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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. 490 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 491 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