2013 03 21 Impacts of Biodiversity Loss On Ocean Ecosystem Services

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Science 3 November 2006:
Vol. 314 no. 5800 pp. 787-790
DOI: 10.1126/science.1132294
RESEARCH ARTICLE
Impacts of Biodiversity Loss on Ocean Ecosystem Services

Boris Worm1,*, Edward B. Barbier2, Nicola Beaumont3, J. Emmett Duffy4, Carl Folke5,6,
Benjamin S. Halpern7, Jeremy B. C. Jackson8,9, Heike K. Lotze1, Fiorenza Micheli10, Stephen R. Palumbi10,
Enric Sala8, Kimberley A. Selkoe7, John J. Stachowicz11, Reg Watson12
- Author Affiliations
1 Department of Biology, Dalhousie University, Halifax, NS, Canada B3H 4J1.

2
Department of Economics and Finance, University of Wyoming, Laramie, WY 82071, USA.
3
Plymouth Marine Laboratory, Plymouth PL1 3DH, UK.
4
Virginia Institute of Marine Sciences, Gloucester Point, VA 23062–1346, USA.
5
Department of Systems Ecology, Stockholm University, Stockholm, SE-106 91 Sweden.
6
Beijer International Institute of Ecological Economics, Royal Swedish Academy of Sciences, SE-104 05,
Stockholm, Sweden.
7 National Center for Ecological Analysis and Synthesis, Santa Barbara, CA 93101, USA.
8 Center for Marine Biodiversity and Conservation, Scripps Institution of Oceanography, La Jolla, CA 92093–
0202, USA.
9 Smithsonian Tropical Research Institute, Box 2072, Balboa, Republic of Panama.
10 Hopkins Marine Station, Stanford University, Pacific Grove, CA 93950, USA.
11 Section of Evolution and Ecology, University of California, Davis, CA 95616, USA.
12 Fisheries Centre, University of British Columbia, Vancouver, BC, Canada V6T 1Z4.
!* To whom correspondence should be addressed. E-mail: [email protected]
ABSTRACT
Human-dominated marine ecosystems are experiencing accelerating loss of populations and

species, with largely unknown consequences. We analyzed local experiments, long-term regional
time series, and global fisheries data to test how biodiversity loss affects marine ecosystem
services across temporal and spatial scales. Overall, rates of resource collapse increased and
recovery potential, stability, and water quality decreased exponentially with declining diversity.
Restoration of biodiversity, in contrast, increased productivity fourfold and decreased variability by
21%, on average. We conclude that marine biodiversity loss is increasingly impairing the ocean's
capacity to provide food, maintain water quality, and recover from perturbations. Yet available data
suggest that at this point, these trends are still reversible.
What is the role of biodiversity in maintaining the ecosystem services on which a growing human
population depends? Recent surveys of the terrestrial literature suggest that local species richness
may enhance ecosystem productivity and stability (1–3). However, the importance of biodiversity
changes at the landscape level is less clear, and the lessons from local experiments and theory do not
seem to easily extend to long-term, large-scale management decisions (3). These issues are
particularly enigmatic for the world's oceans, which are geographically large and taxonomically
complex, making the scaling up from local to global scales potentially more difficult (4). Marine
ecosystems provide a wide variety of goods and services, including vital food resources for millions of
people (5, 6). A large and increasing proportion of our population lives close to the coast; thus the
loss of services such as flood control and waste detoxification can have disastrous consequences (7,
8). Changes in marine biodiversity are directly caused by exploitation, pollution, and habitat
destruction, or indirectly through climate change and related perturbations of ocean biogeochemistry
http://www.sciencemag.org/content/314/5800/787.full Page 1 of 11
(9–13). Although marine extinctions are only slowly uncovered at the global scale (9), regional
ecosystems such as estuaries (10), coral reefs (11), and coastal (12) and oceanic fish communities (13)
are rapidly losing populations, species, or entire functional groups. Although it is clear that particular
species provide critical services to society (6), the role of biodiversity per se remains untested at the
ecosystem level (14). We analyzed the effects of changes in marine biodiversity on fundamental
ecosystem services by combining available data from sources ranging from small-scale experiments
to global fisheries.
Experiments. We first used meta-analysis of published data to examine the effects of variation in
marine diversity (genetic or species richness) on primary and secondary productivity, resource use,
nutrient cycling, and ecosystem stability in 32 controlled experiments. Such effects have been
contentiously debated, particularly in the marine realm, where high diversity and connectivity may blur
any deterministic effect of local biodiversity on ecosystem functioning (1). Yet when the available
experimental data are combined (15), they reveal a strikingly general picture (Fig. 1). Increased
diversity of both primary producers (Fig. 1A) and consumers (Fig. 1B) enhanced all examined
ecosystem processes. Observed effect sizes corresponded to a 78 to 80% enhancement of primary and
secondary production in diverse mixtures relative to monocultures and a 20 to 36% enhancement of
resource use efficiency (Fig. 1, A and B).
Fig. 1.
Marine biodiversity and ecosystem functioning in

controlled experiments. Shown are response ratios
[ln(high/low diversity) ±95% confidence interval (CI)] of
ecosystem processes to experimental manipulations of
species diversity of (A) primary producers (plants and
algae), and (B) consumers (herbivores and predators).
Increased diversity significantly enhanced all examined
ecosystem functions (0.05 > P > 0.0001). The number of
studies is given in parentheses. (C) Genetic diversity
increased the recovery of seagrass ecosystems after
View larger version:
In this page In a new window overgrazing (solid circles) and climatic extremes (open
Download PowerPoint Slide for Teaching circles). (D) Diet diversity enhanced reproductive capacity
in zooplankton over both the average- and best-
performing monocultures.
Experiments that manipulated species diversity (Fig. 1B) or genetic diversity (Fig. 1C) both found that
diversity enhanced ecosystem stability, here defined as the ability to withstand recurrent
perturbations. This effect was linked to either increased resistance to disturbance (16) or enhanced
recovery afterward (17). A number of experiments on diet mixing further demonstrated the
importance of diverse food sources for secondary production and the channeling of that energy to
higher levels in the food web (Fig. 1D). Different diet items were required to optimize different life-
history processes (growth, survival, and fecundity), leading to maximum total production in the mixed
diet. In summary, experimental results indicate robust positive linkages between biodiversity,
productivity, and stability across trophic levels in marine ecosystems. Identified mechanisms from the
original studies include complementary resource use, positive interactions, and increased selection of
highly performing species at high diversity.
Coastal ecosystems. To test whether experimental results scale up in both space and time, we
compiled long-term trends in regional biodiversity and services from a detailed database of 12 coastal
and estuarine ecosystems (10) and other sources (15). We examined trends in 30 to 80 (average, 48)
economically and ecologically important species per ecosystem. Records over the past millennium
revealed a rapid decline of native species diversity since the onset of industrialization (Fig. 2A). As
predicted by experiments, systems with higher regional species richness appeared more stable,
showing lower rates of collapse and extinction of commercially important fish and invertebrate taxa
over time (Fig. 2B, linear regression, P < 0.01). Overall, historical trends led to the present depletion
(here defined as >50% decline over baseline abundance), collapse (>90% decline), or extinction (100%
decline) of 91, 38, or 7% of species, on average (Fig. 2C). Only 14% recovered from collapse (Fig. 2C);
these species were mostly protected birds and mammals.
Fig. 2.
Regional loss of species diversity and ecosystem services in coastal oceans. (A) Trends of collapse
(circles, >90% decline) and extinction (triangles, 100% decline) of species over the past 1000
years. Means and standard errors are shown (n = 12 regions in Europe, North America, and
Australia). (B) Percentage of collapsed (circles) and extinct (triangles) fisheries in relation to
regional fish species richness. Significant linear regression lines are depicted (P < 0.01). (C to E)
Relative losses or gains in (C) biodiversity, (D) ecosystem services, and (E) risks that are associated
with the loss of services. The number of studies is given in parentheses; error bars indicate
standard errors.

In this page In a new window
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These regional biodiversity losses impaired at least three critical ecosystem services (Fig. 2D): number
of viable (noncollapsed) fisheries (–33%); provision of nursery habitats such as oyster reefs, seagrass
beds, and wetlands (–69%); and filtering and detoxification services provided by suspension feeders,
submerged vegetation, and wetlands (–63%). Loss of filtering services probably contributed to
declining water quality (18) and the increasing occurrence of harmful algal blooms, fish kills, shellfish
and beach closures, and oxygen depletion (Fig. 2E). Increasing coastal flooding events (Fig. 2E) are
linked to sea level rise but were probably accelerated by historical losses of floodplains and erosion
control provided by coastal wetlands, reefs, and submerged vegetation (7). An increased number of
species invasions over time (Fig. 2E) also coincided with the loss of native biodiversity; again, this is
consistent with experimental results (19). Invasions did not compensate for the loss of native
biodiversity and services, because they comprised other species groups, mostly microbial, plankton,
and small invertebrate taxa (10). Although causal relationships are difficult to infer, these data
suggest that substantial loss of biodiversity (Fig. 2, A and C) is closely associated with regional loss of
ecosystem services (Fig. 2D) and increasing risks for coastal inhabitants (Fig. 2E). Experimentally
derived predictions that more species-rich systems should be more stable in delivering services (Fig.
1) are also supported at the regional scale (Fig. 2B).
Large marine ecosystems. At the largest scales, we analyzed relationships between biodiversity and
ecosystem services using the global catch database from the United Nations Food and Agriculture
Organization (FAO) and other sources (15, 20). We extracted all data on fish and invertebrate catches
from 1950 to 2003 within all 64 large marine ecosystems (LMEs) worldwide. LMEs are large (>150,000
km2) ocean regions reaching from estuaries and coastal areas to the seaward boundaries of
continental shelves and the outer margins of the major current systems (21). They are characterized
by distinct bathymetry, hydrography, productivity, and food webs. Collectively, these areas produced
83% of global fisheries yields over the past 50 years. Fish diversity data for each LME were derived
independently from a comprehensive fish taxonomic database (22).
Globally, the rate of fisheries collapses, defined here as catches dropping below 10% of the recorded
maximum (23), has been accelerating over time, with 29% of currently fished species considered
collapsed in 2003 (Fig. 3A, diamonds). This accelerating trend is best described by a power relation (y
= 0.0168x1.8992, r = 0.96, P < 0.0001), which predicts the percentage of currently collapsed taxa as a
function of years elapsed since 1950. Cumulative collapses (including recovered species) amounted to
65% of recorded taxa (Fig. 3A, triangles; regression fit: y = 0.0227x2.0035, r = 0.96, P < 0.0001). The
data further revealed that despite large increases in global fishing effort, cumulative yields across all
species and LMEs had declined by 13% (or 10.6 million metric tons) since passing a maximum in 1994.
Fig. 3.
Global loss of species from LMEs. (A) Trajectories of

collapsed fish and invertebrate taxa over the past 50 years
(diamonds, collapses by year; triangles, cumulative
collapses). Data are shown for all (black), species-poor
(<500 species, blue), and species-rich (>500 species, red)
LMEs. Regression lines are best-fit power models
corrected for temporal autocorrelation. (B) Map of all 64
LMEs, color-coded according to their total fish species
richness. (C) Proportion of collapsed fish and invertebrate
taxa, (D) average productivity of noncollapsed taxa (in
In this page In a new window percent of maximum catch), and (E) average recovery of
Download PowerPoint Slide for Teaching catches (in percent of maximum catch) 15 years after a
collapse in relation to LME total fish species richness. (F)
Number of fished taxa as a function of total species
richness. (G) Coefficient of variation in total catch and (H) total catch per year as a function of the
number of fished taxa per LME.
Consistent with the results from estuaries and coastal seas (Fig. 2B), we observed that these collapses
of LME fisheries occurred at a higher rate in species-poor ecosystems, as compared with species-rich
ones (Fig. 3A). Fish diversity varied widely across LMEs, ranging from ∼20 to 4000 species (Fig. 3B),
and influenced fishery-related services in several ways. First, the proportion of collapsed fisheries
decayed exponentially with increasing species richness (Fig. 3C). Furthermore, the average catches of
non-collapsed fisheries were higher in species-rich systems (Fig. 3D). Diversity also seemed to
increase robustness to overexploitation. Rates of recovery, here defined as any post-collapse increase
above the 10% threshold, were positively correlated with fish diversity (Fig. 3E). This positive
relationship between diversity and recovery became stronger with time after a collapse (5 years, r =
0.10; 10 years, r = 0.39; 15 years, r = 0.48). Higher taxonomic units (genus and family) produced very
similar relationships as species richness in Fig. 3; typically, relationships became stronger with
increased taxonomic aggregation. This may suggest that taxonomically related species play
complementary functional roles in supporting fisheries productivity and recovery.
A mechanism that may explain enhanced recovery at high diversity is that fishers can switch more
readily among target species, potentially providing overfished taxa with a chance to recover. Indeed,
the number of fished taxa was a log-linear function of species richness (Fig. 3F). Fished taxa richness
was negatively related to the variation in catch from year to year (Fig. 3G) and positively correlated
with the total production of catch per year (Fig. 3H). This increased stability and productivity are likely
due to the portfolio effect (24, 25), whereby a more diverse array of species provides a larger number
of ecological functions and economic opportunities, leading to a more stable trajectory and better
performance over time. This portfolio effect has independently been confirmed by economic studies of
multispecies harvesting relationships in marine ecosystems (26, 27). Linear (or log-linear)
relationships indicate steady increases in services up to the highest levels of biodiversity. This means
that proportional species losses are predicted to have similar effects at low and high levels of native
biodiversity.
Marine reserves and fishery closures. A pressing question for management is whether the loss of
services can be reversed, once it has occurred. To address this question, we analyzed available data
from 44 fully protected marine reserves and four large-scale fisheries closures (15). Reserves and
closures have been used to reverse the decline of marine biodiversity on local and regional scales (28,
29). As such, they can be viewed as replicated large-scale experiments. We used meta-analytic
techniques (15) to test for consistent trends in biodiversity and services across all studies (Fig. 4).
Fig. 4.
Recovery of diversity and ecosystem services in marine

protected areas and fisheries closures. Shown are the
response ratios (inside versus outside the reserve or
before and after protection ±95% CI) of (A) species
diversity and (B to D) ecosystem services that correspond
to fisheries productivity, ecosystem stability, and tourism
In this page In a new window revenue, respectively. Positive values identify increases in
Download PowerPoint Slide for Teaching the reserve relative to the control; error bars not
intersecting zero indicate statistical significance (P <
0.05). Solid circles represent unweighted averages; open circles are weighted by sample size (see
supporting online methods for details). The number of studies is shown in parentheses. CPUE,
catch per unit of effort.
We found that reserves and fisheries closures showed increased species diversity of target and
nontarget species, averaging a 23% increase in species richness (Fig. 4A). These increases in
biodiversity were associated with large increases in fisheries productivity, as seen in the fourfold
average increase in catch per unit of effort in fished areas around the reserves (Fig. 4B). The
difference in total catches was less pronounced (Fig. 4B), probably because of restrictions on fishing
effort around many reserves. Resistance and recovery after natural disturbances from storms and
thermal stress tended to increase in reserves, though not significantly in most cases (Fig. 4C).
Community variability, as measured by the coefficient of variation in aggregate fish biomass, was
reduced by 21% on average (Fig. 4C). Finally, tourism revenue measured as the relative increase in
dive trips within 138 Caribbean protected areas strongly increased after they were established (Fig.
4D). For several variables, statistical significance depended on how studies were weighted (Fig. 4,
solid versus open circles). This is probably the result of large variation in sample sizes among studies
(15). Despite the inherent variability, these results suggest that at this point it is still possible to
recover lost biodiversity, at least on local to regional scales; and that such recovery is generally
accompanied by increased productivity and decreased variability, which translates into extractive (fish
catches around reserves) and nonextractive (tourism within reserves) revenue.
Conclusions. Positive relationships between diversity and ecosystem functions and services were
found using experimental (Fig. 1) and correlative approaches along trajectories of diversity loss (Figs.
2 and 3) and recovery (Fig. 4). Our data highlight the societal consequences of an ongoing erosion of
diversity that appears to be accelerating on a global scale (Fig. 3A). This trend is of serious concern
because it projects the global collapse of all taxa currently fished by the mid–21st century (based on
the extrapolation of regression in Fig. 3A to 100% in the year 2048). Our findings further suggest that
the elimination of locally adapted populations and species not only impairs the ability of marine
ecosystems to feed a growing human population but also sabotages their stability and recovery
potential in a rapidly changing marine environment.
We recognize limitations in each of our data sources, particularly the inherent problem of inferring
causality from correlation in the larger-scale studies. The strength of these results rests on the
consistent agreement of theory, experiments, and observations across widely different scales and
ecosystems. Our analysis may provide a wider context for the interpretation of local biodiversity
experiments that produced diverging and controversial outcomes (1, 3, 24). It suggests that very
general patterns emerge on progressively larger scales. High-diversity systems consistently provided
more services with less variability, which has economic and policy implications. First, there is no
dichotomy between biodiversity conservation and long-term economic development; they must be
viewed as interdependent societal goals. Second, there was no evidence for redundancy at high levels
of diversity; the improvement of services was continuous on a log-linear scale (Fig. 3). Third, the
buffering impact of species diversity on the resistance and recovery of ecosystem services generates
insurance value that must be incorporated into future economic valuations and management
decisions. By restoring marine biodiversity through sustainable fisheries management, pollution
control, maintenance of essential habitats, and the creation of marine reserves, we can invest in the
productivity and reliability of the goods and services that the ocean provides to humanity. Our
analyses suggest that business as usual would foreshadow serious threats to global food security,
coastal water quality, and ecosystem stability, affecting current and future generations.
Supporting Online Material

www.sciencemag.org/cgi/content/full/314/5800/787/DC1
Methods and Data Sources
Tables S1 to S5
References
Received for publication 10 July 2006.

Accepted for publication 3 October 2006.
References and Notes

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Impacts of Biodiversity Loss on Ocean Ecosystem Services

1 Department of Biology, Dalhousie University, Halifax, NS, Canada B3H 4J1.

!* To whom correspondence should be addressed. E-mail: [email protected]

Human-dominated marine ecosystems are experiencing accelerating loss of populations and

Marine biodiversity and ecosystem functioning in

View larger version:

Global loss of species from LMEs. (A) Trajectories of

Recovery of diversity and ecosystem services in marine

Supporting Online Material

Received for publication 10 July 2006.

References and Notes

2. M. Palmer et al., Science 304, 1251 (2004). Abstract/FREE Full Text

3. D. U. Hooper et al., Ecol. Monogr. 75, 3 (2005). CrossRef Web of Science

5. C. H. Peterson, J. Lubchenco, in Nature's Services: Societal Dependence on Natural Ecosystems , G.

7. F. Danielsen et al., Science 310, 643 (2005). Abstract/FREE Full Text

8. W. N. Adger, T. P. Hughes, C. Folke, S. R. Carpenter, J. Rockstrom, Science 309, 1036 (2005).

9. N. K. Dulvy, Y. Sadovy, J. D. Reynolds, Fish Fish. 4, 25 (2003).

14. D. Raffaelli, Science 306, 1141 (2004). Abstract/FREE Full Text

20. R. Watson, A. Kitchingman, A. Gelchu, D. Pauly, Fish Fish. 5, 168 (2004).

26. H. Wacker, Res. Energy Econ. 21, 89 (1999). CrossRef

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