Rain and Rodents: Complex Dynamics of Desert Consumers

Water is the lifeblood of the desert. It comes in rains that are typically scant and sporadic, but can be so intense as to cause flooding. Because water is the resource in shortest supply, the amount and timing of precipitation directly limits plant growth and primary production. Seasons of exceptionally heavy and frequent rains produce the spectacular desert blooms shown in nature films and magazines. Seasons of exceptionally high rainfall are also thought to cause increases in rodent populations and outbreaks of rodent-borne diseases such as hantavirus and plague. El Niño is supposed to cause exceptionally heavy winter rainfall in the deserts of southwestern North America, leading in turn to plant growth, abundant seeds and insects, high populations of small mammals, density-dependent increases in parasites and diseases, and increased contact between rodents, their pathogens, and humans, resulting in disease epidemics. Thus, the outbreak of the Sin Nombre strain of hantavirus that killed 27 people in the Four Corners region of the southwestern United States in the summer of 1993 was attributed to the rains, plant production, and rodent increases triggered by the El Niño events of 1991–1992 and 1992–1993 (Harper and Meyer 1999). Ecologists have long been interested in these kinds of complicated pathways of interactions and particularly in how relationships between resources and consumers affect the structure and dynamics of ecosystems. The “bottom-up” pattern of regulation described above occurs when pulsatile resource inputs are transmitted up food chains, causing increases first in plants and then in successively higher trophic levels. This contrasts with “top-down” regulation, in which the feeding activities of top carnivores cascade down food chains to affect successively lower trophic levels (e.g., Hairston et al. 1960, Oksanen et al. 1981, Carpenter and Kitchell 1988). But ecological systems are complex, and there is reason to believe that resource–consumer relationships can exhibit chaotic or other forms of complicated nonlinear dynamics (e.g., Schaffer and Kot 1985, Hanski et al. 1993, Hastings et al. 1993, Lima et al. 1999). Long-term ecological studies provide unique opportunities to study resource–consumer relationships in realistically complex natural settings. Since 1977 we have been monitoring the weather, plants, and rodents in the Chihuahuan Desert near Portal, Arizona (figure 1; Brown 1998, Ernest et al. 2000). The resulting data allow us to evaluate the relationship between El Niño events and rainfall, the dependence of plants on precipitation, and the ways in which episodic rains affect desert rodent populations. After 23 years of study, we are far from understanding the dynamics of this ecosystem. One thing that is clear, however, is that simple bottom-up regulation does not occur. The responses of desert consumers to precipitation are complex and nonlinear. Figure 2 depicts a qualitative model for water resource regulation of desert rodent populations. Precipitation leads to germination, growth, and reproduction of plants, and the resulting increases in food supply in the form of seeds, fruits, and leaves lead to increases in rodent populations. The model assumes simple trophic transmission of pulses of resources from precipitation to plants to herbivores and, by implication, on upward through carnivores and higher trophic levels. According to this model, a cause-and-effect chain of resource limitation is transmitted up the trophic chain. If this model is correct, then at each trophic level, after an appropriate time lag, fluctuations in population should vary directly with fluctuations in available water caused by precipitation events. This simple model is not without theoretical foundation or empirical support. Water is the primary limiting resource for desert plants, so it would seem logical that the quantity and timing of germination, growth, and reproduction would be closely tied to precipitation events. Since most desert rodents obtain nearly all their food and water from plants, it would seem equally logical that fluctuations in rodent populations would be closely tied to variation in plant production, and therefore also to variation in precipitation. Indeed, this simple model does seem to work well some of the time, at certain spatial and temporal scales. Data from geographic comparisons across large spatial scales, as well as from some short-term observations, provide strong evidence for dynamic linkages from precipitation through plants to rodent populations. One kind of evidence comes from patterns of rodent abundance, distribution, and diversity in geographic gradients of varying precipitation. Comparative studies of rodents from small patches of relatively uniform habitat across the southwestern United States reveal clear trends. These studies have used standardized methods to census rodents in habitats of comparable soil type and vegetation structure, thereby holding constant habitat variables that are known to affect rodent ecology (Rosenzweig and Winakur 1969, Rosenzweig 1973, Brown 1975, M'Closkey 1978, Price 1978, Brown et al. 1979, Kotler and Brown 1988, Price and Podolsky 1989). The most arid parts of the Mojave and Colorado Deserts receive on average about 100 millimeters (mm) of precipitation per year, and typical habitats support low populations of only one or two granivorous rodent species. As precipitation increases in geographic gradients to the east and north, there are strong trends of increasing rodent species richness and overall rodent abundance. There are two pronounced peaks, one in the transition between the Sonoran and Chihuahuan Deserts in southeastern Arizona and southwestern New Mexico, and the other in the Great Basin Desert of northwestern Nevada. In these regions, which receive 52 to 321 mm of annual precipitation, it is not uncommon to find 5 to 10 species coexisting in shrubby habitats with sandy soils. So, along these gradients, both rodent species richness and total rodent populations are correlated with mean annual precipitation (figure 3; Brown 1973, 1975, Brown and Harney 1993, Shenbrot et al. 1994). These geographic patterns undoubtedly reflect the role of precipitation in limiting producers and consumers in arid regions. Rosenzweig (1968; see also Hillel and Tadmor 1962) showed that long-term average primary production in arid regions is closely correlated with average precipitation and actual evapotranspiration, and there is abundant evidence that seed production is correlated with primary production and precipitation. There is also considerable information on how rodent abundance and species diversity are influenced by food resources. With increasing precipitation and food availability, rodents become more specialized for particular food types and microhabitats, resulting in more complete and efficient exploitation of the food resources by a greater number of individuals and species (Brown and Lieberman 1973, Brown 1975, M'Closkey 1976, Shenbrot et al. 1994, Kelt et al. 1996). There is also evidence from these geographic studies that rodent population dynamics and community structure are affected by factors in addition to precipitation and food availability. Nearby habitats with nearly identical precipitation can differ markedly in rodent abundance and species composition. Often these differences appear to reflect variation in risk of predation (Rosenzweig and Winakur 1969, Rosenzweig 1973, Price 1978, Thompson 1982, Kotler 1984, Kotler and Brown 1988, Brown 1989). This raises the possibility that rodent populations are regulated not only from the bottom up by resource availability but also from the top down by predation. Short-term studies of rodent populations and community dynamics also appear to support the simple model of bottom-up regulation of desert rodent populations arising from fluctuations in precipitation and food resources. We can divide these studies into three groups. The first group documents rodent responses to single- or one-season rainfall events. Most of these studies have taken advantage of opportunities to study the consequences of rare, extreme precipitation regimes in extremely arid ecosystems. Their almost universal observation was that drought-breaking precipitation was followed by increases in rodent populations, and that extreme precipitation events—either single episodes of exceptionally heavy rainfall or entire seasons of far-above-average precipitation—were followed by exceptionally high rodent populations. A classic example is Beatley's (1967, 1969) documentation of plant and rodent responses to a single rainfall event in the northern Mohave Desert, but several other studies (e.g., Reynolds 1958, French et al. 1974, O'Farrell et al. 1975, Whitford 1976, Meserve et al. 1995) fall into this first group. The second group of studies documents longer-term correlations between precipitation inputs and rodent responses. Some of these studies also provide evidence for the intermediary link, that is, some kind of plant response such as increased productivity or cover following high rainfall. For example, Ernest and colleagues (2000) recently documented the relationship between precipitation, plant production, and rodent populations over an 8-year period at the Sevilleta Long-Term Ecological Research (LTER) site in central New Mexico. In general, this study found positive correlations, with successive time lags, among three variables—total seasonal precipitation, plant cover, and total abundance of all rodent species—in five habitats ranging from desert shrubland through arid grassland to juniper woodland. Differences in summer rainfall patterns among habitats were reflected in differences in plant responses and rodent populations. Other studies in this second group are by Petryszyn (1982), Brown and Heske (1990), Brown and Harney (1993), and Madsen and Shine (1999). The third group of studies focuses on the apparent influence of precipitation associated with El Niño events or with the El Niño–Southern Oscillation (ENSO) pattern. The last decade has seen considerable progress in understanding the linkages between oceanographic events and climate, especially those linkages between changes in currents in the eastern Pacific and shifts in climate in the western regions of both North and South America. The ENSO phenomenon has been linked to changing patterns of precipitation and related ecological dynamics in the southwestern United States and other arid regions, such as northern Chile. Several studies have reported increases in desert rodent populations following single or multiple El Niño events. Brown and Heske (1990) pointed out that three peaks in rodent populations at Brown's long-term study site between 1977 and 1987 appeared to be associated with higher-than-normal winter precipitation coinciding with the three El Niño events that occurred during that period. Similarly, Meserve and colleagues (1995) reported a large increase in rodents at their long-term research site in coastal Chile following the El Niño event of 1991–1992. These relatively short-term studies have encouraged widespread promulgation and acceptance of the simple model for the bottom-up influence of precipitation on rodents and other consumers in arid ecosystems. This model has been widely applied not only to account for the dynamics of desert rodent populations but also to explain how outbreaks of hantavirus and peaks of predator populations can be related to the trophic chain extending from precipitation through plants and mammalian herbivores to higher trophic levels (Jaksic et al. 1997, Polis et al. 1998). Compilation and analysis of data from our long-term studies near Portal, Arizona, in the Chihuahuan Desert suggest that the simple bottom-up trophic model is too simplistic. At least at our site, population and community dynamics of desert rodents are complex and nonlinear (“nonlinear” refers simply to the lack of a consistent monotonic relationship). At Portal, fluctuations in rodent populations cannot be explained simply in terms of pulses of limiting resources being passed with successive time lags up trophic chains following precipitation events. We illustrate this point by describing three results from Portal and their The first is that the apparent relationship between El Niño events and peaks in rodent abundance that we in the and to in the (figure There were two El Niño events in the a El Niño in 1991–1992 and 1992–1993 and a strong El Niño in was followed by an increase in rodent abundance. In rodents near low during and after the 1991–1992 and 1992–1993 after in the rodents high in the summer of 1997, but this was not associated with an El Niño It is to that the El Niño not in high winter precipitation at the study In this El which was to be the one in the far to the along the Pacific and the El Niño cause exceptionally heavy winter precipitation, most of the well to the of our study This observation that El Niño is a complex and there be simple relationship between in the and winter precipitation in the southwestern United results have from a short-term study documented peaks in populations of rodents, especially the species following El Niño et al. 1999). longer-term and comparisons across that El were not followed by increases in populations et al. 1999). In populations showed dynamics that were out of with each other and out of with This observation Lima and colleagues to that populations exhibit chaotic The second is that 23 years of data from Portal there has been simple relationship between precipitation plant and rodent population There was a positive between abundance of annual plants and total seasonal precipitation, but rodent abundance was not correlated with the quantity of precipitation or the abundance of plants et al. 2000). we the Portal study, we that with a long time of it would be to clear relationships between the temporal pattern of precipitation and variation in plant growth and seed production, and rodent population As the of the time has however, the relationships have become more Indeed, the of the between seasonal precipitation and rodent abundance, increasing or at least with increasing time, to (figure Some for this and for the lack of a consistent response to El from analysis of time from the Sevilleta site, at the northern of the Chihuahuan Desert about of These time positive correlations with appropriate lags between seasonal precipitation, plant cover, and rodent populations et al. 2000). also that can have patterns of precipitation, plant and rodent of differences in summer precipitation. precipitation, that associated with El comes from systems that over the Pacific and then across the southwestern United precipitation comes from intense which are but influenced by and other Ernest and colleagues (2000) showed that the dynamics of plants and rodents are influenced by summer as well as winter precipitation and that correlations between precipitation, plants, and rodents cannot be the nature of summer precipitation is taken into Because to of the precipitation at both the Sevilleta and Portal can be attributed to summer the high spatial and temporal of these can the rodent and plant dynamics of only a In there are strong responses that can be attributed to El Niño events these at Sevilleta reveal some of the in variation in plant and rodent responses to patterns of precipitation, are not in understanding the more complex dynamics at A rainfall at Portal, and we that the plants, but not the rodents, showed consistent responses to seasonal precipitation. The third to explain rodents to to precipitation events that caused peaks in plant production at It is clear that there is not a simple of more or relationships between precipitation plant production, and rodent population The rodent responses are complex and nonlinear. on the temporal as well as the total of seasonal precipitation and on other such as the abundance of we have not resources to the of rodents at We however, that the response of rodents to precipitation has a nonlinear heavy rainfall can cause in rodent populations. this is in to the increases that would be the of precipitation are through plant production and food availability. Figure the fluctuations in the of the two rodent species that were most abundant at Portal when we our study in that the second most abundant the showed a over the winter of This followed during a period mm of precipitation, nearly the annual average for the study site et al. The in can be attributed to the that this seeds in large and and food were and rodent the and several species of all of which seeds in at the that other factors be to account for the of to following this event et al. Figure that the most abundant rodent species on the study site, in We with that this was to a single intense that more mm of in a period of 2 on This caused over the site to a of nearly a to in water by in the that other are to of were to from the that that the killed the of and the individuals of a third that were on the was only affected by it does not seeds in and the rainfall was over a period that there was These point out one reason for the lack of consistent relationships over the long between seasonal precipitation plant production, and rodent population Because extreme precipitation events can cause in rodent populations or population increases through increased food supply, the nonlinear of extreme events consistent relationship between precipitation, plant and rodent abundance. There is reason to believe that there are other nonlinear relationships that the relationships between desert rodents and their resources. It is that a We at least populations of and increase in response to population peaks in their rodent It is to that seasons of high rainfall and plant production high predator populations that have up in response to the first or a rodent increase in response to the second the other seasons are by time, so that have increased have then the rodent populations increase relatively by data to such a nonlinear of are and, in the of Portal, Lima and colleagues this kind of nonlinear of to explain the chaotic dynamics of rodent populations in response to ENSO events in Chile. It is that diseases, and other and factors also have nonlinear or of precipitation on rodents or other We have our to desert rodents, our long-term data allow us to with some we believe that of the from rodents are to other kinds of the last several we have seen a simple for the bottom-up influence of precipitation on desert rodents be receive and be There are some the simple model is not it is too to the complex dynamics of desert ecosystems. deserts seem be relatively simple with systems such as are and The in the simple model are undoubtedly The availability of water of the structure and dynamics of arid the temporal pattern of precipitation and primary productivity and seed and the availability of seeds and other plant resources populations of But other factors responses to precipitation not on the total quantity of rainfall a but also on the and timing of rainfall events and on other factors as and interactions as and fluctuations in rodent populations not only on availability of food resources but also on other both and such as extreme events and The is that simple model is to be to realistically the large number of variables and ecological that affect population This is for a single species population and also for total abundance of all species a or such as there is reason to believe that such complex interactions and nonlinear dynamics should be to a particular or trophic We that responses of plants to precipitation would be and more those of higher trophic and some of our data from Portal would support this the plants exhibit complex In the winter of there were heavy rains at Portal, and There was precipitation during the of the however, and nearly all of the without model that would account for plant responses to precipitation the timing as well as the of rainfall events. Since the simple are it be to the structure and dynamics of these it be in some to the of fluctuations after have it be almost to the of the in the The of extreme rainfall events on the illustrate this There are The Sin Nombre strain of which caused in the Four Corners region of the southwestern United States in the is in populations of The model for the outbreak of hantavirus is a of the bottom-up trophic model for the influence of precipitation on According to this model, El Niño events cause exceptionally heavy winter high precipitation peaks in plant growth and seed high food availability increases in rodent high abundance of rodent species and frequent among individuals hantavirus leading to high in rodent high populations increased of rodents into with and contact with and of rodents transmission of hantavirus to et al. 1993, et al. 1999). This model was on one of the above events that occurred following the 1991–1992 and 1992–1993 El The to high levels of hantavirus in rodents or in the Four Corners region following the El Niño that the simple bottom-up model is too simplistic. evidence comes from the to consistent relationship between El Niño events and rodent populations at populations of the which to be the primary for the Sin Nombre strain of hantavirus (figure We have about other studies that that outbreaks of rodent-borne diseases can be from simple cause-and-effect of limiting factors transmitted through chains of ecological One example is disease in the United studies fluctuations in of disease to a chain of ecological interactions extending from climate through production of and other to increases in populations and then through to et al. et al. 1998). In the of and other rodent-borne diseases, we not the of events that has been or the interactions that have been to explain We however, that the of the complex relationships between precipitation and rodent population dynamics from Portal and Chile provide reason to the of simple These long-term studies suggest that variables and events can affect the and dynamics of transmission of pulsatile through chains of ecological studies allow of but be to reveal the of the should to obtain long-term data to evaluate and should in of we have in this should be taken as the that water is the primary limiting resource that the structure and dynamics of arid ecosystems. This is it is almost But the reason that water such a large role in arid supply of water is by precipitation events as pulses of widely varying and it to have complex nonlinear on the of desert ecosystems. from our long-term studies however, that research be to the and consequences of water limitation in arid ecosystems. If we are to the responses of desert plants and rodents to temporal and spatial variation in rainfall, a of the nonlinear relationships be Since outbreaks of rodent-borne diseases are more from the pulses of precipitation, both in the chain of ecological interactions and in time, to and these be an greater We are to the more 100 people have on the Portal and to the over the last 23 We are also to the for most recently with Research in We and for on the Figure of our long-term research in the Chihuahuan Desert near Portal, Arizona, we have been data on precipitation, plants, and rodents Figure A simple model how pulses in resource availability are thought to be transmitted with time lags up food chains to affect successively higher trophic levels. This in type the of precipitation on plant production and of plant food resources on rodent populations. The of El Niño on precipitation and of rodent populations on hantavirus are shown in a Figure between number of rodent total rodent abundance, and mean annual precipitation along a of increasing rainfall from the Colorado and Mojave Deserts of to the Great Basin Desert of northwestern Nevada. number of species and overall abundance of rodents increase with increasing precipitation. data in Brown Figure dynamics of rainfall and rodent populations at our long-term study site in southeastern Arizona in the top are winter and summer precipitation and and total abundance of all rodents in a period In the bottom are populations of rodent two and a and the shown in both are the El Niño events and and two extreme rainfall events in fall and an intense in summer that occurred during this period. that there is consistent relationship between rodent populations and rainfall or El Niño but the two extreme rainfall events caused in rodents, of and in after and of in after the caused by the Figure and for relationships between total rodent abundance and mean precipitation for at the long-term site in southeastern Arizona for three of increasing time and were on all and in the data and then that the for the entire time is lower for increasing with increasing of the time as would be the relationship between precipitation and rodent abundance were