www.elsevier.com/locate/marpolbul

Marine Pollution Bulletin 47 (2003) 325–330

SeaWiFS satellite monitoring of oil spill impact onprimary production in the Gal�aapagos Marine Reserve

Stuart Banks

Charles Darwin Research Station, Puerto Ayora, Isla Santa Cruz, Gal�aapagos, Ecuador

Abstract

Near daily satellite monitoring of ocean colour using sea viewing wide angle of field viewing sensor (SeaWiFS) allowed the

oceanic and near coastal chlorophyll-a distributions to be followed across the Gal�aapagos Marine Reserve (GMR) from space. In the

aftermath of the Jessica spill early indications suggested that, compared to the three preceding years 1998–2000, local chlorophyll

concentrations over January 2001 were elevated across the Gal�aapagos Marine Reserve [Biological Impacts of the Jessica Oil Spill on

the Gal�aapagos Environment: Preliminary Report. Charles Darwin Foundation, Puerto Ayora, Gal�aapagos, Ecuador, 2001]. At the

time of the spill the central and eastern extent of the archipelago was experiencing a spatially extensive moderate bloom event (0.5–

2.5 mg m�3 chl-a) extending over the central islands, including the source of the spill and areas of known impact such as the islands

of Santa F�ee, eastern Santa Cruz and Floreana directly in the advection path.

Further investigation shows that chlorophyll across the affected regions of western San Crist�oobal, Santa F�ee, southeast Santa

Cruz, eastern Floreana and eastern Isabela declined in the week directly following the spill event, yet rose in the successive month to

levels analogous to preceding years. Although there may have been a localised effect of the spill upon near coast phytoplankton

primary production in the short term, the observed variance in the weeks following the spill was not significant in comparison to the

normal high variation between years and within the El Ni~nno/Southern Oscillation signal.

� 2003 Elsevier Science Ltd. All rights reserved.

Keywords: Gal�aapagos; Jessica; Phytoplankton; Marine reserve; Hydrocarbons; Primary production; SeaWiFS

1. Introduction

Within an inherently variable marine system such as

Gal�aapagos (Houvenghel, 1974) it might be expected that

phytoplankton populations have a certain tolerance or

viability against natural stresses (predominantly tem-

perature and nutrient deprivation effects) under seasonal

and El Ni~nno/Southern Oscillation (ENSO) conditioning.

However, in the history of Gal�aapagos, phytoplanktonpopulations have not been subject to novel anthropo-

genic stressors of the magnitude of the Jessica spill

event, particularly bioaccumulation and toxic effects.

Phytoplankton, alongside coral and macrophytic algae,

which are spatially restricted in the GMR and much

more localized, provide the primary influx of energy

to the coastal food web. Under normal conditions,

the physical and biochemical conditions that defineGal�aapagos marine ecosystems are largely driven by the

E-mail address: sbanks@fcdarwin.org.ec (S. Banks).

0025-326X/03/$ - see front matter � 2003 Elsevier Science Ltd. All rights re

doi:10.1016/S0025-326X(03)00162-0

surface expression of upwelled nutrient rich EquatorialUndercurrent waters upon the western coasts of the

archipelago and warmer nutrient deprived surface flow

under wind forcing from the southeast. The resulting

oceanographic conditioning tends to generate local bio-

geographic patterns in fish, macroinvertebrate and ses-

sile species, and presumably must influence local

plankton species groupings, their relative abundances

and their life history strategies. Perturbations to thefood web at the phytoplankton trophic level cause major

impacts upon marine ecosystems, with the extent of

these impacts depending on the magnitude of changes to

phytoplankton, the species groups involved, and water

properties, such as concentrations of dissolved organic

compounds, redox potential, temperature, salinity,

thermocline formation and stability, current advection,

nutrient loading etc. (Daly and Smith, 1993).In comparison to chronic emissions, for example from

port zones and drilling operations, large spill events

contribute a very small proportion of the total oil input

to the world�s oceans. Sustained low-level contamination

served.

326 S. Banks / Marine Pollution Bulletin 47 (2003) 325–330

such as that observed from drill heads has been shown to

produce long-term changes in marine systems with the

research focus upon toxic and enrichment effects upon

the marine benthos.In this case, the concern perhaps lies in oil entrain-

ment in protected bays and high risk sites close to the

release area that increase local toxic exposure and may

inhibit photosynthetic processes. Following changes

in spectral properties of light to depth, and/or a toxic

effect at high concentrations, it is known that oil layer-

ing reduces light transmission and alters its spectral

properties, which theoretically may affect production,particularly upon stratified water columns with subsur-

face chlorophyll maxima (Angel et al., 1982). Oil degrad-

ing bacteria may actively compete with phytoplankton

populations for nutrients that are then, in turn, grazed

by ciliates altering the redox environment under organic

enrichment. Tentative conclusions by the National Fish-

eries Service after the venting of heavy fuel oil from the

December 1976 Argo Merchant Spill in Nantucket, sug-gested that it triggered a decrease in phytoplankton

abundance yet also a local bloom of toxic blue-green

algae (Kerr, 1977). This type of effect has been observed

in eutrophic waters on scales that have threatened entire

ecosystems and fisheries resources. Enclosed ecosystem

experiments by Davenport (1982) have shown that at low

hydrocarbon concentrations (<40 ng g�1) microflagel-

lates were stimulated whereas diatom numbers fell, whileat higher hydrocarbon concentrations (>100 ng g�1) phy-

toplankton production was largely unaffected. However

zooplankton populations, particularly key predator

groups such as chaetognathes, were greatly reduced.

Observations from other spill accidents suggest that the

oil disperses rapidly in open water coastal environments

such as Gal�aapagos but can have persistent toxic effects

for many years in protected coves and mangroves (Kerr,1977).

The adaptation of phytoplankton to sublethal expo-

sure to crude oil is poorly understood and may be

complicated by the use of chemical dispersants for oil

spill remediation. An analysis of phytoplankton com-

munities three years after a crude oil spill in the Cha-

nomi creek, lower Niger Delta system, showed no

adverse effects from use of a silicon based dispersant,nor an effect upon biomass and photosynthetic ability of

phytoplankton communities against untreated and

treated oil (Nwadiaro, 1990). A study after the 1993 spill

in the Bombay High region, India, showed that a few

phytoplankton species such as Nitzschia sp. were dam-

aged by black poly-hydrocarbon coating, and that levels

of chlorophyll were patchy and unevenly distributed

(Gajbhiye et al., 1993). Studies upon exposure of Is-

ochrysis galbana, a marine phytoflagellate, to crude oil

showed significant increases in heat shock protein pro-

duction indicative of stress, particularly when exposed

to naphthalene, an aromatic hydrocarbon found in oil

spills and drilling mud (Wolfe et al., 1999). Concentra-

tions as low as 1–2 mg dm�3 of oil have been found in

laboratory tests to induce chlorophyll-a inhibition, al-

though no specific changes in the composition of specieswere observed (Padros et al., 1999).

Direct and indirect impacts upon phytoplankton

from oil pollution remain poorly quantified due to the

complications presented by inherent patchiness, variable

grazing by zooplankton, and the variability in the

hydrocarbon composition between spill events and lab-

oratory tests comparisons (including the use of unreal-

istically high treatments of oil). Additionally theoceanographic variation structuring the phytoplankton

in the water column complicates representative field

sampling (Davenport, 1982). Here, use of daily satellite

SeaWiFS coverage, circumvents that monitoring pro-

blem by directly inferring phytoplankton concentrations

from chlorophyll-a derivations (to 2/3rd of the euphotic

depth) as commonly applied in in situ productivity

studies (Chretiennot et al., 1993).Analysis of the SeaWiFS imagery collected during the

week preceding the Jessica oil spill to the west of Puerto

Baquerizo Moreno (89.62095W, 0.89455S), Isla San

Crist�oobal, showed that the central and eastern part of

the archipelago was experiencing a moderate phyto-

plankton bloom event (0.5–2.5 mg m�3 Chl-a) that was

advected in surface waters under wind forcing to the

west (Fig. 1). Early indications suggested that, eightdays after the release of oil, chlorophyll levels had de-

clined substantially across the archipelago (Banks,

2001). Here that analysis is elaborated upon and the

time series analysis extended to successive weeks after

the event. This focuses upon the worst-affected coastal

sites and the assumed area of greatest spatial impact in

the open water advection path between Bah�ııa Naufragio

(San Crist�oobal) and southeastern Santa Cruz.By comparing areas over the period immediately

preceeding and after the spill, this study aims to test for

localized depression of chlorophyll close to the site of

release and worst-affected coastal regions as an indicator

of toxicity or smothering effects. Since the Gal�aapagos

phytoplankton standing stock is normally subject to

strong ENSO variability, a comparison of the same

month in previous years is included in order to acertainthe significance of any observed changes.

2. Methods

The NASA SeaWiFS spectrophotometric sensor

mounted on the commercial ORBIMAGE satellite Se-

astar detects visible light radiation over eight channels atwavelengths relevant to the derivation of chlorophyll-a

in the water column across the world�s oceans. Traveling

at 705 km above the earth�s surface in a sun synchro-

nous orbit it collects global area coverage (GAC) data at

Fig. 1. Level 1-A Georeferenced chlorophyll abundances derived from

ocean colour observations taken over the duration of the spill from the

SeaWiFS sensor. Black areas correspond to cloud masking at the time

of midday overpass. (A) 9th January 2001; (B) 16th January 2001

(grounding date); (C) 24th January 2001.

S. Banks / Marine Pollution Bulletin 47 (2003) 325–330 327

4 km resolution in a bi-daily global repeat pattern and

relays that information to the NASA Goddard Space

Flight Center where it is archived and made available

for research and educational use (Feldman, 2002;

Froidefond et al., 1998; Keiner and Brown, 1999; Joint

andGroom, 2000; Behrenfeld et al., 2001;Robinson et al.,

2000; Afanasyev et al., 2001). Higher resolution local

area coverage data (1.2 km2) is available for a subset of

the global coverage, depending largely on the distribu-tion of regional receiving stations such as that installed

at the Charles Darwin Research Station. The NASA-

GSFC SeaWiFS project has been providing the research

community with global ocean colour data products since

September 1997 and in the aftermath of the strong 1997/

98 El Ni~nno event was applied to great effect in the study

of global, regional and local primary production in the

Eastern Pacific. Such high resolution spatial and tem-poral coverage has allowed tracking of phytoplankton

distributions over small to large time scales (cloud

coverage notwithstanding) including before, during and

after the Jessica spill event in Gal�aapagos waters.

Local Area Coverage data (1.2 km2 resolution) re-

corded onboard the satellite and archived at the NASA

Goddard Distributed Active Archive Centre are used

here to examine localized productivity across areas di-rectly associated with the Jessica spill, while also pro-

viding an analysis of possible larger scale effects away

and to the west downstream from those regions. Raw

telemetry data (level 0) were processed to level 1A

chlorophyll products using the IDL based SeaDAS

software on a UNIX platform at the NASA-GSFC as

part of the SeaWiFS mission. After SeaDAS atmo-

spheric correction (for cloud cover and spectral scat-tering) and geo-referencing, a chlorophyll abundance

map on a false colour logarithmic scale provides a proxy

for phytoplankton standing stock and primary produc-

tion across the marine reserve. This map clearly differ-

entiates low concentrations in potentially oligotrophic

surface waters from highly productive upwelling sites

and oceanic fronts.

The SeaWiFS data sets used for analysis were neardaily overpasses across the Gal�aapagos Marine Reserve

for the month of January 1998, 1999, 2000 and 2001,

and early 2001 data covering the spill event itself (1 week

before to 6 weeks after). Since computational resources

for the handling of such large datasets for statistical

manipulation purposes were limited at the time of

analysis, sampling points to assess spill effects were re-

stricted to cover areas determined as being closest to thedensest concentrations of oil following preliminary ob-

servations by Lougheed et al. (2001) (Fig. 2). These in-

clude the area of Isabela determined as having the

greatest (moderate) contamination, the advection path

between Bah�ııa Naufragio, San Crist�oobal (spill site),

Santa F�ee, southeastern Santa Cruz, and eastern Flore-

ana. Nineteen evenly distributed control points were

selected around the reference island of Santiago, whichshowed no evidence of oil contamination following the

spill.

To reduce the demands on processing, a subset cov-

ering the area of interest was extracted from the Level

Fig. 2. Distribution of sample points extracted from the L1A chlorophyll product used in this analysis: (A) Western San Crist�oobal release site;

(B) Spill advection path; (C) Santa F�ee; (D) Southeastern Santa Cruz; (E) Eastern Floreana; (F) Eastern Isabela; (G) Control sites (unaffected

coastlines) Santiago.

328 S. Banks / Marine Pollution Bulletin 47 (2003) 325–330

1-A data set. A multispectral analysis package (Multi-

Spec) was used to generate matrices of standardized

chlorophyll range values from the validated SeaDAS

prepared images as provided by the NASA-GSFC. This

somewhat convoluted step was necessary since the equip-

ment to run SeaDAS, which under normal circum-stances has full functionality for such analysis, had yet

to be installed at the Gal�aapagos research station. Sample

sites as described were selected against a GIS represen-

tation of the Gal�aapagos Marine Reserve at a distance of

5 km from the coast to ensure no pixel overlap with the

land. Those sample points were matched to correspond-

ing positions in the chlorophyll matrix using a spread-

sheet editor that allowed accurate mapping and errorchecking of each position. Once the position of the sam-

ple points had been validated against the satellite data, a

data set of sample point values were extracted from each

daily chlorophyll matrix. Each sample point constitutes

1.2 km2 of ocean coverage. Weekly and monthly means

were used to reduce the problem of incidental cloud

cover.

ANOVA analyses were used to test differences be-tween years and for the series from a week preceding to

6 weeks after the spill event (January–March 2001) over

affected and reference locations.

3. Results and discussion

SeaWiFS derived chlorophyll-a concentrations takenfor January 1998, 1999, 2000 and 2001 showed signifi-

cant variation in mean values (ANOVA df¼ 3/141,

F ¼ 4:814, P ¼ 0:003) between years for all sites. A

general trend was evident for increasing average primary

production in the month of January across the sampled

sites after the last El Ni~nno (Fig. 3A). Primary produc-

tion, depressed during 1997, recovered dramatically in

Gal�aapagos over 2 weeks in May 1998 as the eastern

Pacific cold tongue re-established across the eastern

Pacific (NASA-GSFC; SeaWiFS Project, 2001). The

inclusion of an El Ni~nno year (1998) in the analysis issuggestive of the lower limit typical of natural variability

in phytoplankton production in Gal�aapagos under the

ENSO signal with a significant elevated mean difference

of 1.92 mg m�3 chlorophyll-a between January 1998 and

January 2001.

Differences in potential primary production between

sample sites in the month following the spill event (Fig.

3B) were also significant (ANOVA df¼ 5/219,F ¼ 4:230, P < 0:001), with the greatest variation be-

tween eastern Santa Cruz, which was experiencing a

mean difference of elevated production in the order of

0.89 mg m�3 chl-a (student�s t-test P ¼ 0:012) in com-

parison to Santa F�ee, San Crist�oobal and the open water

between these islands (following Tukey multiple pair-

wise analysis of means). An independent analysis of year

2000 SeaWiFS data (unpublished Banks, 2001) supportsprevious observations (Houvenghel, 1974) that the

southeast of Santa Cruz is among those sites in Gal�aapa-

gos that support increased net phytoplankton produc-

tion (other highly productive areas include western

Isabela and western shores of most islands). Although

production was significantly higher in southeast Santa

Cruz after the spill, it cannot be directly attributed to a

direct enrichment event from the oil in surface watersince it falls within the range of variability observed for

that region in the same month in previous years.

Gal�aapagos coastal waters are largely heterogeneous with

respect to primary production and we might expect such

variation between sites. A mean significant difference of

Fig. 3. Mean chlorophyll-a concentrations (mgm�3 chl-a) at sampled

affected sites by year for the month of January (A), between affected

sites a month after the event (B), between affected and unaffected sites

1–6 weeks after the spill (C), and the week preceding and 6 weeks after

the spill event (D).

S. Banks / Marine Pollution Bulletin 47 (2003) 325–330 329

0.58 mg m�3 chl-a in the mean chlorophyll-a concen-

trations between oiled sites and the unaffected coastal

Table 1

Two-way ANOVA tests using chlorophyll level data for impacted versus ref

weeks 1, 2 and 3 after the spill

Source df Week 1 post-spill Wee

MS F -ratio P MS

Region 1 22.00 1.24 0.268 0.60

Week 1 0.46 0.03 0.872 1.19

Region�week 1 1.37 0.08 0.782 7.64

Error 109 17.78 4.43

waters of Santiago (ANOVA F ¼ 3:606, df¼ 1/395,

P ¼ 0:058) in the six weeks following the event, although

suggestive of a low level enrichment effect, is more likely

a factor of normal elevated productivity between thecontrol region and test sites (Fig. 3C).

The weekly means taken across each sample site one

week before and 1–6 weeks after the spill event indicated

that variation in chlorophyll level over time was not

significant (ANOVA df¼ 6/254, F ¼ 0:827, P ¼ 0:550).

An average chlorophyll concentration of 2.5 mg m�3

chl-a at the sampled sites in this study in the week pre-

ceding the spill rose slightly by 0.37 mg m�3 in the weekfollowing the event, then fell by 1.13 mg m�3 in the

second week. By the third week production had in-

creased and then dropped again by week four, slowly

increasing to levels analogous to pre-spill conditions a

full month and a half after the event (Fig. 3D). The

observed pattern falls well within normal variability for

Gal�aapagos waters within the month of January, and is

elevated substantially in comparison with observationstowards the end of the 1997/98 El Ni~nno. It is possible

that there were localized nutrient enrichment or stimu-

lation effects after a week where the oil was more con-

centrated. Dispersal of the oil into more spatially

extensive scattered patches under wind forcing and

mixing processes in the following weeks may have re-

sulted in a localized decline in production due to the

effect of the surface slick upon light attenuation in sur-face waters. However, few of the observed differences

could be directly attributed to spill effects.

A lack of clear impacts was reinforced in a before-

after-control-impact comparison (Green, 1979) involv-

ing analysis of chlorophyll levels during the week prior

to the spill versus the week after, and for sites in the path

of the spill and distant reference sites. For this analysis,

any impacts of oiling should be detectable as a signifi-cant interaction term in the two-way ANOVA with

week (before and after spill) and region (impacted and

reference zone) as treatments. No significant interaction

was detected (Table 1). Similarly, significant interactions

were not detected when data for the week prior to the

spill were compared with data obtained in week 2 (day

7–14) post-spill, nor when pre-spill data were compared

with data obtained during week 3 post-spill (day 14–21).These latter two tests were conducted to assess the

erence regions and the week prior to the spill versus data obtained in

k 2 post-spill Week 3 post-spill

F -ratio P MS F -ratio P

0.14 0.713 32.06 3.98 0.048

0.27 0.605 2.48 0.31 0.580

1.73 0.192 4.59 0.57 0.452

8.05

330 S. Banks / Marine Pollution Bulletin 47 (2003) 325–330

possibility that the oil spill affected productivity over

temporal scales longer than 1 week. Given that no effects

were detected over the first three weeks, longer-term

changes were considered unlikely and not tested.

4. Conclusion

It appears that the spill had no obvious impact upon

phytoplankton primary production over the worst af-

fected coastal sites in the Gal�aapagos Marine Reserve,

with chlorophyll levels at the sites examined not ex-tending outside of �non-spill� variability. In this sense El

Ni~nno presents a far more significant perturbation to the

Gal�aapagos marine system. As has been observed in a

number of similar cases, oil tends to disperse rapidly in

open coastal waters with the majority of damage fo-

cused in areas of accumulation. It is hoped that the

thorough coastal clean-up operation will reduce any low

level chronic leaching of hydrocarbons from settlingsites that might still have toxic effects for many years in

protected areas. While short- to medium-term oiling

effects may well have been obscured by normal natural

variation, ecosystems in Gal�aapagos presumably have

evolved a buffering capacity to cope with such relatively

small-scale variability in phytoplankton abundance

outside of ENSO events. Yearly monitoring of primary

production of the marine reserve will continue as part ofthe ongoing SeaWiFS project to address any long-term

changes in productivity.

Acknowledgements

This work was partially funded by subcontract under

NASA research grant NAG5-8865 through NorthCarolina State University, US. Many thanks go to Dr.

Graham Edgar for his comments during document re-

vision; Dr. Gene Feldman SeaWiFS project NASA-

GSFC, Maryland, US and Dr. John Morrison, Charles

Gabriel, North Carolina State University, US for their

collaboration and invaluable support in installation and

development of the Galapagos HRPT station at the

Charles Darwin Research Station.

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