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Research Cite this article: McCluney KE, Sabo JL. 2016 Animal water balance drives top-down effects in a riparian forest—implications for terrestrial trophic cascades. Proc. R. Soc. B 283: 20160881. http://dx.doi.org/10.1098/rspb.2016.0881

Received: 19 April 2016 Accepted: 26 July 2016

Subject Areas: ecology Keywords: water web, food web, drought, precipitation, predation, herbivory

Animal water balance drives top-down effects in a riparian forest—implications for terrestrial trophic cascades Kevin E. McCluney† and John L. Sabo School of Life Sciences, Arizona State University, Tempe, AZ 85287-4501, USA KEM, 0000-0002-3574-0354 Despite the clear importance of water balance to the evolution of terrestrial life, much remains unknown about the effects of animal water balance on food webs. Based on recent research suggesting animal water imbalance can increase trophic interaction strengths in cages, we hypothesized that water availability could drive top-down effects in open environments, influencing the occurrence of trophic cascades. We manipulated large spider abundance and water availability in 20  20 m open-air plots in a streamside forest in Arizona, USA, and measured changes in cricket and small spider abundance and leaf damage. As expected, large spiders reduced both cricket abundance and herbivory under ambient, dry conditions, but not where free water was added. When water was added (free or within moist leaves), cricket abundance was unaffected by large spiders, but spiders still altered herbivory, suggesting behavioural effects. Moreover, we found thresholdtype increases in herbivory at moderately low soil moisture (between 5.5% and 7% by volume), suggesting the possibility that water balance may commonly influence top-down effects. Overall, our results point towards animal water balance as an important driver of direct and indirect species interactions and food web dynamics in terrestrial ecosystems.

1. Introduction Author for correspondence: Kevin E. McCluney e-mail: [email protected]



Present address: Department of Biological Sciences, Bowling Green State University, Bowling Green, OH 43403, USA. Electronic supplementary material is available at http://dx.doi.org/10.1098/rspb.2016.0881 or via http://rspb.royalsocietypublishing.org.

The evolution of terrestrial life has been driven by the challenge of maintaining water balance with scarce freshwater resources, but effects of animal water limitation on terrestrial food webs have received little attention, in contrast to plant-mediated bottom-up effects [1,2–5]. This is a significant gap in our understanding of ecological dynamics, because over 40% of the earth’s land surface is classified as drylands [6] and precipitation limits diversity of plants and animals at all but the highest latitudes globally, even outside of drylands [7]. Moreover, both animal water demand and the availability of water are being altered by global changes in temperature, precipitation, urbanization and water infrastructure [8]. If water balance influences food webs, it may also alter ecosystem form and function in ways that directly impact humans (e.g. crop production in agroecosystems). Water availability probably has both bottom-up and top-down effects on food webs [9], but evidence for top-down effects comes mostly from observational research [5,10–12], limited field manipulations [13,14] or cage experiments [15]. This evidence suggests that consumers may meet water demands by consuming large amounts of moist food when environmental water sources (e.g. saturated soil or open water) are unavailable [9,10,15]. In these situations, terrestrial food webs can be viewed as water webs, with water driving trophic interactions [15]. Large-scale, open-air manipulative experiments examining the direct importance of animal water balance in structuring food webs are generally lacking (but see [16]). Systems with strong top-down effects can shift dramatically with relatively small changes to the food web, leading to trophic cascades [17–19]. Trophic cascades, where predators affect the abundance of primary producers by altering

& 2016 The Author(s) Published by the Royal Society. All rights reserved.

(a) Overview We examined the changes in the abundance of crickets and spiders in 24 of 20  20 m open-air plots in two large (3– 4 ha)

(b) Study site Our study site was along a section of the San Pedro River, in southeast Arizona, USA (a biodiversity hotspot) with intermittent flow frequency (see the electronic supplementary material, text S1 for more information). The river was flowing at the beginning of the measurement period, but dried prior to initiation of experimental treatments (dried on 19 May; figure 2). This site was the driest of the three floodplains included in a previous study of the effects of water limitation on riparian animal populations [16], but has experienced greater flow permanence than many other parts of this river [38]. In recent years, increasing withdrawals of groundwater from the regional aquifer by rapidly growing cities, as well as local climate shifts, have resulted in declining baseflows and increasing frequency of river drying in the dry season [39]. Monsoon rains began during the last few days of experimental surveys, in the third experimental period (25 June; figure 2), and major flood disturbance occurred shortly thereafter, which would have prevented continuation of the experiment. Flooding during the monsoon season is likely to be important in driving population dynamics for our focal species, but in this study, we focused on the dry season to help us better understand how animal water balance influences food web dynamics in general.

(c) Design After the initial pre-manipulative measurement period, we began reducing the abundance of the top invertebrate predators, large wolf spiders (mostly Hogna antelucana, more than 1 cm head to cephalothorax), via nightly removal by hand capture (electronic supplementary material, text S1). Removal occurred across plots (four treatment plots plus three additional spider removal only plots; electronic supplementary material, figure S1) within three randomly selected sections of the two experimental floodplains, leaving another three sections with ambient large spider abundance. Floodplain sections were separated from one another by more than 60 m of floodplain forest (electronic supplementary material, figure S1). We manipulated large spider abundance but not cricket abundance, because we were primarily interested in the influence of water balance on top-down effects from spiders to crickets to leaf consumption. Additionally, simultaneously manipulating spider and cricket abundance would be untenable in large, open-air plots. Using a split-plot design, we crossed the spider manipulations with alteration of water availability, either directly as free water (R-Zilla cricket water pillows—pouches filled with a hydrated polymer that moistens a cotton mesh surface; Central Garden and Pet Company, Walnut Creek, CA) or indirectly as ‘trophic water’ contained within freshly picked moist cottonwood (Populus fremontii) leaves (electronic supplementary material, text S1). Addition of moist leaves contributed only approximately 0.04%, on average, to the existing leaf litter of

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2. Methods

floodplains along the semi-arid San Pedro River (electronic supplementary material, figure S1), during three experimental periods: (i) ambient, baseline conditions for 16 days (t0, starting 7 May 2012), (ii) water supplementation and spider removal for 23 days from selected plots in a split-plot factorial design (t1, starting 23 May 2012), and (iii) only spider removal for 12 days, stopping water addition to simulate drying (t2, starting 15 June 2012; electronic supplementary material, text S1 and figure S2a; figure 2). At the end of each experimental period, we measured the rates of herbivory in each plot. We focus on the rate of change within plots across the first two experimental periods, using a before-after-control-impact design, with results from the third period (simulated drying) shown and discussed mostly within the electronic supplementary material. Comparing rates of change across treatments allows us to control for initial differences among plots when examining treatment effects.

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density or behaviour of intermediate trophic levels (sensu [20 –22]), were once considered to be ‘all-wet’, occurring predominantly in freshwater ecosystems [23– 25]. However, recent research has demonstrated that terrestrial trophic cascades are common and widespread, but often difficult to detect [17,26,27]. Trophic cascades may be driven by direct reductions in density of herbivores by predators, or by predator modifications of herbivore foraging behaviour (e.g. ‘fear’) [28 –31]. Previous research suggests that the magnitude of top-down effects may be influenced by consumer size and metabolic rate, the existence of plant defences, the diversity of herbivores, the choice of plant response metric and environmental conditions such as solar radiation, temperature, rainfall or disturbance [5,26,27,32,33]. Additionally, traitmediated indirect interactions, like anti-predator behaviour, often play a large role in driving these cascades [28,29,31,34], with the strength of these effects, relative to density-mediated indirect interactions (direct consumption), probably driven by predator hunting modality (i.e. sit and wait) and habitat use relative to prey [29]. As yet, the importance of animal water balance in determining the strength of top-down effects or the likelihood of trophic cascades has received surprisingly little attention. Previous work has shown that water balance can influence consumption of moist food for particular consumers [9,15]. We hypothesized that this alteration of consumption would lead to changes in the strength of top-down effects in real food webs. We designed and executed a large and intensive open-air manipulation of water resources (free water and water contained in moist leaves) and the density of predators (large wolf spiders), measuring effects on lower trophic levels, in a streamside forest in Arizona, USA. Moreover, we simultaneously measured soil moisture and temperature, in the hope we could identify the range of environmental conditions under which water balance might influence top-down effects. We predicted that adding free water (direct water supply, available to all arthropods) would lead to reductions in the strength of top-down effects of large spiders on crickets and crickets on leaves (figure 1, A1 versus A2). However, we expected an increase in the effect of large spiders on small spiders based on the hypothesis that large spiders would switch from consuming water-laden crickets to consuming high-nutrient small spiders as water became less limiting and presumably nutrients became more limiting (sensu [35,36]). When we added water contained in moist leaves (indirect water supply, not available to spiders), we did not expect a change in the effect of spiders on crickets (figure 1, A1 versus A3), following results from a previous experiment [15]. However, we predicted that adding moist leaves would lead to an increase in the abundance of crickets across spider treatments (through cricket dispersal) and that greater abundance of crickets would lead to slight increases in the effects of large spiders on small spiders, owing to apparent competition [37]. Supplementing water directly (free water) versus indirectly (via moist leaves) allowed us to better separate the effects of spider water balance from effects of cricket dispersal or behaviour.

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Figure 1. Comparison of predicted and observed effects of large (.1 cm) ground spiders, under three water treatments, on a desert riparian food web. The water drop symbol indicates the experimental supplementation of free water (via water pillows), and the leaf symbol indicates fluxes of water in moist leaf material (natural and experimental). Water was supplemented 2.5 the ambient rate of water flux (via natural greenfall). The width of arrows represents the qualitative size of fluxes of water (grey arrows) or the strength of top-down effects (black arrows). Mathematical symbols indicate direction of effects, whereas numbers are parameter estimates of the rate of change (table 1). Under dry ambient conditions (left) and with added moist leaves (right), we expected large spiders to have strong negative effects on cricket abundance and positive effects on leaf abundance, but we expected these effects to disappear with free water (middle). Additionally, we expected large spiders to switch between consumption of crickets (without water) and small spiders (with water). Observed patterns matched the expectation that free water would greatly influence top-down effects. However, water addition was insufficient to ‘quench’ cricket leaf consumption (sensu [15]), large spiders did not reduce cricket abundance with moist leaf additions, and the effects of large spiders on herbivory where water was added were probably behavioural, because there were no effects of large spiders on cricket abundance in those treatments. It is unclear if the effects of large spiders on small spiders matched expectations, because of a lack of significant post-hoc differences within water treatments, despite an overall significant effect across water treatments. (Online version in colour.) these plots (approx. 0.0025 m3 of leaves were added to 6.4 m3 of existing litter), but added leaves increased water availability 2.5 above the natural rate of addition of fresh green leaves from the overlying canopy [10]. Water pillows were added to achieve the same rate of water supplementation, 2.5 the natural flux in leaves. Because we contributed little to habitat structure or food available to crickets (dry leaf litter), moist leaf addition primarily manipulated water available to primary consumers (crickets), but not predators (spiders). This allowed us to better separate the effects of spider water balance from effects on dispersal or behaviour of crickets. To track changes in the density of crickets and spiders, we conducted nightly surveys along transects. Each plot contained three parallel transects running the length of the plot (20 m) and spaced 5 m apart, with each transect demarcated with twine. A pair of observers with identical 200 lumen headlamps (Icon, Black Diamond) counted juvenile and adult crickets (Gryllus alogus) and small and large ground spiders (1 cm head to cephalothorax) within a 1 m band along each transect (electronic supplementary material, text S1). The location of initiation of surveys rotated nightly and responses were averaged across a complete rotation of starting locations (3 days) to reduce effects of temporal differences in activity.

On the final day of each experimental period, we measured herbivory (leaf damage) by placing four freshly picked cottonwood (P. fremontii) leaves, attached to a wooden shim, on the ground at the centre of each transect and recording the per cent consumption of each leaf in 10% categories the following day (electronic supplementary material, text S1). During surveys, every 1–2 nights, we measured soil moisture (readings from three locations within 1 m2) near the centre of each floodplain section using a Delta-T soil moisture sensor (ML2X Theta Probe with HH2 meter, Dynamax, Inc.). We also measured ground temperature using Hobo microstation data loggers equipped with smart sensors (Onset, Bourne, MA) housed in 15  21  19 cm white, plastic, ventilated, radiation shields, placed on the ground.

(d) Data processing and statistical analysis Analyses of nightly surveys were conducted, using likelihood ratio tests of linear-mixed models, with time, water addition and spider removal as fixed factors, and floodplain section, plot and transect as nested random factors. Fixed factors were dropped, one at a time, from a full model, testing for significant changes in likelihood (sensu [40]). If a significant interaction between water addition and spider removal was detected, we

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Figure 2. Changes in soil moisture (a), air temperature (a) and spider abundance (b – d) over the duration of the experiment. Error bars are standard error of the mean. (c,d) represent estimates of the rate of change in large spider abundance per unit time, between each of the experimental periods, from model parameter estimates, which controls for plot differences. Spider removal significantly reduced the abundance of large spiders by the end of the supplementation period (electronic supplementary material, table S1). tested our specific predictions using post hoc general linear hypothesis tests (Dunnet’s), examining if large spiders had an effect on crickets, small spiders or leaves under different water addition treatments. All analyses were conducted in R v. 3.0.2 [41], with nlme [42], lme4 [43] and multcomp [44] packages. We also examined the relationship between rates of herbivory and soil moisture in the true control plots (electronic supplementary material, text S1 and figure S1) across the entire experiment using glmm on individual leaves and breakpoint regression (via the ‘segmented’ package in R [45]) on plot averages. See the electronic supplementary material, text S1 for more details.

3. Results (a) Environmental conditions Two large rain events with an intervening dry, hot period characterized our 51 day study (figure 2a). Declining soil moisture and streamflow followed the initial, aseasonal rain event, with complete river drying prior to initiation of experimental manipulations (day 13). Another rain event near the end of the experiment (during the simulated drying period) raised soil moisture and signalled the start of the monsoon season.

plots (figure 2c); this translated into a mean of a 55% reduction in large spiders in the reduced spider plots during the supplementation period (0.044 versus 0.020 spiders m22). We found no significant effects of water manipulation on large spider abundance (electronic supplementary material, table S1).

(c) Predator effects on primary consumers—crickets— with altered water resources Large spiders reduced the abundance of crickets (G. alogus) under dry ambient conditions, but not when either free water or moist leaves were experimentally added (i.e. significant water  spider interaction, table 1 and electronic supplementary material, table S1; figure 3). Cricket abundance increased in all plots across the first two experimental periods, but spiders reduced the rate of increase by 37% in dry ambient conditions (figure 3); this translated into a mean of a 23% reduction in crickets in ambient spider, dry control plots, during the supplementation period (1.48 versus 1.14 crickets m22). With cessation of water addition (simulated drying) in the third experimental period, cricket abundance declined, especially in moist leaf addition plots, but this reduction did not appear to be influenced by large spiders according to post hoc tests (electronic supplementary material, figure S2 and table S2).

(b) Efficacy of spider removal We removed 2691 large ground spiders (mostly H. antelucana) over 35 days (23 May–15 June), significantly lowering the abundance of this top invertebrate predator (figure 2b–d and electronic supplementary material, table S1). Large spider abundance declined across all plots—possibly reflecting natural seasonal variability unrelated to removal—but the rate of decline was 14 greater in removal plots than the ambient

(d) Predator effects on intraguild predators—small spiders—with altered water resources We found significant interactive effects of large spiders and water addition on the abundance of small spiders, seemingly suggesting a positive effect of large spiders on small spiders under dry conditions, but not with added water or moist

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Figure 3. Effects of large spiders on crickets, small spiders and leaves, reported as the rate of change from the initial, pre-manipulation period to the end of the spider removal, water addition period. Plots are divided into ambient water plots (‘control’, ‘C’, black symbols), free water supplemented plots (‘water’, ‘W’, blue symbols), and moist leaf supplemented plots (‘moist leaves’, ‘ML’, green symbols). ‘A’ and ‘R’ on the x-axes refer to ambient and reduced densities of large spiders. Error bars are standard error of the mean. Effect sizes are estimates of the rate of change in each response per unit time (3 day survey blocks for crickets and spiders, experimental periods for leaves), based on model parameter estimates, which controls for plot differences. Large spiders had a significant negative effect on crickets in control plots and positive effect on moist leaves in all treatments (but note the effect is opposite for free water) according to post hoc Dunnet’s tests (table 1). The response of moist leaf material is displayed as the amount remaining so that it is more easily comparable to other graphs, but this means that it displays the inverse of consumption (noted by the arrow on the right-hand side). Post hoc tests for small spiders do not show significant differences (electronic supplementary material, table S2), despite an overall significant time  water  spider removal interaction (electronic supplementary material, table S1). Results for the post water addition, ‘simulated drying’ period (figure 2) are reported in the electronic supplementary material. See the electronic supplementary material figures S2– S4 for plots of full timeseries. Table 1. Post hoc general linear hypothesis tests (Dunnet’s) for the effects of spiders on crickets or leaf material, within each water treatment, following finding of a significant interaction between spider treatments and water supplementation treatments in the full model (during the first two periods, pre-experiment and supplementation). (Italicized rows are those with statistically significant effects at alpha ¼ 0.05.)

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leaves (figures 1 and 3; electronic supplementary material, table S1). However, despite an overall significant water  spider removal interaction, post hoc comparisons did not reveal significant differences (electronic supplementary material, table S2). Thus, water influenced the effect of the large focal predators on smaller intraguild predators, but the exact pattern and mechanism is unclear. Cessation of water addition (simulated drying) coincided with increases in

small spider abundance, particularly in previously free-water supplemented plots, but effects did not vary with large spider removal (electronic supplementary material, figure S2 and table S1 and S2). This pattern might be indicative of higher survival or reproduction of spiders in previously water supplemented plots, but we did not test this directly.

(e) Top-predator effects on herbivory with altered water resources Herbivory (leaf damage) increased between pre-treatment and supplementation periods as soil moisture declined naturally (figure 2), but, the magnitude differed between water and spider removal treatments (figure 3; electronic supplementary material, table S1 and table 1). Spiders depressed herbivory under dry ambient conditions and where moist leaves were added, but slightly enhanced leaf consumption with free water addition (figure 3 and table 1). These effects were reversed on the final date of the experiment, when soil moisture was again high owing to rainfall, with leaf consumption near zero in all plots (electronic supplementary material, figure S2 and tables S1–S2).

(f ) Soil moisture and herbivory Across treatments, herbivory was most strongly and significantly correlated with soil moisture (electronic supplementary material, table S1), with herbivory dropping sharply above 6.8% soil moisture (the maximum value with more than 50% consumption of leaves) or with consumption declining at 5.51% soil moisture on average (breakpoint regression; figure 4).

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Figure 4. Soil moisture versus herbivory in each true control plot. Scatterplot of the mean consumption of leaves per plot, per measurement date, showing maximum soil moisture with more than 50% consumption (6.8% by volume) and average point of decline in consumption (5.51%) from breakpoint ( piecewise) regression (solid line).

4. Discussion Here, we show that variation in water availability can modify the strength of top-down effects (figure 1b). Population-level effects of large spiders on crickets varied with water availability, as predicted from previously observed shifts in per capita consumption in cages [15]. Specifically, large spiders reduced cricket populations under dry ambient conditions, but had no effect with water supplementation (figure 1, B1 versus B2). This result followed expectations from previous research in cages [15], and thus supports the hypothesis that short-term, small-scale changes in per capita effects can roughly predict longer-term population-level dynamics [19]. Similarly, as predicted, large spiders had positive effects on moist leaf material (reduced herbivory) under dry conditions (figure 1, B1), but in contrast to predictions (no effect), large spiders increased herbivory where direct free water was added (reverse of a trophic cascade; figure 1, B2). Moreover, large spiders reduced herbivory with moist leaf addition, even though the abundance of crickets was unaffected by large spiders (figure 1, B3). Water also influenced the effects of large spiders on small spiders, but the mechanism remains unclear, requiring further exploration. Taken together, our results suggest that free water availability controlled the size and direction of multi-level top-down effects in this system, but not always as predicted. The increase in herbivory associated with spiders when free water was added (reverse trophic cascade) was unexpected (expectation ¼ no effect). Although we cannot directly test the mechanism behind this observation, we hypothesize it may be owing to large spiders deterring crickets from accessing water pillows (J. Sblendorio and L. Ford II video observation; sensu [46]), forcing crickets to rely more greatly on moist leaves to meet water demands [10]. Another unexpected result was the lack of an effect of spiders on cricket abundance in moist leaf additions. We hypothesize this could be owing to high rates of recruitment of crickets to these plots masking potential evidence of top-down effects (see rate of increase in crickets in moist leaf plots in figure 3) or perhaps could be associated with an increased water content of crickets in those plots leading to lower per capita consumption by spiders. Despite the lack of an effect of large spiders on cricket abundance with moist leaf additions, large spiders still

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reduced herbivory in that treatment (see spider effect on moist leaves in figures 3 and 1, B3). Although we cannot directly test a mechanism for this observation, we hypothesize that this could be a consequence of a trait-mediated indirect interaction—‘fear’ of predation by large spiders could have led to reductions in rates of leaf consumption, especially when these leaves were more abundant (sensu [29,46]). However, we admit there are other, more complex possibilities. For instance, if spider consumption of crickets led to compensatory dispersal of crickets into high spider plots at higher rates, new crickets could have changed competitive interactions within these plots or showed other differences in behaviour that could have reduced herbivory. But, overall, we believe it is most likely that trophic cascades in this system are being driven by a combination of density-mediated indirect interactions (consumption) and trait-mediated indirect interactions (behaviour), agreeing with expectations from theory for a sit-and-pursue predator with prey confined to the same habitat as predators (see [29]). Moreover, although other possibilities exist, we hypothesize that the balance of trait-mediated and density-mediated effects may depend on water availability—consumers may perform a cost– benefit analysis: with limited water (free or in food), direct consumptive effects may outweigh behavioural effects, whereas with greater water availability (free or in food), behavioural effects may become more pronounced. We believe that water balance may play a large role in driving the behaviour of terrestrial animals—dehydration can occur quickly and may pose more certain risks than predation ( perhaps epitomized by species interactions surrounding watering holes in the African savannah [47]). However, testing the above-outlined hypotheses requires additional experimentation. Levels of leaf damage were highly correlated with soil moisture (more strongly than water addition treatments) with a nonlinear, threshold-type transition from almost full consumption to almost zero consumption between 5.5% (breakpoint regression) and 6.8% volumetric soil moisture (maximum soil moisture with more than 50% leaf consumption). This level probably represents the point at which crickets switch from obtaining water from moist leaf material to obtaining water from environmental sources. We believe this transition point could vary considerably among taxa and ecosystems, owing to differences in physiological traits (e.g. cutaneous water loss), drivers of water loss (e.g. temperature, humidity) and availability and quality of trophic water sources (e.g. chemically defended leaves). However, to provide some guidance as to the potential frequency of water-mediated top-down effects, we examined volumetric soil moisture measurements across the United States (US) using the COSMOS Soil Moisture Network database [48] and found that soil moistures below 6.81% can be found in 49% of the 65 US measurement locations, over the 7 year period from 2008 to 2014—even mesic locations in the southeastern US and in northern Wisconsin and Michigan showed values below this threshold, but the greatest frequency was within the US sunbelt (electronic supplementary material, figure S5). These results correspond well to previous suggestions that patterns of animal species richness are at least partially limited by water at all but the highest latitudes (energy only at more than 508; [7]). If the effects of soil moisture on arthropod foraging behaviour and population dynamics found here can be generalized beyond our study

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interactions could underlie food web responses to changes in spatial and temporal patterns of water availability expected with global climate change, groundwater pumping and human infrastructure. Data accessibility. Data are available in the electronic supplementary material.

Authors’ contributions. K.M. designed, conducted and analysed the study and wrote the manuscript. J.S. provided advice on the design and analysis of the study and edited the manuscript.

Competing interests. We have no competing interests. Funding. The US National Science Foundation provided financial

ham and Monica Palta for advice on the design of the experiment. Additionally, we thank Martin Vega, Ruben Marchosky, Zachary Lancaster, Tyna Yost, Joanna Sblendorio, LaMarcus Ford II, Robin Greene, Karl Wyant and Israel Leinbach for extensive assistance in the field. The US Bureau of Land Management provided permission for this experiment and access to the site. Finally, we thank Shannon Pelini, Karen Root, Evan Preisser, James Brown and several anonymous reviewers for feedback on our manuscript.

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support (DEB-0842410).

Acknowledgements. We thank Dan Allen, Dave Spiller, Kathy Cotting-

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Animal water balance drives top-down effects in a riparian forest-implications for terrestrial trophic cascades.

Despite the clear importance of water balance to the evolution of terrestrial life, much remains unknown about the effects of animal water balance on ...
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