© 2001 by The Society for Integrative and Comparative Biology
Plant Secondary Compounds as Diuretics: An Overlooked Consequence1
1 Department of Biology, University of Utah, Salt Lake City, Utah 84112
2 Department of Wildlife Ecology, University of Wisconsin, Madison, Wisconsin 53706
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Plant secondary compounds are deterrents and toxins to a variety of herbivores. The effect of secondary compounds on water balance of herbivores is virtually unexplored, yet many secondary compounds are renowned for their diuretic effects in humans and laboratory rats. We review data from the ethnopharmocological literature on plants with diuretic effects. We also present our data from experiments on water intake of specialist (Neotoma stephensi) and generalist woodrats (N. albigula) consuming plant secondary compounds from their natural diet. We measured effects of dietary secondary compounds on voluntary water consumption, urine volume and urine osmolarity. Ingestion of secondary compounds increased water intake and urine output and decreased urine osmolarity in both species. However, the generalist was more impacted by dietary secondary compounds than the specialist. Our results combined with that from the literature suggest that diuresis may be a prevalent consequence of ingestion of secondary compounds. Many herbivores live in arid habitats with limited access to free-standing water, thus an increase in the desire for water may have profound consequences on foraging behavior and fitness.
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INTRODUCTION |
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The ingestion of plant secondary compounds by a herbivore can result in a multitude of physiological consequences. Outcomes of secondary compound ingestion include but are not limited to numerous toxic effects, disturbance of acid-base homeostasis, emetic stimulation and mineral wasting (Foley and Hume, 1987
; Foley and McArthur, 1994; Foley et al., 1995; Iason and Murray, 1996; Iason and Palo, 1991; Lindroth and Batzli, 1984; Lindroth et al., 1986; McArthur and Sanson, 1993; McLean et al., 1993; Meyer and Karasov, 1989; Thomas et al., 1988). In addition, various secondary compounds have been documented as feeding deterrents that reduce or eliminate consumption of particular species of plant (Reichardt et al., 1990a, b, 1984; Sinclair et al., 1988; Snyder, 1992; Vaughn and Czaplewski, 1985). The proposed mechanisms underlying deterrency include any of the physiological consequences listed above as well as yet undescribed ones (Pass and Foley, 2000).
Theoretically, consumption of secondary compounds could drastically affect the water balance of herbivores. Two separate lines of evidence suggest that ingestion of secondary compounds detrimentally impact water balance and that this effect may be a prevalent one. First, a multitude of plants or specific secondary compounds has been documented to negatively effect water balance in vertebrates, particularly humans (e.g., Adsersen and Adsersen, 1997). Second, herbivores consuming secondary compounds exhibit elevated sodium excretion (Iason and Palo, 1991; Perhson, 1983). Sodium excretion, or natriuresis, almost inevitably increases urinary excretion (Hardman and Limbird, 1996). Therefore, the water balance of animals excreting increased quantities of sodium may have been severely altered.
The effect of plant secondary compounds on water balance of herbivores has been largely ignored by ecologists. In this paper, we review the literature on diuretic effects of plant secondary compounds on humans and laboratory animals such as rats. We also present data on water intake, urine output and concentration of herbivores consuming plants with secondary compounds. The results suggest that plant secondary compounds act as diuretics on herbivores and that diuresis may be a general consequence of the ingestion of secondary compounds irrespective of the particular class of compound.
PSC as diuretics
Diuretics are defined as compounds that increase urine flow (Hardman and Limbird, 1996). A primary therapeutic use of diuretic compounds is to lower hypertension by decreasing blood volume through the excretion of water in the urine (Hardman and Limbird, 1996). In general, diuretics decrease Na+ reabsorption in the kidney and other epithealial tissues thereby leading to increased urine output. There are approximately 6 different modes of action by which diuretics increase urine volume (Table 1, Hardman and Limbird, 1996). Most diuretic drugs typically act through a single route (Hardman and Limbird, 1996).
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The most efficacious diuretics known are compounds that produce diuresis by acting on sodium reabsorption in the ascending limb of the loop henle (Hardman and Limbird, 1996
). Compounds acting in this manner are referred to as "high ceiling" or "loop diuretics." There are at least 8 drugs classified as high-ceiling diuretics (Hardman and Limbird, 1996). They exhibit little chemical similarity and can not be classified on the basis of a particular functional group (Hardman and Limbird, 1996). Furosemide (LASIX) represents an example of a high-ceiling diuretic commonly used in the USA.
Although the concept of plant secondary compounds as diuretics is a novel one in the field of plant-herbivore interactions, the diuretic effects of plant secondary compounds on humans have been documented for millennia (Adsersen and Adsersen, 1997; Beaux et al., 1999; Johnson et al., 1999; Navarro et al., 1994). Myriad plants are employed worldwide as medicines to control hypertension by reducing blood volume through diuresis. The compounds in these plants are typically administered to the patient orally as an infusion of leaves in hot water. A few are administered through direct consumption of leaves. With the popularity of bioprospecting for natural compounds and the ongoing search for diuretic drugs that do not increase potassium excretion, many "traditional medicines" with proposed diuretic effects have recently been evaluated under experimental conditions. Here we review data from ethnopharmacological literature on plants typically used as diuretics. Although the literature is replete with information on plant compounds proposed to cause diuresis, we present only data for which there were controlled studies.
There were 4 studies that each evaluated a number of plant species available in a particular region such as India, for reputed hypertension or diuretic pharmacological activity (Table 2). Three of these studies evaluated diuretic activity using an in vitro system that tests for the ability of a plant extract to inhibit angiotension converting enzyme, ACE (Adsersen and Adsersen, 1997; Nyman et al., 1998; Somanadhan et al., 1999). A result of 50% inhibition is correlated with diuresis in whole animal systems. One study investigated diuretic effects by orally administering plant extracts and measuring urine volume (Ribeiro et al., 1988). Concentration of the extract was roughly equivalent to 5 g fresh leaf material/kg body mass of the animal. The results of all 4 studies were similar in that a large proportion of the plants produced diuretic effects (Table 2). Some plants produced diuretic effects comparable to the high-ceiling diuretic furosemide (Ribeiro et al., 1988). The areas from which the plants were collected were geographically distinct (India, South America and Reunion Island). Moreover, plants with diuretic effects were from a huge range of species and families. For example in these studies, plants with diuretic effects were found in the Asteraceae, Brassicaceae, Erythroxaceae, Flacourtaceae, Graminaceae, Leaceae, Rubeaceae, Zygophyllaceae and Zingiberaceae, as well as other families.
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In addition to these large-scale studies using primarily in vitro assays, we found several studies that investigated the diuretic potential of one or a few species of plant in whole animal systems, humans and rats. Nearly all these studies measured sodium excretion as well as urine output. Ten species of plants from 8 families increased urine output in whole animals (Table 3). Nine of these species simultaneously increased sodium excretion. The amounts of plant material in effective doses were quantities that could be ingested by a herbivore in the course of day or even a single meal. For example, in many cases, ingestion of
2 g of plant leaves by an animal the size of a rat caused significant diuresis. This amount corresponds to 10–15% of the total daily food intake of an animal the size of a rat. Many of these plant extracts were as effective as commercial diuretic drugs.
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Of all the species in Table 3, Othrosiphon aristatus has received the most attention. This plant from southeast Asia has been used as a tea in Indonesia to treat hypertension and diabetes (Matsubara et al., 1999
). Water extracts of the whole plant cause diuresis and naturesis in rats similar in extent to that produced by the high-ceiling diuretic, furosemide. Three compounds in this species have been found thus far to elicit a diuretic effect (Table 3).
Humans regularly ingest as part of their daily diet, a variety of plant compounds with diuretic properties. Coffee, black tea and chocolate contain compounds that are potent diuretics in humans. Simple water extracts of coffee and black tea contain quantities of caffeine great enough to cause water imbalance in humans. For example, if a human ingests 2 liter/day of fluid with 900 mls of this amount as coffee ( equal to (2) 16 oz cups), severe negative water balance will result (Neuhaser-Berthold et al., 1997).
Plant secondary compounds with documented diuretic effects occur across the major classes of plant compounds (Table 3). Diuretics can be found in terpenes, phenolics and alkaloids. No one functional group or class of compounds appears to be correlated with a diuretic effect. This result is consistent with the diversity of chemical structures present among commercial diuretic drugs (Hardman and Limbird, 1996). Thus, a wide variety of chemical compounds can produce diuretic effects.
The diuretic effects may be far more pronounced in herbivores that consume the entire leaf rather than a water extract of the plant. In the majority of the studies we reviewed, the material administered to the animal was the dried filtrate of a water extract that had been prepared from dried leaves. The drying process drives off many of the volatile secondary compounds and inactivates other types of compounds. Extraction with water selects for compounds that are hydrophilic. Both of these processes could reduce the concentration of diuretic compounds present in leaves.
In summary, the ethnopharmacological literature indicates that many species of plants produce diuretic effects. These effects are not restricted to a particular family or group of plants. In our review of the literature, we found examples of over 85 species from an extremely diverse set of families that exhibited diuretic effects. The secondary compounds present in these plants represent all major classes of compounds such as terpenes, phenolics and alkaloids (Table 3). This result is consistent with the diversity of chemical structures present among commercial diuretics (Hardman and Limbird, 1996). Thus, a wide variety of plant chemical compounds produce diuresis in mammals.
Studies on natural plant-herbivore systems
To investigate the effects of ingestion of secondary compounds on water intake, we conducted experiments with two species of mammalian herbivores, N. stephensi, Stephen's woodrat and N. albigula, whitethroat woodrat. N. stephensi and N. albigula occur sympatrically in Great Basin ecotones in Arizona. N. stephensi and N. albigula consume one-seeded juniper, Juniperus monosperma. One-seeded juniper contains a number of secondary compounds, particularly monoterpenes and phenolics, which are toxic to mammals. Juniperus communis, a close relative of one-seeded juniper, has been reported to have diuretic properties (de Medina et al., 1994).
We tested 3 specific hypotheses to determine whether juniper compounds affected various components of water balance of woodrats. Hypothesis 1: Ingestion of plant secondary compounds increases water intake. We fed woodrats control diets (no toxins) and treatment diets (with juniper toxins) and monitored voluntary water intake. We predicted that if plant secondary compounds influence water consumption, water intake should increase on toxic diets compared with controls.
Hypothesis 2: Plant secondary compounds act as diuretics. For a compound to be considered a diuretic, urine volume per ml of water consumed must increase. This relationship suggests that urine volume should be analyzed with total water intake as a co-variate. To determine whether the plant secondary compounds acted as a diuretic, we measured urine production and osmolarity of urine of woodrats on control and toxic diets. If secondary compounds act as diuretics, we predicted that urine volume would increase and urine osmolarity would decrease on the toxic diets.
Hypothesis 3: Extensive prior experience with specific toxins lessens the impact of toxin ingestion on water intake. We compared the performance of a specialist-generalist pair comprised of N. stephensi and N. albigula. N. stephensi is a juniper specialist, 65–95% of its year round diet consists of juniper. N. albigula, also consumes juniper, but it never comprises more than 35% of its diet. In the laboratory, N. stephensi can tolerate higher doses of juniper toxins than N. albigula (Dearing et al., 2000). Because the specialist regularly ingests higher quantities of juniper toxins than the generalist, we predicted that the specialist should be physiologically more adept at consuming juniper toxins than the generalist and that water intake of the specialist should be less impacted than the generalist.
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Collection of woodrats and plants
Neotoma stephensi and N. albigula were trapped on Woodhouse Mesa, AZ (35°30'N; 111°27'W). This site was the same as used by Dial (1988)
; we trapped at many of the exact locations as indicated by trap markers. Additional N. albigula were trapped in Castle Valley, UT (38°38'N; 109°18'W). Woodrats were captured using Tomahawk and Sherman live traps baited with peanut butter and oats. Pieces of cotton batting were placed in all traps to keep animals from freezing. Traps were opened late in the afternoon and checked immediately after sunrise. Vegetation in both trapping areas was similar, see Dearing et al. (Dearing et al., 1998) for a detailed description. We confirmed that N. stephensi was consuming more juniper than N. albigula by analyzing feces from trapped woodrats for juniper fragments. Juniper (J. monosperma) used in the experiment was collected from the Woodhouse Mesa study site. Foliage was collected randomly from several trees (ca. 10) and combined. Foliage was kept frozen (–20°C) until the day of the experiment and was thawed prior to presentation to woodrats. Woody stems were removed from juniper branches such that woodrats were given only terminal tips, the portion they consume in nature.
Juniper experiment
We compared the water intake of specialist, N. stephensi, and generalist, N. albigula woodrats on control and juniper diets to determine whether the addition of whole juniper to the diet altered water intake. We fed 8 N. stephensi and 10 N. albigula control, acclimation and juniper treatments. Each treatment was fed for 3 days and in the following sequence control, acclimation, and juniper diets. The control treatment consisted of chow whose N (1.25%) and fiber (23% ADF) levels were similar to that of juniper (1% N; 24% acid detergent fiber; Dearing et al., 2000). For a complete description of the diet formulations see Dearing et al., 2000. The control was followed by a 3 day acclimation period where control chow and fresh juniper were provided ad lib. Three days was given as the acclimation period as this is the amount of time required for induction of the detoxification system (Dearing et al., 2000). Following the acclimation period, woodrats were provided with juniper ad lib. and a reduced amount of control chow, equal to 15% of each animal's food intake on the control diet. It was necessary to provide this minimal amount of chow in the juniper treatment because some woodrats on juniper alone lose weight too quickly to remain in the experiment for 3 days. We provided 50 g of freshly thawed juniper daily during the acclimation and juniper treatments. This amount is approximately twice the juniper that woodrats require to maintain weight (Vaughn, 1982). Food was replaced daily and any leftovers were collected, dried at 45°C and weighed. We monitored food intake and body mass daily as part of another study (Dearing et al., 2000).
Total water consumption included water consumed from free water i.e., that in the water bottle plus that contained in the food. Free water consumption was estimated from the daily change in weight of the water bottles. Three control water bottles did not show significant change in water (100 µl/day) through evaporation or spillage, therefore, we did not adjust for loss through evaporation or spillage. We measured the amount of water consumed in the food by multiplying the dry weight amount of food consumed by the amount of water per unit dry weight of food. Dry weight of food consumed was estimated daily as the amount of dry weight offered minus the dry weight of leftovers. Dry weight estimates of food consumed are more accurate than wet weights as wet weights can vary significantly during the experiment due to the loss of water through evaporation. The amount of water in all foods (juniper and chow) was estimated daily by drying a known mass of food in an oven at 45°C and weighing after drying.
On day 3 of each treatment, woodrats were confined to a portion of their cage (16 x 19 x 20 cm) that allowed for the separate collection of urine and feces. We collected urine during the last 24 hr of each treatment. The collection vial for urine was embedded in a frozen freezer pack to keep the urine cold and decrease evaporation. Temperature of urine in the coolers ranged from 0–5°C. Urine was stored at –20°C until it was analyzed.
Urine volume was measured in graduated cylinders. The osmotic pressure of the urine was measured with a Wescor 510B Vapor Pressure Osmometer. The concentration of the samples exceeded the capacity of the osmometer and therefore were diluted with distilled water (1:1 or 1:2 urine:water depending on concentration of sample) prior to the measurement.
Water intake, urine volume and urine concentration was compared in separate repeated measures ANOVAs with woodrat species as the main effect and diet treatment as the repeated measure. Data from the acclimation treatment for juniper were not included in the statistical analysis as the acclimation diet was not an experimental treatment but rather a period to allow the animals to adapt to the consumption of juniper. Tukey's tests were performed to compare differences between woodrat species within a treatment. Differences between treatments within a species were compared with paired t-tests. To compare differences in urine volume between treatments while controlling for water intake, we performed analyses of covariance with water intake as the co-variate and species or treatment as the main effect.
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RESULTS |
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On the juniper treatment, food intake by the specialist was 1.6x that of the generalist (data in Dearing et al., 2000
). Neither the specialist nor the generalist consumed 100% of their maintenance food intake on the juniper treatment. On the juniper treatment, the specialist consumed 66% ± 7 of maintenance whereas the generalist consumed only 41% ± 1 of maintenance. Both species consumed all of the control food offered during the juniper treatment. The generalist lost significantly more weight than the specialist (4% vs. 8%) on the juniper treatment (Dearing et al., 2000). There was a significant effect of diet treatment on total water intake (Fig. 1a). The generalist increased its total water intake by 1.7x on juniper treatment diet compared to the control (paired t-test, t = 3.6, P = 0.004). There was a marginal increase in water intake of the specialist on the juniper treatment versus the control (paired t-test, t = 2.3, P = 0.06). In the repeated measures analysis (RMA), there was not a significant difference between species of woodrats nor was the interaction term significant (Table 4).
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Urine volume output increased on the treatment diet (Table 4, Fig. 1b). There was no significant effect of species nor was the interaction term significant. However, even though there was not a significant species effect, the specialist and generalist responded differently to the treatment with respect to urine output. The generalist produced 2x the volume of urine on the treatment diet versus the control (paired t-test, t = 3.4, P = 0.009). Urine output did not change significantly for the specialist on the control versus treatment diet (paired t-test, t = 1.0, P = 0.33).
There was a significant effect of diet treatment on osmotic pressure of the urine. Osmolarity of the urine declined significantly with the addition of juniper to the diet (Table 4, Fig. 1c). There was a significant interaction between species and treatment. The generalist produced a significantly more concentrated urine than the specialist on the control diet only. On the treatment diet, there was no difference between species in urine concentration; both species produced urine approximately 2x as dilute as urine produced during the control diet.
Specialists differed significantly from generalists in urine ouptut when water intake was statistically controlled using an ANCOVA (Table 5). Because of this difference, we performed separate ANCOVAs for each species to investigate urine volume on control and treatment diets. The specialist excreted significantly more urine per ml of water ingested on the treatment diet than that predicted by the control diet as indicated by significantly different slopes in an ANCOVA (Table 5, Fig. 2). The generalist did not exhibit this pattern. There was no significant effect of treatment or treatment by water intake for generalists on the control and treatment diets.
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DISCUSSION |
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A central goal of this experiment was to determine whether the addition of plant secondary compounds to the diet affects water use of herbivores. The results are consistent with this hypothesis. In the generalist herbivore, N. albigula, water intake and urine volume increased while urine osmolarity decreased when plant secondary compounds in the form of whole juniper were added to the diet. The specialist, N. stephensi, excreted significantly more urine per ml of water ingested on the diet containing secondary compounds compared to the control. Thus, the addition of juniper to the diets of two species of herbivore altered water use.
We attribute the change in water use parameters of woodrats on the control versus juniper treatment to the secondary compounds in the juniper treatment. The primary difference between the two treatments was the presence of secondary compounds. The control diet was free of secondary compounds whereas the juniper treatment being primarily juniper foliage contained the miscellany of compounds present in fresh juniper. The nitrogen and fiber contents of the control diet were similar to that of juniper foliage (Dearing et al., 2000). Therefore, it is unlikely that nutritional differences between the control and treatment diet were responsible for the differences in water balance.
We do not know which secondary compounds in juniper caused the diuretic effects. The secondary compounds of juniper are diverse. Juniper contains 2 different classes of secondary compounds, terpenes and phenolics (Adams et al., 1981; Dearing et al., 2000; Holchek et al., 1990). Examples of diuretic compounds are known from both of these classes (Consolini et al., 1999; Matsubara et al., 1999). The phenolics in juniper are a mixture of simple phenolics, hydrolyzable tannins and condensed tannins. The structures of these compounds and their quantities have not been evaluated. Thirty-five monoterpenes in juniper have been identified (Adams et al., 1981). The primary monoterpene is alpha-pinene, which comprises approximately 60% of the terpene content and 2% of the dry weight of the plant (Adams et al., 1981). Alpha-pinene is a documented central nervous system depressant but has not been evaluated for diuretic effects (Adams et al., 1981; Eriksson and Levin, 1990; Hedenstierna et al., 1983; Koppel et al., 1981). Given its abundance and pharmacological activity on other systems, alpha-pinene may significantly contribute to the diuretic effects of juniper.
Another objective of this experiment was to contrast the effects of plant secondary compounds on water use of specialist and generalist herbivores. The prediction was that the specialist, whose diet consists of juniper foliage, should be less impacted with respect to water use when consuming juniper than the generalist. In some respects, the data support this prediction. The specialist did not significantly increase water intake or urine output with the addition of juniper to the diet, whereas the output for both of these parameters nearly doubled in the generalist. Moreover, even though both species exhibited a decrease in urine concentration on the juniper diet, they had similar urine concentrations on this treatment. This result is surprising given that diuretics act in a dose dependent fashion and that the specialist was consuming 55% more juniper toxins compared to the generalist. Thus, even though its toxin load was greater the specialist performed the same as the generalist with respect to urine concentration.
However, the water use of the specialist was not unaltered by the ingestion of juniper. The results of the ANCOVA revealed that the specialist excreted significantly more urine per ml of water consumed on the treatment diet than that predicted from its performance on the control (Fig. 2). The generalist did not exhibit this pattern. These results could be interpreted two ways. First, the generalist may respond differently to the diuretic effects of juniper toxins than the specialist. Conversely, the dose of juniper toxins ingested by the generalist may have been below the threshold dose necessary to produce a diuretic effect. Minimum doses to produce diuresis have been documented for a number of secondary plant compounds. The specialist consumed 1.6x the dose of juniper toxins as the generalist, which may have been above the threshold necessary to generate elevated urine excretion per ml of water consumed. More studies set in a phylogenetic context are needed to adequately compare the water use efficiencies of specialist and generalist herbivores on toxic diets.
The data presented in this paper represent a preliminary investigation of possible diuretic effects of secondary compounds on herbivores. A few caveats should to be considered in evaluation of these data. First, we did not experimentally control water intake. Rather, we statistically controlled for differences in water intake when evaluating urine output through ANCOVA. In the case of the specialist, the interpretation of the data is straightforward because there were significant differences between urine output per ml of water consumed on the treatment versus the control diets. The specialist excreted 2.5x more urine per ml of water consumed on the treatment diet than on the control. This result supports the hypothesis that juniper compounds act as a diuretic. However, it is impossible to distinguish decisively between two alternatives in the absence of significant differences in slope of urine output and water intake, as exemplified by the result from the generalist. The increased urinary output of the generalist on the juniper treatment could have been a function of the increased water intake with no diuretic effect of juniper. It is possible that the addition of juniper to the diet caused the generalist to consume more water (e.g., a response to different tastes) which in turn resulted in an increase in urine output. Alternatively, juniper consumption could have increased urine excretion and the animal could have compensated by the increasing water intake to match urine output. The only means to discriminate between these alternatives is to experimentally control water availability.
We also did not control for differences in food intake. On the treatment diet, food intake and urine concentration decreased significantly for both the specialist and generalist. Because osmolarity of urine is affected by osmolyte load in the diet the decreased osmolarity of the urine may have resulted from the decreased in food intake. However, the relationship between food intake and urine concentration can not completely explain the urine concentration results on the treatment diet. There was no difference in urine concentration between the specialist and generalist on the treatment diet yet the specialist was consuming 30% more food.
Because the mechanism of action of most diuretic drugs is through the blocking of sodium reabsorption, such compounds typically result in large losses of sodium. Could the loss of sodium be more important to the herbivore than the loss of water? The relative importance of the loss of water and sodium should be commensurate with the abundance of these compounds in the environment. The herbivores we studied in this experiment are desert dwellers that acquire the majority of water from their diet (Dial, 1988). They have access to free standing water only during the rainy season. In the desert environment, sodium is abundant in the soil. Thus for desert dwellers, the loss of water may have a far greater impact that the loss of sodium.
In contrast, herbivores that inhabit alpine and mesic areas may be much more impacted by the sodium loss associated with diuretic plant compounds rather than loss of water. Soils in most mesic and alpine habitats are deplete of sodium to the extent that sodium availability is thought to be a primary force driving diet selection and animal distribution (Robbins, 1993). For example, diet selection by moose is governed by selection for plants with high concentrations of sodium. Thus, a diuretic plant compound could severely impact a herbivore in the desert through increased water loss but could also significantly affect animals where water is abundant through excess sodium loss.
In summary, we suggest that a general effect of many secondary compounds could be to negatively impact the water use efficiency of herbivores. The enthnopharmacological data suggest that diuretic compounds in plants are widespread and that these effects are manifest in quantities that would be obtained in the diets of herbivores. Moreover, animals in environments other than ones where water is limiting could be severely impacted by diuretic compounds through via disruption of sodium balance. Future investigations into the diuretic effects of plant secondary compounds should consider adding plant extracts or specific compounds to the control diet, holding water intake constant and monitoring sodium levels in the urine. It is possible that animals are able to compensate for water lost in the urine by decreasing water lost via other routes such as feces. Thus, studies on the diuretic effects of secondary compounds should take into account the entire water budget of the organism. Lastly, experiments that address whether minimum water requirements are elevated by secondary compounds would be useful in determining whether diuretic effects of secondary compounds limit food intake.
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ACKNOWLEDGMENTS |
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We thank Sandra Camissa, Robert Lemke, Sean Agger, Micheal Fryda, Michelle Arizmendi and Amanda Dobron for care of woodrats and assistance with experiments. This study was supported by NSF (BIR 9508492) to MDD. Rebecca Boyle provided helpful comments on the manuscript.
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FOOTNOTES |
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1 From the Symposium An Integrative Approach to the Study of Terrestrial Plant-Animal Interactions presented at the Annual Meeting of the Society for Comparative and Integrative Biology, 5–8 January 2000, at Atlanta, Georgia.
2 E-mail: dearing{at}biology.utah.edu
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References |
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