Extreme climatic events shape arid and semiarid ecosystems

REVIEWS REVIEWS REVIEWS Extreme climatic events shape arid and semiarid ecosystems Milena Holmgren1*, Paul Stapp2*, Chris R Dickman3, Carlos Gracia4, Sonia Graham5, Julio R Gutiérrez6, Christine Hice7, Fabián Jaksic8, Douglas A Kelt9, Mike Letnic10, Mauricio Lima8, Bernat C López4, Peter L Meserve11, W Bryan Milstead12, Gary A Polis13, M Andrea Previtali11, Michael Richter14, Santi Sabaté4, and Francisco A Squeo6 Climatic changes associated with the El Niño Southern Oscillation (ENSO) can have a dramatic impact on terrestrial ecosystems worldwide, but especially on arid and semiarid systems, where productivity is strongly limited by precipitation. Nearly two decades of research, including both short-term experiments and long-term studies conducted on three continents, reveal that the initial, extraordinary increases in primary productivity percolate up through entire food webs, attenuating the relative importance of top-down control by predators, providing key resources that are stored to fuel future production, and altering disturbance regimes for months or years after ENSO conditions have passed. Moreover, the ecological changes associated with ENSO events have important implications for agroecosystems, ecosystem restoration, wildlife conservation, and the spread of disease. Here we present the main ideas and results of a recent symposium on the effects of ENSO in dry ecosystems, which was convened as part of the First Alexander von Humboldt International Conference on the El Niño Phenomenon and its Global Impact (Guayaquil, Ecuador, 16–20 May 2005). Front Ecol Environ 2006; 4(2): 87–95 E l Niño Southern Oscillation (ENSO) is fundamentally a climatic and oceanographic phenomenon, but it has profound effects on terrestrial ecosystems as well. Although the ecological effects of ENSO are becoming increasingly known from a wide range of terrestrial ecosystems (Holmgren et al. 2001; Wright 2005), their impacts have been most intensively studied in arid and semiarid systems. Because inter-annual variability in precipitation is such a strong determinant of productivity in dry ecosystems, increased ENSO rainfall (Panel 1) is crucial for plant recruitment, productivity, and diversity in these ecosystems. Several long-term studies In a nutshell: • El Niño Southern Oscillation (ENSO) events have a profound impact on arid and semiarid ecosystems, with important implications for agriculture, human populations, and natural resources conservation and restoration • Although most ecological effects are mediated by increases in plant growth, changes in resources and population levels can trigger complex trophic interactions involving multiple resources, prey, and predator species • Because ENSO effects may persist for months or even years, their consequences are best elucidated by long-term, ecosystem-scale, comparative studies 1* Resource Ecology Group, Wageningen University, Bornsesteeg 69, Building 119, 6708 PD Wageningen, The Netherlands (milena. holmgren@wur.nl); 2*Department of Biological Science, California State University, PO Box 6850, Fullerton, CA 92834–6850, USA (pstapp@fullerton.edu); 3Institute of Wildlife Research, University of Sydney, NSW 2006, Australia; (continued on p 95) © The Ecological Society of America show that this pulse in primary productivity causes a subsequent increase in herbivores, followed by an increase in carnivores, with consequent changes in ecosystem structure and functioning that can be quite complex and pervasive. We begin by discussing the effects on plant communities, then move to studies of populations of higher-level consumers and entire food webs. Where appropriate, we discuss the implications of ENSO events for land-use practices, natural resource management, and humans. We conclude with a brief synthesis, including suggestions for additional work needed in this important area.  Plant responses Production of herbaceous plants and seed banks Herbaceous plants in arid and semiarid ecosystems respond very rapidly to pulses of precipitation by germinating, growing, and producing large quantities of seed (Figure 1). For instance, Julio Gutiérrez and colleagues have been studying the arid scrub communities in northcentral Chile since 1989, and have described changes in ephemeral plant cover, from 11–16% pre-El Niño 1989–90 to 54–80% during El Niño 1991–92 and back to 13–21% post-El Niño 1993–94 (Gutiérrez et al. 1997). Comparable responses have been described for the Galápagos Islands (Hamann 1985), islands in the Gulf of California (Polis et al. 1997), and the Atacama Desert in Chile (Vidiella et al. 1999) and Peru (eg Block and Richter 2000). Plant species composition also changes in El Niño www.frontiersinecology.org 87 Climatic events shape arid ecosystems (a) 88 M Holmgren et al. ephemeral plants to rainfall pulses seem to be related to the rainfall regime in previous years. For instance, at one experimental site in Chile, the cover of ephemeral plants in 1991 (223 mm rainfall) peaked at 80% and then decreased to 54% in 1992, despite this also being a comparably wet year (229 mm). These observations suggest that other factors, such as nutrients, become limiting after the first rainy pulse (Gutiérrez et al. 1997). Effects in dry forests and shrublands (b) Courtesy of L Albán and R Rodríguez (c) Figure 1. Effects of El Niño rainfall on the forests of northwest Peru. The normally sandy landscapes with scattered Prosopis pallida trees (a) become covered by pastures (b) and by new recruited trees (c). years. Some species that are absent or rare during non-El Niño years become dominant during the rainy events. Annual species that respond strongly to infrequent rainfall pulses, such as those ocurring in El Niño years, appear to be able to survive in the system, buffering the absence of sufficient water during dry years, by producing large seed reserves during rainy pulses. As a consequence, there is very little correlation between seed bank composition and the species found growing during dry years (Gutiérrez et al. 2000). It is interesting to note that the responses of www.frontiersinecology.org ENSO events represent large interannual rainfall pulses of long duration. These resource pulses can trigger responses in many types of organisms, including not only those species that are able to use short pulses of increased superficial soil water, but also deeper-rooted shrubs and trees (Schwinning and Sala 2004; see also additional papers in the same volume of Oecologia). A major consequence of rainy conditions associated with ENSO is the regeneration of woody vegetation (Figure 1). Examples include increased shrub cover in the Chihuahuan desert (Brown et al. 1997) and the successful establishment of cactus seedlings in the Sonoran desert (Bowers 1997) during rainy El Niño events, as well as the regeneration of mulga, Eucalyptus, and conifer woodlands in semiarid Australia during wet La Niña episodes (Austin and Williams 1988). In northwest Peru, spectacular natural regeneration of several tree species has been observed during the very strong ENSO events of 1982–83 and 1997–98. Bernat C López and colleagues studied growth and recruitment in one of the most dominant native tree species of the Peruvian dry forests (Prosopis pallida) and compared this with Prosopis chilensis in north-central Chile. They found that in northwest Peru, mean annual growth rate (López et al. 2005) and recruitment of new P pallida trees were positively correlated with annual rainfall, and were almost twice as high during ENSO years than during nonENSO years. In contrast, neither recruitment nor growth rate of P chilensis in northern Chile was significantly correlated to rainfall and ENSO conditions. These results make sense in light of the differences in ENSO-related precipitation between the two regions; precipitation in northwest Peru increases enormously during ENSO years (up to 25 times higher than during non-ENSO years) but only moderately (1.6 times) in north-central Chile. Implications for land-use management and restoration Although one might imagine that an ecosystem basically tracks the fluctuations in environmental conditions, a fundamentally different trajectory may be seen in ecosystems that have alternative stable states. Semiarid ecosystems can have alternative vegetation states (eg dry forests and shrublands vs degraded savannas and barren soil) depending on grazing and water availability (eg Rietkerk © The Ecological Society of America M Holmgren et al. Climatic events shape arid ecosystems © The Ecological Society of America Grazing pressure Vegetation biomass and van de Koppel 1997). This may (b) (a) Collapse Fc have considerable implications for Low biomass their response to variability in climate Fr such as ENSO events and global cliAlternative Recovery stable Recovery Fc mate change (Scheffer et al. 2005), states High biomass El Niño which may result in catastrophic regime shifts (Scheffer and Carpenter Collapse 2003). Holmgren and Scheffer (2001) Fr Herbivore control hypothesized that ENSO episodes of increased rainfall can be used together Grazing pressure Water with grazing control to enhance plant establishment and produce permanent Figure 2. (a) Equilibrium biomass of vegetation in semi-arid regions as a function of shifts in ecosystem state (Figure 2). grazing pressure. The inflection points (dots) of the curve are fold bifurcations that mark Together with colleagues, Milena critical biomass removal rates. At grazing pressures higher than Fc the vegetation can Holmgren has been searching for evi- only be in a state with low biomass. At grazing pressure lower than Fr a high biomass dence of this in the semiarid ecosys- condition is the only stable state. At intermediate grazing pressure (between Fc and Fr), tems of north-central Chile and north- a high biomass state and a low biomass state are alternative equilibria (solid lines) of the west Peru, using tree-ring studies in system. Here, the dashed middle section of the sigmoidal curve represents an unstable natural populations and field experi- equilibrium that marks the border of the basins of attraction of these two stable branches. ments with seedlings. They found that (b) Critical thresholds of biomass removal as a function of water availability. Under rainy El Niño episodes can indeed trig- wetter conditions, equilibrium biomass and the critical grazing pressure for collapse (Fc) ger forest regeneration, but that, as dis- or recovery (Fr) are higher. A certain reduction of biomass removal rate (eg herbivory cussed earlier, large regional differ- control) indicated by the vertical arrows may be sufficient to induce woodland recovery ences exist. Experiments revealed that in a wet (“El Niño”) year, but not in a dry year. (Reproduced courtesy of Springer this is due not only to the smaller Science and Business Media; Holmgren and Scheffer 2001.) ENSO signal in Chile, but also to a much greater mortality caused by herbivores. The huge the occurrence of conditions that are conducive to sucimpact of species in Chile seems to be the combined cessful establishment (Howden et al. 2004). The primary productivity boost described previously result of slower plant growth and greater pressure from exotic species (especially European rabbits and hares). and its potential application in ecosystem restoration These results suggest that ENSO events may be used as could be overshadowed by fires and overgrazing. “windows of opportunity” to trigger forest recovery if her- Although plant regeneration improves when herbivore bivores are controlled at the right moment. Clearly, the pressure declines (Holmgren and Scheffer 2001), oversuccessful use of ENSO events in restoration programs grazing during the subsequent dry years is likely to will depend on a combination of climatic, ecological, and become a problem, because both native herbivores and social conditions (Scheffer et al. 2002). Currently, El livestock increase numerically during the rainy pulse. In Niño forecasts are being used for the implementation of addition, abundant dry grasses serve as high fuel loads, reforestation programs in northwest Peru, although with facilitating the initiation and spread of large fires. Clear no systematic control of herbivores and with varying links between ENSO and fire are found in arid lands in Australia (Skidmore 1987), northwest Peru (Block and degrees of success (eg Vilela 2002). While studies conducted in the Western Hemisphere Richter 2000; Richter and Ise 2005), and the southwesthighlight the importance of boosts in primary productiv- ern US (Westerling et al. 2003). This is reflected in the ity associated with ENSO-related pulses in rainfall, striking similarity between fire histories in the southwestresearch in Australia also demonstrates the implications ern US and northern Patagonia over the past century, of ENSO-related drying events for restoration and refor- with major fires happening during dry La Niña events estation efforts. Numerous tree species in Australia have (Kitzberger et al. 2001). The frequency and intensity of developed drought tolerance, but high seedling death wildfires in tropical systems are also influenced by ENSO rates due to water and heat stress are common for both and can release large amounts of carbon to the atmosnatural populations and planted seedlings. Indeed, while phere (Page et al. 2002; Cochrane 2003). recruitment of many plant species fails during dry El Niño conditions, rainy La Niña years stimulate primary produc-  Consumer population and food-web responses tivity and woodland regeneration (Austin and Williams 1988). Research is currently being undertaken to investi- Notwithstanding the ground-breaking work by Peter and gate how ENSO-related dry periods and La Niña-related Rosemary Grant on the ecology and evolution of wet periods affect native tree establishment and to assess Darwin’s finches on the Galápagos Islands (Grant and how seasonal climate forecasting may be used to both Grant 1989; Grant et al. 2000), some of the best evidence reduce the risk of unsuccessful establishment and predict for the ecological effects of ENSO events on consumer www.frontiersinecology.org 89 M Holmgren et al. Climatic events shape arid ecosystems 90 Panel 1. The ENSO cycle and its weather effects (from McPhaden 2004) The El Niño Southern Oscillation (ENSO) cycle is the most prominent source of interannual climatic variation on our planet.This oscillation has two opposite phases, known as El Niño and La Niña. Normally, trade winds along the equator blow from east to west, piling warm, superficial seawater in the western Pacific (Figure 3b).As a consequence, cold, deep water is pushed deeper in the west and elevated in the east, which facilitates the upwelling of cold water off the western coast of South America. As the trade winds blow, they collect heat and moisture from the ocean.The warm humid air becomes less dense and rises over the warm western Pacific waters, a region with low atmospheric pressure. Deep convection produces heavy precipitation.The air then returns eastwards and sinks over the cooler waters of the eastern Pacific, La Niña conditions (a) (b) Normal conditions (c) El Niño conditions generating a high-pressure region. El Niño begins when the trade winds Convective loop weaken as atmospheric pressure rises in the western Pacific and falls in the eastern Equator Equator Pacific.Weakened trade winds allow water Equator from the warm seawater pool in the western Pacific to move eastward, reducing Thermocline Thermocline Thermocline coastal upwelling of deep cold water 120˚E 80˚E 120˚E 80˚E 120˚E 80˚E (Figure 3c). As surface sea temperature warms up in the eastern Pacific, convective Figure 3. Diagram showing the sea–atmospheric system during (a) La Niña, (b) normal, cloudiness and rainfall migrate eastwards. and (c) El Niño conditions. (From McPhaden 2004.) This process further weakens the trade winds, shifting the rain zone towards the central and eastern Pacific. As a result, drought conditions affect large portions of Australia, Indonesia, and the El Niño Philippines, while torrential rains often occur in the island (a) states of the central Pacific and along the west coast of South America.This shift in the rainfall convective zone also leads to changes in atmospheric circulation (known as teleconnections) that propagate the influence of El Niño worldwide.As a consequence, during an El Niño episode, rainfall dramatically increases in certain areas of the world, while severe droughts occur in other regions (Figure 4a). Dry The El Niño phase lasts approximately one year before the Wet climatic conditions reverse.The next phase, known as La Niña, is characterized by stronger than normal trade winds and a shift in heavy rainfall to the far western tropical Pacific (Figure 3a). La Niña produces roughly the opposite climate patterns from those seen during an El Niño episode (Figure 4b).The oscillation between El Niño and La Niña is irregular, but typically occurs once every 3–6 years (Allan et al. 1996; McPhaden 2004). (b) The strength of the ENSO effects varies both spatially and temporally. For example, during an El Niño year, rainfall may La Niña double in north-central Chile, while it can be more than 25 times higher than normal in northern Peru. The strength, Figure 4. Regions showing increased precipitation (blue) and drier duration, and frequency of ENSO events seem to be affected conditions (orange) during (a) El Niño and (b) La Niña phases. by other climatic oscillations, such as the Pacific Decadal (From Allan et al. 1996.) Oscillation (PDO). populations has come from studies involving small mammals, which are important components of arid and semiarid ecosystems. In addition, because many small mammals are commensal, or interact with humans directly or indirectly, population irruptions during ENSO events are often viewed as pest outbreaks, which may lead to increased agricultural damage or a higher risk of zoonotic diseases such as hantavirus (Hjelle and Glass 2000) and plague (Stapp et al. 2004). Population responses of small mammals and their predators ENSO events in semiarid Chile result in predictable increases in rainfall, which trigger flushes in vegetation and the associated size of the seed bank, especially by ephemerals (Jaksic 2001). In turn, with delays of 6–12 months, small www.frontiersinecology.org mammal numbers increase in response to primary productivity, usually reaching irruption levels of 100 individuals ha-1 (Jaksic and Lima 2003). Mauricio Lima and colleagues conducted detailed time-series analyses to evaluate the relative importance of direct (eg survival and reproduction) and indirect effects (eg through a limiting resource) of climate on rodent abundance in semiarid Chile (Lima et al. 1999, 2002). Their findings indicate that fluctuations in rodent demographic rates are mainly the result of indirect effects of rainfall, implying that these small rodent populations are strongly food-limited and that rainfall represents a proxy for food availability. Food limitation and intraspecific competition, therefore, are dominant forces influencing the dynamics of these rodent populations. Populations of local predators track fluctuations in rodent prey (Jaksic et al. 1992); these responses are complex, however, because different predators consume different prey and © The Ecological Society of America M Holmgren et al. Climatic events shape arid ecosystems Carnivorous birds (No 2500 ha-1) because predator numbers are limited 40 by both density-dependent and interspecific interactions (Lima et al. 2002). 35 In Auco, north-central Chile, Fabián Jaksic and collaborators have been 30 able to detect increases in mouse numbers following precipitation associated y = 18.5* log10 (1.03*X); r2 = 0.86 25 with four ENSO events (1987, 1991, 1997, and 2002) over an 18-year 20 period. Associated with these mouse irruptions, carnivorous mammals and 15 birds of prey display a variety of responses at all levels of organization. 10 At the individual level, for instance, 5 burrowing owls shift their consumption of prey over time, depending on 0 the relative abundance of prey. 0 10 20 30 40 50 60 Essentially, burrowing owls increase -1 the consumption of irrupting mamSmall mammals (No ha ) mals, shifting away from less energetically rewarding prey such as arthropods Figure 5. Numerical response of carnivorous birds to the abundance of small rodents in (see also Silva et al. 1995). At the pop- north-central Chile. ulation level, Jaksic and collaborators have identified a numerical response, with carnivorous tude (229–356 mm), each episode triggered strong birds displaying population fluctuations to reflect mam- responses in small mammal numbers, apparently in malian prey changes, essentially tracking their temporal response to increasing food availability (Figure 6; Meserve course of abundance (Figure 5; Jaksic et al. 1992). Never- et al. 2001). Individual species, however, showed variations in theless, this numerical response is not perfect and the curve of predator versus prey numbers saturates quickly, which response time and magnitude of population increases. For may explain why carnivorous birds are not able to control instance, some species increase rapidly in response to a rainy pulse and reach about the same maximum numbers, their mammalian prey. Finally, at the community level, the predator assemblage regardless of the duration of rainfall episodes or the annual as a whole shows important rearrangements of richness, amount (eg Phyllotis darwini and Akodon olivaceus). Others composition, and structure. The most prevalent guild show a longer delay in response time with increased preresponse is for predators to form looser guilds, with less diet cipitation and reach higher abundance levels during more similarity, during ENSO events. This occurs because during prolonged rainfall episodes (eg Octodon degus). Following ENSO years there is greater abundance and a broader vari- the rainy pulse, some species crash numerically (eg A oliety of available prey, so that predators can diverge in diet. vaceus), while others maintain oscillations (though During La Niña years, on the other hand, with reduced smaller) in normal to dry years (P darwini). These changes abundance and less variety of prey, predators must converge seem to be related to diet (eg granivore vs herbivore) and on the few prey available, thus increasing their diet similar- to reproductive rate (Meserve et al. 2001). Results from factorial experiments to exclude most verteity (Jaksic et al. 1993). Top predators in semiarid ecosystems may be considered as periodically bouncing between times brate predators (ie foxes, owls, raptors) and the largest putaof plenty (El Niño) and lean times (La Niña), in terms of tive competitor (O degus) also varied between species. Although competition seemed weak (Meserve et al. 1999, their prey. 2003), it appeared that the relative importance of interspecific interactions, such as predation and competition, can Complex interactions between competition and become stronger during dry periods. These experiments also predation revealed unexpected facilitative interactions among these In order to understand the effects of rainfall variability on rodents. For instance, the presence of the larger O degus the whole food-web structure, since 1989 Peter Meserve apparently has an indirect positive effect on P darwini, by and his collaborators have been conducting a large-scale, modifying habitat and creating more suitable conditions, ie experimental study of small mammals in a semiarid thorn opening the vegetation canopy and providing burrows. scrub community in north-central Chile (mean annual Thus, while many patterns in the structure of this small rainfall = 143 mm). This project has spanned three high- mammal assemblage may be explained by extrinsic factors rainfall episodes usually associated with the warm phase of such as high variability in rainfall leading to changes in ENSO. Though ranging in duration (1–3 years) and magni- resource availability, the role of interspecific interactions © The Ecological Society of America www.frontiersinecology.org 91 Climatic events shape arid ecosystems a diminished ability to retain soil nutrients and moisture, thus limiting potential growth responses to future rainfall events. 10 Once dried, the plentiful vegetation produced during La Niña events provides ample fuel for mas0 100 Phyllotis darwini sive wildfire events in arid Australia (Figure 7). Such events were recorded in 1916–1918, 1951, 10 1974–75, and 2001–02, and encompassed millions of square kilo0 meters (Letnic et al. 2005). These 100 Akodon olivaceus catastrophic wildfires have devastating impacts on native ecosys10 tems and severe consequences for human communities (Skidmore 1987). Because periods of top-down 0 trophic regulation and wildfires 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 coincide about one year after La Time (months) Niña events, these high rainfall Figure 6. Fluctuations in the abundance of small mammals in response to changes in plant periods should be regarded as critiproductivity driven by rainfall variability in semiarid north-central Chile. The green cal for wildlife conservation in arid background indicates an unusually high rainfall period due to the occurrence of an El Niño Australia, rather than as “boom event or to local climatic factors. times”, as has traditionally been the case. such as predation and competition cannot be discounted. The ecology of terrestrial ecosystems in Australia is inexThese complex relationships could not have been detected tricably linked to ENSO. A major challenge for sustainable without long-term experimental studies. management of natural resources and biodiversity in this country is to incorporate climatic forecasting into adaptive management strategies that can respond to ENSO-driven Responses of Australian mammals to La Niña and variability in rainfall. wildfires 100 Octodon degus Minimum number known alive grid-1 92 M Holmgren et al. In Australia, the El Niño and La Niña phases of ENSO are associated with drought and floods, respectively. The pulse of primary productivity that occurs during La Niña is a fundamental and periodic process that structures terrestrial ecosystems throughout Australia. For example, La Niña rains provide opportunities for the successful recruitment of annual herbs, perennial shrubs and trees, and successful breeding by waterfowl (Nicholls 1991; Kingsford et al. 1999; Figure 7). As in South America, this pulse of plant growth results in widespread irruption of rodents (Letnic et al. 2005), followed in turn by an increase in the populations of predators, including domestic cats (Felis catus) and red foxes (Vulpes vulpes). These introduced species have been implicated in the extinction or endangerment of 26 species of native mammals throughout arid Australia. During the periods of high predator abundance that follow La Niña events, trophic pathways are temporarily reversed, as predation, competition, and disease increase in importance as factors limiting rodent populations (Letnic et al. 2004, 2005). During droughts associated with the El Niño phase, mammal populations crash (Dickman et al. 1999, 2001) and overgrazing by livestock, kangaroos, and feral animals can lead to massive soil erosion (Ludwig et al. 1997). These erosion events can produce dysfunctional landscapes that have www.frontiersinecology.org ENSO effects on marine inputs and terrestrial food webs on desert islands The dynamics of coastal arid ecosystems are largely driven by low, variable primary productivity and inputs from the adjacent ocean. On islands in the Gulf of California, inputs of nutrients and energy from a very productive marine system act as spatial trophic subsidies, contributing to high consumer densities in typical dry years. However, episodic ENSO events bring rainfall that stimulates plant productivity, replenishes detritus and seed banks, and provides resources for insular consumers that may remain in the system after dry conditions resume (ie as temporal trophic subsidies). A decade of research led by Gary Polis and his colleagues has focused on interactions between marine inputs and pulsed ENSO resources as determinants of primary and secondary production and trophic interactions on small, rocky islands off Baja California (Polis et al. 1997; Stapp et al. 1999; Sánchez Piñero and Polis 2000; Stapp and Polis 2003). A few of these islands host nesting colonies of seabirds which provide food, in the form of carrion (ie remains of dead fishes, crabs, etc), for arthropod scavengers. Other islands are used by seabirds only for roosting and are influenced indirectly by the addition of guano, which adds © The Ecological Society of America M Holmgren et al. Climatic events shape arid ecosystems 93 Figure 7. ENSO-related impacts in the Simpson Desert, central Australia. (a) Craven’s Peak station in the northeastern part of the desert following flood rains associated with the La Niña phase of ENSO in 1999–2000. (b) The same area following a wildfire that burnt > 10 000 km2 of the desert in the summer of 2001–2002. The fire, ignited by lightning strikes, was exacerbated by a heavy fuel load of dry vegetation resulting from the earlier La Niña rains. Fires of this magnitude have occurred four times over the past century, and have followed flood rains on each occasion. nutrients to soil that can be used by plants when water is available. There are striking differences in the ecology of these two types of islands. Polis et al.’s research coincided with three ENSO events (1991–92, 1994–95, 1997–98) in the region, during which winter precipitation (142 mm) was five times higher than in the intervening dry years (28 mm). Peaks in plant cover, particularly annuals, were associated with these wet years, increasing plant cover approximately threefold, especially on islands used by seabirds. As a result, flying insects and their primary predators, web spiders, also peaked in abundance in those years, although the increases were most pronounced on seabird islands. This indicates more bottom-up control than was suggested in previous analyses that pooled seabird and nonbird islands (Polis et al. 1997). Omnivorous rodents (Peromyscus spp) also increased fourfold during the 1997–98 El Niño conditions, but populations crashed the following year. The numerical response of these rodents contrasted with that of granivorous rodents (Chaetodipus spp), which experienced only a modest increase (1.6 times), but whose populations remained much more stable once dry conditions resumed (Stapp and Polis 2003). These results suggest very different responses to ENSO-related pulses, in which some species (eg omnivorous rodents, web spiders) show strong, immediate population increases, whereas others (eg granivores, scavenging arthropods) may display more muted or extended responses, mediated by interactions with other species or the availability of marine resources (Sánchez Piñero and Polis 2000; Stapp and Polis 2003). Results from stable carbon and nitrogen isotope analyses have confirmed the overwhelming importance of marine resources for many consumers in dry years, while marine and insular systems remain largely distinct during wet years, except for the profound, indirect effects of seabird guano on terrestrial productivity (Stapp et al. 1999). © The Ecological Society of America This insular system is unique in its tight linkage between the marine and terrestrial components. Additional work is needed on the persistence of pulsed resources (eg seed/litter banks, consumer tissue), and on the potential impacts of ENSO-related changes in marine productivity on inputs to insular food webs. In addition to reinforcing the notion that episodic, ENSO-driven rainfall events are critical factors in the ecology of arid and semiarid systems, this work demonstrates the interdependence of ocean and terrestrial systems and the key role of seabirds in some insular food webs. This, in turn, underscores the importance of a healthy marine environment and the protection of seabirds to the conservation of insular ecosystems. Interactions between ENSO and zoonotic disease As in other arid regions, rodent populations in the southwestern US are markedly affected by ENSO-related rainfall (Brown and Ernest 2002). Because some of these species can transmit diseases to humans, understanding their population dynamics and behavior has important health implications. Since 1994, researchers at the University of New Mexico and Centers for Disease Control and Prevention (CDC) have been studying the effects of climate variability on rodent populations and hantavirus produced by the Sin Nombre virus (SNV). SNV was first discovered in New Mexico following an outbreak of hantavirus pulmonary syndrome after the 1992–93 ENSO; this was eventually traced back to an increase in numbers of deer mice (Peromyscus maniculatus) and other rodents in the family Muridae. Clearly, the numerical response of deer mice to ENSO events has important consequences for the ecology of hantavirus. Deer mice can take rapid advantage of increased food resources during ENSO events because they reproduce several times per year and have large numwww.frontiersinecology.org M Holmgren et al. Climatic events shape arid ecosystems 94 bers of offspring. Other species, including rodents such as kangaroo rats (Dipodomys spp; Heteromyidae) do not transmit the disease and apparently do not respond as strongly to ENSO pulses. Kangaroo rats typically have only one litter per year, making them less able to increase in abundance in response to improved food availability. Moreover, their territorial behavior often makes space, not food resources, the limiting factor. Current research aims to identify, through satellite imagery, the characteristics of sites that act as refugia for Peromyscus populations during dry years, thereby serving as sources for high rodent numbers in outbreak years that are associated with ENSO events.  Synthesis and conclusions Two decades of research using a combination of long-term observations and experimental field studies have demonstrated profound and persistent impacts of ENSO-related rainfall variability on the dynamics of arid and semiarid ecosystems. Some general patterns were apparent in the three continents studied; however, there are regional differences in the relative importance of ENSO events, as well as in the magnitude of its effects. The basic pattern is that a rainy episode triggers a pulse in plant growth, leading to an increase in herbivores, and later in carnivores. In subsequent dry periods, top-down effects can become strong and food again becomes a limiting factor in these elevated populations. Within trophic levels, species clearly differ in their response to ENSO events, often in surprising ways that may be mediated by interactions with other species. Many of the studies described above focus on biotic effects, which may be important at local or relatively short temporal scales. Additional time-series data, collected from across a range of representative sites, are clearly needed to scale-up these local processes to relevant regional scales, and to permit generalizations about the ecological importance of ENSO and other broad-scale external factors. Importantly, ENSO-related changes in terrestrial ecosystems can have substantial effects on human communities and land use. Accumulated dry plant material, for example, can fuel wildfires after the rainy period is over. In contrast, forest regeneration and expansion could be a longlasting result of a wet ENSO event, because trees and shrubs become relatively less sensitive to drought and herbivory once they reach a certain critical size. Although ENSO conditions can pose substantial challenges in wildlife conservation and the management of vectors and hosts of human diseases, such events also represent opportunities for novel approaches in restoration and natural resources management. Future research should focus on how seasonal and long-range ENSO forecasting could be applied to adaptive management of these issues (eg current models used to predict likelihood and severity of fire season by ecologists and fire meteorologists in the US; www.nifc.gov/nicc/predictive/predictive.htm). The climatic extremes associated with ENSO events, especially in arid and semiarid systems, also provide prime opportunities www.frontiersinecology.org for natural experiments to test fundamental questions about ecosystem stability and the direct and indirect consequences of pulsed resources in food webs.  Acknowledgments We gratefully acknowledge the efforts of the technicians, students, and volunteers who contributed to the success of these projects, as well as the governmental agencies that facilitated our research. These results were collected with generous, long-term support from the EU–INCO project (M Holmgren and colleagues; www.biouls.cl/enso/), US National Science Foundation (P Stapp, P Meserve and colleagues), FONDECYT (Chile; J Gutiérrez and colleagues), Australian Research Council (C Dickman, M Letnic and colleagues), and US Centers for Disease Control and Prevention (C Hice). S Graham thanks the Land and Water Australia’s Managing Climate Variability Program for their ongoing support. JR Gutiérrez and FA Squeo thank the BBVA Foundation Prize in Research and Conservation Biology (Spain) for their support. We are particularly grateful to MJ McPhaden (NOAA/PMEL/TAO Project Office) for generously helping us prepare Panel 1.  References Allan R, Lindesay J, and Parker D. 1996. El Niño Southern Oscillation and climatic variability. Collingwood, Australia: CSIRO. www.publish.csiro.au/pid/184.htm. Austin MP and Williams O. 1988. Influence of climate and community composition on the population demography of pasture species in semi-arid Australia. Vegetatio 77: 43–49. Block MA and Richter M. 2000. Impacts of heavy rainfalls in El Niño 1997/98 on the vegetation of Sechura Desert in Northern Peru. Phytocoenologia 30: 491–517. Bowers JE. 1997. Demographic patterns of Ferocactus cylindraceus in relation to substrate age and grazing history. Plant Ecol 133: 37–48. Brown JH and Ernest SKM. 2002. Rain and rodents: complex dynamics in desert communities. BioScience 52: 979–87. Brown JH, Valone TJ, and Curtin CG. 1997. Reorganization of an arid ecosystem in response to recent climate change. P Natl Acad Sci USA 94: 9729–33. Cochrane MA. 2003. Fire science for rainforests. Nature 421: 913–19. Dickman CR, Mahon PS, Masters P, and Gibson DF. 1999. Longterm dynamics of rodent populations in arid Australia: the influence of rainfall. Wildlife Res 26: 389–403. Dickman CR, Haythornthwaite AS, McNaught GH, et al. 2001. Population dynamics of three species of dasyurid marsupials in arid central Australia: a 10-year study. Wildlife Res 28: 493–506. Grant PR and Grant BR. 1989. Evolutionary dynamics of a natural population: the large cactus finch of the Galápagos. Chicago, IL: University of Chicago Press. Grant PR, Grant BR, Keller LF, and Petren K. 2000. Effects of El Niño events on Darwin’s finch productivity. Ecology 81: 2442–57. Gutiérrez JR, Arancio G, and Jaksic FM. 2000.Variation in vegetation and seed bank in a Chilean semi-arid community affected by ENSO 1997. J Veg Sci 11: 641–48. Gutiérrez JR, Meserve PL, Herrera S, et al. 1997. Effects of small mammals and vertebrate predators on vegetation in the Chilean semiarid zone. Oecologia 109: 398–406. Hamman O. 1985. The El Niño influence on the Galápagos vegetation. In: Robinson G and Del Pino EM (Eds). El Niño en las Islas © The Ecological Society of America M Holmgren et al. Galápagos: el evento de 1982–1983. Quito, Ecuador: Fundación Charles Darwin para las Islas Galápagos. Hjelle B and Glass GE. 2000. Outbreak of hantavirus infection in the Four Corners region of the United States in the wake of the 1997–1998 El Niño–Southern Oscillation. J Infect Dis 181: 1569–73. Holmgren M and Scheffer M. 2001. El Niño as a window of opportunity for the restoration of degraded arid ecosystems. Ecosystems 4: 151–59. Holmgren M, Scheffer M, Ezcurra E, et al. 2001. El Niño effects on the dynamics of terrestrial ecosystems. Trends Ecol Evol 16: 89–94. Howden SM, Crimp S, Carter J, et al. 2004. Enhancing natural resource management by incorporating climate variability into tree establishment decisions – final report for Land and Water Australia. Collingwood, Australia: CSIRO. Jaksic FM. 2001. Ecological effects of El Niño in terrestrial ecosystems of western South America. Ecography 24: 241–50. Jaksic FM and Lima M. 2003. Myths and facts on ratadas: bamboo blooms, rainfall peaks and rodent outbreaks in South America. Austral Ecol 28: 237–51. Jaksic FM, Jiménez JE, Castro SA, and Feinsinger P. 1992. Numerical and functional response of predators to a long-term decline in mammalian prey at a semi-arid neotropical site. Oecologia 89: 90–101. Jaksic FM, Feinsinger P, and Jiménez JE. 1993. A long-term study on the dynamics of guild structure among predatory vertebrates at a semi-arid neotropical site. Oikos 67: 87–96. Kingsford RT, Wong PS, Braithwaite LW, and Maher MT. 1999. Waterbird abundance in eastern Australia, 1983–92. Wildlife Res 26: 351–66. Kitzberger T, Swetnam TW, and Veblen TT. 2001. Inter-hemispheric synchrony of forest fires and the El Niño–Southern Oscillation. Global Ecol Biogeogr 10: 315–26. Letnic M, Tamayo B, and Dickman CR. 2005. The responses of mammals to La Niña (ENSO) – associated rainfall, predation and wildfire in arid Australia. J Mammal 86: 689–703. Letnic M, Dickman CR, Tischler M, et al. 2004. The responses of small mammals and lizards to fire and rainfall in arid Australia. J Arid Environ 59: 85–114. Lima M, Keymer JE, and Jaksic FM. 1999. ENSO-driven rainfall variability and delayed density dependence cause rodent outbreaks in western South America: linking demography and population dynamics. Am Nat 153: 476–91. Lima M, Stenseth NC, and Jaksic FM. 2002. Population dynamics of a South American small rodent: seasonal structure interacting with climate, density-dependence and predator effects. P Roy Soc Lond B Bio 269: 2579–86. López BC, Sabaté S, Gracia CA, and Rodríguez R. 2005. Wood anatomy of Prosopis pallida from Peru and its suitability for dendrochronology. J Arid Environ 61: 541–54. Ludwig J, Tongway D, Freudenberger D, et al. 1997. Landscape ecology function and management: Principles from Australia’s rangelands. Collingwood, Australia: CSIRO. McPhaden MJ. 2004. Evolution of the 2002/03 El Niño. B Am Meteorol Soc 85: 677–95. Meserve PL, Milstead WB, Gutiérrez JR, and Jaksic FM. 1999. The interplay of biotic and abiotic factors in a semiarid Chilean mammal assemblage: results of a long-term experiment. Oikos 85: 364–72. Meserve PL, Milstead WB, and Gutiérrez JR. 2001. Results of a food addition experiment in a north-central Chile small mammal assemblage: evidence for the role of “bottom-up” factors. Oikos 94: 548–56. Meserve PL, Kelt DA, Milstead WB, and Gutiérrez JR. 2003. Thirteen years of shifting top-down and bottom-up control. BioScience 53: 633–46. Page SE, Siegert F, Rieley JO, et al. 2002. The amount of carbon released from peat and forest fires in Indonesia during 1997. Nature 420: 61–65. © The Ecological Society of America View publication stats Climatic events shape arid ecosystems Polis GA, Hurd SD, Jackson CT, and Sánchez Piñero F. 1997. El Niño effects on the dynamics and control of an island ecosystem in the Gulf of California. Ecology 78: 1884–97. Richter MA and Ise M. 2005. Monitoring plant development after El Niño 1997/98 in northwestern Peru. Erdkunde 59: 136–55. Rietkerk M and van de Koppel J. 1997. Alternate stable states and threshold effects in semiarid grazing systems. Oikos 79: 69–76. Sánchez Piñero F and Polis GA. 2000. Bottom-up dynamics of allochthonous input: direct and indirect effects of seabirds on islands. Ecology 81: 3117–32. Scheffer M and Carpenter SR. 2003. Catastrophic regime shifts in ecosystems: linking theory to observation. Trends Ecol Evol 18: 648–55. Scheffer M, Westley F, Brock WA, and Holmgren M. 2002. Dynamic interaction of societies and ecosystems: linking theories from ecology, economy and sociology. In: Gunderson LH and Holling CS (Eds). Panarchy: understanding transformations in human and natural systems. Washington, DC: Island Press. Scheffer M, Holmgren M, Brovkin V, and Claussen M. 2005. Synergy between small and large-scale feedbacks of vegetation on the water cycle. Global Change Biol 11: 1003–12. Schwinning S and Sala OE. 2004. Hierarchy of responses to resource pulses in arid and semi-arid ecosystems. Oecologia 141: 211–20. Silva SI, Lazo I, Silva-Aránguiz E, et al. 1995. Numerical and functional response of burrowing owls to long-term mammal fluctuations in Chile. J Raptor Res 29: 250–55. Skidmore AK. 1987. Predicting bushfire activity in Australia from El Niño Southern Oscillation Events. Aust Forest Res 50: 231–35. Stapp P, Antolin MF, and Ball M. 2004. Patterns of extinction in prairie-dog metapopulations: plague outbreaks follow El Niño events. Front Ecol Environ 2: 235–40. Stapp P and Polis GA. 2003. Influence of pulsed resources and marine subsidies on insular rodent populations. Oikos 102: 111–23. Stapp P, Polis GA, and Sánchez Piñero F. 1999. Stable isotopes reveal strong marine and El Niño effects on island food webs. Nature 401: 467–69. Vidiella PE, Armesto JJ, and Gutiérrez JR. 1999. Vegetation change and sequential flowering after rain in the southern Atacama Desert. J Arid Environ 43: 449–58. Vilela P. 2002. Reforestación participativa en Piura durante el Fenómeno El Niño 1996–1997. Peru: Serie Lecciones Aprendidas No 8, INRENA – Proyecto Algarrobo. Westerling AL, Gershunov A, Brown TJ, et al. 2003. Climate and wildfire in the western United States. BAMS May: 595–604. Wright SJ. 2005. The influence of the El Niño Southern Oscillation on tropical forests. In: Bermingham E, Dick C, and Moritz C (Eds). Tropical rainforests: past, present and future. Chicago, IL: University of Chicago Press. 4 Departamento d’Ecologia, Fac de Biologia, Universidad de Barcelona, Av Diagonal 645, 08028 Barcelona, Catalunya, Spain; 5CSIRO Sustainable Ecosystems, GPO Box 284, Canberra ACT 2601, Australia; 6Departamento de Biología, Universidad de La Serena, Casilla 599 and Centro de Estudios Avanzados en Zonas Áridas (CEAZA), La Serena, Chile; 7Department of Biology, University of New Mexico, Albuquerque, NM 87131, USA; 8Center for Advanced Studies in Ecology and Biodiversity (CASEB), Santiago, Chile; 9Department of Wildlife, Fish and Conservation Biology, University of California, Davis, Davis, CA 95616, USA; 10Parks and Wildlife Service of Northern Territory, PO Box 30, Palmerston NT, Australia 0831; 11 Northern Illinois University, DeKalb, IL 60115, USA; 12National Park Service, University of Rhode Island, Kingston, RI 02881, USA; 13 Department of Environmental Science and Policy, University of California, Davis, Davis, CA 95616, USA (deceased); 14Institute of Geography, FAU, Kochstr. 4/4, D 91054 Erlangen, Germany www.frontiersinecology.org 95