Effects of Fruit Toxins on Intestinal and Microbial ß-Glucosidase Activities of Seed-Predating and Seed-Dispersing Rodents (Acomys spp.).

Plant secondary compounds (PSCs) have profound influence on the ecological interaction between plants and their consumers. Glycosides, a class of PSC, are inert in their intact form and become toxic on activation by either plant ß-glucosidase enzymes or endogenous ß-glucosidases produced by the intestine of the plant-predator or its microbiota. Many insect herbivores decrease activities of endogenous ß-glucosidases to limit toxin exposure. However, such an adaptation has never been investigated in nonmodel mammals. We studied three species of spiny mice (Acomys spp.) that vary in their feeding behavior of the glycoside-rich fruit of Ochradenus baccatus. Two species, the common (Acomys cahirinus) and Crete (Acomys minous) spiny mice, behaviorally avoid activating glycosides, while the golden spiny mouse (Acomys russatus) regularly consumes activated glycosides. We fed each species a nontoxic diet of inert glycosides or a toxic diet of activated fruit toxins and investigated the responses of intestinal and microbial ß-glucosidase activities. We found that individuals feeding on activated toxins had lower intestinal ß-glucosidase activity and that the species that behaviorally avoid activating glycosides also had lower intestinal ß-glucosidase activity regardless of treatment. The microbiota represented a larger source of toxin liberation, and the toxin-adapted species (golden spiny mouse) exhibited almost a fivefold increase in microbial ß-glucosidase when fed activated toxins, while other species showed slight decreases. These results are contrary to those in insects, where glycoside-adapted species have lower ß-glucosidase activity. The glycoside-adapted golden spiny mouse may have evolved tolerance mechanisms such as enhanced detoxification rather than avoidance mechanisms.

Warmer ambient temperatures depress liver function in a mammalian herbivore.

Diet selection in mammalian herbivores is thought to be mainly influenced by intrinsic factors such as nutrients and plant secondary compounds, yet extrinsic factors like ambient temperature may also play a role. In particular, warmer ambient temperatures could enhance the toxicity of plant defence compounds through decreased liver metabolism of herbivores. Temperature-dependent toxicity has been documented in pharmacology and agriculture science but not in wild mammalian herbivores. Here, we investigated how ambient temperature affects liver metabolism in the desert woodrat, Neotoma lepida. Woodrats (n = 21) were acclimated for 30 days to two ambient temperatures (cool = 21°C, warm = 29°C). In a second experiment, the temperature exposure was reduced to 3.5 h. After temperature treatments, animals were given a hypnotic agent and clearance time of the agent was estimated from the duration of the hypnotic state. The average clearance time of the agent in the long acclimation experiment was 45% longer for animals acclimated to 29°C compared with 21°C. Similarly, after the short exposure experiment, woodrats at 29°C had clearance times 26% longer compared with 21°C. Our results are consistent with the hypothesis that liver function is reduced at warmer environmental temperatures and may provide a physiological mechanism through which climate change affects herbivorous mammals.

Physiological and behavioural effects of fruit toxins on seed-predating versus seed-dispersing congeneric rodents.

Fleshy, ripe fruits attract seed dispersers but also seed predators. Although many fruit consumers (legitimate seed dispersers as well as seed predators) are clearly exposed to plant secondary compounds (PSCs), their impact on the consumers' physiology and foraging behaviour has been largely overlooked. Here, we document the divergent behavioural and physiological responses to fruit consumption of three congeneric rodent species in the Middle East, representing both seed dispersers and seed predators. The fruit pulp of the desert plant Ochradenus baccatus contains high concentrations of glucosinolates (GLSs). These GLSs are hydrolyzed into active toxic compounds upon contact with the myrosinase enzyme released from seeds crushed during fruit consumption. Acomys russatus and A. cahirinus share a desert habitat. Acomys russatus acts as an O. baccatus seed predator, and A. cahirinus circumvents the activation of the GLSs by orally expelling vital seeds. We found that between the three species examined, A. russatus was physiologically most tolerant to whole fruit consumption and even A. minous, which is evolutionarily naïve to O. baccatus, exhibits greater tolerance to whole fruit consumption than A. cahirinus. However, like A. cahirinus, A. minous may also behaviourally avoid the activation of the GLSs by making a hole in the pulp and consuming only the seeds. Our findings demonstrate that seed predators have a higher physiological tolerance than seed dispersers when consuming fruits containing toxic PSCs. The findings also demonstrate the extreme ecological/evolutionary lability of this plant-animal symbiosis to shift from predation to mutualism and vice versa.