLL:.N(1970) Oceanography of the coastal waters o f Pcru. Boletin lnstituto del Mar del Peru, 2, 157-324. ZUTA S., T. RIVERA and A. BUSTAMANTE(1978) Hydrologic aspects of the main upwelling areas off Peru. In: Upwelling ecosystems, R. BOJE and M. TOMCZAK, editors, Springcr-Verlag, New York, pp. 235-257.