Friend or foe? Disparate plant–animal interactions of two congeneric rodents (original) (raw)

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.

Predators and dispersers: Context-dependent outcomes of the interactions between rodents and a megafaunal fruit plant

Scientific Reports, 2020

Many plant species bear fruits that suggest adaptation to seed dispersal by extinct megafauna. Present-day seed dispersal of these megafaunal plants is carried out by rodents, which can act as predators or dispersers; whether this interaction is primarily positive or negative can depend on the context. Here, we parameterized a stochastic model using data from the field and experimental arenas to estimate the effect of rodents on the recruitment of Myrcianthes coquimbensis -an Atacama Desert shrub with megafaunal fruits- and examine whether environmental conditions can alter the sign and strength of these rodent-plant interactions. We show that the outcome of these interactions is context-dependent: in wet conditions seed removal by rodents negatively impacts the recruitment probability of M. coquimbensis; in contrast, in dry conditions, the interaction with rodents increases recruitment success. In all cases, the strength of the effect of rodents on the recruitment success was deter...

Taste and physiological responses to glucosinolates: seed predator versus seed disperser

PloS one, 2014

In contrast to most other plant tissues, fleshy fruits are meant to be eaten in order to facilitate seed dispersal. Although fleshy fruits attract consumers, they may also contain toxic secondary metabolites. However, studies that link the effect of fruit toxins with seed dispersal and predation are scarce. Glucosinolates (GLSs) are a family of bitter-tasting compounds. The fleshy fruit pulp of Ochradenus baccatus was previously found to harbor high concentrations of GLSs, whereas the myrosinase enzyme, which breaks down GLSs to produce foul tasting chemicals, was found only in the seeds. Here we show the differential behavioral and physiological responses of three rodent species to high dose (80%) Ochradenus' fruits diets. Acomys russatus, a predator of Ochradenus' seeds, was the least sensitive to the taste of the fruit and the only rodent to exhibit taste-related physiological adaptations to deal with the fruits' toxins. In contrast, Acomys cahirinus, an Ochradenus se...

Factors affecting selection of native seeds in two species of Australian desert rodents

Journal of Arid Environments, 1997

The preferences for different species of native seeds by two species of Australian desert rodents, the sandy inland mouse, Pseudomys hermannsburgensis, and the spinifex hopping-mouse, Notomys alexis, were investigated. In two sets of cafeteria trials providing low and high numbers of different seed species, both rodent species showed discrimination, preferentially consuming certain seed species, while avoiding others. In one of the two trials, P. hermannsburgensis selected seeds with the highest free water content, while N. alexis showed no clear mechanism of seed choice in either trial. It is suggested that although both species of rodents are omnivorous, P. hermannsburgensis relies more on seeds than does N. alexis, and is thus the more efficient seed harvester.

Frequency‐dependent seed predation by rodents on Sonoran Desert winter annual plants

Ecology, 2017

Numerous mechanisms may allow species to coexist. We tested for frequency‐dependent predation, a mechanism predicted by theory and established as a foraging behavior for many types of animals. Our field test included multiple prey species exposed in situ to multiple predator species and individuals to determine whether the prey species experienced predation patterns that were frequency dependent. The prey were seeds of three species of Sonoran Desert winter annual plants while the predator species were a guild of nocturnal seed foraging heteromyid and murid rodents that co‐occur naturally in the same community as the desert annuals at Tumamoc Hill near Tucson. Seeds of one species were much preferred over the other two. Nonetheless, we found the net effect of rodent foraging to be positively frequency dependent (the preference for each species is higher when it is common than when it is uncommon) as has been previously hypothesized. This frequency‐dependent predation should function...

Functional diversity in fruit-frugivore interactions: a field experiment with Mediterranean mammals

Using field seed sowings, we assessed how four mammal species (Meles meles, Vulpes vulpes, Sus scrofa, and Oryctolagus cuniculus) influenced seed germination in three fleshy-fruited Mediterranean shrubs (Corema album, Pyrus bourgaeana, and Rubus ulmifolius). We predicted that gut passage and removal away from mother plants would enhance the quantity, speed, and asynchrony of seed germination. Results showed that percent germination was altered by gut passage, but that the magnitude and even the direction of such effects varied according to plant and disperser species. Likewise, dispersal away from mother plants affected the percentage and germination speed in some species but not others. Gut passage increased asynchrony of germination in Rubus and Pyrus, and removal from the mother plant increased asynchrony in Rubus, which likely enhances plant fitness in unpredictable environments. Gut passage generally had a stronger effect on germination than removal away from mother plants, but for some species both factors were similarly influential. Therefore, the combined effects of both seed dispersal services varied individually among fruit and frugivore species, leading to unusually high functional diversity in this seed dispersal mutualism.

Fruits of alien shrubs and deer mice: a test of the persistent fruit defense hypothesis.

Journal of the Pennsylvania Academy of Science, 1999

Because of extended exposure to potential seed predators and pathogens, persistent fruits of woody plants have been hypothesized to be chemically defended against biotic depredations. The "persistent fruit defense hypothesis" was tested using the deer mouse, Peromyscus maniculatus, in laboratory feeding trials with fruits of four alien shrubs naturalized in eastern North America: Ligustrum vulgare (common or European privet), Lonicera japonica (Japanese honeysuckle), Lonicera maackii (Amur honeysuckle and Rosa multiflora (multiflora rose). Anecdotal observations suggested potential chemical defense against small mammal predation for fruits of Ligustrum vulgare and Lonicera maackii due to toxicity and extreme pericarp bitterness, respectively. In contrast, fruits of Lonicera japonica and Rosa multiflora are known to be readily eaten by smalI mammals and so apparently lack chemical defense. It was hypothesized that levels of deer mouse consumption of fruits and the seeds within would be lowest in Ligustrum vulgare and Lonicera maackii due to defensive unpalatability and greatest in non-defended Lonicera japonica and Rosa multiflora. Deer mice readily extracted and consumed seeds from persistent fruits of Ligustrum vulgare, Lonicera japonica, Lonicera maackii and Rosa multiflora at comparable levels during most feeding trials and generally showed no distinct preference for, or aversion to, fruits of any species. Thus, the persistent fruit defense hypothesis was not supported for fruits of these alien shrubs under laboratory conditions.

Yucca brevifoliafruit production, predispersal seed predation, and fruit removal by rodents during two years of contrasting reproduction

American Journal of Botany, 2016

The distribution of Yucca brevifolia , a keystone species of the Mojave Desert, may contract with climate change, yet reproduction and dispersal are poorly understood. We tracked reproduction, seed predation, and fruit dispersal for two years and discuss whether Y. brevifolia is a masting species. METHODS: Fruit maturation, seed predation (larval yucca moths), and fruit dispersal (rodents) were monitored on a random sample of panicles during 2013 and 2014, which were years of high and low reproduction, respectively. Fates of fruits placed on the ground and in canopies were also tracked. Rodents were live-trapped to assess abundance and species composition. KEY RESULTS: In 2013, 66% of infl orescences produced fruit of which 53% escaped larval predation; 19.5% of seeds were destroyed in infested fruits. Total seed production was estimated to be >100 times greater in 2013 than 2014. One-third of the fruit crop fell to the ground and was removed by rodents over the course of 120 d. After ground fruits became scarce, rodents exploited canopy fruits. Rodent numbers were low in 2013, so fruits remained in canopies for 370 d. In 2014, fruit production was approximately 20% lower. Larvae infested the majority of fruits, and almost twice the number of seeds were damaged. Fruits were exploited by rodents within 65 d. CONCLUSIONS: High fertilization, prolifi c seed production, and low predispersal predation in 2013 suggests that pollinator attraction and satiation of seed predators infl uence masting in Y. brevifolia. Abundant, prolonged fruit availability to seed-dispersing rodents likely extends recruitment opportunities during mast years.

Foraging by fearful frugivores: combined effect of fruit ripening and predation risk

Functional Ecology, 2006

Plant defensive compounds and predation risk are main determinants of herbivore foraging, though empirical studies have seldom measured the combined effects of these two factors. By considering the interaction between the herb Helleborus foetidus and its main fruit and seed predator, the Wood Mouse Apodemus sylvaticus , we evaluated whether the defensive role against seed predators of compounds present in H. foetidus unripe fruits holds across a micro-landscape that differs in foraging costs (i.e. predation risk). 2. First, we used standardized food patches that simulated fruiting H. foetidus plants to ascertain fruit preferences of captive mice. Then, by means of field experiments, we assessed the combined effects of fruit ripening and predation risk on foraging by freeranging mice. 3. Captive mice avoided plants with unripe fruit and avoided consuming unripe fruits within a particular plant. Free-ranging mice also avoided unripe fruits in safe microhabitats (rocky substrate), but not in risky microhabitats (bare ground) where few fruits were consumed. This unexpected result may be driven by predation risk experienced by mice foraging on H. foetidus fruits, and/or plant defensive compounds acting in a dosedependent manner. 4. Frugivorous mice responded to both chemical defences present in unripe H. foetidus fruits as well as to predation cost though such response was sequential. Plant defence compounds appeared to play a part in mouse foraging only after mice selected low predation risk microhabitats. 5. Our study indicates that both digestive and ecological factors influence foraging decisions, which in turn affects pressures exerted by herbivores on plant populations.