Population biology of the subtidal kelps Macrocystis ...temporales de Tetrapygus niger (erizo negro), el pastoreador bentónico más conspicuo del norte de Chile, produjo la extinción

33EL NIÑO EFFECTS ON SUBTIDAL KELP IN NORTHERN CHILERevista Chilena de Historia Natural78: 33-50, 2005

Population biology of the subtidal kelps Macrocystis integrifoliaand Lessonia trabeculata (Laminariales, Phaeophyceae)

in an upwelling ecosystem of northern Chile:interannual variability and El Niño 1997-1998

Biología poblacional de huirales submareales de Macrocystis integrifolia y Lessoniatrabeculata (Laminariales, Phaeophyceae) en un ecosistema de surgencia del norte de

Chile: variabilidad interanual y El Niño 1997-1998

J.M. ALONSO VEGA1, 2, JULIO A. VÁSQUEZ1, 2,* & ALEJANDRO H. BUSCHMANN3

1 Departamento de Biología Marina, Facultad de Ciencias del Mar, Universidad Católica del Norte,2CEAZA, Centro de Estudios Avanzados de Zonas Áridas, Casilla 117, Coquimbo, Chile

3I-MAR, Universidad de Los Lagos, Casilla 557, Puerto Montt, Chile*Autor para correspondencia: e-mail: [email protected]

ABSTRACT

This paper describes the population biology of Lessonia trabeculata and Macrocystis integrifolia during andafter the 1997-1998 El Niño in an area of permanent coastal upwelling in northern Chile. Spatial and temporalpatterns of distribution were evaluated seasonally for adult and juvenile sporophytes of both species between1996 and 2003. These two kelp form an assemblage distributed between 2 and 15 m depth, with disjunctpatterns along a bathymetric gradient, including two morphs of L. trabeculata, the occurrence of whichdepends on the presence or absence of M. integrifolia. During the 1997-1998 El Niño the spatial-temporalpatterns of abundance of the kelp assemblage were maintained by the continuity of coastal upwelling, whichbuffered and moderated superficial warming of the sea and depletion of nutrients. In this context, localitiesassociated with coastal upwelling areas could function as “sources” of reproductive propagules after passageof El Niño, thus increasing kelp recolonization rates in “sink” localities, which suffered local kelp extinctions.Intensification of upwelling processes after the 1998-2000 La Niña increased nutrient inputs into subtidalhabitats, favoring the productivity of the kelp assemblage. However, an abrupt change in the spatial-temporalpatterns of abundance of the black sea urchin Tetrapygus niger, the most conspicuous benthic grazer innorthern Chile, produced local extinctions of M. integrifolia and compression of the range of bathymetricdistribution of L. trabeculata. Top-down (mortality of benthic carnivores during the 1997-1998 El Niño) andbottom-up effects (intensity and frequency of upwelling) in this subtidal coastal ecosystem appear to regulatethe kelp-herbivore interactions in the study area. The main sources of reproductive propagules for the re-establishment of the assemblage kelp were fertile sporophytes which included isolated, low density patches ofM.integrifolia located within the bed of L. trabeculata, although drifting kelp rafts and “seed banks” ofmicroscopic dormant stages may provide supplementary recruitment. In the temperate SE Pacific,oceanographic events that act on different spatial-temporal scales plus low frequency biological processes(changes in grazer abundance), which act on local scales, produce inter-annual variability in the long-termdymanics of kelp populations. Furthermore, the interactive effects between centers of permanent upwellingand the oscillating temporal periodicity of oceanographic events that produce positive (El Niño) and negative(La Niña) thermal anomalies modify the spatial arrangement of subtidal kelp populations on a latitudinalgradient.

Key words: subtidal habitats, population and community ecology, extinction and re-colonization processes,kelp-herbivore interaction, El Niño, La Niña.

RESUMEN

Este trabajo describe la biología poblacional de Macrocystis integrifolia y Lessonia trabeculata durantey después de El Niño 1997-1998, en un área de surgencia costera permanente en el norte de Chile. Lospatrones de distribución espacio-temporales de esporofitos adultos y juveniles de ambos huiros fueronevaluados estacionalmente entre 1996 y 2003. Ambos huiros conforman un ensamble que se distribuyeentre 2-15 m de profundidad con patrones disjuntos a lo largo del gradiente batimétrico, y con dos

34 VEGA ET AL.

morfos de L. trabeculata que dependen de la presencia o ausencia de M. integrifolia. Durante El Niño1997-1998, los patrones espacio-temporales de abundancia del ensamble de huiros son mantenidos por lacontinuidad de los procesos de surgencia costera que amortiguan y moderan el calentamiento superficialdel mar y la disminución de nutrientes. En este contexto, después de un evento El Niño las localidadesasociadas a áreas con surgencia permanente pueden funcionar como áreas “fuentes” productora depropágulos reproductivos incrementando la tasa de recolonización en áreas “sumideros” adyacentesdonde se produjo extinción local de huiros. Durante La Niña 1998-2000, la intensificación de losprocesos de surgencia incrementa la entrada de nutrientes hacia hábitat submareales favoreciendo laproductividad del ensamble de huiros. Sin embargo, un repentino cambio en los patrones espacio-temporales de Tetrapygus niger (erizo negro), el pastoreador bentónico más conspicuo del norte de Chile,produjo la extinción local de M. integrifolia y la compresión del rango de distribución batimétrica de L.trabeculata. Efectos cascada abajo (mortalidad de carnívoros bentónicos durante El Niño 1997-1998) ycascada arriba (intensidad y frecuencia de surgencia) en este ecosistema submareal costero parecenregular la interacción huiros-herbívoros en el área de estudio. La principal fuente productora depropágulos para el reestablecimiento del ensamble proviene de esporofitos fértiles que configuranparches aislados de baja densidad de M. integrifolia ubicados dentro de la pradera de L. trabeculata,aunque huiros flotando a la deriva y “bancos de semilla” de estados latentes microscópicos podríanactuar como estrategias complementarias . En el Pacíf ico Sudamericano temperado, eventosoceanográficos que actúan a distintas escalas espacio-temporales y procesos biológicos estocásticos debaja frecuencia (cambios en la abundancia de pastoreadores) que actúan a escala local, generanvariabilidad interanual en la dinámica de las poblaciones de huiros a largo plazo. Además, el efectointeractivo entre centros de surgencia permanente y la periodicidad temporal oscilatoria de eventosoceanográficos que generan anomalías térmicas positivas (El Niño) y negativas (La Niña) modifican elarreglo espacial de las poblaciones submareales de huiros en el gradiente latitudinal.

Palabras clave: hábitat submareales, ecología de poblaciones y comunidades, procesos de extinción yrecolonización, interacción planta-herbívoro, El Niño, La Niña.

INTRODUCTION

The spatial-temporal patterns of kelpassemblages are generally determined by thediversity and population biology of theconstituent species (Dayton et al. 1999).Seasonality of physical (e.g., temperature,water movement, quantity and quality of light)and chemical (e.g., nutrients) parameters areimportant in the regulation of reproductive andvegetative processes of specific componentswithin kelp assemblages (Graham et al. 1997,Hernández-Carmona et al. 2001, Buschmann etal. 2004), and may covary in subtidalenvironments to produce synergisticinteractions (Kain 1989). Conversely,biological processes such as inter- and intra-specific competition, pest and herbivoryregulate kelp assemblage structure, modifyingspatial and temporal patterns of speciesabundance (Dayton 1985, Vásquez &Buschmann 1997, Scheibling et al. 1999), andmorphology (Vásquez 1991).

Long-term studies in the NorthernHemisphere have shown that El Niño SouthernOscillation events (ENSO), which includealternation of a warm phase (El Niño) with acold phase (La Niña), alter the structure andorganization of subtidal kelp in temperate

latitudes, modifying patterns of persistence,stability, succession, species diversity, andabundance (Dayton et al. 1992, 1999, Tegner etal . 1997). In the Southern Hemisphere,depending on the magnitude and intensity, ElNiño can produce localized kelp extinctions(Camus 1994) and subsequent re-colonizationthat modify the spatial-temporal distributionand abundance of local populations (Camus etal. 1994, Martínez et al. 2003). Still, moststudies of subtidal kelp population biology inthe Southern Hemisphere are short-term (oneyear, see Vásquez 1993, Camus 1994,Buschmann et al. 2004, Tala et al. 2004), or arelimited to high latitudes (≥ 40º S), where theinfluence of ENSO is minimal (Moreno &Sutherland 1982, Santelices & Ojeda 1984,Dayton 1985). As such, there are no long-termdata concerning the effects of large-scale, lowfrequency events such as ENSO on kelppopulation biology. These oceanographicevents are probably important in regulatinginterannual variability in the northern Chilebiogeographic region (ca. 18-30º S, see Camus1990, Vásquez et. al. 1998).

The persistence of kelp populations on thenorthern Chilean coast during and after El Niñohas been associated with coastal upwellinglocated at specific geographic areas (Martínez

35EL NIÑO EFFECTS ON SUBTIDAL KELP IN NORTHERN CHILE

1999). One of the most important coastalupwelling centers of northern Chile is locatednear the Mejillones Peninsula (ca. 23º S), whichis seasonal, and related to the annual cycle ofdriving winds from the SW (Escribano et al.2004). In this region, one of the main watermasses being upwelled is that of EquatorialSubsuperficial Water (ESSW), characterized bylow dissolved oxygen concentrations, lowtemperatures, and high concentration ofnutrients (González et al. 1998). These watermasses are transported shoreward by polewardflow in the first 200 m (Marín et al. 2001,Escribano et al. 2004). Interest in the MejillonesPeninsula sector has increased markedly inrecent decades because some studies havereported that subsuperficial upwelling occurs inthe area year round (Fonseca & Farias 1987,Escribano 1998). This promotes continuous,high primary and secondary production in thewater column (Marin et al. 1993, Escribano &McLaren 1999, Fernández et al. 2002) as well asin the shoal litoral benthos (Vásquez et al. 1998,Camus & Andrade 2001), even duringsuperficial warming generated by El Niño(González et al. 2000, Ulloa et al. 2001,Vásquez & Vega 2004).

On the northern coast of Chile (ca. 23° S),the 1997-1998 El Niño occurred as two pulsesof positive thermal anomaly at the surface andsea level associated with strong poleward flowsin the first 100 m (Takesue et al. 2004). Thethermocline/oxycline and nutricline thatnormally rise to 40-60 m were depressed to150-200 m depths between April and May1997, and between Novembre 1997 and January1998 (Ulloa et al. 2001). The 1997-1998 ElNiño was immediately followed by La Niñaconditions, characterized by a mild andmoderate cooling of the water during 1998-1999, with cooling of greater intensity in 1999-2000 (Takesue et al. 2004). The 1998-2000 LaNiña promoted the emergence of SW windsdriving coastal upwelling, and intensifying theupsurge of subsuperficial water in the area ofthe Mejillones Peninsula (Lagos et al. 2002).The transition to a cold, nutrient-rich condition(La Niña) following a high-intensity warmingevent (El Niño) facilitates and increases thelocal recovery rates of kelp assemblages andtheir associated communities (Edwards 1994,Martínez et al. 2003). Within this context, along term monitoring program of subtidal kelp

at a site on the Mejillones Peninsula (beginningin 1996) permitted evaluation of the interactiveeffects of the ENSO cycle (1997-1998 El Niñoand 1998-2000 La Niña events) and effects ofcoastal upwelling on the population biology ofSouth American subtidal kelps.

In Chile, between 18 and 32º S, two kelpspecies, Macrocystis integrifolia Bory andLessonia trabeculata Villouta et Santelices,coexist in subtidal rocky environments, forminga broad subtidal assemblage from the intertidalto 15-20 m depths (Alveal et al. 1973, Vásquezet al. 2001). Both kelps have biphasicheteromorphic life cycles, with alternation of amicroscopic gametophytic (n) generation, whichis short lived, and a long-lived macrophyticperennial sporophytic generation (2n)(Buschmann et al. 2004, Tala et al. 2004). Whilethere are some reports in the literature regardingthe population biology of L. trabeculata(Villouta & Santelices 1984, Vásquez 1991,1992, 1993, Tala et al. 2004), data are scarce onthe population biology of M. integrifolia and theM. integrifolia - L. trabeculata assemblage. Theavailable information is restricted only toevaluations of standing stock at some localitiesand observations on reproductive activity incontrolled environments and in the field (Dieck1993, Buschmann et al. 2004). In this context,the present study evaluated aspects of thepopulation biology of the subtidal kelpassemblage formed by the canopy kelp M.integrifolia and the bottom kelp L. trabeculatain an area of intense upwelling in northernChile. Specifically, we considered sporophytedistribution, abundance and reproductivephenology of both species. These data are thefirst to address the effects of the ENSO cycle(1997-1998 El Niño and 1998-2000 La Niña) onthe South American subtidal kelp assemblage,and are contrasted with the effects of other ElNiño events documented in both hemispheres.

MATERIAL AND METHODS

Study area

The density and reproductive phenology of M.integrifolia and L. trabeculata were evaluatedon a seasonal basis between July 1996 andOctober 2003 at Caleta Constitución, on theMejillones Peninsula (Fig. 1). This locality is

36 VEGA ET AL.

within a bay, which is semi-protected fromdominant SW winds and waves by the presenceof Santa María Island. The basal stratum of thesubtidal kelp assemblage is composed ofvarious foliose, turf, and crustose macroalgae.The macroalgae include crustose Corallinales,turfs of Gelidiales and/or Ceramiales, and oftenpatches of Halopteris spp., Glossophora kunthii(C. Ag.) J. Ag., Asparagopsis armata Harleyand Rhodymenia spp. and Chondruscanaliculatus (C. Ag.) Grev. (Vásquez et al.2001). Detailed descriptions of the study siteand the marine ecosystem are given by Vásquezet al. (1998) and Vásquez & Vega (2004).

Oceanographic conditions

Mean daily in situ water temperature valueswere obtained using continuous-registerthermographs (Onset Computer Corporation,Bourne, Maine, USA) placed at three meterdepth along the shoal boundary of the kelpassemblage. When in situ records ofoceanographic variables were discontinued,large-scale climatic indexes were used, whichpermitted description of oceanographicconditions, and provided approximations ofecological processes that acted on smallerscales (Stenseth et al. 2003). Here, warm and

Fig. 1: Geographic location of the study area.Ubicación geográfica del área de estudio.


cool phases of the ENSO were determinedusing monthly averages of the the SouthernOscillation Index (SOI) and the Multivariate ElNiño Index (MEI) for the study period (1996-2003), from the Bureau of Metereology,Australia (www.bom.gov.au/climate/current/)and Climate Diagnostic Center of NOAA(www.cdc.noaa.gov/~kew/MEI/mei.html),respectively. Information on the temporalvariability of upwelling events in the region(23-25º S), was obtained from the monthlyaverage index of upwelling (offshore Eckmantransport, OET) between 1996 and 2001,obtained from the Pacific EnvironmentalLaboratory (PFEL, (www.pefg.noaa.gov/products/PFELindices.html). A detaileddescription of this calculation, andcharacteristics of the area of influence of theSOI, MEI and OET indexes have beenpresented by Navarrete et al. (2002).

Patterns of distribution and abundance of sub-tidal kelp assemblages

The spatial distribution of populations of M.integrifolia and L. trabeculata was evaluatedseasonally (four t imes a year includingsummer, fall, winter, and spring) using fourpermanent transects laid perpendicular to thecoast between the shoreline and 15 m depth,including the entire ranges of distribution of thekelp assemblage. The transects were 160 m inlength and one meter in width, and weresubdivided every 10 m to give 17 samplingunits of 10 m2. Juvenile and adult sporophyteswere counted in each sampling unit. Juvenilesporophytes of M. integrifolia y L. trabeculatawere plants with up to two lanceolate andlaminar fronds without reproductive structures,and maximum holdfast diameter of ≤ 1cm.Sporophyte densities were expressed as thenumber of sporophytes per 10 m2. Fertilesporophytes were recognized by the presence ofsori on the sporophylls of M. integrifolia, or onthe fronds of L. trabeculata.

The relative abundance and cover ondifferent types of substrate in the study areawere visually estimated in each sampling unitat the time of each seasonal sampling in orderto estimate the abundance of substrate suitablefor settlement of reproductive propagules.Substrate classifications included: (1) “barrenground” dominated by crustose calcareous

coralline algae and two species of sea urchins(Tetrapygus niger Molina and Loxechinus albusMolina), (2) boulder fields, (3) consolidatedrock, and (4) shell sand. The abundance of kelpspecies on the different substrates was alsoquantified.

Morphological variability of Lessonia trabecu-lata in the subtidal kelp assemblages

From 1996-1999, a total of 209 M. integrifoliaand 203 L. trabeculata sporophytes weresampled haphazardly from each kelp bed. Also,46 L. trabeculata sporophytes from below thecanopy of M. integrifolia were randomlysampled, to contrast their morphologies withsporophytes collected from monospecificstands of L. trabeculata. Five morphologicalvariables were determined after Vásquez(1991); these included the maximum diameter(cm) and weight (g) of holdfasts, the number ofstipes, total plant length (cm) and total drainedwet weight (kg) for each plant.

Kelp-herbivore interactions

The most conspicuous herbivorous grazer in theshallow rocky subtidal zone of the study site(and northern of Chile) is the sea urchinTetrapygus niger (Vásquez & Buschmann1997). Temporal changes in density of thisspecies, related to the 1997-1998 El Niño and1998-2000 La Niña, were determined byseasonal evaluation of 64 quadrats of 0.25 m2

each, using steel frames haphazardly tossedamong the perpendicular transects describedabove. The densities of sea urchins wereexpressed as the number of individuals per m2.A correlation analysis between the averagedensities of the herbivores T. niger and L. albus(another sea urchin frequent in the area, butless abundant; Vásquez & Vega 2004) and theaverage densities of M. integrifolia and L.trabeculata, was carried out to evaluate thepotential effect of herbivory on the spatio-temporal patterns and interannual variation inabundance of kelps.

Statistical methods

A nested analysis of variance (ANOVA) usingthe year as the main variable and seasons of theyear as nested factors was used to evaluate the

38 VEGA ET AL.

hypothesis that ENSO generated interannualvariability in patterns of abundance of M.integrifolia and L. trabeculata . For this,transects were considered as replicates,averaging the 10 m2 quadrats within eachtransect. The nested analyses of variance(ANOVA) was done after visual determinationof normality of the data and homocedasticity ofvariances by means of Bartlett tests (Sokal &Rohlf 1981), using SYSTAT 8.0® computationalsoftware for Windows; transformations (Logabundance + 1) were applied when necessary toimprove homoscedasticity (Sokal & Rohlf1981). An a posteriori Tukey test (Sokal &Rohlf 1981) was used order to determine whichgroups differed from others. The year 2000 wasexcluded from the analyses of abundance ofjuveniles of M. integrifolia since no juvenileswere found that year. The relationship betweenpopulation variables and the substrate, andherbivore abundance (sea urchins) was examiendusing Pearson correlation analyses (Sokal &Rohlf 1981).

A mult ivariate discr iminate funct ionanalysis was applied to compare morphologiesof the L. trabeculata sporophytes betweeninside and outside of the M. integrifoliacanopy using SYSTAT 8.0. Discriminatanalysis has been previously used to evaluatemorphological variability between populationsof M. integrifolia (Druehl 1978, Druehl &Kemp 1982).

RESULTS

Oceanographic conditions

The in situ sea temperature showed a seasonalpattern, with warm water between Decemberand March (summer) and cool water betweenJune and September (winter) (Fig. 2A). Duringthe study period between April 1997 and March1998 the seawater was unusually warm, withmaximum positive thermal anomaliesfluctuating between + 2 and + 2.5 °C. Anexception occurred between August andNovember 1997 when upwelling eventslowered the seawater temperatures, interruptingthe anomalous warm period. Immediatelyafterward, beginning in April 1998, cooling ofthe water began with weak, moderate, andstrong La Niña event when the seawater

anomaly ranged between -0.5 and -1.5 °C untilthe end of 2000 (Fig. 2A). The southernoscillation index (SOI, Fig. 2B) and themultivariate El Niño index (MEI, Fig. 2B)showed normal conditions in 1996 lasting untilsummer 1997. The El Niño event was clearbetween May 1997 and March 1998, coincidingwith the thermal anomaly detected by the insitu temperature records (Fig. 2A). Followingthe nearly normal, weakly-cold period of 1998-2000, a new warmer period was observedbetween April 2002 and April 2003, which wasof low to moderate intensity (Fig. 2B), casusinga positive thermal anomaly of 1 ºC. Meanvalues for the upwelling index (OET) werealways positive during the study period,showing the persistence over time of offshoreEkman transport conditions in the region (Fig.2C). The upwelling index showed greateroffshore transport between September andDecember (spring), and lower intensitiesbetween April and July (Fig. 2C). The highestupwelling activity occurred during the spring of1996, decreasing significantly in May 1997 atthe beginning of the 1997-1998 El Niño.Nevertheless, the Ekman transport remainedactive, constant, and intense between July 1997and February 1998 (Fig. 2C) during themaximum thermal anomalies of the 1997-1998El Niño (see also Ulloa et al. 2001, Navarreteet al. 2002).

Patterns of spatial distribution of subtidal kelpassemblages

Under “normal” oceanographic conditions(winter 1996 to summer 1997), the kelpassemblage formed by M. integrifolia and L.trabeculata at Caleta Constitución wasdistributed from 2 to 15 m depth, although thetwo kelp species demonstrated differentbathymetric distributions. The maximumabundance of M. integrifolia occurred atonshore depths, between 5-8 m, while themaximum abundance of L. trabeculataoccurred between 8 and 13 m (Fig. 3A).Between 9 and 11 m depth, both kelp speciesreached similar abundances (Fig. 3A). Thepercentage of consolidated rocky substratumper sampling unit was correlated significantlyand positively with kelp abundance (Pearson r= 0.74, P < 0.001). There were no significanttemporal modifications in the form of the


Fig. 2: Seawater temperature to 3 m depth into of kelp assemblage (A), Multivariate El Niño (MEI)and Southern Oscillation (SOI) indexes (B), and upwelling index (Eckman transport, OET) (C)during the study period.Temperatura del agua de mar a 3 m de profundidad dentro del ensamble de huiros (A), índices Multivariado de El Niño(MEI) y de la Oscilación del Sur (SOI) (B) y índice de surgencia (Transporte de Ekman, OET) (C) durante el período deestudio.

substrate during the study period over thelength of the bathymetric gradient studied. Thedensity of M. integrifolia decreased in shoalbottoms onshore as the percentage of barrenground covered with crustose coralline algaeincreased (Fig. 3B). In contrast, from 13 m

depth to offshore, the frequency of shell sandincreased, marking the deeper limit of kelpdistribution due to a decrease in consolidatedrocky bottom (Fig. 3B). At depths greater than15 m shell sand completely covered the bottomand neither kelp species was present.

Sou

them

Osc

illa

tion

Ind

ex (

SO

I)

Multiva ria te E

l Niño Index (M

EI)

40 VEGA ET AL.

Patterns of temporal distribution of subtidalkelp assemblages

The density of M. integrifolia adult sporophytesdiffered significantly (F6,21 = 35.40; P < 0.001)between years in which measurements were made(Fig. 4A). The seasonal patterns of abundance ofadult sporophytes differed significantly amongyears (F21,84 = 8.57, P < 0.001), particularlyduring the 1997-1998 (El Niño event) and the1999-2000 (La Niña event). Paradoxically thepassage of the 1997-1998 El Niño coincided withan increase in the abundance of adult sporophytesof M. integrifolia. Between fall 1999 and spring2000 (Fig. 4B) no M. integrifolia juveniles were

Fig. 3: Spatial patterns of abundance of adult sporophytes of Macrocystis integrifolia and Lessoniatrabeculata (A) and relative frequency of different substrates across the bathymetric profile in thestudy area (B) in no El Niño condictions between 1996-1997. Data are means ± SD.Patrones espaciales de la abundancia de esporofitos adultos de Macrocystis integrifolia y Lessonia trabeculata (A) yfrecuencia relativa de los distintos sustratos a lo largo del perfil batimétrico en el área de estudio (B), durante condicionesno El Niño entre 1996-1997. Los datos corresponden a medias ± DE.

Den

sity

(s

poro

phyt

es 1

0 m

-2)

Sub

stra

te (

%)

Depth (m)

Depth (m)

Macrocystis integrifolia

Lessonia trabeculata

Barren ground

Boulders

Sand and shells

Consolidated rocky

observed in the sampling units (10 m2), not in thestudy area, where additional exploratory divingwas carried out. Aside from this period, juvenileM. integrifolia were present throughout the yearwithout a defined seasonal pattern (Fig. 4B).Significant seasonal increases or decreases (F18,72

= 5.63, P < 0.001) in the long term abundances ofjuveniles appeared to be determined by theintensity of upwelling events during the 1997-1998 El Niño, based on the significant decreasesin adult sporophytes (1999) and characteristics ofthe re-establishment process of the M.integrifoliapopulation (2001-2003).

Seasonal patterns in the abundance of adultL. trabeculata sporophytes differed significantly


Fig. 4: Temporal patterns in the abundance of adult (A) and juvenil (B) of sporphytes of Macrocys-tis integrifolia and adult (C) and juvenil (D) of sporophytes of Lessonia trabeculata. Data aremeans ± 2EE.Patrones temporales en la abundancia de esporofitos adultos (A) y juveniles (B) de Macrocystis integrifolia y de esporofi-tos adultos (C) y juveniles (D) de Lessonia trabeculata. Los datos corresponden a medias ± 2EE.

(F21,84 = 88.18, P < 0.001) between years, but incontrast with M. integrifolia, the populationmaintained a mean annual abundance of about3.9 ± 1.5 plants per 10 m2 over the entire periodof the study. The 1997-1998 El Niño negativelyaffected the abundance of L. trabeculata inspring 1997 and summer 1998, while the 1998-2000 La Niña increased the abundances (Fig.4C). The abundance of juveniles L. trabeculatawas significantly higher in spring (F21,84 =193.95, P < 0.001). In spite of the preceding, there-establishment of adult sporophytes after the1997-1998 El Niño and the mortality of theseplants due to herbivore pressure (1999-2001)modified the seasonal pattern of abundance ofjuveniles between years (Fig. 4D).

Interannual variability of spatial patterns ofsubtidal kelp assemblages

The disjunct pattern of distribution of kelp overthe bathymetric profile was persistent over the

Den

sity

(ju

veni

le s

poro

pyte

s 10

m-2

)D

ensi

ty (

adul

t sp

orop

ytes

10

m-2

)eight years of the study. Nevertheless, thespatial patterns of abundance of the adult andjuvenile sporophytes of M. integrifolia over thebathymetric gradient differed for adult andjuvenile sporophytes among years (Fig. 5). Thecontinuous incorporation of M. integrifoliajuveniles to the system between 1996 and 1999permitted the maintenance of spatialdistribution patterns of the adult sporophytes.Although during the transition period betweenthe El Niño and La Niña events (1998) anincrease was detected in juveniles over thelength of the bathymetric profile, the patternsof distribution and abundance of the adultsporophytes were not altered during thefollowing year (1999). During 2000 a few shoaladult sporophytes (1-2 m depth) remainedunder the L. trabeculata canopy (> 10 m depth)in the study area; in contrast, no sporophytejuveniles were detected (Fig. 5). Re-establishment of the subtidal kelp M. integrifoliaoccured by successful recruitment, demonstrated

Macrocystis integrifolia Lessonia trabeculata

42 VEGA ET AL.

Fig. 5: Interannual variability patterns in the average abundance of adult and juveniles sporophytesof Macrocystis integrifolia along bathimetric profile.Patrones de variabilidad interanual de la abundancia promedio de esporofitos adultos y juveniles de Macrocystis integrifo-lia a lo largo del perfil batimétrico.

Den

sity

(sp

orop

hyte

s 10

m-2

)by the establishment of juveniles whichsurrounded the few surviving adult sporophytes,and generating a nucleus which expandedtowards the extremes of the bathymetric gradient(2001, Fig. 5). New recruitment of juvenilesporophytes in following years expanded thekelp (e.g., 2002-2003), until a kelp forest wasformed which was similar to that observed at thebeginning of this study (Fig. 3 and 5).

The patterns of abundance of the adult andjuvenile sporophytes of L. trabeculata differedover the bathymetric gradient between years(Fig. 6). The spatial pattern of abundance of L.trabeculata became modified during 2000 atthe end of the 1998-2000 La Niña and notduring the 1997-1998 El Niño (Fig. 6). Over

the eight years of the study, the maximumabundances of adult sporophytes occured at thelimits of depth of its distribution, with thejuveniles occurring over the entire bathymeticdistribution of this kelp (Fig. 6).

Reproductive phenology of subtidal kelpassemblages

Adult sporophytes of M. integrifolia and L.trabeculata with reproductive structures(sporophylls and sori on the fronds, respectively)were present throughout the entire study period(Fig. 7). During the 1997-1998 El Niño, thepercentage of reproductive plants of both kelpspecies remained above 70 %. During the 1999-



Fig. 6: Interannual variability patterns in the average abundance of adult and juveniles sporophytesof Lessonia trabeculata along bathimetric profile.Patrones de variabilidad interanual de la abundancia promedio de esporofitos adultos y juveniles de Lessonia trabeculata alo largo del perfil batimétrico.

Herbivore-kelp interactions

The sea urchin T. niger was the mostconspicuous herbivore at Caleta Constitución,coexisting with another, less abundant urchin, L.albus. The temporal patterns of abundance of T.niger showed three significant (F6,21 = 18.032, P< 0.001) maxima over the study period, whichwere different from each other (Fig. 8). The seaurchins showed low levels of abundancebetween 1996 and 1999, including the 1997-1998 El Niño (Fig. 8). During the 1998-2000 LaNiña (fall 1999-spring 2000) the mean density ofblack urchins increased three fold between 1996and 1998 (Fig. 8). During 2000 the black sea

2000 La Niña, all of the few sporophytes of M.integrifolia (average densities of 0.1 to 0.6individuals 10 m-2) were reproductive (Fig. 7A),while the percentage of fertile sporophytes of L.trabeculata remained above 75 % (Fig. 7B).During 2001-2002 the percentage of fertilesoporophytes of M. intergrifolia was less, as aconsequence of the increases in infertile juvenilesporophytes as the population became re-established (Fig. 7A). Between 2001 and 2003 thedecrease in fertile L. trabeculata sporophytes byincorporation of juveniles was markedly seasonal(summer-fall 2001, and fall 2003), however, thefrequency of reproductive plants was maintainedover 50 % (Fig. 7B).

Den

sity

(sp

orop

hyte

s 10

m-2

)


44 VEGA ET AL.

urchins formed herds over hard substrates atshoal depths from 8 to 10 m depth. This changein spatial-temporal patterns of abundance of T.niger coincided with the local extinction of theM. integrifolia population and the decrease inabundance of L. trabeculata at its depth limit.An inverse and significant correlation suggestedthat the density of juvenile and adult M.integrifolia sporophytes decreased with anincrease in abundance of T. niger (Tabla 1). Incontrast, non-significant correlations occurredbetween T. niger and L. trabeculata or betweenL. albus and both kelp species (Tabla 1).Beginning in 2001, the abundance of T. nigerbegan to decrease until the end of 2003, givingvalues similar to those encountered between1996 and 1999 (Fig. 8).

Fig. 7: Reproductive frecuencies of sporo-phytes of Macrocystis integrifolia (A) and Les-sonia trabeculata (B) during study period.White bars indicate fertile sporophytes andblack bars indicate infertile sporophytes.Frecuencia de esporofitos reproductivos de Macrocystis in-tegrifolia (A) y Lessonia trabeculata (B) durante el perio-do de estudio. Barras blancas indican esporofitos fértiles ybarras negras indican esporofitos sin estructuras reproduc-tivas.

Fre

cuen

cy (

perc

enta

ge f

erti

le s

poro

phyt

es)

TABLE 1

Pearson correlation coefficient (probability inparéntesis) between sea urchins and kelp

abundance. Significant association at alpha = 0.05

Coeficiente de correlación de Pearson (probabilidad enparéntesis) entre erizos de mar y abundancia de huirales.

Asociaciones significativas a un alfa = 0,05

Tetrapygus Loxechinusniger albus


Adults -0.67 -0.17(0.0001) (0.3631)

Juveniles -0.51 0.06(0.0036) (0.7374)


Adults -0.22 0.30(0.2343) (0.1075)

Juveniles -0.36 0.25(0.0507) (0.1868)

Morphological variability of Lessonia trabecu-lata in subtidal kelp assemblage

We observed two different morphologies of L.trabeculata as previously described by Vásquez(1992) within the assemblage of subtidal kelpover the bathymetric gradient at CaletaConstitución. These included a “bushy” morphconsisting of sporophytes with large numbers ofsmall stipes, where the total weight of the plantwas distributed among the many, highly flexiblestipes. A second “arborescent” morph, wasformed of sporophytes with few, long, thickstipes in which the weight of the plant wasconcentrated; these stipes showed littleflexibility. Discriminate function analysisshowed the number of stipes and the maximumdiameter of the holdfast to be the main functionsuseful in discriminating between the twoLessonia morphs. L. trabeculata sporophyteswith the bushy morph occurred mostly in standsdominated by M. integrifolia (Fig. 9).Conversely, monospecific beds of L. trabeculatawere made up of sporophytes with thearborescent morphology (Fig. 9), particularly atthe deeper limits of their distribution. Thebathymetric distribution pattern of the bushy andarborescent morphs of L. trabeculata foundwithin the kelp assemblage from 1996 to 1999was re-established at the end of the study period(winter and spring 2003).


Fig. 8: Temporal patterns in the abundance of Tetrapygus niger. Data are means ± 2EE.Patrones temporales en la abundancia de Tetrapygus niger. Los datos corresponden a media ± 2EE.

Sea

urc

hin

dens

ity

(ind

ivid

uals

m-2

)

Discriminant function 1

Dis

crim

inan

t fu

ncti

on 2

Fig. 9: Analysis of discriminate functions using five morphological parameters to differentiatejuvenile and adult plants of Lessonia trabeculata in presence/absence of Macrocystis integrifolia.Análisis de funciones discriminantes usando cinco parámetros morfológicos para diferenciar de plantas juveniles y adultasde Lessonia trabeculata en presencia/ausencia de Macrocystis integrifolia.

46 VEGA ET AL.

DISCUSSION

The structure of subtidal kelp assemblages onthe exposed rocky shores of northern Chile issimple, and represented by monospecific standsof bottom kelp L. trabeculata (Villouta &Santelices 1984, Vásquez 1992, Tala et al.2004). On semi-exposed and protected subtidalrocky shores, M. integrifolia forms the canopythat grows to the surface while the bottom kelp,L. trabeculata, forms the sub-canopy, althoughwith disjunct distributions over the bathymetricgradient. This is in contrast to subtidal kelpassemblages found at equivalent latitudes in theNorthern Hemisphere, where there ishierarchical organization through interspecificcompetition among the several components ofkelp forests (Dayton et al. 1992, 1999, Tegneret al. 1997).

Spatial patterns of abundance in subtidal kelpassemblages

It has been proposed that the segregatedpatterns of bathymetric distribution in kelpassemblages are a reflection of species-specificmorphological adaptations to wave exposure(Santelices & Ojeda 1984, Druelh & Kemp1986, Utter & Denny 1996), species-specificphysiological adaptations based on light andnutrient requirements for photosynthesis and/orgrowth (Druelh 1978, Gómez et al. 1997,Apprill & Lesser 2003), and on endogenousfactors such as circadian or circannual rhythmsthat respond differentially to environmentalchanges (Schaffelke & Lünning 1994).Interspecific competition has also beensuggested as a structural agent in kelpassemblages over bathymetric gradients (Reed& Foster 1984, Santelices & Ojeda 1984,Tegner et al. 1997). At Caleta Constitución, thehigher rate of colonization and growth of M.integrifolia during 2002-2003 produced anegative effect on the recruitment and growthof L. trabeculata juveniles between 2 and 7 mdepth. This appears to induce a modification ofthe morphology of the adult sporophytes of L.trabeculata under the M. integrifolia canopy.The potential effect of a M. integrifolia stand inreducing wave action and this, in turn,influencing L. trabeculata morphology insteadof or in addition to competition must beexplored. Hypotheses that explain the patterns

of distribution of M. integrifolia and L.trabeculata over bathymetric gradients are notexclusive. Species-specific morphological and/or physiological adaptations, as well asinterspecific competition may interact atdifferent depth levels of the assemblage toproduce a segregated pattern of distribution,generating different morphs of L. trabeculataover the range of bathymetric distribution. Thishypothesis needs to be tested in the future bymeans of in situ experimental removal andcompetitive exclusion experiments, in order toevaluate recruitment and species-specificgrowth rates.

Temporal patterns of abundance in subtidalkelp assemblages

The abundances of M. integrifolia and L.trabeculata differed markedly between yearsduring the study period. These annualdifferences are a reflection of modifications inseasonal patterns of both kelps. Temporalvariations in the abundances of kelp intemperate environments of the NorthernHemisphere are correlated with thermalanomalies coupled to annual temperatureoscillations. These co-vary inversely with theavailability of nutrients (Dayton et al. 1992),generating different seasonal patterns ofabundance (Dayton et al. 1999). Nevertheless,physical, (e.g., storms and swells) and/orbiological (e.g., pests, herbivory) disturbancesof low frequency and intensity produce breaksin spatial-temporal distributions (Tegner et al.1987, Dayton et al. 1998), adding additionalrandomness to long-term patterns ofabundance. Populations of M. integrifolia andL. trabeculata in northern Chile are formed byperennial and long-lived sporophytes, whichmaintain their levels of abundance during theyear, with seasonal variability in growth andreproduction (Buschmann et al. 2004, Tala etal. 2004). This apparent temporal stability(annual variability) in the population dynamicsof the South American kelp is, however,interrupted (interannual variability) by: (1)positive thermal anomalies during El Niño,which generate mortalities correlated withlatitude (Tomicic 1985, Camus 1994, Godoy2000), and (2) site-dependent recolonizationevents of varying intensity during cool andnormal years (Camus 1994, Martínez et al.


2003). In this context, our results have shownthat in the study area: (1) during the 1997-1998El Niño the patterns of abundance of both kelpdid not change significantly, (2) kelpproductivity during the 1998-2000 La Niñaevent was reduced to minumum levels due tothe extinction of M. integrifolia in shallowdepths and decrease in abundance of L.trabeculata, and (3) the re-establishment of thekelp assemblage occurred post La Niña, duringthe mild, and poorly documented 2002-2003 ElNiño event.

The temporal pattern of recruitment ofsporophytes differed between the two kelps.While M. integrifolia showed recruitmentthroughout the year (as in other wave-protectedenvironments, see Graham et al. 1997), L.trabeculata showed seasonal recruitmentduring the winter, producing greater abundanceof juveniles during the spring. Thesedifferences in recruitment pattern (annualversus seasonal) imply differing reproductivestrategies between the kelp species, which mayin part explain the temporal dynamics of theassemblage and require clarification throughapplication of experimental protocols in thefuture.

Spatial-temporal patterns of distribution insubtidal kelp assemblages

Spatial-temporal patterns of distribution andabundance of M. integrifolia and L. trabeculatadid not become significantly modified duringthe 1997-1998 El Niño.This is in contrast withlocal extinction processes during this El Niñodocumented for other kelp-dominated areas inPeru and Chile (Fernández et al. 1999, Godoy2000, Lleellish et al. 2001) and California(Ladah et al. 1999, Edwards 2004). Thepersistence of spatial and temporal patterns inkelp assemblages during the 1997-1998 ElNiño in the study area may be explained by thefrequency and intensity of coastal upwelling(González et al. 1998, Vásquez et al. 1998,Lagos et al . 2002), which buffers andminimizes superficial heating of the sea andimpoverishment of nutrients in littoral waters(González et al. 1998, Takesue et al. 2004).Based on our results it can be suggested thatthe persistence of kelp populations in the abovementioned upwelling areas during the 1997-1998 El Niño might function as local “sources”

which “export” propagules to other localities“sinks” without upwelling where massmortalities have occurred (Camus 1994).

The recovery rate of kelp populations inlocalit ies in which extinction processesoccurred as a result of the El Niño is favoredwhen there is a rapid transition to cool periodsor La Niña (Edwards 1994). La Niña conditionsreinforce coastal upwelling processes,generating conditions favorable for the growthand development of juvenile kelp sporophytes(Tegner et al. 1987, Dayton et al. 1998). Duringthe period of the present study, La Niña (1998-2000) conditions occurred almost immediatelyafter passage of the 1997-1998 El Niño.However, the spatial-temporal pattern ofdistribution de M. integrifolia and L.trabeculata became modified in the study areaduring the 1998-2000 La Niña due tosignificant changes in the patterns ofdistribution and abundance of the sea urchin T.niger during 1999-2000.

Kelp-herbivore interactions

An increase in grazing pressure wasdocumented as simultaneously occurring withwarming of coastal surface waters at lowlatitudes (10-23º S) of both Hemispheresduring the 1997-1998 El Niño (Halpin et al.2004). In this context, posit ive thermalanomalies and bathymetric migrations ofgrazers produce a sinergistic effect, causinglocal extinctions of Macrocystis spp. (Godoy2000, Llellish et al. 2001), and decreases inthe bathymetric range of L. trabeculata(Fernández et al. 1999, Vásquez & Vega2004). In contrast, the present study showedan absence of local extinctions during the1997-98 El Niño. A combination of “top-down” and “bottom-up” effects appear toregulate these ecosystemic changes, including(1) the 1997-1998 El Niño significantlydecreased the density of starfish between 2and 10 m depths, the bathymetric range withthe highest density of M. integrifolia (Vásquez& Vega 2004). These benthic organisms formthe most important guild of carnivores on theSE Pacific coastline (Vásquez & Buschmann1997). (2) Warming of surface waters in thestudy area, moderated by upwelling eventsduring 1997-1998, induced many sea urchinspawnings which produced successful

48 VEGA ET AL.

recruitment during the 1999-2000 La Niña(Vásquez & Vega 2004); (3) the dephase inlocal extinction of kelp populations two yearsafter the 1997-1998 El Niño occurredatypically during the 1999-2000 La Niña. Themass mortality of M. integrifolia in the studyarea thus seems to be a consequence of therelation of predator-prey abundances. Top-down and bottom-up regulation generated bythe El Niño in communities dominated byMacrocystis pyrifera in California haverecently been reviewed by Halpin et al (2004).

The survival of a few fertile sporophytesafter local extinctions of M. integrifolia in 2000appears to have been the main source ofreproductive propagules for the re-establishment of the subtidal assemblage atCaleta Constitución. Drifting rafts of kelp, and“seed banks” of microscopic dormant stagesmay be considered as complementary strategiesfor the re-establishment of assemblages of kelp(Dayton et al. 1992, Ladah et al. 1999,Buschmann et al. 2004, Edwards 2004)

Centers of upwelling may act to modify thelittoral biota, but in contrast with El Niñoevents, they act on a local scale. Permanentupwelling has an upwardly cascading or“bottom-up” regulation of the communities oncoastal ecosystems (Vásquez et al. 1998,Camus & Andrade 1999, Nielsen & Navarrete2004). The permanent subsidy of nutrient-richwaters and low temperature has beenconsidered important factors in the increase inbiodiversity and productivity of coastal zoneswhere it occurs (Bosman et al. 1987, Ormond& Banaimoon 1994, Nielsen & Navarrete2004). Our study suggests, as well, that areaswith permanent upwelling decrease the effectsof upper-layer warming generated by high-intensity El Niño events, permitting thepersistence of kelp populations. Here, thecorrespondence between intensity andfrequency of coastal upwelling during El Niñoevents may explain variability among effectsproduced in coastal communities by thisoceanographic event. In the present study area,the 1982-1983 El Niño caused mass mortalitiesof intertidal and subtidal kelp (Tomicic 1985),with a recovery time of over 10 years (Martínezet al. 2003). In contrast, superficial warmingduring the 1997-1998 El Niño did not modifythe spatial and temporal patterns of the coastalkelp assemblages at Caleta Constitución.

Infrequent and hard-to-predict disturbances,such as the significant increase in herbivoresduring the 1998-2000 La Niña event, furtheradd randomness to the spatial-temporal patternsof the distribution and abundance of organismsinhabiting communities dominated by kelp.Other poorly predictable biologicaldisturbances that document changes in patternsof abundance and distribution of kelp speciesinclude pests (Graham et al. 1997), and massmortalities of benthic grazers (Dayton et al.1998), as well as mortalities of high-levelpredators (Estes et al. 1998). Although coastalupwelling processes and large-scaleoceanographic events such as El Niño and LaNiña produce local variability, their effectshave been studied and documented separarelyboth on a temporal and spatial basis. Ourresults suggest the need for maintaining long-term studies, which allow integration ofphysical and biological processes on a localscale (e.g. , upwelling, predator-preyinteractions, plant-plant interactions, pests,mass mortalities), with low frequency, large-scale climatic event (El Niño-La Niña).

ACKNOWLEDGEMENTS

The authors are thankful for the collaborationreceived from D. Veliz, L.M. Pardo, C. Cerda,F. Veliz, J. Rivera, N. Godoy, E. Rojas, C.Ibacache, P. Bravo and N. Piaget during thedemanding days of diving research. Also theauthors thank S. Navarrete, M. Graham, M.Edwards and one anonymous reviewer forhelpful comments on the manuscript. This workwas supported by FONDECYT-SECTORIAL5960001, FONDAP 0 & BM N°3, FONDECYT1000044-1010706. This research is part ofMasters of Science Thesis of the first author, inthe Master Program in Marine Sciences at theUCN.

LITERATURE CITED

ALVEAL K, H ROMO & J VALENZUELA (1973)Consideraciones ecológicas de las regiones deValparaíso y de Magallanes. Revista de BiologíaMarina (Chile) 15:1-29.

APPRILL AM & MP LESSER (2003) Effects of ultravioletaradiation on Laminaria saccharina in relation todepth and and tidal height in the Goulf of Main.Marine Ecology Progress Series 256: 75-85.


BOSMAN AL, PAR HOCKEY & WR SIEGFRIED (1987)The influence of coastal upwelling on the functionalstructure of rocky intert idal communities.Oecologia 72: 226-232.

BUSCHMANN A, JA VÁSQUEZ, P OSORIO, E REYES,L FILUN, MC HERNÁNDEZ-GONZÁLEZ & AVEGA (2004) The effect of water movement,temperature and salinity on abundance andreproductive patterns of Macrocystis spp.(Phaeophyta) at different latitudes in Chile. MarineBiology 145: 849-862.

CAMUS PA (1990) Procesos regionales y fitogeografía enel Pacífico Suroriental: el efecto de “El Niño-Oscilación del Sur”. Revista Chilena de HistoriaNatural 63: 11-17. 1990.

CAMUS PA (1994) Dinámica geográf ica en laspoblaciones de Lessonia nigrescens Bory(Pheophyta) en el norte de Chile: importancia de laextinción local durante eventos El Niño de granintensidad. Revista de Investigaciones Científicasy Tecnológicas, Serie Ciencias del Mar (Chile) 3:58-70.

CAMUS PA & AN ANDRADE (1999) Diversidad decomunidades intermareales rocosas del norte deChile y el efecto potencial de la surgencia costera.Revista Chilena de Historia Natural 72: 389-410.

CAMUS PA, EO VÁSQUEZ, EO GONZÁLEZ & LEGALAZ (1994) Fenología espacial de la diversidadintermareal en el norte de Chile: Patronescomunitarios de variación geográfica e impacto delos procesos de extinción y recolonización post ElNiño 82/83. Medio Ambiente (Chile) 12: 57-68.

DAYTON PK (1985) The structure and regulation of somesouth American kelp communities. EcologicalMonographs 55: 447-468.

DAYTON PK, MJ TEGNER, PE PARNELL & PBEDWARDS (1992) Temporal and spatial patterns ofdisturbance and recovery in kelp forest community.Ecological Monographs 62: 421-445.

DAYTON PK, MJ TEGNER, PB EDWARDS & K RISER(1998) Slinding, ghost, and reduced expectations inkelp forest communities. Ecological Applications 8:309-322.

DAYTON PK, MJ TEGNER, PB EDWARDS & KLRISER (1999) Temporal and spatial scales of kelpdemography: the role of oceanographic climate.Ecological Monographs 69: 219-250.

DIECK TI (1993) Temperature tolerance and survival indarckness of kelp gametophytes (Laminariales,Phaeophyta): ecological and biogeographicalimplications. Marine Ecology Progress Series 100:253-264.

DRUELH LD (1978) The distribution of Macrocystisintegrifolia in British Columbia as related toenviroment parameters. Canadian Journal of Botany567: 69-79.

DRUELH LD & L KEMP (1986) Morphological andgrowth responses of of geographically isolatedMacrocystis integrifolia populations when grown ina common enviroment. Canadian Journal of Botany60: 1409-1413.

EDWARDS MS (2004) Estimating scale-dependency indisturbance impacts: El Niño and giant kelp forestsin the northeast Pacific. Oecologia 138: 436-447.

ESCRIBANO R (1998) Population dynamics of Calanuschilensis in the Chilean eastern boundary Humboldtcurrent. Fiheries Oceanography 7: 245-251.

ESCRIBANO R & IA MCLAREN (1999) Producción ofCalanus chilensis in the upwell ing area ofAntofagasta, northern Chile. Marine EcologyPregress Series 177: 147-156.

ESCRIBANO R, SA ROSALES & JL BLANCO (2004)Understanding upwell ing circulation offAntofagasta (northern Chile): a three-dimensionalnumerical-modeling approach. Continental ShelfResearch 24: 37-53.

ESTES JA, MT TINKER, TM WILLIAMS & DF DOAK(1998) Killer whale predation on sea otter linkingoceanic and nearshore ecosystem. Science 282:473-476.

FERNÁNDEZ E, C CÓRDOVA & J TARAZONA (1999)Condiciones del bosque submareal de Lessoniatrabeculata en la Isla Independencia durante elevento El Niño 1997-1998. Revista Peruana deBiología, Volumen Extraordinario: 47-59.

GÓMEZ I, G WEYKAM, H KLÖSER & H WIENCKE(1997) Photosybthetic l ights requeriment s ,metabolic carbon balance and zonation ofsublittoral macroalgae in King George Island(Antártica). Marine Ecology Progress Series 148:281-293.

GONZÁLEZ HE, VC ORTIZ & M SOBARZO (2000) Therole of faecal material in the particulate organiccarbon flux in the northern Humboldt Current (23ºS) before and during the 1997-1998 El Niño.Journal of Plankton Research 22: 499-529.

GODOY NE (2000) Macrocystis integrifolia(Laminariales, Phaeophyta) en el norte de Chile:distribución espacial y fauna asociada. Tesis paraoptar al Título de Biólogo Marino, Facultad deCiencias del Mar, Universidad Católica del Norte,Coquimbo, Chile. 58 pp.

GRAHAM MH, C HARROLD, S LISIN, K LIGHT, JMWATANABE & MS FOSTER (1997) Populationsdynamics of giant kelp Macrocystis pyrifera along awave exposure gradient. Marine Ecology ProgressSeries 148: 269-279.

HALPIN PA, PT STRUB, WT PETERSON & TRBAUMGARTNER (2004) An overview ofinteractions among oceanography, marineecosystems, climatic and human disruptions alongthe eastern margins of the Pacific Ocean. RevistaChilena de Historia Natural 77: 371-410.

HERNÁNDEZ-CARMONA G, D ROBLEDO & ESERVIERE-ZARAGOZA (2001) Effect of nutrientavailability on Macrocystis pyrifera recruitment andsurvival near its sourthern limit off Baja California.Botánica Marina 44: 221-229.

KAIN JM (1989) The season in the subtidal. BritishPhicologycal Journal 24: 203-215.

KREBS CJ (1989) Ecological methodology. HarperCollins Publishers, New York, New York, USA.654 pp.

LADAH LB, JA ZERTUCHE-GONZÁLEZ & GHERNÁNDEZ-CARMONA (1999) Giant kelp(Macrocystis pyrifera, Pheophyceae) recruitmentnear its sourthern limit in baja california after massdissapearance during ENSO 1997-1998. Journal ofPhycology 35: 1106-1112.

LAGOS NA, ID BARRÍA & P PAOLINI (2002)Upwelling ecosystem of northern Chile: integratingbenthic ecology and coastal oceanography throughtremote sensing. In: Castilla JC & JL Largier (eds)The oceanography and ecology of the nearshore andbays in Chile: 117-141. Ediciones UniversidadCatólica de Chile, Santiago, Chile.

LLEELLISH J, E FERNÁNDEZ & Y HOOKER (2001)Disturbancia del bosque submareal de Macrocystispyrifera durante El Niño 1997-1998 en la Bahía dePucusana. In: Alveal K & T Antezana (eds)Sustentabilidad de la biodiversidad. Un problemaactual: bases científico técnicas, teorizaciones y

50 VEGA ET AL.

proyecciones: 331-350. Ediciones Universidad deConcepción, Concepción, Chile.

MARTÍNEZ EA (1999) Latitudinal differences in thermaltolerance among microcopic sporophytes of thekelp Lessonia nigrescens (Phaeophyta:Laminariales). Pacific Science 53: 74-81.

MARTÍNEZ EA, L CÁRDENAS & R PINTO (2003)Recovery and genetic diversity of the intertidal kelpLessonia nigrescens 20 years after El Niño 1982-83. Journal of Phycology 39: 504-508.

MARÍN VH, R ESCRIBANO, R DELGADO, LEOLIVARES & G HIDALGO (2001) Nearshorecirculation in a coastal upwelling site off thenorthern Humboldt Current System. ContinentalShelf Research 21: 1317-1329.

MORENO C & JP SUTHERLAND (1982) Physical andbiological processes in a Macrocystis pyriferacommunity near Valdivia, Chile. Oecologia 55: 1-6.

NAVARRETE SA, B BROITMAN, EA WIETERS, GRFINKE, RM VENEGAS & A SOTOMAYOR(2002) Recruitment of intertidal invertebrates in thesoutheast Pacific: interannual variability and the1997-1998 El Niño. Limnology and Oceanography47: 791-802.

ORMOND RFG & SA BANAIMOON (1994) Ecology ofintert idal macroalgae assemblages on theHadramout coast of sourthern Yemen, an area ofseasonal upwelling. Marine Ecology Pregress Series105: 105-120.

REED DC & MS FOSTER (1984) The effects of canopyshading on algal recruitment and growth in a giantkelp forest. Ecology 65: 937-948.

SANTELICES B & FP OJEDA (1984) Population dynamicof coastal forest of Macrocystis pyrifera in PuertoToro, Isla Navarino, sourthern Chile. MarineEcology Progress Series 14: 175- 183.

STENSETH NC, G OTTERSEN, JW HURRELL, AMYSTERUD, M LIMA, K CHAN, NG YOCCOZ &B ADLANDSVIK (2003) Studyng climate effects onecology through the use of climate indices: the NorthAtlanthic Oscillation, El Niño Southern Oscillationand beyond. Proceedings of the Royal Society ofLondon, Biological Sciences 270: 2087-2096.

SCHAFFELKE B & K LÜNING (1994) A circannualrhythm controls seasonal growth in the kelpsLaminaria hyperborea and L. digitata fromHelgoland (North Sea). European Journal ofPhycology 29: 49-56.

SCHEIBLING RE, AW HENNIGAR & T BALCH (1999)Destructive grazing, epiphytism and disease: thedynamic of sea urchins-kelp interaction in NovaScotia. Canadian Journal Fisheries and AquaticsScience 56: 1-15.

SOKAL RR & FJ ROHLF (1981) Biometry: principles andpractice of statistical in biological research. W.H.Freeman & Company, San Francisco, California,USA. 776 pp.

SYSTAT (1992) Statistics. Version 8.0 ed. SYSTAT Inc.,Evanston, Illinois, USA.

TALA F, M EDDING & J VÁSQUEZ (2004) Aspect ofthe reproductive phenology of Lessonia trabeculata(Laminariales: Phaeophyceae) from threepopulations in northern Chile. New Zealand Journalof Marine and Freshwater Research 38: 255-266.

TAKESUE RK, A VAN GEEN, JD CARRIQUIRY, EORTIZ, L GONIDEZ-ORTA, I GRANADOS, MSALDÍVAR, L ORTLIEB, N GUZMÁN, JC

CASTILLA, M VARAS, M SALAMANCA & CFIGUEROA (2004) Influence of coastal upwellingand ENSO on nearshore water along baja Californiaand Chile: shore-based monitoring during 1997-2000. Journal of Geophysical Research-Oceans 109:3009, doi: 10.1029/2003JC001856.

TEGNER MJ, PK DAYTON, PB EDWARDS & KLRISER (1997) Large-scale, low frequencyoceanographic effects on kelp forest succession: atale of two cohorts. Marine Ecology Progress Series146: 117-134.

TOMICIC JJ (1985) Efectos del fenómeno de El Niño1982-1983, en las comunidades litorales de lapenínsula de Mejillones. Investigaciones Pesqueras(Chile) 32: 209-213.

ULLOA O, R ESCRIBANO, S HORMAZÁBAL, RQUIÑÓNEZ, M RAMOS & R GONZÁLEZ (2001)Evolution and biological effects of the 1997-1998El Niño in northern Chile. Geophysical ResearchLetters 28: 1591-1594.

UTTER BD & MW DENNY (1996) Wave-induced forceson the giant kelp Macrocystis pyrifera (Agardh):Field test of a computacional model. Journal ofExperimental Biology 199: 2645-2654.

VÁSQUEZ JA (1991) Variables morfométricas yrelaciones morfológicas de Lessonia trabeculataVillouta & Santelices, 1986, en una poblaciónsubmareal del norte de Chile. Revista Chilena deHistoria Natural 64: 271-279.

VÁSQUEZ JA (1992) Lessonia trabeculata, a subtidalbottom kelp in northern Chile: a case study for astructural and geographical comparason. In:Seeliger U (ed) Coastal plants of Latin America:77-89. Academics Press, San Diego, California,USA.

VÁSQUEZ JA (1993) Patrones de distribución depoblaciones submareales de Lessonia trabeculata(Laminariales, Phaeophyta) en el norte de Chile.Facultad de Ciencias del Mar, Universidad Católicadel Norte, Serie Ocasional (Chile) 2: 187-211.

VÁSQUEZ JA & A BUSCHMANN (1997) Herbivore-kelpinteractions in Chilean subtidal communities: areview. Revista Chilena de Historia Natural 70: 41-52.

VÁSQUEZ JA & JMA VEGA (2004) El Niño 1997-1998en el norte de Chile: efectos en la estructura y en laorganización de comunidades submarealesdominadas por algas pardas: 119-135. In: Avaria S,J Carrasco, J Rutland & E Yáñez (eds) El Niño-LaNiña 1997-2000 sus efectos en Chile. CONA,Valparaíso, Chile.

VÁSQUEZ JA, PA CAMUS & FP OJEDA (1998)Diversidad, estructura y funcionamiento deecosistemas rocosos del norte de Chile. RevistaChilena de Historia Natural 71: 479-499.

VÁSQUEZ JA, E FONCK & JMA VEGA (2001)Diversidad, abundancia y variabilidad temporal deensambles de macroalgas del submareal rocoso delnorte de Chile. In: Alveal K & T Antezana (eds)Sustentabilidad de la biodiversidad. Un problemaactual: bases científico técnicas, teorizaciones yproyecciones: 351-365. Ediciones Universidad deConcepción, Concepción, Chile.

VILLOUTA E & B SANTELICES (1984) Estructura de lacomunidad submareal de Lessonia (Phaeophyta,Laminariales) en Chile norte y central. RevistaChilena de Historia Natural 57: 111-122.

Associate Editor: Sergio NavarreteReceived April 14, 2004; accepted December 1, 2004

Documents

Population biology of the subtidal kelps Macrocystis ...temporales de Tetrapygus niger (erizo negro), el pastoreador bentónico más conspicuo del norte de Chile, produjo la extinción