EUT ROPHI CAT I ON, AQUAT I C 209

contain less than 510 g L

-1
phosphorus and less than 250
600 g L
-1
nitrogen. These nutrient concentrations are at
least 2 to 10 times as high in eutrophic waters and can have
major effects on biotic communities, including the loss of
biodiversity and the invasion of nonnative species (Fig. 1).
NATURAL AND ANTHROPOGENIC
EUTROPHICATION
Eutrophication is a slow natural process. The slow accu-
mulation of nutrients is especially prevalent in deposi-
tional environments, such as lakes and wetlands, where
nutrients and sediments derived from a watershed are
collected in a basin and permanently or temporarily
immobilized and stored. For example, estuaries are natu-
rally eutrophic, and hence very productive, because they
receive nutrients derived from watersheds and tidal ows.
Lakes accumulate sediments and organic matter and over
time convert into productive and nutrient-rich shallow
lakes and emergent marshes. Other naturally eutrophic
systems are areas along the coast where upwelling con-
veys nutrient-rich water to the surface. As an ecosystems
nutrient status changes over millennial time scales, so
does its community structure, with local extinction and
colonization of new species working in concert to pro-
duce species-rich and productive ecosystems.
However, the process of eutrophication can be greatly
accelerated by human activities, such as runoff of excess fer-
tilizer, sewage efuent, and stormwater runoff. In Australia,
for example, sites affected by human activity have mean lev-
els of 780 g L
-1
N and 95 g L
-1
P compared to 300 g L
-1

N and 21 g L
-1
P at less impacted sites. Because estuaries
eradication an achievable goal. However, resprouting of cut
trees from stumps or lignotubers, which is advantageous in
some situations, makes control of eucalypts difcult. Con-
tinuously cutting back the regrowth can eventually kill
the tree, but this is a labor-intensive and expensive control
method. Herbicide applications (triclopyr or glyphosate) to
freshly cut stumps can greatly reduce resprouting. Because
eucalypts are valued as timber and ornamental trees in many
settings, biological control is very unlikely as an option.
SEE ALSO THE FOLLOWING ARTICLES
Allelopathy / Fire Regimes / Forestry and Agroforestry /
Invasiveness / Mycorrhizae / Propagule Pressure / Trees and Shrubs
FURTHER READING
Coates, P. 2006. American Perceptions of Immigrant and Invasive Species.
Berkeley: University of California Press.
Dez, J. 2005. Invasion biology of Australian ectomycorrhizal fungi intro-
duced with eucalypt plantations into the Iberian Peninsula. Biological
Invasions 7: 315.
Doughty, R. W. 2000. The Eucalyptus: A Natural and Commercial History
of the GumTree. Baltimore: The Johns Hopkins University Press.
Keane, P. J., G. A. Kile, F. D. Podger, and B. N. Brown, eds. 2000. Dis-
eases and Pathogens of Eucalypts. Collingwood, Australia: CSIRO
Publishing.
Nicolle, D. 2006. A classication and census of regenerative strategies in
the eucalypts (Angophora, Corymbia and EucalyptusMyrtaceae), with
special reference to the obligate seeders. Australian Journal of Botany
54: 391407.
Poore, M. E. D., and C. Fries. 1985. The Ecological Effects of Eucalyptus.
FAO Forestry Paper 59: 187. Rome: FAO.
Rejmnek, M., D. M. Richardson, S. I. Higgins, M. J. Pitcairn, and E.
Grotkopp. 2005. Ecology of invasive plants: State of the art (104161).
In H. A. Mooney, R. N. Mack, J. A. McNeely, L. E. Neville, P. J. Schei,
and J. K. Waage, eds. Invasive Alien Species: A New Synthesis. Washington,
DC: Island Press.
Ritter, M., and J. Yost. 2009. Diversity, reproduction, and potential for
invasiveness of Eucalyptus in California. Madroo (in press).
Slee, A. V., M. I. H. Brooker, S. M. Duffy, and J. G. West. 2006. Euclid:
Eucalypts of Australia, 3rd ed. Collingwood, Australia: CSIRO.
Williams, J., and J. Woinarski, eds. 1997. Eucalypt Ecology: Individuals to
Ecosystems. Cambridge: Cambridge University Press.
EUTROPHICATION,
AQUATIC
KATHARINA A. M. ENGELHARDT
University of Maryland Center for Environmental Science,
Frostburg
Eutrophication is the natural or anthropogenic accumula-
tion of nutrients in soil or water (from Greek eu = well and
trophe = nourished). Oligotrophic (low-nutrient) waters
FIGURE 1 The impacts of eutrophication on aquatic ecosystems.
(Figure developed by the Integration and Application Network of the
University of Maryland Center for Environmental Science.)
05_Simberloff10_E_p169-222.indd 209 9/13/10 10:02:36 AM
From Daniel Simberloff and Marcel Rejmnek, editors, Encyclopedia of Biological Invasions,
Berkeley and Los Angeles: University of California Press, 2011.
210 EUT ROPHI CAT I ON, AQUAT I C
Under nutrient-limited conditions, M. spicatum is a poor
competitor, owing to its poor root system and the ener-
getic demands of producing allelopathic compounds. But
under nutrient-rich conditions, M. spicatum is a superior
competitor because the species contains polyphenols that
render it allelopathic towards epiphytic algae. Native spe-
cies, on the other hand, accumulate algae on their leaves
and are therefore not as efcient in competing for light. In
the presence of algivorous snails, however, the abundance
of M. spicatum and native species reverses because the
snails decrease epiphytic biomass on the leaves of native
species, and the native species become less light limited.
Disturbance
Since Charles Elton published his famous book The Ecol-
ogy of Invasions by Animals and Plants on species inva-
sions in 1958, ecologists have argued that the risk of
invasion increases with declining species diversity. A pos-
sible explanation for this relationship is that a decline in
native species richness decreases nutrient uptake by the
community. Disturbance events may physically remove
biomass or change environmental conditions enough to
affect native species abundance and richness. Thus, dis-
turbances, through their effects on the existing commu-
nity, can decrease the ability of native species to respond
to eutrophication, thereby providing opportunities for
exotic species to invade and proliferate in an environment
with ample nutrients and fewer competitors.
Enemy Release
Species that are adapted to high resource availability gain
the most from being released from their native enemies
(enemy release). This is because high resource-adapted
and lakes typically attract large human populations, many
estuaries and lakes throughout the world are now highly
eutrophic. Unlike the slow natural eutrophication process,
anthropogenic eutrophication (or cultural eutrophication)
may be manifested in only a few years, leaving existing biota
little time to adjust. Thus, anthropogenic eutrophication
is typically associated with higher primary productivity
(greater than 1 g carbon/m/day), higher oxygen demand,
lower species richness, and changes in species abundances.
Owing to their high-nutrient status and stressed exist-
ing biotic communities, eutrophic water bodies are also at
higher risk of invasion by nonnative species, which can have
their own positive or negative feedbacks on eutrophication.
MECHANISMS OF INVASION
Competition
Changes in community structure with eutrophication are
predicted by plant competition theory. Competition for
belowground nutrients is predicted to drive the outcome
of species interactions under nutrient-limited conditions.
In contrast, competition for light is the dominant mecha-
nism when nutrients are abundant (Fig. 1). Thus, species
with high belowground biomass are predicted to prevail
under nutrient limitation, and species allocating biomass to
light harvesting leaves will succeed when nutrients are in
excess and light is more limiting. Not surprisingly, invasive
species are often weedy, with high aboveground growth
rates under nutrient-rich conditions. These same species are
often poor competitors when nutrients are limiting and the
native community is intact. Invasive species may be initially
very successful under nutrient-rich conditions, but without
new nutrient additions, they may decline in population size
as nutrients are immobilized and become more limiting.
Phosphorus is typically considered the main limiting
nutrient in freshwater systems, while nitrogen is typi-
cally the more limiting nutrient in saltwater, although
the nature of nutrient limitation varies greatly among
ecosystems. Increasing the abundance of nutrients in sys-
tems that are nutrient-limited can dramatically change
the competitive balance of plant communities (and entire
food webs that depend on them) by releasing plants from
competition and allowing some species to manifest their
invasive potential. For example, the community structure
of New England salt marshes has in some places shifted
to monocultures of the invasive common reed, Phrag-
mites australis (Fig. 2), owing to nitrogen eutrophica-
tion derived from shoreline development. Myriophyllum
spicatum, an invasive submersed aquatic macrophyte of
lakes and estuaries in the United States, gains competitive
advantage over native species in eutrophic conditions.
FIGURE 2 Common reed, Phragmites australis, in a mid-Atlantic marsh
of the United States. (Photograph courtesy of the author.)
05_Simberloff10_E_p169-222.indd 210 9/13/10 10:02:37 AM
EUT ROPHI CAT I ON, AQUAT I C 211
explain biologically generated internal eutrophication: (1)
root oxidation or respiration can change the redox poten-
tial of the sediments, which can bind or release nutrients
from the sediments (see above), and (2) plants can facili-
tate the release of nutrients to the water column when their
leaves turn over rapidly throughout the growing season.
plant species typically have high growth rates and do not
produce energetically costly antiherbivory defenses. In
their native habitat, therefore, these species are controlled
by coevolved herbivores and do not become abundant.
However, they become invasive when they are released
from their enemies in the introduced habitat. Thus,
enemy release and competitive release may act synergisti-
cally to allow invasive species adapted to high resource
availability to establish and expand quickly under eutro-
phic conditions. Biocontrolthe introduction of ene-
mies to combat invasive speciesis a way of curbing the
success of these invasive species.
INTERNAL EUTROPHICATION
Shallow lakes and wetlands are known for their ability
to remove nutrients from water through direct uptake
by plants, physical settlement of particles, and chemi-
cal immobilization of nutrients in sediments. However,
long-term observations in the Netherlands have shown
that wetlands can release nutrients bound in wetland
sediments. The increase of nutrient concentrations with-
out the external supply of nutrients is called internal
eutrophication and is most prevalent when water lev-
els are not allowed to uctuate naturally. This changes
the reduction-oxidation potential of the sediments. For
example, ferric iron bonds with phosphorus to form an
insoluble compound in aerobic conditions. But when
sediments are constantly ooded, ferric iron is reduced to
ferrous iron, and the iron complex releases the phospho-
rus. This process has led to changes in shoreline vegeta-
tion in Manitoba and Indiana. In Wisconsin, stable water
levels and internal eutrophication have been associated
with the expansion of invasive cattails (Typha sp.), which are
phosphorus limited and can take immediate advantage of
the released nutrients through clonal expansion (Fig. 3).
Internal eutrophication can also be caused by the
invasion of novel species with different phenologies or
ecophysiological traits. For example, purple loosestrife
(Lythrum salicaria) is rapidly displacing native vegetation
in some North American wetlands. The conversion of
cattail wetlands to loosestrife wetlands alters the timing of
litter input and releases phosphorus during a time when
other plants cannot use it. This asynchrony in phenology
increases downstream phosphorus loads, which effectively
accelerates eutrophication in downstream water bodies.
The subtropical cyanobacterium Cylindrospermopsis raci-
borskii has invaded shallow areas of Lake Balaton, Hun-
gary. It is a superior competitor for light and nutrients, and
its invasion success is attributed, in part, to its ability
to generate internal phosphorus. Two mechanisms can
FIGURE 3 Expansion of nonnative cattail (Typha glauca and T. angus-
tifolia) in a Wisconsin wetland with stabilized water levels (A) and T.
angustifolia and the native T. latifolia in a nearby wetland with uctuat-
ing water levels (B) over a period of 37 years. Radii of the clones spread
almost 4 m per year under stable water level conditions and 2.5 m under
uctuating conditions. (Figure courtesy of J. Zedler and A. Bairs.)
05_Simberloff10_E_p169-222.indd 211 9/13/10 10:02:38 AM
212 EUT ROPHI CAT I ON, AQUAT I C
can grow more quickly. However, after extensive public
comment, introduction of the Asian oyster was not rec-
ommended, owing to its invasion risk and potential com-
petitive effects on the native oyster.
MANAGEMENT OF TWO INSEPARABLE
ISSUES: EUTROPHICATION AND INVASION
Eutrophication and invasive species are typically assessed
as isolated problems in lake management, yet they are
often inseparably linked in aquatic ecosystems. The
proliferation of invasive aquatic species is in most cases
a result of anthropogenic eutrophication, often associ-
ated with other disturbances that decrease the integrity
of existing communities. Managing eutrophication and
invasive species needs to be done on a case-specic basis,
and no management strategy will t all cases because
the aquatic community, the watershed properties, and
the nature of limiting resources differ for each water
body. Invasive species can contribute to eutrophication
or ameliorate it. However, one thing is clear: to curb
the success of invasive species and minimize eutrophica-
tion, external nutrient loading must be decreased, which
requires a watershed approach that effectively and sub-
stantially decreases the multiple anthropogenic inputs
of nutrients into water bodies. In addition, the native
community may need to be actively restored to ensure
that native species can replace introduced species in the
food web.
SEE ALSO THE FOLLOWING ARTICLES
Competition, Plant / Enemy Release Hypothesis / Genotypes,
Invasive / Invasibility, of Communities and Ecosystems / Lakes /
Nitrogen Enrichment / Wetlands
FURTHER READING
Bertness, M. D., P. J. Ewanchuck, and B. R. Silliman. 2002. Anthropo-
genic modication of New England salt marsh landscapes. Proceedings
of the National Academy of Sciences USA 99: 13951398.
Blumenthal, D. M. 2006. Interactions between resource availability and
enemy release in plant invasion. Ecology Letters 9:887895.
Chase, J. M., and T. M. Knight. 2006. Effects of eutrophication and snails
on Eurasian watermilfoil (Myriophyllum spicatum) invasion. Biological
Invasions 8: 16431649.
Hastwell, G. T., A. J. Daniel, and G. Vivian-Smith. 2008. Predicting inva-
siveness in exotic species: Do subtropical native and invasive exotic
aquatic plants differ in their growth responses to macronutrients?
Diversity and Distributions 14: 243251.
Horne, A. J., and C. R. Goldman. 1994. Limnology. New York: McGraw-
Hill, Inc.
Khan, F. A., and A. A. Ansari. Eutrophication: An ecological vision. The
Botanical Review 71: 449482.
Scheffer, M. 1998. Ecology of Shallow Lakes. Dordrecht, The Netherlands:
Kluwer Academic Publishers.
AMELIORATING EUTROPHICATION
The proliferation of invasive species under eutrophic con-
ditions can have tremendous negative consequences for
ecosystem services (e.g., decreased water supply, altered
food web support through changes in sh and shellsh
populations, lowered recreational opportunities, impeded
navigation, damaged dams and support infrastructure).
However, through their enormous productivity, invasive
species have the capacity to remove nutrients from water,
which ameliorates the effects of eutrophication. If addi-
tional anthropogenic eutrophication does not occur, inva-
sive species may increase water quality and allow native
species to return and outcompete invasive species.
Human-made lakes often experience an initial period
of internal nutrient loading, which subsides as the eco-
system establishes. These lakes are often initially colo-
nized by invasive species, such as water hyacinth in Lake
Chivero, Zimbabwe, and water lettuce (Pistia statiotes) in
Lake Volta, Ghana. The invasive plants are highly produc-
tive initially, covering a big portion of the lake surface, but
then they often disappear or diminish in population size.
These boom and bust periods of aquatic invasive plant
species are typical and are often associated with changes
in the external and internal nutrient loading of the water
body, suggesting that the invasive species may ameliorate
the effects of eutrophication. If anthropogenic eutrophica-
tion is minimized, therefore, invasive aquatic weed infesta-
tions may correct themselves with or without additional
control measures.
The zebra mussel (Dreissena polymorpha), a freshwater
mussel native to southeast Russia, has become a prob-
lematic invasive species in many countries and was rst
detected in the United States and Canada in 1988. Since
then, the species has spread to many waterways with neg-
ative ecological and economic consequences. However,
zebra mussels are lter feeders and can therefore amelio-
rate the effects of nutrient pollution. This has beneted
native algae, which can grow to greater depths owing to
higher water clarity, and smallmouth bass (Micropterus
dolomieu) populations in Lake Erie.
Sometimes eutrophication may be ameliorated by the
intentional introduction of a new species. For example,
oysters are an important species in estuaries, where they
lter water and ameliorate the effects of pollution. In the
eastern United States, the native Eastern oyster (Cras-
sostrea virginica) declined in the Chesapeake Bay, owing
to many factors, including eutrophication of the estuary.
The suminoe, or Asian oyster (Crassostrea ariakensis), was
proposed for introduction in the Chesapeake Bay in the
United States because it is more resistant to disease and
05_Simberloff10_E_p169-222.indd 212 9/13/10 10:02:39 AM
EVOLUT I ONARY RES PONS E, OF NAT I VES TO I NVADERS 213
these changes must also be established in order to attri-
bute changes in natives to evolution, as opposed to plastic
responses of natives to invaders.
EVIDENCE FOR EVOLUTION IN NATIVES
CAUSED BY INVASIONS
We have relatively few examples of evolutionary changes
in native species caused by introduced species, despite the
probable ubiquity of this phenomenon. This paucity of
examples arises largely from a lack of documentation of
native traits prior to introductions. To document rigor-
ously that invaders are the causal agent of evolution in
natives, one would ideally have samples of individu-
als from the same native populations both before and
after invasion. One would also like to observe paral-
lel responses in multiple native populations that have
experienced independent invasions by the same invader.
Breeding experiments would then be required to docu-
ment that the observed changes in traits of native species
are heritable. Together, such data would provide compel-
ling circumstantial evidence that invaders are likely the
source of differences in native populations before and
after invasion.
We rarely have such a complete body of evidence. Some
of the best cases in which there is documented evolution
in response to an invader come from insect herbivores
and their host shifts onto introduced host plants. Soap-
berry bugs (Jadera) and their close relatives (Leptocoris)
have colonized several species of introduced ornamental
trees and vines in the Sapindaceae that are related to the
bugs native host plants in the United States and Australia.
Initially, performance of bugs on introduced hosts was
lower than on native hosts, but bugs evolved behavioral,
morphological (including longer beak size), physiological,
and life history adaptations that increased the efciency
of host exploitation over 30 to 50 years (fewer than 100
generations). Similarly, some populations of Euphydryas
editha butteries have evolved to prefer an introduced
weed Plantago lanceolata over their native host plants.
In general, exotic plants are probably exerting selection
on many native insect herbivore taxa and are likely caus-
ing evolutionary changes in these insects. For example,
82 of 236 buttery species (34%) in California have been
reported as ovipositing or feeding on introduced plant
taxa. Not all of these host shifts require genetic changes,
but the ability to use new hosts effectively likely does, as
the cases above demonstrate. Few of these host shifts have
been rigorously investigated with respect to their under-
lying genetic basis and their impacts on the evolution of
native insects.
Wetzel, R. G. 2001. Limnology: Lake and River Ecosystems. San Diego, CA:
Academic Press.
Williams, A. E., and R. E. Hecky. 2005. Invasive aquatic weeds and
eutrophication: The case of water hyacinth in Lake Victoria (187
225). In M. V. Reddy, ed. Restoration and Management of Tropical
Eutrophic Lakes. Enfield: Science Publishers, Inc.
EVOLUTIONARY
RESPONSE, OF NATIVES
TO INVADERS
SHARON Y. STRAUSS
University of California, Davis
Introduced species may act as strong agents of selection
on native species, either as a result of their direct inter-
actions with natives or through indirect interactions. The
ways in which introduced species can inuence natives
are as complex as the ways that any species can interact
with any others in complex and diverse communities.
Evolutionary changes of large magnitude can occur very
rapidly, over decades or less, and are not relegated to geo-
logical timescales. Some of the best-documented cases of
rapid evolution have come from human-caused impacts
on natural populations, such as overharvesting or the
effects of species introductions.
THE DYNAMISM OF SPECIES AND THE
DETECTION OF CHANGE
It is generally a mistake to think of either native or inva-
sive species as static entities; the outcomes and impacts of
invaders on native ecosystems will depend on the dynamic
capacity of both introduced and native species to evolve.
The ability of natives to evolve in response to invaders
may lessen the negative impacts of some invaders or even
allow natives to benet from them. Alternatively, the
inability of natives to adapt to antagonistic invaders can
lead to extirpation or massive declines in native species.
While we expect that there have already been dramatic
effects of invaders on the evolution of many native spe-
cies, the ability to detect evolutionary changes in natives
that one can ascribe specically to effects of exotic spe-
cies requires painstaking experimentation and correlative
work. Often, we rely on time series data or historical col-
lections to compare changes in traits as a result of history
of a native with an invader. Moreover, the genetic basis of
05_Simberloff10_E_p169-222.indd 213 9/13/10 10:02:40 AM