lli

stec fos toon,we

minants of EBUE characteristics. First, trade winds accumulate heat and mass in the western side of the

coastas ofSverdorthw

nition of special food web attributes and sh production in theseecosystems (Ryther, 1969). Originating in the United States butinternational in its scope and execution during the 1970s, theCoastal Upwelling Ecosystem Analysis (CUEA) program visitedthree of the four upwelling regions mentioned above: California,Northwest Africa and Peru. A comparative synthesis of the CUEA

brief, sometimes provocative synthesis and update with an empha-sis on disagreements and uncertainties. There is a bias towards thePacic resulting from the authors past research history.

2. Major Eastern Boundary Upwelling Ecosystems (EBUEs)

The analytical aspects of this contribution focus on the 10 bandof most active upwelling in the Benguela, California, Iberia/Canaryand Humboldt ecosystems. The full EBUEs extend over much lar-ger areas and each is composed of a series of fairly well dened re-

* Corresponding author. Address: MBARI, 7700 Sandholdt Road, Moss Landing, CA95039, USA. Tel.: +1 831 775 1709.

Progress in Oceanography 83 (2009) 8096

Contents lists availab

Progress in Oc

elsevier .com/locate /poceanE-mail address: chfr@mbari.org (F.P. Chavez).ered by upwelling from moderate depths due to the action of pre-vailing northwesterly winds, but this upwelling does not exerciseinuence as widespread as does corresponding upwelling off thecoasts of southwest Africa or, particularly, as does that off the westcoasts of North and South America. The authors point out thatinformation on Northwest Africa was decient in 1942 a de-ciency that persists today (see Arstegui et al., in this issue). Easternboundary coastal upwelling research accelerated following recog-

clude ocean chemistry and biology (Conkright et al., 2002); and(3) novel observing systems and synthetic models are continuouslybeing developed and rened. Here we use the rst two develop-ments to compare four Eastern Boundary Upwelling Ecosystems(EBUEs; Fig. 1). Several extensive reviews of eastern boundariesin general can be found in the literature, the most recent an excel-lent effort by Mackas et al. (2006). This contribution is not in-tended to repeat these extensive reviews but instead provide a1. Introduction

The history of eastern boundarylong and varied. Early comparisonupwelling systems can be found intemperature close to the coast (of N0079-6611/$ - see front matter 2009 Elsevier Ltd. Adoi:10.1016/j.pocean.2009.07.032basins, deepening the thermocline in the west and raising it in the east. Second, and especially prominentin the Pacic, these properties are redistributed eastwards on interannual and multidecadal time scales,reducing the characteristically high biological productivity found in the eastern basin margins. Thirdly,northsouth patterns of thermocline doming on the equator and deepening in the subtropical gyres,and high latitude weather-driven mixing makes latitude an important characteristic of each EBUE. Assuch each EBUE has 34 well-dened latitudinally distributed biomes. Many enigmas remain regardingEBUEs including: (1) Why do EBUEs differ dramatically in sh but not in primary production? (2) Whatnutrients or other physical properties limit EBUE primary production? (3) What roles do subsurface oxy-gen minimum zones play in EBUE ecosystems? (4) What role do euphausiids play in the transfer ofenergy through EBUE food webs? (5) What are the roles of EBUE food webs in the biogeochemical cyclingof elements? (6) How inter-connected are biomes of EBUE ecosystems? and (7) Most importantly forsociety, how will EBUEs respond to climate and global change.

2009 Elsevier Ltd. All rights reserved.

l upwelling research isthe four main coastalrup et al. (1942): Theest Africa) is also low-

program was published in 1981 (Barber and Smith, 1981a). Sincethat time several important advances in the ocean sciences haveoccurred: (1) satellite remote sensing has provided an unprece-dented spatial (and evolving temporal) view of the surface ocean(SST, chlorophyll, wind, sea level, etc.); (2) global data bases, rststarted for temperature and salinity, have been expanded to in-A comparison of Eastern Boundary Upwe

Francisco P. Chavez *, Monique MessiMonterey Bay Aquarium Research Institute, Moss Landing, CA 95039, USA

a r t i c l e i n f o

Article history:Received 7 January 2009Received in revised form 10 June 2009Accepted 16 July 2009Available online 29 July 2009

a b s t r a c t

Coastal upwelling along eapling between atmospheriencouraged oceanographermon. Following that traditimajor Eastern Boundary Up

journal homepage: www.ll rights reserved.ng Ecosystems

rn boundaries has fascinated oceanographers for decades. The strong cou-rcing, ocean circulation, biogeochemical cycling, and food web dynamicsconduct multidisciplinary scientic studies that have since become com-an interdisciplinary approach is taken to highlight differences between thelling Ecosystems (EBUEs). Ocean basin-scale settings are important deter-le at ScienceDirect

eanography

in OF.P. Chavez, M. Messi / Progressgions or biomes typically separated by sharp biological andphysical transitions (e.g. Lderitz in Benguela, Point Conceptionin California). How organisms, in particular sh and top predatorscapable of moving by their own means between regions, exploit ordepend on the different biomes remains uncertain. After a focusedanalysis of the 10 bands we return briey to discuss the full EBUE

Fig. 1. Basin-scale maps of mean sea surface temperature (SST) and winds (a). Chloroph2008 (d) showing the location of the Eastern Boundary Upwelling Ecosystems (EBUE) d1981 to February 2007; winds are QuikSCAT monthly averaged from July 1999 to April 2analysis uses the same methodology as produces the Pacic Decadal Oscillation (PDO; Mpixel, but in this case for the Atlantic and Pacic basins (and globally in Chavez et al., 2ceanography 83 (2009) 8096 81towards the end of the paper. Below we introduce EBUEs in gen-eral and then provide a brief description of each of the foursystems.

EBUEs General description. The EBUE considered are associ-ated with the subtropical gyres of the Atlantic and the Pacic.The southern anks of these gyres are driven by the trade winds

yll (b), rst empirical orthogonal function of SST (c), and trend in SST from 1981 toiscussed in this paper. SST is Reynolds et al., 2007 monthly averaged from October008; chlorophyll is SeaWiFS monthly climatology averaged over the year. The EOFantua et al., 1997), rst removing the global trend and then seasonal cycle at each008) rather than just the North Pacic.

ODeragpri

hinh ex

82 F.P. Chavez, M. Messi / Progress in Oceanography 83 (2009) 8096(Fig. 1). Equatorward winds along the eastern anks (Figs. 1 and 2)feed the trades and drive the broad and slow eastern boundaryBenguela, California, Iberia/Canary and Humboldt currents. Nearshore (order 25150 km), interaction with earths rotation (Coriolis)and presence of the coastal boundary, produces a shallow (order50 m) wind-driven offshore surface Ekman ow which is replacedby cool and nutrient-rich waters from below; such coastal upwell-

Fig. 2. Higher resolution maps of SST, winds and chlorophyll for each EBUE. SST is Maveraged from September 1997 to September 2007; winds are QuikSCAT weekly av(0.25 0.25) prior to averaging. The insert in the chlorophyll map shows the meanthe reported sh catches (Fish and Agriculture Organization, FAO) were made witsensing of chlorophyll and the Behrenfeld and Falkowski (1997) model. Peru sh catcsimilar.ing leaves a strong imprint on sea surface temperature and chloro-phyll (Figs. 1 and 2). Over the shelf and slope an undercurrentows poleward so that average currents within 100 km from thecoast are opposite the surface winds; further offshore the Bengu-ela, California, Iberia/Canary and Humboldt currents ow. Thephysical process of coastal upwelling with its equations has been

Table 1Comparison of annual mean properties in a 10 latitude coastal (0150 km) band for the fouNOAA). Calculations for upwelling, mean nitrate concentration at 60 m and the potentialwere calculated by dividing Ekman transport by the Rossby radius of deformation (obtaturbulence is given as the cube of the wind speed. Chlorophyll concentration, 1 mg m3

0.25 0.25, geometric mean); primary production was calculated following Behrenfeldproles following the Naval Research Laboratory Mixed Layer Depth (NMLD) methodolocalculated from the model of Mahowald and Luo (2003).

Benguela28S18S

Coriolis parameter f (s1) 5.7e05Area (1011 m2) 1.67Average wind speed (m s1) 7.2Upwelled volume (Sv) 1.5Average vertical speed by ektrans (105 m s1) 3.18Average vertical speed by ekpump (105 m s1) 0.32Percentage ektrans/total 77.0Average [NO3] at 60 m (lmol Ll) 16.9Potential new production (g C m2 yr1) 517SeaWiFS primary production (g C m2 yr1) 976SeaWiFS chlorophyll (mg m3) 3.11 mg m3 Chl extension (km) 160Turbulence (m3 s3) 444MLD (m) 44.8PAR (E m2 d1) 43.1Dust deposition (g m2 yr1) 11.7described repeatedly (see Allen, 1973; Barber and Smith, 1981a;Smith, 1995; Bakun, 1996; Hill et al., 1998). In addition to thestrength of the upwelling-favorable equatorward winds, water col-umn stratication, coastal topography, and latitude-dependence ofthe Coriolis parameter play an important role; at low latitude,favorable winds produce more upwelling than at high latitude(Table 1). The shallow offshore ow, often termed Ekman

IS monthly averaged from July 2002 to April 2008; chlorophyll is SeaWiFS monthlyed from July 1999 to July 2008. All products were regridded on the QuikSCAT gridmary productivity (PP) and sh catch for the years 19982005. It was assumed that100 km from the coast. Primary productivity was estimated from satellite remoteceeds that from the other areas by an order of magnitude even though PP levels aretransport, is balanced by onshore subsurface ow beneath theEkman layer. Planktonic organisms, including larval sh andinvertebrates, can exploit this conveyor belt and be retained inthe coastal productive habitat (Peterson et al., 1979; Barber andSmith, 1981b; Peterson, 1998; Carr et al., 2008). The upwelling-favorable winds typically increase offshore to maximum mean

r EBUE. Winds are from QuikSCAT (0.25 0.25, 8-day, 19992008, provided by PFEL,new production are described in Messi et al. (in this issue). Vertical upwelling ratesined from Chelton et al., 1998) and for pumping by dividing by the 150 km band;chl distance from shore, and PAR are calculated from SeaWiFS (9-km degraded onand Falkowski (1997). Mixed layer depth were calculated from in situ temperaturegy (depth where temperature = temperature at 10 m 0.8 C). Dust deposition was

California NW Africa Peru34N44N 12N22N 16S6S

9.18e05 4.26e05 2.78e05

7.8 6.8 5.71.0 1.4 1.63.30 2.35 1.550.18 0.36 0.5277.5 74.9 68.614.9 19.0 16.8323 539 566479 1213 8551.5 4.3 2.449 164 120610 371 22543.3 28.9 30.734.0 47.6 43.30.3 33.1 0.3

more irregularly than in the Pacic (Gammelsrd et al., 1998;Philander, 1986). The processes responsible for thermocline uctu-

in Ovelocities 50200 km offshore before reaching a plateau or weak-ening further offshore. A spatially varying wind velocity is termedwind stress curl and in the case of an increasing wind offshoredrives an upwelling process referred to here as Ekman pumping(see Messi et al., in this issue). This process has been known fordecades (Sverdrup et al., 1942) but its role in eastern boundarythermocline deepening/shoaling (Halpern, 2002), undercurrentdynamics (Capet et al., 2004) and EBUE ecosystem dynamics(Rykaczewski and Checkley, 2008) has only recently been recog-nized and debated. Both coastal upwelling and offshore Ekmanpumping produce surface water with high nutrient levels, whichlead to the characteristically enhanced biological production ofEBUEs (Fig. 2; Pennington et al., 2006).

Coastal topography strongly modies the coastal upwellingprocesses; coastline irregularities such as capes and bays producevariations in coastal wind, alongshore currents, chemistry andbiology. Strong upwelling and horizontal advection occur atwind-exposed capes while in their lee, often in bays behind head-lands, winds, upwelling and horizontal advection are weaker. As aresult of the slower physical dynamics and increased stratication,biological processes proceed without being advected or mixed off-shore and dense phytoplankton blooms often develop in theseupwelling shadows. Strong gradients or fronts form betweenthe freshly upwelled waters off a cape and the protected shadowwaters behind the cape. These convergent fronts are typically sitesof intense biological activity, attracting a diverse community ofpredators. If the upwelling shadow is large enough, as is the casein the Southern California Bight or off southern Peru and northernChile, surface shadow waters become nutrient-exhausted andprimary productivity drops. The water column stratication thatdevelops in the upwelling shadows often fosters red tides (Ryanet al., 2008).

California The California Current System (CCS) is often parti-tioned into several regions: (a) The Pacic Northwest with strongwinter storms, associated freshwater runoff, and seasonalupwelling restricted mostly to summer; (b) Central California withspring and summer upwelling and typically dry conditions; (c) TheSouthern California Bight, a large and relatively stable upwellingshadow; and (d) Baja California with year-round but weakerupwelling (Mackas, 2006). The strongest upwelling occurs in alatitudinal band from 34 to 44N. The readers are directed to thecontribution by Checkley and Barth (in this issue) for a currentreview of the CCS.

Benguela The Benguela Current System (BCS) ranges from thetip of Africa (35S) to about 14S off Angola (Field and Shillington,2006). The region from 15 to 30S has year-round upwellingwhile further south upwelling has a seasonal summer maximumtypical of the higher latitude coastal upwelling systems. The majordifference between the BCS and the other EBUEs is the stronginuence of the circulation at the tip of the continent: the AgulhasCurrent and retroection. No other EBUE has its terminusconnected to a west wind drift or is inuenced by another basinswestern boundary (through the Agulhas Current). The Benguelaregion of permanent upwelling from 18 to 28S is analyzed here.Readers are directed to Hutchings et al. (in this issue) for the mostcurrent review of the BCS.

Iberia/Northwest Africa The Iberia/Canary Current System(ICCS) is perhaps the least studied or understood EBUE due tothe paucity of information from coastal Northwest Africa and alsoto the regions complex topography and circulation (Arstegui et al.,2006). Upwelling along the Iberian Peninsula (3644N) and offMorocco (2536N) is seasonal and relatively weak, with latesummer and summer maxima, respectively. Further south, the re-

F.P. Chavez, M. Messi / Progressgion between 20N and 25N is characterized by weak seasonal-ity and between 10 and 20N upwelling becomes semi-continuouswith a spring maximum (Lathuilire et al., 2008). The entrance toations at multi-decadal scales are thought to be associated withchanges in the speeds of the subtropical gyres and the overturningmeridional circulation but are less well understood (Chavez et al.,2003). At centennial scales it has been postulated that theInterTropical Convergence Zone (ITCZ) is pushed southward acrossthe equatoward as a result of a growing northern polar icecap(Gutirrez et al., 2008). This essentially shuts down the Walkercirculation once again deepening the eastern margin thermocline.Local wind-driven variability further modulates thermocline andmixed layer depth at any given location, and is of greater relativeimportance at higher latitudes. A full description of the eastwestdynamics, the modulation of thermocline depth and their biologi-cal consequences can be found in Chavez (2005).

Northsouth large-scale thermocline pattern also plays a role inthe productivity of EBUEs. The thermocline/nutricline shoals on theequator, deepens in the subtropical gyres and then shoals again atthe poleward margins of the subtropical gyres in the west winddrifts (Fig. 3). Equatorial nutricline shoaling contributes to in-creased nutrient supply, where the ICCS and the HCS impinge onthe equator (Fig. 3). At lower, mid-latitudes the equatorward-ow-the Mediterranean inuences the connectivity between the IberianPeninsula and Northwest Africa. The region from 12 to 22N offNorthwest Africa is analyzed here. Readers are directed to Arste-gui et al. (in this issue) for the most current review of the ICCS.

Humboldt or PeruChile The Humboldt Current System (HCS)is notable for its amazing anchoveta production (Chavez et al.,2008; Montecino et al., 2006). The HCS extends from SouthernChile (45S), where the west wind drift intersects the SouthAmerican continent to northern Peru (4S), where cool-upwelledwaters collide with warm tropical waters forming the EquatorialFront (EF). The HCS includes three dened biomes: (1) a highly pro-ductive seasonal (summer) upwelling system off southern Chile(3040S); (2) a large, moderate to low productivity upwellingshadow off northern Chile and southern Peru (1826S); and(3) the highly productive year-round Peru upwelling system(416S). The greatest upwelling occurs off central/northern Peruand this paper analyzes a band from 6 to 16S. Readers are directedto a recent volume in the same journal (Bertrand et al., 2008a) andthe contribution by Montecino and Lange (in this issue) for currentreviews of the HCS.

3. Large-scale patterns of spatial and temporal variability

The large-scale patterns of thermocline topography clearlydetermine the character of EBUEs. The rst and more commonlystudied is that associated with eastwest dynamics (Barber andChavez, 1983, 1986). The basin-scale west (deep) to east (shallow)thermocline slope is one of the key elements in the characteristi-cally high productivity of EBUEs; high concentrations of nutrientsare found very close to the sea surface in the eastern margins.Interannual to multidecadal phenomena (El Nio, El Viejo) modu-late the depth of the eastern Pacic thermocline (and nutricline)resulting in dramatic uctuations in ecosystem productivity(Barber and Chavez, 1983, 1986). During El Nio westerly windbursts in the western Pacic remotely force Kelvin waves thatpropagate eastward along the equator at about 200 km/day anddepress the thermoline (Cane, 1983). When they collide with SouthAmerica they propagate poleward along the continental shelvesand slope as coastally-trapped waves (Eneld and Allen, 1983).An Atlantic El Nio has been recognized although it occurs much

ceanography 83 (2009) 8096 83ing subtropical gyres impinge on the EBUEs, close to the SouthernCalifornia Bight in the CCS, in southern Peru and northern Chile inthe HCS, around Morocco for the ICCS and Namibia for the BCS

POithifor

in OFig. 3. Northsouth section of nitrate, oxygen, and nitrate decit calculated as 16 the eastern boundary. Location of the 10-latitudinal bands chosen for comparison wet al., 2006a,b). The sections were extracted by rst calculating the distance to shoreeach latitude.

84 F.P. Chavez, M. Messi / Progress(Fig. 1). At the higher latitudes, which are at the northern or south-ern limits of the EBUEs (in particular the BCS, CCS, and the HCS), theenhanced mixing of subtropical frontal zones and the west winddrifts mergewith the coastal upwelling of EBUEs further enhancingbiological productivity. North/south dynamics also affect oxygenand nitrate loss by denitrication (Fig. 3). Here we use the termdenitrication to include microbial processes including the re-cently discovered anammox that remove xed nitrogen. The east-ern basin tropical regions experience little storm-inducedmixing ofhigher surface oxygen, are slowly ventilated, have characteristicallyhigh surface primary productivity and therefore have less oxygen insubsurface waters than western boundaries or high latitudes(Fig. 3). Tropical regions are also warmer but it is not clear howimportant temperature-driven enhanced metabolic activity is inthe consumption of oxygen. Sub-euphotic zonewaters of the Pacicare clearly older (less ventilated) than those in the Atlantic, andare characterized by intense oxygen minimum zones (OMZs;Stramma et al., 2008; Paulmier and Ruiz-Pino, in press). The OMZsand their associated denitrication processes are not static and varyon many time scales, a topic discussed below.

The global trend in sea surface temperature (SST) over the last130 years has a rather marked and worrisome ocean warmingsince the early 1980s (see Fig. 3A of Chavez et al., 2008). The warm-ing has not been steady in time or space (Fig. 1d). The spatial pat-tern of the rst EOF of SST is shown in Fig. 1c. The characteristicspatial distribution of the Pacic Ocean temperature anomaliesassociated with both El Nio and El Viejo (the positive phase ofthe PDO lasting between 25 and 40 years) have been well de-scribed (Mantua et al., 1997; Chavez et al., 2003), are apparent inthe spatial distribution of the SST EOF (Fig. 1c) and the trend inSST over the last 30 years (Fig. 1d). When the eastern and the cen-tral equatorial Pacic are anomalously warm the western Pacicand the central subtropical fronts are anomalously cool. The pres-ent-day condition shows the inverse, with anomalously cool SST4 NO3 in the Pacic and Atlantic Oceans following the coast 1000 km offshore ofn each EBUE are shown in black. Data are from the World Ocean Atlas 2005 (Garciaeach grid point, and then extracting the data from the pixel closest to 1000 km for

ceanography 83 (2009) 8096and lower sea level (shallow thermocline) in the eastern PacicEBUEs. Conditions in the Atlantic are almost the inverse of thosein the Pacic (Fig. 1c) but are much weaker. During El Viejo theequatorial and high latitude Atlantic are cool but the tropical wes-tern Atlantic is warm. The range of variability in the Pacic is muchhigher than in the Atlantic, and the HCS is by far the most variableEBUE on interannual and longer scales.

The 20th century multi-decadal uctuations associated with ElViejo and La Vieja are associated with large regime shifts in EBUEecosystems (Schwartzlose et al., 1999; Chavez et al., 2003). WhenEBUEs are warmer, sardines increase in abundance while duringcooler periods anchovies are favored. Analysis of the sedimentaryrecord beneath low oxygen EBUEs (Galbraith et al., 2004; McGre-gor et al., 2007; Gutirrez et al., 2009) have been used to constructtime series extending back hundreds and in some cases thousandsof years. These records document biogeochemical and ecologicalregime shifts of much greater magnitude than observed duringthe 20th century. These shifts are associated with glacial maxima(Galbraith et al., 2004) and the Little Ice Age (McGregor et al.,2007; Gutirrez et al., 2009). In all cases oxygen minimum zonesretreated and denitrication was reduced during glacial periods.During the LIA productivity of the HCS decreased at all levels ofthe ecosystem from primary producers to sh (Gutirrez et al.,2009). The less productive LIA showed very low abundances ofanchovies and sardines in the northern HCS off Peru; both speciesappear in much higher abundances after the end of LIA around1820. The cores show that both anchovies and sardines are favoredand present during a cool and productive EBUE and absent whenthe EBUE collapses for centuries. During the present-day cool andproductive condition there is a second order selection when underslightly warmer/cooler multi-decadal regimes (but still relativelycool and productive) one species appears favored over the other;this multi-decadal variability is also present in the core records.Scientists have confused the issue by referring to sardines as warm

and anchovies as cool species; they are both cool and productiveEBUE species that thrive under slightly different environmentalconditions. It should not be at all surprising that the cores showoverlapping presences of both species.

A rather interesting conundrum arises from the fact that warminterglacials are associated with more productive EBUEs because itis in sharp contrast to modern instrumental records, wherein aglobally warmer ocean (El Nio and El Viejo) is associated withsharply lowered ecosystem productivity in Pacic EBUEs. One thenis left to wonder whether global warming will decrease EBUE pro-ductivity like present day variations, or increase productivity asduring interglacial periods. This is a hotly debated topic. It has beensuggested that a warmer world would lead to a stronger landseatemperature gradient, stronger upwelling-favorable winds and in-creased EBUE productivity (Bakun, 1990). Recent in situ windobservations do not uniformly support this hypothesis and the de-bate will surely continue.

4. Physical comparisons sea level, winds, upwelling, curl,vertical structure

A 14-year time series of satellite altimetry was analyzed foreach of the four EBUEs, and the percentage of the variance ex-plained by interannual (>1 year), seasonal, and intraseasonal(1estimeeach

F.P. Chavez, M. Messi / Progress in Oceanography 83 (2009) 8096 85Fig. 4. Spatial distribution of the percentage of variance in sea level for interannualscales for each EBUE. Peru is dominated by variance at the interannual scale, Northwsimilar levels of the three time scales. A Fourier analysis was performed on weekly tER2 product, CLS, Toulouse, France). The method consists of a Fourier Transform for

interannual), an inverse Fourier transform is performed by keeping the Fourier coefcientThe ratio of the variance of the resulting time series to the variance of the full time seriesscale. The inuence of the Agulhas Current and retroection is notable off Benguela.year, 1st row), seasonal (1 year, 2nd row) and intraseasonal (

with the west wind drift is clearly outlined in the total varianceof the BCS. The total variance does not precisely match the per-centage explained by intraseasonal variance (Fig. 4) suggestingthat part but not all of the eddy activity is a result of thisinteraction.

Peru has the weakest average winds and California the stron-gest (although the differences between California, NorthwestAfrica and Benguela are small; Table 1). These differences areamplied when converted to wind stress (proportional to thesquare of the speed) or turbulence (proportional to the cube ofthe wind speed) (Bakun and Parrish, 1982). The satellite-derivedwinds can also be used to partition total upwelling into that drivenby Ekman transport and pumping (see Messi et al., in this issue).On average, Ekman pumping contributes about 25% or more to thetotal volume of EBUE water upwelled, higher off Peru; this is a low-er bound estimate given the inability of the satellite to samplewithin 2030 km of the coast. Given that total upwelling is an in-verse function of the latitudinally-dependent Coriolis parameterthe average volume upwelled is greatest off Peru even thoughupwelling-favorable winds are weaker. Slightly less upwellingoccurs in Benguela and off Northwest Africa and the lowest isfound off California. The range of EBUE annual average upwellingis 1.2 (California) to 2.2 (Peru) Sverdrups per 10 latitude band(1111 km). For comparison Brink et al. (1995) and Chavez andToggweiler (1995) considered only Ekman transport and estimated1 Sverdrup per 1000 km as the global average for coastal upwellingsystems.

Hydrographic data from each EBUE were compiled (see Messiet al., in this issue) and annual mean proles for the inner 150 kmconstructed (Fig. 5). The distribution of data was not uniform withhigher data densities in some areas (California, Peru) than others(Northwest Africa), but the results are nevertheless useful indescribing the general hydrographic properties of each EBUE. Pro-les for Japan, another productive but non-EBUE system, are alsoincluded. There are striking similarities in the temperature prolesof all of the EBUE, and SST is directly linked to subsurface temper-ature. SST off Northwest Africa is the warmest, followed by Peru,Benguela, California and Japan. Salinity is much more variable.The fresh North Pacic is clearly visible in the proles off Californiaand Japan. Peru and Benguela are intermediate and Northwest Afri-ca is the saltiest. In these annual means, Northwest Africa and Ja-pan are more stratied (sigma-t), followed by California and thenPeru and Benguela.

5. Chemical comparisons nutrients, oxygen, and carbondioxide

The spatial distribution of the concentration of nitrate at 60 mshows the inuence of the large scale nutricline patterns withhigher concentrations, particularly in offshore waters, closer tothe equator (Fig. 6). The concentration of nitrate at 60 m is impor-tant since this is the depth from which upwelled waters commonlyoriginate (Messi et al., in this issue). Nitrate supply (and potentialnew production) can be estimated by combining the transport and

chlo

86 F.P. Chavez, M. Messi / Progress in Oceanography 83 (2009) 8096Fig. 5. Mean vertical proles of temperature, salinity, sigma-t, oxygen, nitrate and

Japan. Available proles were interpolated to standard depths by a cubic interpolation (Mgrid (0.25 0.25 resolution monthly); data greater than 2 standard deviations from tmedian was kept for each 4D-coordinate. Standard errors are plotted around the prolerophyll for each EBUE (within the 10 latitude bands chosen for comparison) plus

essi et al., in this issue). The proles were then binned to a regular spatio-temporalhe mean for each time series (given lon, lat, depth) were taken out. The resultings (dotted lines), but are only visible for chlorophyll and nitrate proles.

in OF.P. Chavez, M. Messi / Progressnitrate concentration (Table 1). The results suggest that Benguela,Northwest Africa and Peru have rather similar levels of nitrate sup-ply and that they are all close to twice that of California (see Messiet al., in this issue).

The large-scale distribution of oxygen shows that tropical east-ern basins lie over regions of low and shallow (due to the thermo-cline doming around the equator) subsurface oxygen (Fig. 3), whilethe western basins are well ventilated (Stramma et al., 2008;Paulmier and Ruiz-Pino, in press). While high rates of EBUEproductivity, followed by sinking and decay, are contributors toOMZs, the large-scale oxygen pattern results primarily from thequiescent nature of EBUE subsurface ow. The EBUEs are venti-lated by distant deep water formation at high latitude, and oxygenlevels progressively decrease towards the equator, with the excep-tion of the Equatorial Undercurrent, an important ventilator on theequator proper (Toggweiler and Carson, 1995). The EquatorialUndercurrents feed the characteristic poleward undercurrents ofthe EBUEs. These undercurrents are originally oxygenated (offnorthern Peru for example) but as they ow away from the equatorcan reach very low levels and eventually advect very low oxygenwaters into the more oxygenated higher latitude seasonal upwell-ing regions of EBUEs (see Castro et al., 2001 for an example offCalifornia). Fig. 5d shows the vertical distribution of oxygen fromeach EBUE. Waters off Peru are the oldest and least ventilated,and have extremely low oxygen that reaches close to the surface;Northwest Africa, Benguela and California follow in order ofincreasing oxygen. The high latitude region off Japan is welloxygenated. An important consequence of very low oxygen is thatnitrate becomes an electron donor and is lost by a process known

Fig. 6. Spatial distribution of nitrate at 60 m for each EBUE. Note the equatorial doming idescribed in Fig. 5, averaged in time, and tted on a surface by using the Matlwww.mathworks.com/matlabcentral/leexchange/8998). Black lines are the 150 km offsceanography 83 (2009) 8096 87as denitrication (Fig. 3). As a result the region off Peru is animportant component of the global and varying denitricationbudget (Codispoti et al., 2001).

While there are signicant differences between the EBUEs inoxygen, there are striking similarities in the mean vertical distribu-tion of nitrate with the possible exception of California which haslower surface but higher deep concentrations; Japan is a hybrid(Fig. 5e). The similarities in nitrate are not expected given theage of the waters. Peru should have much higher nitrate as pre-dicted by the near complete drawdown of oxygen, but has clearlylost nitrate to denitrication. Subsurface waters off California, onthe other hand, have lost much less nitrate to denitrication(Fig. 3) in addition to having high levels of preformed nitrate (thequantity of nitrate in the deep water when it formed at the surface;Hales et al., 2005). These phenomena affect carbon dioxide (CO2)concentrations in upwelled surface waters and airsea ux in theEBUEs. As a result off Oregon and California airsea uxes of CO2are either slightly into the ocean (Hales et al., 2005) or neutral(Chavez et al., 2007; Pennington et al., in press). In contrast off Peru(Friederich et al., 2008) and central and northern Chile (Torreset al., 2002; Paulmier et al., 2008), CO2 ux is strongly out of theocean. A similar pattern has been noted in the BCS, where at highlatitude ux was into the ocean, while at low latitude ux is intothe atmosphere (Santana-Casiano et al., in press). CO2 measure-ments off Northwest Africa are lacking but given the above, onewould predict uxes out of the ocean in the region of study. Thehigher latitude Iberian Peninsula acts as a sink for CO2 (Arsteguiet al., in this issue). What will happen to these uxes in the futurewith global and climate change? Higher fresh water input and

n Peru, Northwest Africa and northern Benguela. Data are from the gridded databaseab function gridt (written by John dErrico and available online at http://hore limit and the Rossby radius of deformation.

stratication at high latitudes are predicted to increase thestrength of the CO2 sink and higher temperatures, lower oxygenand greater denitrication to increase the CO2 source at low lati-tudes. Changing winds will also affect airsea uxes. A focused ef-fort on airsea exchange in the EBUEs is called for.

6. Biological comparisons chlorophyll, primary productivity,zooplankton, and small pelagic sh

The mean vertical proles of chlorophyll for the four EBUE plusJapan are shown in Fig. 5f. Surface chlorophyll is highest in Bengu-ela followed by Northwest Africa, Peru, California and Japan. Giventhe large dynamic range for chlorophyll this property is heavily af-fected by sparse sampling. Even so the relative order is consistentwith nitrate supply with the exception of the high chlorophyll val-ues from Benguela. For further comparison mean SeaWiFS chloro-phyll was estimated as was satellite-derived primary production(Behrenfeld and Falkowski, 1997). The satellite estimates suggestthat Northwest Africa has the highest levels of chlorophyll and pri-mary production followed by Benguela, Peru and California (Table1). It is likely that the Northwest Africa satellite chlorophyll isbiased high due to the presence of Saharan dust which impactsatmospheric correction. The likely order of productivity is: Bengu-ela, Peru, Northwest Africa and California with the rst three beingvery similar to each other. These results are similar to those of Carr

phase. Winter mixing and iron limitation have been suggested asexplanations for this unexpected relationship (Calienes et al.,1985; Chavez et al., 2008; Echevin et al., 2008; Friederich et al.,2008). A further analysis of the SeaWiFS record shows that in threeof the four EBUE (NW Africa is the exception), chlorophyll levelsare increasing over 12 year record (Fig. 8). These trends in generalagree with those in SST (Fig. 1d) in that California and Peru havebeen cooling, Benguela is not warming strongly or warming insome areas and cooling in others but Northwest Africa is denitelywarming. Unfortunately the length of the satellite-derived chloro-phyll and primary production time series precludes conclusionsregarding anthropogenic effects or even multi-decadal variability.

Zooplankton data are sparse although an effort is underway tosynthesize available information (Mackas et al., 2008). Here wecomment only on top-down versus bottom-up control of zooplank-ton and on the interpretation of zooplankton data. In a recent pa-per Rykaczewski and Checkley (2008) suggest that upwelling rateregulates the size structure and abundance of zooplankton inEBUEs; faster rates select for larger plankton and anchovies,slower rates for smaller plankton and sardines. This is an intriguingconcept given that nearshore Ekman transport results in fasterupwelling rates than curl-induced Ekman pumping. Further thedepth from which waters originate may also be different withtransport recruiting deeper water. The corollary is that the relativeratio of transport to pumping may be an important ecosystemproperty. An alternative explanation for the size selection process

(bluxpe

88 F.P. Chavez, M. Messi / Progress in Oceanography 83 (2009) 8096Fig. 7. Seasonal cycles of chlorophyll concentration (black), sea surface temperature(10 latitude band up to 150 km offshore). California and Northwest Africa show the e(2002). An analysis of the seasonal cycles of chlorophyll in relationto SST and vertical transport (upwelling) yields some interestingdifferences (Fig. 7). For California and NW Africa, the seasonal cy-cles of transport (and nitrate not shown) and chlorophyll are inphase as expected, higher nutrient supply leads to enhancedphytoplankton biomass. This is also the case for the southernmostseasonal upwelling region of the HCS (Thomas et al., 2001). ForBenguela the relationship is weaker but this region is not stronglyseasonal and dominated by higher-frequency intraseasonal(eddy-induced) variations in chlorophyll (Figs. 7 and 8). Peru isperplexing transport and chlorophyll are completely out ofseasonal while Peru has an inverse relationship. SST is Reynolds et al. (2007) monthly frQuikSCAT weekly from July 1999 to July 2008. All data were regridded to QuikSCAT (0.2reader is referred to the web version of this article.)of transport and pumping is provided in the following paragraph.The vertical upwelling rate (m s1) resulting from Ekman

transport is highest off California followed by Benguela, NorthwestAfrica and Peru (Table 1). If Rykaczewski and Checkley (2008) arecorrect, there should be more and bigger zooplankton off Californiathan the other EBUEs. We agree that the relative contribution ofcoastal (transport) versus offshore (pumping) upwelling is animportant ecosystem property, but suggest that it is for reasonsother than upwelling rate. Coastal upwelling (transport) is betterfor the ecosystem than offshore curl-induced upwelling, notbecause of differences in vertical speed but because of location.

e) and total vertical transport (Ekman transport plus Ekman pumping) in four EBUEcted positive relationship between transport and chlorophyll. Benguela is not highly

om October 1981 to February 2007; chlorophyll is SeaWiFS climatology; winds are5 0.25). (For interpretation of the references to colour in this gure legend, the

singon a

in OWhy? Coastal upwelling (transport) recruits waters that are in con-tact with the nepheloid layer off the slope and shelf and thereforebrings higher concentrations of iron into the euphotic zone(Johnson et al., 1999) leading to a food web of larger organisms(diatoms, copepods, krill) and accumulation of biomass. Curl-in-duced upwelling recruits subsurface waters further from shore,not in contact with the continental shelves, with low iron to nitrateratios leading to a low biomass and the small ecosystem charac-teristics of high nutrient low chlorophyll (HNLC) regions like theequatorial Pacic (the microbial food web; Chavez et al., 1991).

The general agreement is that bottom-up control of zooplank-ton, like that described above, is dominant in EBUEs. In a recentpaper Ayn et al. (2008) showed that over large spatial scales, zoo-plankton off Peru are regulated by bottom-up processes, but thaton local scales zooplankton can be regulated from the top downby anchoveta. Strong upwelling, horizontal transport and meso-

Fig. 8. Time series of SeaWiFS chlorophyll for each EBUE. The trend line shows increain Northwest Africa. The data are SeaWiFS full resolution monthly (9 km) averaged150 km offshore.

F.P. Chavez, M. Messi / Progressscale activity acts to distribute or disperse a resource. What arethe trophic transfer consequences of this dispersal and does it af-fect overall concentration of phytoplankton and zooplankton?Fisheries oceanographers have argued that there is an optimalenvironmental window for sh (and plankton) (Bakun and Parrish,1982; Parrish et al., 1983; Cury and Roy, 1989). At low wind speedssh productivity is low due to low levels of primary production(Cushing, 1969) and at high speeds sh productivity drops dueto: (1) transport of larvae out of the productive habitat and (2) mis-match of larvae and their prey; sh abundance would be greatestat intermediate upwelling-favorable winds. Barber and Smith(1981a) discuss a similar issue in their critique of Margalef(1978) in that they viewed the quality as well as the quantityof external energy input as important determinants of ecosystemproductivity. In other words strong upwelling and high nutrientsupply do not necessarily lead to greater ecosystem productivity.As we suggest below, and as often the case, both Barber and Smith(1981a) and Margalef (1978) were likely correct.

The small pelagic sh make up the majority of sh caught in thefour EBUEs accounting for approximately 12 of a total of 17 millionmetric tons (mmt) of marine sh taken between 2000 and 2007.This represents around 20% of the global take of marine sh overan area of less than 1% of the global ocean (FAO data extracted fromhttp://www.fao.org/shery/statistics/global-capture-production/query/en). The importance of these sh to local human survivaland economies can be traced back many hundreds of years (seeChavez et al. (2008) for the history off Peru). The rise and fall ofthe sardine shery off California from the early to the mid 20thcentury was documented in the novels of important North Ameri-can writers (Chavez et al., 2003). In the modern scientic historythese regions re-gained notoriety during the rise of the anchovetashery off Peru in the decade of the 1960s. At its peak this shery,over less than 0.01% of the global ocean by area, yielded 20% of theglobal sh catch or the combined total of the four EBUEs today.After returning from an expedition to Peru, Ryther (1969) wrotehis seminal paper on primary productivity and sh production inthe ocean having noted that primary productivity off Peru wasnot substantially higher than productivity in other coastal areasbut that sh productivity was much higher. Ryther concluded thatEBUEs must have higher trophic transfer efciencies from primaryproduction to sh than other productive areas of the world ocean.

What Ryther had not realized was the uniqueness of Peru in

concentrations of chlorophyll in Benguela, California, and Peru, and small decreases0.25 0.25 grid (geometric mean) and then within each 10 latitude band up to

ceanography 83 (2009) 8096 89terms of trophic transfer efciency and that the other EBUE pro-duce much less sh than Peru per unit primary production(Fig. 2). Early analysis of stomach contents suggested a dominanceof phytoplankton in the anchoveta diet and led Ryther to surmisethat high sh productivity was due to a direct transfer of primaryproduction to sh. To complicate matters a reanalysis shows thatthe most important source of calories for anchoveta are zooplank-ton primarily euphausiids and large copepods (Espinoza and Ber-trand, 2008). Anchoveta, as indicated by a long intestine typical ofherbivorous organisms, apparently obtains important nutrientsfrom phytoplankton but most of their energy from zooplankton.This new result forced a revisit of Ryther, 1969 anchoveta para-dox (Bakun and Weeks, 2008; Chavez et al., 2008): How can thePeruvian EBUE produce an order of magnitude more sh per unitof primary production than the other EBUE? The primary produc-tion (PP) and sh data in Fig. 2, together with the assumption ofa 10% energy loss per trophic level, suggest that there are approx-imately 2.5 trophic levels between PP and sh off Peru, 3 off Cali-fornia and 3.54 off Benguela and Northwest Africa. A similarconclusion was reached by Chavez et al. (1989) for Peru. The calcu-lations imply higher transfer efciencies off Peru and reinforce thecentral role of anchoveta off Peru. One possibility is that the com-bination of high primary productivity and relatively weak windslead to high transfer efciencies resulting from optimal conditionsfor growth, reproduction and retention for zooplankton and sh. Asecond possibility is that the shallow and intense OMZ off Peru

concentrates zooplankton prey and exclude anchoveta (and otherzooplankton) predators again increasing transfer efciency. Finally,the high levels of northern HCS El Nio-induced interannual vari-ability (Fig. 1) may act to continually reset the pelagic ecosystemto an r state, favoring fast-growing organisms (diatoms, euphausi-ids, anchoveta) and keeping predators from becoming dominantand providing effective top-down control.

The ip side of the above issue is why Benguela and North Afri-ca have high levels of primary production but low levels of sh

production? Is the transfer from primary production to sh inef-cient? The answer in Benguela may be related to stronger windsand offshore transport together with the high levels of mesoscaleactivity. These affect recruitment as well creating a mismatch be-tween prey and predator: the energy consumed nding dispersedprey is much larger than off Peru. Off Northwest Africa offshoredispersal is also an issue (Arstegui et al., in this issue) as may bedeep mixed layers over the shelf (Barber and Smith, 1981a) whichwould result in low encounters for rst feeding of sh larvae

decerpmajopart

90 F.P. Chavez, M. Messi / Progress in Oceanography 83 (2009) 8096Fig. 9. Cross-shelf distribution of in the upwelling zone of the CCS. There is a steadyMonterey Bay, California, top panel) and pCO2 (quarterly underway measurements pwhen the fresh and equatorward California Current is reached. The location of thiswork (bottom panel). California Undercurrent water, which has a high NO3 and pCO2

Phytoplankton growing in the upwelled water draw down NO3 and CO2 to low levels. Phsubducted below the euphotic zone, where it decays, elevating the NO3 and CO2 levels of sfollowing the trend in chlorophyll offshore but that export is constant in the productiverease in chlorophyll concentration (monthly SeaWiFS perpendicular to the coast offendicular to the coast off Monterey Bay, California, second panel) until a nal dropr front varies seasonally and interannually. The cartoon describes the processes atial pressure, upwells near shore, and is advected offshore into the California Current.

ytoplankton carbon is consumed by zooplankton and sh and eventually sinks or isubsurface waters. We hypothesize that the consumption of new nutrients decreaseshabitat delimited by the California Current.

(Lasker, 1981). In neither ecosystem is the OMZ as shallow or in-tense as off Peru.

7. Biogeochemical cycles in relation to ecology

In EBUEs, bottom-up forcing determines overall ecosystem pro-ductivity (sensu Barber and Chavez, 1983) but the structure of thefood web determines the spatial distribution, rates and pathwaysby which this productivity is cycled through the ecosystem, tothe atmosphere and the deep-sea. It is rather interesting thattwo large international programs, one focused on ocean biogeo-chemical cycles (Joint Global Ocean Flux Study JGOFS) and theother on food webs (Global Ocean Ecosystem Dynamics GLOBEC),operated concurrently but independently for almost a decade,when the two subjects are intimately related. In the following sec-tion we address these issues and focus on the enhanced EBUE pro-ductivity and its export to depth and how export might bemediated by the structure and spatial distribution of the food web.

As Margalef (1978) described them, EBUEs are leaky; there isenhanced new production (sensu Dugdale and Goering, 1967) ofphytoplankton biomass as well as efcient transfer of this newbiomass through the food chain to sh (sensu Ryther, 1969). Theplankton community is composed of large organisms leading tospatiotemporal mismatches between new production, biomassaccumulation, consumption by grazers and vertical loss of organicmaterial from the euphotic zone (Chavez et al., 2002; Penningtonet al., 2009). This is in sharp contrast to open ocean systems thatdo not accumulate biomass (at any trophic level) but are very ef-cient at recycling and retaining the scarce nutrient available in the

the dissolved organic pools, the available data show that EBUEsare the regions with the highest vertical uxes of particulate or-ganic matter (Jahnke et al., 1990; Jahnke, 1996, in press) and pro-duction of dissolved organic matter (Hansell, 2002) in the worldsoceans. While the large-scale patterns of biogeochemical cyclingof elements are not surprising, there are unexpected features inthe spatial distribution of EBUE food webs and vertical ux, mostlydocumented in the California EBUE (Pennington et al., 2009). Forcentral California the productive upwelling habitat is shorewardof the California Current (order 0150 km; Collins et al., 2006).The eastward edge of the California Current can be identied byfresher water and the region of strongest equatorward currents(the California Current jet). Within this zone chlorophyll and pri-mary production are high and increase towards the shore (Fig. 9).Nearshore sediment trap measurements however show that verti-cal ux of organic carbon is much lower than expected for the highlevels of new and primary production (Pilskaln et al., 1996). Inaddition, the seasonal ux lacks the strong seasonality found inprimary production, resulting in a relationship between the e-ratio(ux/primary production) and primary production that was the in-verse of that found between the f-ratio (new/primary production)and primary production. The hypothesis, reproduced in modelexperiments (Olivieri and Chavez, 2000), is that the new phyto-plankton biomass generated close to shore is advected offshoreby the upwelling circulation, assimilated by the food web andeventually deposited vertically over a much larger region thanthe very near-shore high productivity zone. Sediment traps alongan on/offshore transect measured similar uxes in spite of a strongdecrease in primary production (Pennington et al., 2006; Fig. 9).This example clearly illustrates one of the dening characteristicsof EBUEs: the spatial separation of sources and sinks; surface

sterns. Th

F.P. Chavez, M. Messi / Progress in Oceanography 83 (2009) 8096 91Fig. 10. Conceptual model of the trophic structure and spatial organization of an eavariation in time, and the separation of sources and sinks are key attributes of EBUEeuphotic zone. While there is a paucity of data from EBUEs regard-ing the vertical particulate ux of organic matter, and even less onfeed on gelatinous organisms. In general each EBUE seems to be composed of several regLderitz in Benguela, Point Conception in California). How the organisms, in particular thuncertain.nutrients are elevated in the regions of strongest upwelling, phyto-

boundary upwelling ecosystem (EBUE). The spatial organization, together with itse connections should not be taken literally in the sense that the turtles for example

ions or biomes with marked biological and physical transitions between them (e.g.e sh and top predators, exploit or are dependent on the different biomes remains

of these two hypotheses has been conrmed. Recent anoxic eventson the shelf off Oregon (Grantham et al., 2004; Chan et al., 2008)

in Ohave been linked to increases in the upwelling source water and/or upwelling-favorable winds rather than to changes in the foodweb. Further south in the southern California Bight a slow, progres-sive decrease in subsurface oxygen has been detected (Bogradet al., 2008) and on global scales it appears as if OMZs are expand-ing (Stramma et al., 2008) possibly since the end of the LIA. Are thelow oxygen phenomena among the rst dramatic and easily-obser-vable effects of the human-induced global warming suggested byBakun (1990)? The answer is muddled given that natural andanthropogenic processes may be presently working to lower oxy-gen in EBUEs.

8. The spatial organization of EBUEs and top predators

An important attribute of EBUEs is their time-varying spatialstructure (Fig. 10). Bertrand et al. (2008b) refer to this as the oce-anic landscape, a misnomer of course. This landscape has manyscales, the rst we consider is that associated with the productivecoastal upwelling habitat. Inside this productive habitat there is amostly resident food web characteristic of the EBUEs discussedhere. At the center of this food web are the small pelagic sh dis-cussed earlier that feed a diverse community of top predators. EachEBUE has a few different characteristics as discussed below, butthey all tend to support mackerels (jack and horse), seabirds, ceta-ceans and pinnipeds. A second predator group composed of highlymigratory tunas, billsh, turtles, large sharks, whales, etc. foragesat the edges or migrates through the highly productive habitat. Lat-itudinally the productive habitat is modied by coastal topographyand atmospheric forcing, creating biogeographically distinct bio-mes; these are inhabited by different life stages of the small pela-gics and larger predators during normal conditions, or by adults asrefugia during El Nio and El Viejo. To date most research has fo-cused on the smaller scale individual biome and not on the entireEBUE. Benguela appears as the leading example of this holistic ap-proach that will require overcoming of political boundaries to besuccessful.plankton grow at the edges of these regions and further offshore azooplankton maximum is found (Chavez et al., 2002). For verticalorganic carbon ux it is not clear if there is an offshore maximumassociated with the zooplankton or if seasonal accumulation ofzooplankton (and sh) biomass and its spatial distribution servesto distribute ux evenly within the productive habitat. In a recentglobal synthesis (Jahnke, in press), the ux of organic carbon to theslope and rise area were reported to be similar for the four EBUEs(HCS 0.59, CCS 0.51, BCS 0.51 and ICCS 0.44 mol C m2 yr1) butone has to wonder if the uxes are really that even given the pau-city of available data. Shouldnt the OMZ differences between theEBUEs (Fig. 5d) affect these uxes? Do OMZs act as a trap or asieve for the sinking organic carbon?

Walsh (1981) and Bakun and Weeks (2004) have further sug-gested that the large populations of small pelagic sh in EBUEscan play a role in vertical carbon ux. Walsh (1981) postulated thatthe large take of anchoveta by shing off Peru and the collapse ofthe stock in the early 1970s would result in more carbon sinkingto depth (carbon that normally would have passed through thefood chain to sh) and even more intense anoxia off Peru. Bakunand Weeks (2004) suggested that changes in the abundance of sar-dines in Benguela might be responsible for episodic anoxia andproduction of hydrogen sulde; in the absence of the sh, phyto-plankton blooms sink over the shelf where they degrade. Neither

92 F.P. Chavez, M. Messi / ProgressWithin the productive habitat there are further modications ofthe oceanic landscape, associated with freshly upwelled water andits surroundings, with characteristic jets and eddies (Strub et al.,1991), and internal waves (Bertrand et al., 2008b). These meso-scale features are highly variable in space and time and affectthe distribution of prey and their predators. The relative activityof these features has an impact on trophic transfer efciency (seeCushing, 1969). Those EBUEs with higher frequency variability,like Benguela, may suffer greater mismatches between predatorand prey populations than more stable ones like the HCS (Bakunand Weeks, 2008). As eddies become larger and more stable thematch improves (Smith, 2005). The same can be said about fronts:smaller and more ephemeral ones create a greater mismatch thanthe large and stable ones surrounding the productive habitat (i.e.the California Current) that attract a diverse community of foragers(Hyrenbach et al., 2000; Laurs et al., 1984). The key is predictabil-ity. Recently it has been suggested that coastal upwelling eddiesact to reduce nutrient supply (Gruber et al., 2007), the opposite ofwhat has been suggested for open ocean eddies (McGillicuddyet al., 1998). Well constrained in situ experiments will be requiredto resolve the role of eddies in EBUE biogeochemical cycling andecosystem productivity.

A good comparative synthesis of top predators in the EBUEs islacking and a few comparisons from the literature are providedhere. Reliable seabird numbers are available for the Benguela,California and Peru (Chavez et al., 2003; Crawford, 2007; Jahnckeet al., 2004; Tovar et al., 1987;Wolf et al., 2006) and anecdotal onesfor Northwest Africa. Prior to the development of the anchovetashery off Peru the population of seabirds reached levels in excessof 20 million birds dominated by a single species, the guanay cor-morant, that feeds almost exclusively on anchoveta; today the sea-bird population off Peru has declined to around 2 million as a resultof the shery (Muck and Pauly, 1987; Chavez et al., 2003; Jahnckeet al., 2004; Tovar et al., 1987). Pauly (1987) describes how largequantities of anchoveta were consumed by seabirds and larger pre-dators before the onset of shing and how shing replaced thisnatural take. The effect of shing in EBUE on top predators hasbeen shown for other EBUE as well (i.e. Crawford, 2007) and theecosystem in general with food web models (Pauly et al., 2000;Neira et al., in this issue). A full treatment is outside the scope ofthis contribution. Northwest Africa has a very small seabirdpopulation perhaps due to the almost complete absence of coastalislands, a preferred site for seabird rookeries (Cushing, 1969).Benguela was renowned for the large populations of penguins,again prior to heavy shing pressure (Crawford, 2007); the totalseabird population in the BCS was on order of several million, a g-ure similar to that in the CCS (Wolf et al., 2006). As is the case forsh tonnage, it seems as if Peru is able to support an order ofmagnitude more seabirds than the other EBUEs, because of asingle species that feeds almost exclusively on anchoveta.

An analysis of FAO catch statistics for mackerel (primarilyTrachurus sp.) suggests that the HCS is again higher, with the larg-est catches taken off Chile (most taken offshore in the subtropicalfront). Northwest Africa ranks second followed by California andBenguela. In terms of pinnipeds available data suggest that theBenguela, California and Peru have supported just under a millionanimals (Muck and Fuentes, 1987; Takekawa et al., 2004;Crawford, 2007). These two groups, mackerel and pinnipeds, donot appear to show the same dramatic differences between theEBUEs as we have seen for small pelagics and seabirds. A rathersimple hypothesis is that predators that feed almost exclusivelyon anchoveta, like the Peruvian cormorant are more abundant thanin other EBUEs but those that have more varied diets are moreequally distributed. Fron et al. (in this issue) note the relativelyeven biodiversity among the four EBUE; one notable exception isPeru, where the anchoveta is on average dominant and at times

ceanography 83 (2009) 8096the sardine is almost completely absent. Many generalizationsregarding EBUEs (i.e. Ryther, 1969) were developed from observa-tions of a single EBUE (i.e. Peru) and are probably not universal.

Large quantities of external energy (sensu Margalef, 1978)establish the basin-scale patterns of thermocline topography. Local

in Oforcing (sensu Barber and Smith, 1981a) then completes the trans-fer of physical energy (local wind and light) into primary produc-tion and through the food web. The very large Pacic basin (incontrast to the Atlantic) accumulates a large amount of heat andwater in the western equatorial Pacic resulting in a shallow ther-mocline in the eastern Pacic. During normal periods, steadyupwelling links the shallow nutrients from the large scale pro-cesses the shallow tropical eastern Pacic thermocline withsunlight resulting in enhanced biological productivity. Every38 years El Nio causes dramatic changes over the entire Pacicbut especially off Peru (Fig. 1), where positive SST anomalies of10 C occur (Barber and Chavez, 1983). Similar but less intensechanges occur on the scale of the PDO or El Viejo (2550 years)but because of their duration have signicant impact on ecosys-tems leading to so-called regime shifts. On the scale of ice agesthe changes involve many of the same atmospheric componentsbut probably different mechanisms (Gutirrez et al., 2009) andapparently lead to even greater ecosystem consequences: com-plete shutdown of the typical EBUE ecosystems. A second featureof the low latitude Pacic upwelling system is the presence of ashallow and intense OMZ. The intense and shallow OMZ createsan environmental landscape that is favorable to anchoveta, butHake (Merluccius spp.) is the most important demersal resourceand based on recent FAO catch statistics evenly abundant in threeof the four EBUE. Northwest Africa landings have been low in re-cent years but were higher in the past. In the Pacic hake habitatis contracting in response to a combination of shing, expandingoxygen minimum zones and the explosive growth of jumbo squid(Dosidicus gigas). The jumbo squid has been reported to be a vora-cious hake predator off California (Zeidberg and Robison, 2007),where hake populations are migrating poleward possibly in re-sponse to lower oxygen and the northward expansion of the jumbosquid. Why the jumbo squid have been expanding is still debated,is it a result of the strong shift in ocean climate that occurred in themid-1990s, decreasing oxygen (Chavez et al., 2003; Bograd et al.,2008) or to human-driven reductions in the squids predators andcompetitors for the same prey (Zeidberg and Robison, 2007)? Toconclude this section we note a few anomalies in terms of top pre-dators like the presence of salmon and sea otters in the CCS and thealmost complete lack of penguins (or related species) in the north-ern hemisphere EBUEs compared to those in the southern hemi-sphere. The CCS also is home to a large number of species ofrocksh (Sebastes spp.) relative to the other EBUE (Fron et al., inthis issue).

9. Synthesis, enigmas and the future

The character of the four EBUEs is to a rst order dependent onbasin-scale features: circulation of the subtropical gyres, eastwestand northsouth patterns of thermocline and nutricline topogra-phy, and at their poleward margins on high latitude mixing andfrontal zones. The between and within EBUE differences are lati-tude-dependant, with low latitude biomes experiencing mostlyyear-round upwelling (albeit still with seasonal modulation), ashallower nutricline, lower oxygen and broader upwelling. At high-er latitudes upwelling typically occurs in spring and summer, thethermocline and nutricline uplift is over a narrow coastal band,low oxygen is advected into them by poleward undercurrentsand the upwelling zone is narrower. These characteristics deter-mine the spatial organization of biomes within each EBUE (Fig. 10).

F.P. Chavez, M. Messi / Progressnitrate is lost via denitrication ultimately limiting primaryproduction. Denitrication also leads to low pH and loss of carbondioxide to the atmosphere (Chavez et al., 2008).In contrast, Benguela, being further from the equator and in thesmaller Atlantic basin, is less affected by basin scale thermoclineperturbations (Atlantic El Nio) and more affected by smaller scalelocal physical variability. As such the system has more of the rednoise characteristic of the atmosphere (Steele, 1985). This is evi-dent in the high intraseasonal variability in the altimetry signal(Fig. 4) and in the SeaWiFS time-series of chlorophyll (Fig. 8). Itis surmised that this high mesoscale variability hinders efcienttransfer of primary production through the food web to sh. Aquestion of interest is what is the ultimate fate of surface-derivedprimary production in the different EBUEs? Does more of it exitthe system vertically to the sediments in Benguela or Peru? Arezooplankton concentrations higher in Peru or Benguela and if sowhat sizes and types? A compilation of these types of data forthe four EBUE would be highly informative.

While the EBUEs have been intensely studied due to their strik-ing features (high primary production, low oxygen, high sh pro-duction) many enigmas still remain. For example while there area number of ideas (see above) regarding the differences in sh pro-duction of the four EBUEs (Fig. 2), that debate is by no meansclosed. Another mystery is the out of phase seasonality of upwell-ing and chlorophyll off Peru (Fig. 7). The other EBUE have, in gen-eral, strong positive coupling between physical forcing andbiological productivity. Why is this not the case off Peru? Limita-tions by iron and by vertical mixing have been suggested as possi-ble reasons (Echevin et al., 2008; Friederich et al., 2008) butexperimental data are still required. Similarly there is debate overthe importance or role of low oxygen in EBUE ecosystem dynamics,is it favorable to the production of small pelagic sh? The increasedproduction of pelagic sh off Peru clearly comes at the expense ofbenthic resources that are restricted due to low oxygen. The role ofzooplankton in ecosystem dynamics and the production of sh re-main in need of further study. Direct relations between chlorophylland sh have been noted for the California Current System (Wareand Thomson, 2005) and unpublished comparisons for the Peruand Chile indicate similar and strong links. But clearly the solar en-ergy captured by the primary producers has been shown by anal-ysis of stomach contents to ow through zooplankton to sh. Dothese relations exist but just not evident because of the difcultiesassociated with sampling zooplankton? And perhaps more impor-tantly are there strong non-linearities that would make estimatesof zooplankton important, or is chlorophyll sufcient to estimatebottom-up forcing? Euphausiids are repeatedly mentioned as key-stone taxa given their importance to sh and other predators (sea-birds, whales), yet information on euphausiids is severely lacking.Efforts to integrate this information within and among EBUEshould be a top priority.

The greatest enigma and the most important for society is howwill the EBUEs be affected by climate and global change? There aresharp disagreements, for example on the effects of global warming(Fron et al., in press). Will global warming lead to stronger windsand increased productivity in EBUEs? Strong global warming-likecoastal winds develop during El Nio off Peru, but productivity isreduced by increases in nutricline depth. On the other hand glacialconditions seem to lead to a similar low productivity condition(Gutirrez et al., 2009). It is likely that only time will tell the pro-cesses at work. What will be the effects of ocean acidication onEBUEs? A large fraction of the carbon dioxide introduced to theatmosphere by humans is taken up by the ocean, lowering pHand affecting ocean ecosystems in as yet unpredictable ways(Chavez et al., 2007). The EBUE are regions of low pH resultingfrom the biological pumps natural acidication (Chavez et al.,2008). EBUE upwelling brings this acidied water to the surface

ceanography 83 (2009) 8096 93leading to a large (>1 pH unit) range of pH variability in space andtime. How will the present day slow (

in Oresources in EBUE is substantial and for many of the developingcountries on EBUE shores the economic and social benets of har-vest are large. How will these benets be affected by climate andglobal change? Are ecosystem-based approaches the solution orare these so convoluted and complex that theymay actually impedeprogress? What seems abundantly clear is the continued need forintegrated information collection and management systems thatwill allow decisions to be made decisively and with condence.The continued collection of in situ and satellite time series, togetherwith process studies to resolve the enigmas and provide modelswith accurate parameterizations are paramount in this regard.

Acknowledgements

The authors recognize the nancial support of NASA and theDavid and Lucile Packard Foundation. The intellectual and techni-cal support from the Biological Oceanography group at MBARI(http://www.mbari.org/bog) and the NASA-supported FAST group(http://www.mbari.org/bog/FAST) is noted. Finally we thank theparticipants of the Symposium in Las Gran Canarias that led to thisvolume, for stimulating presentations, one-on-one discussion andmany wonderful lunches and dinners. Reviews by two anonymousreferees and J.T. Pennington greatly improved the quality of themanuscript.

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