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And the haplochromines, models of explosive radiation,
continue to evolve rapidly: many remaining species now
display adaptations (such as increased gill surface area for
enhanced oxygen uptake) that facilitate their coexistence
with Nile perch.
The immediate future of the fisheries and remaining biodiversity of Lake Victoria hinges largely on fishing pressure. Recent models suggest that a 20 percent
increase in fishing effort could drive Nile perch biomass
down further—to extinction in some areas, stabilizing
at low levels in others—enhancing the resurgence of the
remnant native fauna. But eradicating the Nile perch
would have complex and unpredictable consequences on
biodiversity and human welfare, many of them undesirable. The seemingly optimal strategy is maintenance of
fishing effort at levels high enough to allow the persistence of native fishes yet not high enough to extinguish
Nile perch, while attempting to reverse eutrophication—a delicate balancing act. At present, management
organizations and the lake’s three governments are incapable of regulating fishing effort so precisely; Lake Victoria remains, for all practical purposes, an open-access
resource.
SEE ALSO THE FOLLOWING ARTICLES
JAE R. PASARI, PAUL C. SELMANTS, HILLARY
YOUNG, JENNIFER O’LEARY AND ERIKA
S. ZAVALETA
University of California, Santa Cruz
Nitrogen (N) is abundant on Earth in the form of atmospheric dinitrogen (N2), but its availability to organisms
is strongly limited by processes that convert N2 to biologically available (reactive) forms. Historically, fixation
by N-fixing microbes and (to a lesser extent) lightning
provided all reactive N. Through the production of synthetic nitrogen fertilizers, land management changes, and
fossil fuel combustion, humans now add approximately
150 Tg/year more reactive nitrogen (N) to the surface
of the Earth, more than doubling the N available to
biotic organisms over the last 200 years. N enrichment
is particularly acute in most of the world’s biodiversity
hotspots, and it is expected to double again in the next
50 to 100 years. N enrichment favors nitrophilic organisms (often exotic invaders) over many native species,
resulting in biodiversity changes and losses.
Eutrophication, Aquatic / Fishes / Invasion Economics / Lakes
NITROGEN ENRICHMENT IN
TERRESTRIAL SYSTEMS
FURTHER READING
Nitrogen Enrichment Effects on
Plant Communities
Balirwa, J. S., C. A. Chapman, L. J. Chapman, I. G. Cowx, K. Geheb, L.
Kaufman, R. H. Lowe-McConnell, O. Seehausen, J. H. Wanink, R. L.
Welcomme, and F. Witte. 2003. Biodiversity and fishery sustainability in the Lake Victoria basin: An unexpected marriage? BioScience 53:
703–715.
Chapman, L. J., C. A. Chapman, L. Kaufman, F. Witte, and J. Balirwa.
2008. Biodiversity conservation in African inland waters: Lessons of
the Lake Victoria region. Verhandlungen Internationale Vereinigung
Limnologie 30: 16–34.
Geheb, K., S. Kalloch, M. Medard, A. Nyapendi, C. Lwenya, and M.
Kyangwa. 2008. Nile perch and the hungry of Lake Victoria: Gender,
status and food in an East African fishery. Food Policy 33: 85–98.
Goldschmidt, T. 1996. Darwin’s Dreampond: Drama in Lake Victoria.
Cambridge, MA: MIT Press.
Goudswaard, P. C., F. Witte, and E. F. B. Katunzi. 2007. The invasion of
an introduced predator, Nile perch (Lates niloticus, L.) in Lake Victoria
(East Africa): Chronology and causes. Environmental Biology of Fishes
81: 127–139.
Kaufman, L. 1992. Catastrophic change in species-rich freshwater ecosystems. BioScience 42: 846–858.
Pringle, R. M. 2005. The Nile perch in Lake Victoria: Local responses and
adaptations. Africa 75: 510–538.
Pringle, R. M. 2005. The origins of the Nile perch in Lake Victoria. BioScience 55: 780–787.
Witte, F. M., J. H. Wanink, and M. Kishe-Machumu. 2007. Species distinction and the biodiversity crisis in Lake Victoria. Transactions of the
American Fisheries Society 136: 1146–1159.
488
NITROGEN ENRICHMENT
NITROGEN ENRICHMENT
Most terrestrial ecosystems are N limited, and 70 percent of global N enrichment occurs on land. The majority of this enrichment is a result of the production of
synthetic nitrogen fertilizers, land management changes,
and fossil fuel combustion. Fertilization of N-limited
environments typically results in increased productivity,
reduction in plant density and diversity, and increases
in the size and abundance of nitrophilic species, particularly grasses. In addition to anthropogenic N enrichment, increases in abundance or extent of plants with
N-fixing symbionts, high N litter, or susceptibility to
periodic mass insect herbivory can also substantially
enrich localized areas, advantaging nitrophilic invaders. These phenomena have increased the abundance of
invasive grasses in coastal California grasslands after N
enrichment from leguminous shrubs and have led to the
dominance of grasses across many northern European
heathlands.
Communities most at risk from N enrichment include
those in historically nutrient-poor environments, those
Disturbance
factors
Increased
N deposition
Stress
factors
(+)
N availability
N uptake
N limitation
P limitation
Competition
stress
Changes in
species
composition
Shoot/Root
ratio
(–)
Mycorrhiza
Productivity
(+)
[N] biomass
Litter
production
(+)
(+)
[N] litter
N
mineralization
FIGURE 1 Schematic representation of the main effects of increased
atmospheric N deposition on vegetation processes in terrestrial ecosystems. (From Aerts, R., and R. Bobbink. 1999. The impact of atmospheric
nitrogen deposition on vegetation processes in terrestrial, non-forest
ecosystems. In S. J. Langan, ed. The Impact of Nitrogen Deposition on
Natural and Semi-natural Ecosystems. Kluwer Academic Publishers.
With kind permission of Springer Science and Business Media.)
containing grasses with a high potential for competitive
dominance after N enrichment, and those containing rare
species that are likely to go locally extinct under competition with expanding nitrophilic species. The response of
plant species to N enrichment varies according to plant
traits, community traits, abiotic factors such as climate
and precipitation, the form of N deposited (ammonia,
nitrate, or gaseous NOx), and the amount of N deposited,
with high deposition leading to acidification in addition
to fertilization (Fig. 1).
Effects of Nitrogen Enrichment on Invasions
Examples of N enrichment facilitating plant invasions are
most pronounced in low-nutrient, forb- and shrub-dominated ecosystems invaded by nitrophilic grasses. These
systems include mesotrophic fens, ombrotrophic bogs,
calcareous grasslands, neutral-acid grasslands, montane
subalpine grasslands, lowland dry heathlands, lowland
wet heathlands, arctic and alpine heaths, serpentine grasslands, and some deserts. Loss of plant species diversity
and the accompanying increase in grass dominance occur
at deposition levels as low as 5 kg/ha/year—levels currently experienced in and around many urbanized regions
worldwide. In addition, ecosystems naturally dominated
by C4 grasses are at risk of invasion by nitrophilic C3
grasses under conditions of long-term, low-level N fertilization, as has occurred in Minnesota tallgrass prairies.
Other, more nutrient-rich systems are also susceptible to
invasion under N enrichment, including forest understories
and cold deserts. In the cold deserts of the Colorado plateau, an N-fixing biological soil crust historically provided
N to plants. Destruction of this crust in combination with
aerial nitrogen deposition has altered the type and timing
(although not the amount) of N deposition, resulting in
increased success of the invasive thistle Salsola iberica.
Finally, there are numerous cases in which nitrogen
enrichment, though expected to advantage certain exotics, has not been found to influence invader impact,
including grass invaders in Dutch dune grasslands and
California sage scrublands, and diffuse knapweed (Centaurea diffusa) in grasslands of western North America.
Mechanisms of Invasion
There are several N use and acquisition stages that
determine a plant’s growth and competitiveness under
N enrichment. These stages include photosynthetic tissue allocation, photosynthetic nitrogen use efficiency,
nitrogen fixation, nitrogen-leaching losses, gross nitrogen mineralization, and plant nitrogen residence time. In
many cases, invasiveness in plants can be traced back to
strategies at one of these stages relative to the strategies
of native competitors. For example, exotic C3 plants are
generally observed to outcompete native C4 grasses in
N-enriched systems because of the lower photosynthetic
N use efficiency of C3 plants, a phenomenon which is
magnified as atmospheric carbon dioxide concentrations
increase. Similarly, one mechanism explaining the success
of alien Eurasian annual grasses in formerly perennialdominated, nutrient-poor California grasslands is the
difference between their photosynthetic tissue allocation
strategies under N enrichment. While native California
grasses and forbs tend to store added N in existing tissues,
Eurasian annuals use added N to produce new shoot tissue, a strategy they evolved in their more fertile region of
origin. Likewise, species that facilitate a high soil nitrification ratio (nitrification rate/ammonification rate × 100)
tend to grow more under N enrichment. Invasive species
in some regions also have higher nitrate reductase activity
than natives, giving the former an advantage.
Even though these traits help explain and predict
plant invasiveness under N enrichment, meta-analyses of
N enrichment experiments suggest that complex interactions among invader traits, community traits, and abiotic environmental factors determine which plants will
win and which will lose under N enrichment. While the
ability of a plant to increase production following enrichment appears to be a good predictor of its invasibility,
NITROGEN ENRICHMENT
489
the impact of N enrichment and invasion on community
richness is also a function of soil cation exchange capacity (CEC) and regional temperatures (with lower CEC
and temperatures resulting in greater impact). Finally,
N enrichment (particularly at high ammonia concentrations) can decrease frost, drought, and disease tolerance,
and thereby reduce the competitive ability of natives
compared to invaders that can tolerate high enrichment
levels and environmental stress.
Cessation of Nitrogen Enrichment
The effects of N enrichment on plant communities can
persist well beyond the period of enrichment. While species richness (but not abundances) returned to preenrichment levels after cessation of N enrichment in Minnesota
tallgrass prairies, periodic cycles of invasion and depressed
richness continued for decades after cessation of N enrichment in Colorado shortgrass steppe, suggesting that N
enrichment can initiate time-lagged biotic inertias that
preclude return to previous conditions.
NITROGEN ENRICHMENT IN COASTAL
MARINE SYSTEMS
Coastal waters are being enriched with N and phosphorus (P) through both point-source and non-point-source
pollution. However, because most coastal systems are N
limited, N generally has a higher impact than P in these
systems. On a global scale, human activity has doubled
the N flux from land to ocean, and most of this increase
has occurred in the last several decades.
N additions to coastal waters can facilitate invasions
of alien marine algae (seaweeds) by increasing their competitiveness relative to native seaweeds. Siphonous, unicellular seaweeds are some of the most common invaders
and include the genera Codium, Caulerpa, and Bryopsis.
These seaweeds grow rapidly, quickly heal wounds, and
can reproduce both sexually and asexually.
One third of all seaweed invasions have occurred in the
Mediterranean Sea. For example, invasive seaweeds Caulerpa taxifolia and C. racemosa outcompete the endemic
Mediterranean seagrasses Posidonia oceanica and Cymodocea nodosa and reduce overall species richness. Caulerpa
spp. especially outcompete natives in areas of high nutrient input from urbanization. While native seagrasses
(such as P. oceanica and C. nodosa) obtain much of their
nutrient demand via roots, seaweeds with rhizomes (such
as Caulerpa spp.) can utilize nutrients in both sediments
and the water column. Furthermore, Caulerpa reduces
the sediment nutrient supply to native seagrasses, leading
to decreased growth and increased mortality.
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NITROGEN ENRICHMENT
Another member of the genus Caulerpa responds similarly to nutrient loading associated with urbanization in
coastal waters along the eastern coast of the United States.
In southeastern Florida’s coral reef habitats, N enrichment
contributes to an explosive invasion of Caulerpa branchypus var. parvifola, which outcompetes native algae because
of lower N limitation.
These examples illustrate how anthropogenically
derived N can enhance the success of invasive seaweeds,
particularly in the genus Caulerpa. However, direct testing of the nutrient enhancement hypothesis has been
limited, and experimental results are mixed. For example,
nutrient additions do not stimulate growth rates for the
red seaweeds Acanthopora spicifera or Hypnea musciformis,
which were introduced from the Caribbean to Hawai‘i.
NITROGEN ENRICHMENT ON
OCEANIC ISLANDS
Island ecosystems are disproportionately impacted by
invasive species. There are many potential drivers for
the apparently higher vulnerability of island ecosystems
to invasions, and the importance of a particular driver
varies by system. However, the relatively high availability
of nutrients, including N, on some islands appears to be
important among these invasion drivers. The high availability of N (as well as other resources) on many oceanic
islands is in part a result of the limited plant communities
present in these systems. The composition of indigenous
plant communities on oceanic islands is usually limited by
both space and propagule availability. These communities
therefore often possess some combination of low species
richness, few specialist species, and missing functional
groups. As a result, island plant communities often use N
incompletely in space and time, creating high net N availability compared to continental systems. Alien species,
which often have stronger growth responses to nutrient
enrichment than native island species, as well as higher
plasticity to varying resource environments, can take better advantage of underutilized N. Invasive plants may also
possess functional traits not represented in native island
flora, allowing acquisition of unexploited N resources and
sometimes triggering further N enrichment.
In Hawai‘i, the establishment of Morella (Myrica)
faya provides an excellent example of a positive feedback
loop between exotic invasion and N enrichment. Morella
(Myrica) faya is an N-fixing tree introduced to Hawai‘i,
where it colonizes recent lava flows, an environment
where no native nitrogen fixing native plants can establish. Morella (Myrica) faya vastly increases N availability, which changes the course of ecosystem development
to further facilitate other invasive organisms. Invasive
grasses, including Andropogon virginicus and Schizachyrium condensatum, and invasive earthworms flourish in
areas enriched by Morella (Myrica) faya. These invaders alter ecosystem processes, including fire regimes and
nutrient cycling, further facilitating invasions.
Islands are also notable for the large quantity of their
N that arrives as subsidies from the marine environment
via marine wash, terrestrial animals foraging in the intertidal, and marine animals that forage at sea but rest or
breed on land (primarily seabirds but also marine mammals and sea turtles). Changes in any of these subsidy
patterns can have large impacts on the entire nutrient
budget of the island and can thus trigger invasions. N
enrichment by ring-billed gulls and king penguins has
facilitated plant invasions on islands in the Georgian Bay
and Great Lakes region, and in the Crozet Archipelago,
respectively.
MANAGEMENT, RESTORATION, AND POLICY
Prevention, management, and restoration of invaded and
N-enriched systems can be attempted at several scales. At
the local scale, managers can apply “ecological filters” to
reduce competitive advantages conferred on nitrophilic
invaders by N enrichment. The majority of research
aimed at managing excess N through the application of
ecological filters has been done in low-nutrient, forband shrub-dominated ecosystems of North America and
western Europe. Amending soil with labile carbon such as
sucrose or sawdust can increase microbial N immobilization, thus reducing N available to introduced nitrophilic
plant species. This approach has been shown to successfully reduce plant-available N and exotic plant biomass in
Minnesota wetland sedge meadows, Colorado shortgrass
steppe, Manitoba and Minnesota tallgrass prairies, and
California coastal grasslands. However, the benefits to
native species are inconsistent, calculating the amount of
carbon necessary to stimulate increased N immobilization
is difficult, the effect is short lived, and repeatedly adding
labile carbon across large areas is expensive. In addition,
enhanced N immobilization by soil microorganisms can
reduce N losses, leading to a greater accumulation of N
within the ecosystem. Repeated prescribed burns have
been used with some success in California chaparral and
tallgrass prairie ecosystems of the central United States to
control invasive annual grasses over the short term, while
volatilizing excess N contained in biomass at the same
time. Prescribed burns are most effective in fireprone
ecosystems; they can be counterproductive in the case of
some invasives such as Bromus tectorum and Taeniatherum
caput-medusae, both of which spread more rapidly with
frequent fires. Light to moderate grazing and mowing
combined with biomass removal before seed set have also
been used to control exotic invasion of N-enriched ecosystems in California serpentine grasslands, European calcareous grasslands, and semiarid grasslands in Utah and
Colorado. Both prescribed fire and grazing result in a net
export of N from the ecosystem, but grazing may be the
more targeted approach because cattle often preferentially
consume exotic, nitrophilic grasses over native forbs. If
grazing is preferred and feasible, then careful monitoring of stocking levels is necessary because overstocking
may exacerbate invasion. A relatively untested approach
to restoring N-enriched ecosystems that are already heavily invaded involves the use of early seral “bridge species”
with traits similar to existing or potential invaders. This
approach may facilitate establishment of natives that can
compete with exotic invaders and can be used in combination with one or more of the N-reducing management
techniques described above.
At regional scales, mitigation and the establishment of
critical loads are the primary policy tools used to address
the spread of invasions under N enrichment. Mitigation
requires that parties that cause N enrichment must purchase and manage sensitive lands to reduce the impacts
of invasive species and preserve native communities. In
addition, some regions in Europe with high levels of N
enrichment have set critical loads that have been calculated to estimate the highest amount of N enrichment
that an ecosystem can tolerate and still maintain its native
plant communities.
SEE ALSO THE FOLLOWING ARTICLES
Eutrophication, Aquatic / Freshwater Plants and Seaweeds / Islands /
Land Use / Mediterranean Sea: Invasions / Transformers
FURTHER READING
Adams, M. B. 2003. Ecological issues related to N deposition to natural
ecosystems: Research needs. Environment International 29: 189–199.
Aerts, R., and R. Bobbink. 1999. The impact of atmospheric nitrogen deposition on vegetation processes in terrestrial, non-forest
ecosystems (85–122). In S. J. Langan, ed. The Impact of Nitrogen
Deposition on Natural and Semi-natural Ecosystems. Kluwer Academic
Publishers.
Fenn, M. E., J. S. Baron, E. B. Allen, H. M. Rueth, K. R. Nydick, L.
Geiser, W. D. Bowman, J. O. Sickman, T. Meixner, D. W. Johnson,
and P. Neitlich. 2003. Ecological effects of nitrogen deposition in the
western United States. Bioscience 53: 404–420.
Galloway, J. N., A. R. Townsend, J. W. Erisman, M. Bekunda, Z. Cai,
J. R. Freney, L. A. Martinelli, S. P. Seitzinger, and M. A. Sutton. 2008.
Transformation of the nitrogen cycle: Recent trends, questions, and
potential solutions. Science 320: 889–892.
Gilliam, F. S. 2006. Response of the herbaceous layer of forest ecosystems
to excess nitrogen deposition. Journal of Ecology 94: 1176–1191.
NITROGEN ENRICHMENT
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Howarth, R. W., A. Sharpley, and D. Walker. 2002. Sources of nutrient
pollution to coastal waters in the United States: Implication for achieving coastal water quality goals. Estuaries 25(4b): 656–676.
Inderjit, D. Chapman, M. Ranelletti, and S. Kaushik. 2006. Invasive
marine algae: An ecological perspective. The Botanical Review 72(2):
153–178.
Scherer-Lorenzen, M., H. O. Venterink, and H. Buschmann. 2007.
Nitrogen enrichment and plant invasions: The importance of nitrogen-fixing plants and anthropogenic eutrophication. In W. Netwig, ed.
Biological Invasions. Springer.
Vasquez, E., R. Sheley, and T. Svejcar. 2008. Creating invasion resistant
soils via nitrogen management. Invasive Plant Science and Management
1: 304–314.
Williams, S. L., and J. E. Smith. 2007. A global review of the distribution,
taxonomy, and impacts of introduced seaweeds. Annual Review of Ecology, Evolution, and Systematics 38: 327–359.
NOVEL WEAPONS
HYPOTHESIS
RAGAN M. CALLAWAY
University of Montana
The novel weapons hypothesis (NWH) is the idea that
some exotic plant species may become invasive because
they produce biologically active secondary metabolites
that are not produced by species in the communities
that are invaded, and that this novelty provides exotics
with advantages against native competitors, consumers,
or microbes that are not adapted to tolerate the chemical. Put another way, the NWH posits that some invasive
exotic plants are spreading through and destroying native
plant communities because they produce and release
harmful chemicals that the naive native inhabitants have
never experienced. So far, evidence for such novel weapons has focused on phytotoxic interactions among plants,
novel defense chemicals, and the biochemical suppression of mutualistic fungi that are crucial for the growth
of native species.
HISTORY
T. A. Rabotnov, an ecologist at Moscow State University,
argued that plants could evolve in response to the chemicals exuded from the roots or washed from the leaves of
their neighbors, stating that the “resistance of plant species to the vital secretions [i.e., secondary metabolites]
of other components of biocenoses [communities] . . .
has been created through the acquisition of properties
[adaptation] by plants preventing the harmful action of
492
NOVEL WEAPONS HYPOTHESIS
secretions of other organisms.” Rabotnov stated that in
natural conditions “allelopathically neutral” or “allelopathically homeostatic” biotic systems form in which
allelopathic interactions are relatively weak because plants
and microbes adapt to the chemicals produced by their
neighbors (much like they rapidly adapt to herbicides
and other chemicals). With this background, he suggested that “disturbed homeostasis” occurs when interactions take place among species without an evolutionary
history—such as occurs with exotic invasions.
BIOGEOGRAPHIC EXPERIMENTS
Centaurea diffusa (diffuse knapweed) is native to Europe
and Asia but invasive in western North America. In experiments with pairs of grass species in the same genera, C.
diffusa suppressed the growth of North American species
by 70 percent more than it suppressed the growth of Eurasian congeners. Activated carbon, which adsorbs to and
deactivates some organic molecules, reduced the inhibitory effects of C. diffusa on the North American plants,
but not the effects of the invader on the Eurasian plants.
Similarly, experimental communities built from North
American grass species were far more successfully invaded
by C. diffusa than were communities built from Eurasian
species. The root exudate 8-hydroxyquinoline may play
a role in these biogeographic differences, as the chemical
applied to plants in field soils suppressed the growth of
North American species about 30 percent more than it
did the growth of Eurasian species. These results raise the
possibility that plant species from the native communities
of C. diffusa have evolved tolerance to its root exudates,
while North American plant species have not.
Phytotoxic, or allelopathic, effects have also been
widely reported for a congener of C. diffusa, C. maculosa
(C. stoebe micranthos, spotted knapweed), also native to
Eurasia and invasive in North America. A number of different chemicals produced by the plant are biologically
active, but a great deal of research has focused on the root
exudate (±)-catechin, an isomeric phenolic compound
exuded from the roots of C. maculosa. The ecological
relevance of (±)-catechin phytotoxicity has been controversial, in part because of widely varying measurements
of soil concentrations and variable results for phytotoxic
effects among species and substrates, but the allelopathic
effects of (±)-catechin, or the isolated (+) or (−) forms,
have been demonstrated in vitro, in sand culture, in controlled experiments with field soils, and in the field at
reasonably natural applied concentrations. Some of the
variation in the effects of (±)-catechin may be due to the
effects of metal-catechin complexes, which can enhance or