Invasions and Extinctions Reshape Coastal Marine Food

Webs

Jarrett E. Byrnes1,2*, Pamela L. Reynolds2, John J. Stachowicz1

1 Center for Population Biology, University of California, Davis, California, United States of America, 2 Bodega Marine Laboratory, Bodega Bay,

California, United States of America

The biodiversity of ecosystems worldwide is changing because of species loss due to human-caused extinctions and species

gain through intentional and accidental introductions. Here we show that the combined effect of these two processes is

altering the trophic structure of food webs in coastal marine systems. This is because most extinctions (,70%) occur at high

trophic levels (top predators and other carnivores), while most invasions are by species from lower trophic levels (70%

macroplanktivores, deposit feeders, and detritivores). These opposing changes thus alter the shape of marine food webs from

a trophic pyramid capped by a diverse array of predators and consumers to a shorter, squatter configuration dominated by

filter feeders and scavengers. The consequences of the simultaneous loss of diversity at top trophic levels and gain at lower

trophic levels is largely unknown. However, current research suggests that a better understanding of how such simultaneous

changes in diversity can impact ecosystem function will be required to manage coastal ecosystems and forecast future

changes.

Citation: Byrnes JE, Reynolds PL, Stachowicz JJ (2007) Invasions and Extinctions Reshape Coastal Marine Food Webs. PLoS ONE 2(3): e295.

doi:10.1371/journal.pone.0000295

INTRODUCTION

The biodiversity of ecosystems around the world is being altered

by species loss due to extinction from human activities [1] and gain

through intentional and accidental introductions [2]. Although

a number of studies have recently considered the consequences of

diversity loss for ecosystem functioning [see reviews by 3, 4], few of

these consider the effects of realistic diversity change scenarios [but

see 5, 6]. At the regional scale, the gain of species most often

equals or outpaces the number lost due to extinction [2],

suggesting that extinctions and invasions might offset one another

with little net change in diversity.

Because different processes drive extinctions and invasion (e.g.,

overfishing versus ballast water transport), the types of species being

gained and lost might differ, however. For example, extinctions

due to anthropogenic stressors such as overfishing and climate

change are thought to impact higher trophic levels first [7,8]. Such

a re-organization of trophic structure (i.e., trophic skew sensu Duffy

[9]) may result in major changes to ecosystem structure and function,

even if the total number of species in a region remains constant

or even increases. These changes can impact a wide variety of

ecosystem level processes [10,11] such as the total biomass and

production and their distribution among trophic levels.

Here we consider how modern invasions and extinctions have

together changed the architecture of marine food webs by

comparing the trophic distribution of invasions and extinctions.

In a recent analysis for a single region, the Wadden Sea, the

taxonomic distribution of extinctions and invasions differed even

though overall richness was relatively unchanged [12]. However,

the generality of this trend is not clear, and this study only

categorized species by coarse taxonomic group, which often does

not correlate with ecological function. In this paper, we classified

all species in lists of global and regional marine species extinctions

[13] and invasions from lists for San Francisco Bay [14], Australia

[15], The Gulf of the Farallones, and the Wadden Sea [16,17] by

trophic level and feeding mode (Fig. 1, see Methods for details).

We then compared the distribution of species among trophic

groups in each exotic species list with that of global and regional

extinctions to assess whether the trophic distribution of species

additions matched that of species deletions and to estimate the net

change in species richness of each trophic level and functional

feeding group. Our results suggest that invasions are biased

towards lower trophic levels whereas extinctions occur higher in

the food web. We discuss the potential implications of these

changes in trophic skew [9] for marine ecosystems.

RESULTS

The top two trophic levels (secondary consumers and predators)

contained 70% of the 133 documented global and regional marine

extinctions (Fig. 2). Conversely, in each invasion list, approximately 70% of exotic species belonged to trophic level two, the

majority of which were suspension feeders that directly consume

plankton, deposit feeders that consume sediment organic material,

or detritivores that consume decaying organic matter (Fig. 2). A

comparison of the trophic distribution of extinctions with each

invasion data set shows that species loss is skewed toward species

from higher trophic groups relative to species gain, which is

skewed towards lower order consumers (San Francisco Bay

x2

10= 163.03 p,0.0001, Gulf of the Farallones National Marine

Sanctuary x2

9= 126.64 p,0.0001, Australia x210= 90.02

p,0.0001). The functional groups most responsible for this skew

are top predators (24.1% of extinctions but 6.1% of invasions on

average), secondary consumers (37.6% of extinctions but 2.2% of

Academic Editor: David Lusseau, Dalhousie University, Canada

Received December 29, 2006; Accepted February 18, 2007; Published March 14,

2007

Copyright:  2007 Byrnes et al. This is an open-access article distributed under

the terms of the Creative Commons Attribution License, which permits

unrestricted use, distribution, and reproduction in any medium, provided the

original author and source are credited.

Funding: Funding and other support for this study was provided by the UC Davis

IGERT on Biological Invasions (NSF-DGE No. 0114432) and the National Science

Foundation Biological Oceanography program (OCE 03-17778 to JJS).

Competing Interests: The authors have declared that no competing interests

exist.

* To whom correspondence should be addressed. E-mail: jebyrnes@ucdavis.edu

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invasions), and suspension feeding macroplanktivores (10.5% of

extinctions but 44.6% of invasions). Changes in primary producers

from invasions roughly match those due to extinctions. The

distribution of introduced species among functional groups is

remarkably similar among regions.

These patterns of trophic skew from invasions and extinctions

remain intact when analyses are restricted to spatially congruent

subsets of the data for the Wadden Sea (Fig. 3, x2

10= 41.47

p,0.0001). Both invasions and extinctions in the Wadden Sea differ

in their pattern of species distributions among trophic levels from the

trophic distribution of our reconstructed pre-disturbance species list

(Fig. 3, Invasions x2

10= 24.79 p = 0.0058, Extinctions x210= 57.93

p,0.0001). The pre-invasion and extinction species list shows

a classic ‘‘pyramid’’ in shape with decreasing numbers of species with

increasing trophic level (Fig. 4A). The differential distribution of

invasions and extinctions among trophic groups have already caused

measurable changes in the relative distribution of species among

trophic levels, even with invasions and extinctions each comprising

only 5.1% of the total species (Fig 4D). While species richness has

remained nearly the same, there are now 14% fewer predator species

and 8.6% more primary consumer species.

These results suggest that marine ecosystems have already

experienced a shift in food web architecture, with shrinking

numbers of predatory species being replaced by an increasing

diversity of suspension and deposit feeders. More extreme shifts will

likely result from continued species invasions and extinction (Fig. 4E).

For example, when the number of invasions and extinctions equals

25% of the total number of species, predator diversity will decline by

65% while primary consumer diversity will increase by 50%.

Although this level of community turnover may seem extreme, some

taxa such as birds and plants on some island ecosystems have

already experienced similar or greater changes [18].

DISCUSSION

Our results show that, for the coastal marine systems we examined,

extinctions are reducing the number of predatory species and

secondary consumers while invasions are greatly increasing the

number of primary filter feeders, detritivores, deposit feeders, and

other primary consumers. We suspect the bias of extinctions toward

higher trophic levels and invasions toward lower trophic levels will be

consistent in other systems, although subtle differences may occur.

For example, the influence of invasions in altering trophic skew may

be reduced in open coast or oceanic environments relative to

estuaries [19], although the loss of top predators appears to be

a global phenomenon. Marine and terrestrial systems also likely

differ in the trophic distribution of invaders due to differences in the

relative importance of different vectors of introduction. In marine

systems there are surprisingly few plant or macroalgal invasions

relative to the large number documented on land [e.g., 18], while the

numerically most abundant group of marine invaders, sessile

planktivores, are virtually absent in terrestrial systems. Thus while

heavily invaded coastal marine ecosystems experience a net increase

in primary consumer richness, terrestrial systems may experience

greater species gain at the producer level.

Research on the consequences of these types of changes in the

number of species at multiple trophic levels is still relatively new

[11], despite a thorough understanding of the consequences of

changing the numbers of individuals at different trophic levels

[20]. Some recent mesocosm and laboratory experiments with

simplified communities suggest that, in both marine and terrestrial

communities, loss of predator species alone may enhance the

abundance and diversity of species at lower trophic levels even

without invasions [11,21–25]. While these results are largely from

controlled experiments that may only include relatively strongly

interacting species, they appear to be robust and match patterns

observed from field surveys [22] and fisheries data [4] that

incorporate total community richness or diversity. Additionally,

with increasing deletions of large numbers of predator species and

additions of planktivores, the likelihood of gaining or losing species

with a particularly strong effect on ecosystem function increases.

Indeed, both invasions and extinctions of strong interactors have

been documented [e.g., 26, 27]. Even if many of the species on our

lists of invasions and extinctions are not strong interactors, adding

weakly interacting species can still have strong impacts on

ecosystem stability [28] and have episodic strong effects with long

lasting consequences [29].

Several studies also illustrate the difficulty of predicting the

consequences of changing diversity at one trophic level without

considering diversity at other trophic levels [30,31]. For example,

Figure 1. Food web showing the connections between all trophic functional groups. Arrows represent one group consuming the group to which

the arrow points. Shading indicates trophic level (none = 1, light = 2, moderate = 3, dark = 4).

doi:10.1371/journal.pone.0000295.g001

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decreased predator diversity in California kelp forests is associated

with increases in the abundance of herbivores and a concomitant

reduction in kelp abundance [22]. This effect is caused by

complementary responses of different species of herbivores to

different species of predators, and therefore would not occur in

systems with low herbivore diversity. Reductions in consumer

diversity in a variety of eelgrass experiments have consistently

resulted in enhanced epiphyte growth and reductions in sediment

organic matter [32,33], but the effects of herbivore diversity are

strongest in the presence of predators [11].

A recent example from the Gulf of Maine is illustrative of the

potential consequences of this multi-trophic phenomenon [34,35].

Within the Gulf, overfishing has removed predatory fishes like cod,

allowing native herbivore populations (particularly urchins) to

increase, leading to a decline in native kelp. This decline has been

exacerbated by two invasions at lower trophic levels: (1) an

epiphytic bryozoan (Membranipora membranacea) that makes kelp

brittle and more palatable to native grazers and (2) a grazer

resistant alga, Dead Man’s Fingers (Codium fragile), that fills gaps in

the canopy and inhibits kelp recruitment. This fundamental shift

in the subtidal landscape due to the synergistic effects of local

extinctions of top predators and invasions of producers and

suspension feeders has caused a major change in the structure of

communities, including reductions in the recruitment of some

native fish [34].

Given that the opposing patterns of trophic skew in extinctions

and invasions we identify are consistent across a number of

locations (Fig. 2 and 3), complex changes in trophic function are

likely to be increasingly common. However, the general

consequences of these multitrophic shifts may be quite variable.

A recent meta-analysis shows that exotic herbivores are better than

natives at controlling native plants. Native herbivores, in contrast,

are better than exotics at controlling exotic plants [36]. This is the

opposite of the preference found in the Gulf of Maine example. If

this conclusion is as robust for other consumers as it appears to be

for herbivores, introduction of exotic herbivores and elimination of

Figure 2. Trophic skew in regional invasions versus combined global and regional extinctions broken down by percentage of species in each

trophic group. Colors indicate trophic level (white = 1, light grey = 2, dark grey = 3, black = 4). Extinctions are skewed towards trophic levels 3 and 4

(secondary consumers and predators) while invasions are skewed towards trophic level 2 (primary consumers).

doi:10.1371/journal.pone.0000295.g002

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native predators as suggested by our data could have a synergistically negative effect on native plants. The contradictory outcomes

in these examples highlight our current inability to make specific

predictions about the effects of simultaneous changes in species

composition at multiple trophic levels. We therefore urge

additional focused investigation into the ecological consequences

of simultaneous diversity change at multiple trophic levels within

these and other highly impacted ecosystems.

METHODS

To determine whether, at regional scales, the structure of marine

food webs is being altered, we examined lists of marine species

extinctions and invasions, classified species by trophic level and

feeding mode, and then compared the trophic skew of invasions

against that of extinctions. For species extinctions, we used the list

of documented local and global marine extinctions from Dulvy

Figure 3. Trophic skew in the Wadden Sea in (A) uninvaded intact communities, (B) exotic species that have successfully established and (C)

species that have gone extinct. Data presented as the percentage of species in each trophic group. Colors indicate trophic level (white = 1, light

grey = 2, dark grey = 3, black = 4). Patterns match those in the larger global/regional data set (Fig. 2), with extinctions and invasions occurring within

different trophic groups, and neither matching the natural trophic distribution of species.

doi:10.1371/journal.pone.0000295.g003

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[13] (n = 133 species). Because the consequences of diversity loss

on ecosystem functioning are felt at the ecosystem (regional) level,

we considered both global and regional extinctions in our analysis.

In other words, if a species has been driven extinct from a region,

it no longer performs any role in the food web of that region and

thus for the purposes of regional ecosystem functioning is extinct.

Therefore, both scales of extinction were relevant, as we were

interested in loss of function at the scale of organisms within a food

web.

For species introductions, we looked at published lists for San

Francisco Bay [14] (n = 166 species), Australia [15] (n = 153

species), the Wadden Sea [16] (n = 34 species) and a previously

unpublished list for the Gulf of the Farallones National Marine

Sanctuary in Northern California (n = 141 species). We were able

to directly compare invasions and extinctions (n = 38 species) in

the Wadden Sea where patterns of changing functional group

abundance have been previously documented [12,37] in order to

assess whether broader patterns held when considering invasions

and extinctions for the same region. We then compared these data

sets with a reconstruction of the ‘‘pre-disturbance’’ list of species in

the Wadden Sea as estimated by taking an extant species list [17],

excluding any invasive species and adding regionally extinct ones

(n = 716 species total). Meiofauna, protozoans, and phytoplankton

were only included in a minority of species lists (i.e., the Wadden

Sea invasions, Australian invasions, and the ‘‘natural’’ Wadden

Sea lists). They were not included in any of the extinction lists,

potentially due to taxonomic uncertainty or difficulty of detecting

extinctions in these poorly known groups. We therefore excluded

them from our analysis. We also limited our analysis to species that

occurred in marine or estuarine environments. The data for each

extinction and invasion list are presented in Supplementary Tables

S1, S2, S3, S4, and S5 (accompanied by References S1).

For each list of species lost or gained, we classified species into

twelve different groups based on their primary food source and

mode of feeding (Fig. 1). We aggregated these groups into four

trophic levels. Trophic level one consisted of primary producers:

vascular plants, benthic and multicellular algae, and phytoplankton (excluded from analysis, see above). Trophic level two

consisted of A) herbivores, which consume vascular plants and

algae, B) deposit feeders, which consume both sediment organic

matter and detritus encountered in the sediment, C) detritivores,

which specialize on detrital matter, D) zooplankton, which are

both planktonic themselves and consume both phytoplankton and

other zooplankton, and E) macroplanktivores, which are either

benthic or pelagic, consume phytoplankton and/or zooplankton,

and are large enough not to be consumed by other planktivores.

Trophic level three consisted of consumers, which eat one or more

species in trophic level two, and may also consume other members

of trophic level three. Trophic level three also contained

omnivorous consumers, which eat species from both trophic level

one and two, and may also eat other species in trophic level three.

Trophic level four consisted of predators, which eat either

Figure 4. Trophic distribution of species in the Wadden Sea represented as trophic pyramids. Bar widths are scaled to the proportion of species in

each trophic level and numbers indicate percentage of species loss or gain in each trophic level. Colors indicate trophic level (white = 1, light grey = 2,

dark grey = 3, black = 4). (A) Pre-Disturbance (B) Skew of extinctions (C) Skew of Invasions (D) Current distribution after invasions and extinctions

resulting in 5.1% community turnover (i.e., equal numbers of extinctions and invasions) (E) Projected change in the trophic distribution of species in

the Wadden Sea for 25% community turnover. Note the dramatic reduction of the proportion of species in the top two trophic levels, and the

increasing dominance of primary consumers.

doi:10.1371/journal.pone.0000295.g004

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consumers or omnivorous consumers, and parasites which utilize

animals at all trophic levels.

We assigned species to trophic groups based on published

literature. Plants and algae were classified without a reference.

Cnidarians, sponges, ascidians, bryozoans, barnacles, and mussels

were all classified as macroplanktivores based on their feeding

biology. When the trophic group of a species could not be

determined, we used information known about the trophic status

of the lowest possible taxonomic group containing the species. In

some cases, species fit in multiple trophic groups. As they added

multiple functions to the food web, and we wished to look at

changes in food web structure rather than total biodiversity per se,

we included species in multiple categories for our functional group

analyses. Species were only counted once when looking at change

in number of species per trophic level. By design of our trophic

groupings, no species fit in multiple trophic levels.

We recognize that classification of some feeding groups into

particular trophic levels is not straightforward given widespread

omnivory. In particular, many benthic and pelagic planktivorous

organisms are facultatively if not obligately omnivorous and thus

could be considered ‘‘omnivorous consumers’’ in trophic level

three instead of in trophic level two where we placed them. As

there were few zooplankton in our data set, we do not think that

their classification in level two or three is likely to qualitatively alter

the results. We retain the ‘‘macroplanktivores’’ which are mostly

benthic suspension feeders in trophic level 2 rather than 3 because

the types of organisms that consume them are similar to those that

consume other members of trophic level two (herbivores,

detritivores) and these predators largely reside themselves within

trophic level three. In other words, had we moved macroplanktivores to trophic level 3, we would have then shifted the species at

trophic level 3 and 4 to levels 4 and 5. Thus the placement of

planktivores in trophic level 2 or 3 would not fundamentally alter

our conclusions.

Trophic skew was assessed using contingency analysis in R to

compare the number of species in each trophic group (both

trophic level and functional feeding group) in the list of species

extinctions to each list of species invasions. Results of both analyses

are presented and do not qualitatively differ.

SUPPORTING INFORMATION

Table S1 Lists of marine species extinctions from Dulvy (2003),

their trophic group, and reference for trophic group from literature survey. Reference list follows in supplementary references S1.

Found at: doi:10.1371/journal.pone.0000295.s001 (0.32 MB

DOC)

Table S2 Lists of marine species invasions in San Francisco Bay

from Cohen and Carlton (1995), their trophic group, and

reference for trophic group from literature survey. Reference list

follows in supplementary references S1.

Found at: doi:10.1371/journal.pone.0000295.s002 (0.37 MB

DOC)

Table S3 List of marine species invasions in the Gulf of the

Farallones National Marine Sanctuary, their trophic group, and

reference for trophic group from literature survey. Reference list

follows in supplementary references S1.

Found at: doi:10.1371/journal.pone.0000295.s003 (0.34 MB

DOC)

Table S4 List of marine species invasions in Australia from

NIMPIS, their trophic group, and reference for trophic group

from literature survey. Reference list follows in supplementary

references S1.

Found at: doi:10.1371/journal.pone.0000295.s004 (0.36 MB

DOC)

Table S5 List of marine species invasions in the Wadden Sea

from Nehring (2006), their trophic group, and reference for

trophic group from literature survey. Reference list follows in

supplementary references S1. For a full list of all species in the

Wadden Sea classified in trophic groups, please contact the

authors.

Found at: doi:10.1371/journal.pone.0000295.s005 (0.11 MB

DOC)

References S1 Reference list for trophic classification from

literature survey of all species in supplementary tables S1, S2, S3,

S4 and S5.

Found at: doi:10.1371/journal.pone.0000295.s006 (0.08 MB

DOC)

ACKNOWLEDGMENTS

Thanks to J. Emmett Duffy and two anonymous reviewers whose

comments greatly improved this manuscript. Thanks to Jan Roletto, Ruth

Howell, and the staff of the Gulf of the Farallones National Marine

Sanctuary for providing resources for JEB’s work on invasive species lists.

Author Contributions

Conceived and designed the experiments: JS JB. Performed the experiments: JS JB PR. Analyzed the data: JB. Wrote the paper: JS JB PR.

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