DOI: 10.1126/science.1173651, 734 (2009);324 Science

Marnie E. Rout and Ragan M. CallawayAn Invasive Plant Paradox

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8 MAY 2009 VOL 324 SCIENCE www.sciencemag.org734

PERSPECTIVES

Oscillation (NAO) is the main mode of interan-

nual to interdecadal climate variability in the

North Atlantic. By altering circulation patterns

in the northwest Atlantic, the NAO can affect

the bottom temperatures throughout the region.

During positive NAO conditions, volume

transport in the Labrador Current increases,

resulting in colder bottom temperatures and

lower salinities in the shelf waters north of the

tail of Newfoundland’s Grand Banks (3). The

reverse occurs during negative NAO condi-

tions. Paradoxically, because of a bifurcation in

the Labrador Current near the tail of the Grand

Banks, responses to the NAO downstream of

this point are reversed, with bottom waters

tending to be warmer and saltier during positive

NAO conditions and colder and fresher during

negative NAO conditions.

During the 1960s, negative NAO condi-

tions predominated, and the Gulf of Maine

stock of northern shrimp thrived in the colder

bottom temperatures. During the 1970s, the

NAO shifted into a predominantly positive

phase and the stock collapsed. Although

overfishing cannot be excluded as a con-

tributing factor to this collapse (1), environ-

mental conditions in the gulf were certainly

more favorable physiologically for northern

shrimp in the 1960s than the 1970s.

The NAO has remained in a predominantly

positive phase since the 1970s, yet northern

shrimp stocks throughout the northwest

Atlantic increased to relatively high abun-

dances during the early 1990s (1). This

increase has been attributed to two factors.

First, the abundance of groundfish predators

(especially cod) that feed on northern shrimp

declined, mostly as a result of overfishing (4).

This release of predation pressure must have

boosted shrimp survivorship dramatically.

Second, atmospheric changes in the Arctic

resulted in two large salinity anomalies—

pulses of anomalously cold, low-salinity

water—entering the northwest Atlantic’s shelf

circulation (5). Throughout the region, surface

waters freshened and became more stratified,

enhancing phytoplankton production during

autumn and winter. Favorable feeding condi-

tions during these seasons may have con-

tributed to the reproductive success and larval

survival of northern shrimp.

The future distributional range of northern

shrimp will reflect the interplay between cli-

mate-associated changes in the ocean and the

demographic responses of a stock-structured

population. It is commonly assumed that more

northerly species will contract their ranges in

response to climate warming, but just the

opposite has been seen during recent decades

in at least one part of the northwest Atlantic

(5). In shelf ecosystems upstream of the tail of

the Grand Banks, the predominantly positive

NAO conditions since the 1970s have led to

colder bottom waters that are physiologically

favorable for boreal species like the northern

shrimp. Episodic large salinity anomalies have

reinforced this bottom-water cooling for sev-

eral years in each decade since the 1970s (6).

Colder bottom temperatures not only

offer physiological advantages for northern

shrimp; they also provide an ecological

advantage by slowing the growth and repro-

ductive rates of cod, its principal predator

(7). The recovery of cod stocks from over-

fishing has been suppressed by the same cold

temperatures that have enabled stocks of

northern shrimp and snow crab to flourish.

The expanded shrimp and snow crab fish-

eries have been more lucrative than the cod

fishery ever was. The sustainability of

marine fisheries will depend on scientific

advances that enable managers to better

anticipate the responses of stock-structured

populations to an ever-changing climate (8).

References and Notes

1. P. Koeller et al., Science 324, 791 (2009).

2. Marine Ecosystem Responses to Climate in the North

Atlantic Working Group, Oceanography 14, 76 (2001).

3. J. W. Loder et al., Deep-Sea Res. II 48, 3 (2001).

4. B. Worm, R. A. Myers, Ecology 84, 162 (2003).

5. C. H. Greene et al., Ecology 89 (suppl.), S24 (2008).

6. I. M. Belkin, Geophys. Res. Lett. 31, L08306;

10.1029/2003GL019334 (2004).

7. G. A. Rose, B. deYoung, D. W. Kulka, S. V. Goddard, G. L.

Fletcher, Can. J. Fish. Aquat. Sci. 57, 644 (2000).

8. C. H. Greene et al., Oceanography 22, 210 (2009).

9. R. Ueyama, B. C. Monger, Limnol. Oceanogr. 50, 1820

(2005).

10. This Perspective was developed during the synthesis

phase of the U.S. Global Ocean Ecosystem Dynamics

Northwest Atlantic/Georges Bank Program. We thank I.

Belkin, P. Koeller, D. Mountain, and G. Rose for their

comments.

10.1126/science.1173951

One reason that invasive plants may thrive in

new environments is their interactions with soil

microbes that increase nitrogen cycling.An Invasive Plant ParadoxMarnie E. Rout and Ragan M. Callaway

PLANT SCIENCE

Why some plants attain extremely

high densities in communities

where they are exotic, yet remain at

low densities in their native ranges is a mys-

tery. The pattern has been called a “paradox”

because it conflicts with long-held ideas about

the importance of local adaptation for the eco-

logical performance of organisms (1). This

biogeographical shift may be connected to

other apparent ecological paradoxes that occur

with plant invasions involving processes medi-

ated by soil microbes. Invasions can decrease

plant species diversity but also increase

plant productivity. Rather than depleting soil

resources as productivity increases, invasions

often increase soil stocks, pools, and fluxes of

nitrogen through processes regulated by

microbial communities.

Plant species richness and functional diver-

sity can increase local net primary productivity

(see the figure), predominantly through more

complete use of resources, or “niche comple-

mentarity” (2). Exotic plant invasions locally

reduce native plant diversity, often to the point

of becoming the only plant species present (3).

However, contrary to what diversity-produc-

tivity experiments would predict, net primary

productivity typically increases with exotic

invasions (4–6). In a recent meta-analysis of 94

studies, the average increase in annual net pri-

mary productivity was over 80% in invaded

ecosystems (6). This “invasion-diversity-pro-

ductivity” paradox cannot be explained by

niche complementarity, but differences in

plant-soil-microbe interactions in the invaded

and native ranges could perhaps provide part

of the answer. Soil microbes can have strong

density-dependent effects on plants, often

called plant-soil-microbe feedbacks (7). These

feedbacks are usually neutral or negative for

plants in soils from their native ranges, but can

be positive for invasive plants in soils from

invaded ranges (8, 9). This directional shift is

likely due to the absence of evolved species-

specific plant-pathogen relations for the inva-

sive plants (9). This absence likely enhances

the competitive dominance of plant species in

new ranges and increases their productivity.

Nitrogen is the primary factor limiting net

primary productivity in most ecosystems (10),

Division of Biological Sciences, University of Montana,Missoula, MT 59812, USA. E-mail: marnie.rout@mso.umt.edu

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and short-term increases in this productivity

(for example, as a result of agricultural prac-

tices) typically deplete nitrogen and other soil

resources. By contrast, plant invasions

increase soil nitrogen pools and total ecosys-

tem nitrogen stocks (6, 11, 12). Soil nitrogen

is regulated by the activity of soil-dwelling

and mutualistic microbes. On average,

invaders double litter decomposition rates,

and increase both soil nitrogen mineralization

and nitrification by over 50% (6). For exam-

ple, the invasive trees Acer platanoides and

Ailanthus altissima increase net nitrogen min-

eralization, net nitrification, and soil nitrogen

availability compared to native tree species,

including the congener Acer saccharum (13).

How do invasive plants decrease species

diversity but increase soil nitrogen and net pri-

mary productivity? Invaders might possess

morphological or biochemical traits that differ

from those of native species in ways that

increase nitrogen cycling in the soil. For exam-

ple, thinner chlorophyll-enriched leaves that

are also lower in structural carbon (characteris-

tics that promote rapid growth) could be impor-

tant traits for invasive success. Such character-

istics would allow more rapid leaf decomposi-

tion, creating litter that contains a higher con-

centration of nitrogen (higher litter quality).

Increased litter deposition rates or litter quality

(14) could then explain increased nitrogen

pools, stocks, and fluxes in soil. However, leaf

traits may not provide all of the answers.

Invaders vary widely in leaf traits, and invasive

plant species do not appear to initiate the same

chain of ecosystem changes in their home

ranges. For example, Spartina alterniflora is

native to eastern North America but is an

aggressive invader in China where it has a

greater leaf area index [(LAI), the ratio of leaf

surface areas to ground surface area]. A higher

LAI indicates that a plant produces a denser

canopy (larger sized and greater quantity of

leaves) in the invaded range (5). Reciprocally,

Phragmites australis is native to China but is a

highly successful invader in North America

where it has greater net primary productivity

(5). If invasive species enhance net primary

productivity and nitrogen cycling in invaded

ranges but not in their native ranges, then the

inherent traits of plants are unlikely to drive

these processes as these alterations should

also be occurring in the native ranges.

Alternatively, invasive plants may undergo

rapid natural selection for such key leaf traits

only in invaded ranges. For example, the inva-

sive aster Ageratina adenophora (see the fig-

ure), which is native to Mexico, is an invader

throughout the subtropics and appears to have

evolved increased nitrogen allocation to pho-

tosynthesis and reduced allocation to cell

walls in the absence of specialist herbivores

(15). This would make leaves easier to decom-

pose and suggests a potential mechanism by

which invaders might possess leaves with

traits that enhance nitrogen cycling in the soil

of invaded ecosystems.

Soil microbes might simply be passengers

in the process of increasing nitrogen pools and

fluxes. However, invaders and soil microbes

might interact in a biogeographically explicit

way, as is often seen for plant-soil-microbe

feedbacks (9), allowing the microbial com-

munity to drive changes in the nitrogen cycle

that occur with plant invasions. Such shifts in

plant-soil-microbe feedbacks would indicate

that communities of soil microbes and plants

have regional evolutionary trajectories in dif-

ferent parts of the world, and that mixing

plants and soil microbes from different evolu-

tionary trajectories might alter ecosystem

functions. If microbial communities responsi-

ble for various ecosystem processes (includ-

ing nitrogen fixation, nitrification, ammonifi-

cation, and organic matter decomposition)

interact with invasive plants in ways deter-

mined by evolution and biogeography, then

this may help to explain the apparent paradox

of increased nitrogen pools and fluxes with

plant invasions.

What is needed are biogeographical com-

parisons of soil microbial communities and

of the processes by which they drive plant

invasions, specifically in native and invaded

ranges. For example, invasion by some exotic

grasses corresponds with increased soil nitri-

fication rates and higher abundance and

diversity of ammonia-oxidizing bacteria in

invaded ranges (16). Additionally, nitrifica-

tion rates positively correlate with changes in

the bacterial community, suggesting a mech-

anism for increased nitrogen cycling in these

invaded soils. As our understanding of micro-

bial biogeography and associated functional

differences expands, we may learn much

about regional evolutionary relationships

among plants and soil microbes and how this

affects ecosystem functioning.

References and Notes1. D. Sax, J. H. Brown, Global Ecol. Biogeogr. 9, 363 (2000).

2. D. U. Hooper et al., Ecol. Monogr. 75, 3 (2005).

3. W. M. Ridenour, R. M. Callaway, Oecologia 126, 444

(2001).

4. S. Vanderhoeven et al., Plant Soil 275, 169 (2005).

5. C. Liao et al., Ecosystems 10, 1351 (2007).

6. C. Liao et al., New Phytol. 177, 706 (2008).

7. W. H. van der Putten, C. van Dijk, B. A. M. Peters, Nature

362, 53 (1993).

8. R. M. Callaway et al., Nature 427, 731 (2004).

9. K. O. Reinhart, R. M. Callaway, New Phytol. 170, 445

(2006).

10. P. M. Vitousek, R. W. Howarth, Biogeochemistry 13, 87

(1991).

11. J. G. Ehrenfeld, Ecosystems 6, 503 (2003).

12. M. E. Rout, T. H. Chrzanowski, Plant Soil 315, 163 (2009).

13. L. Gomez-Aparicio, C. D. Canham, Ecol. Monogr. 78, 69

(2008).

14. R. R. Blank, Invasive Plant Sci. Manage. 1, 226 (2008).

15. Y.-L. Feng et al., Proc. Natl. Acad. Science U.S.A. 106,

1853 (2009).

16. C. V. Hawkes et al., Ecol. Lett. 8, 976 (2005).

17. Data from table 1 and figure 3 (flow chart) of (6) were

used to generate the dashed line in the figure. The

data used were the mean increase of 83% net primary

productivity (NPP, also called ANPP in table 1) in

invaded systems.

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Number of plant species

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0 1 2 3 4 5 6 7 8 9 10 11

Invaded communities

Native communities

Diversity and productivity. Plant productivity increases to an asymptote as plant diversity increases [solidline; derived from (2) with permission from the Ecological Society of America]. Higher productivity correlateswith losses in native species richness, and invasives dominate [dashed line; estimated from (6); see (17)]. Theasymptote remains higher due to invader presence in the system at lower relative densities. (Inset) The photoshows A. adenophora.

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