Fleshy-fruited Plants and Frugivores in Desert Ecosystems

Proposal Abstract

1. The impact of environmental conditions on the morphology, nutritional value and secondary metabolites in Ochradenus baccatus fruits.

   Many plants disperse their seeds by fleshy fruit that is consumed by animals. The chemical, morphological and phenological traits of these fruits may control plant fitness, because they determine how many fruits will be consumed, by whom, how far the seeds will be transferred, where the seeds will be deposited and in what shape. Likewise, these traits simultaneously affect seed predators and pathogens and hence determine the level of seed damage. These fruit characteristics are related to species phylogeny but also to some extent to the characteristics of the potential seed dispersers and predators within the distribution region of the plant. Although intraspecific variation is the raw material of natural selection, little is known about the intraspecific variation of fruit traits and how it is affected by the abiotic environment.

   In this study we have examined the effect of environmental conditions on different fruit traits (morphology, nutritional value and secondary metabolites) in Ochradenus baccatus, a desert shrub that produces fleshy fruits, a rare phenomenon in the arid environment. First, we assessed the intraspecific variation of several fruit characters by comparing four O. baccatus populations along a north-south geographical gradient in its natural habitat in Israel. Then, we related this variation to the variation of water and other soil attributes such as mineral content. In order to examine the effect of specific abiotic variables on fruit traits, we performed two manipulation experiments: an irrigation experiment in the desert environment, and fertilization experiment in a controlled greenhouse.

   We found that although O. baccatus is a desert plant exposed to limited and unpredictable water conditions, its fruits have similar chemical content and morphological attributes to fleshy fruits from other habitats. O. baccatus pulp has high water content, which tends to be an attractive feature to dispersers, especially in arid habitats where it grows. However, we also found high intraspecific variation in several fruit morphological and chemical traits. This spatial and temporal variation was detected among populations, within populations and between seasons. The results indicate that a large proportion of this variation is explained by differences in the environmental conditions in the microhabitat of each plant. As water conditions improve, along with some enhancement (but to a lesser extent) of nitrogen and other soil minerals, O. baccatus fruits are larger but have lower dry weight, protein, fat and secondary metabolites. This trend was significant when all sampled plants (n=40) were examined, but not significant when each population was examined separately. Because the arid environment is water-limited, water is the main factor in the environment axis, affecting fruit morphology and chemistry. Moreover, plant water potential by itself was positively correlated with fruit size and water content, and negatively correlated with several chemical variables. These relationships were found among as well as within populations.

   This is the first time that glucosinolates have been found in fleshy fruits. Their concentration in the pulp is higher than in the seeds. The two main glucosinolates [2-(a-l-Rhamno pyranosyloxy) Benzylglucosinolate; and 0-(a-Arabinosyloxy) enzylglucosinolate] have chemical structure which is typical to the Resedaceae family, one of those is new to science. The considerable intraspecific variation of glucosinolate content in the pulp was also partially explained by the variation in the environmental conditions. The greenhouse experiment indicated that glucosinolate concentration in fruit pulp was mainly affected by the sulfur content in soil. To a lesser extent, the pulp glucosinolate concentration was negatively related to water availability. Glucosinolate level varied among sites and between seasons, and was depended upon extrinsic rather than intrinsic factors of the plant. These findings support the theory that the level of secondary metabolites in fruit pulps is a non-adaptive trait. Nevertheless, many questions about the role of glucosinolates in plants and about the factors that govern their production remained unsolved.

   In sum, we detected considerable intraspesific variation in fruit attributes. We also showed that this variation is partially explained by abiotic environmental conditions. Nevertheless, part of this variation is probably due to factors that were not examined here, such as differential selective pressures by different fruit consumers (dispersers and predators) or genetic differences among individuals and among populations.

2. Seed dispersal of a flashy fruited desert shrub by birds: The influence of disperser behavior, the transition through the digestive system and the spatial structure of the site on seed dispersion patterns.

   Fleshy fruited plants are found in nearly all ecosystems. In desert ecosystems, fleshy fruits are produced only by very few species, and thus relatively little attention has been given to the study of seed dispersal by frugivores in this type of ecosystem.

   Since resources in the desert environment are limited, fleshy fruits may be a significant source of nutrition and water for a variety of consumers. In this sense, the dispersal process is very important in both determining the spatial distribution of resources and in influencing the consumer's population dynamics. In addition, the relatively open and simple spatial structure of vegetation in desert ecosystems enables the simple quantification (relative to systems with more complex structure) of different parameters of the dispersal system, and thus a better understanding of dispersal mechanisms.

   This study dealt with the plant- dispersal agent interaction between the shrub Ochradenus baccatusand one of its main dispersal agents, the yellow- vented bulbul (Pycnonotus xanthopygos) in Wadi Rahaf, located in the Judean desert, Israel. Field data were collected during the winter season of 2002-2003. Controlled laboratory experiments were also performed in order to quantify dispersal-related parameters.

   All Ochradenus individuals in the site were tagged and mapped. The size, sex and fruit abundance and coordinates were recorded for all individuals. Bird movements in the site were recorded. The time allocation of birds among microhabitats in the site was found to be nonrandom. The birds spent significantly longer time periods on Ochradenus baccatus plants and Acacia trees than in open space. The birds selected large plants, which had many fruit and were close to refuges. However, contrary to predictions, within the preferred plant group, it appeared that the time spent in the shrub and the visitation frequency to the shrub were unrelated to plant size, fruit abundance or distance from a refuge.

   Another factor influencing the seed dispersion pattern was gut retention time. In the lab experiments conducted, fruits were fed to birds and the time until seed excretion was measured. The majority of seeds were excreted within 30 minutes of consumption, although a few seeds remained in the birds' digestive system up to 145 minutes. The shape of the seed gut retention time distribution was similar when the digestion system is empty or full; yet, retention times were longer when the digestion system is empty.

   The influence of passage in the birds' digestion system on O. baccatus seeds was investigated by germination experiments in a controlled environment. Whole fruits and seeds manually separated from the fruit pulp were used as control treatments. The results indicate that seed passage through the digestion system improved the percentage of successful germination by 29% ± 3.6%, and shortened the time until germination by 153 ± 3.5 hours. The positive influence of the passage through the digestion system on seed germination appeared to be a result of fruit pulp removal rather than seed coat erosion. Successive experiments tested germination percentage and time to germination in seeds of different retention times. These experiments revealed no influence of retention time on germination.

   Quantitative data on the parameters relating to the disperser movement and its influence on seed germination permitted the construction of a mechanistic simulation model of seed dispersion. This model predicts a patchy distribution of seeds, in which the majority of dispersed seeds are found under Acacia trees and Ochradenus baccatusshrubs. Low seed densities are found in the open area. Previous studies in desert ecosystems have found that both germination and recruitment conditions are favorable in vegetation patches compared to open areas. The predicted seed dispersion patterns may fit the directed dispersal hypothesis, which attributes great importance to the identity of the patch at which seeds arrive. At the scale of tenths of a meter and in the desert ecosystem studied here, the identity of seed deposition site is more important then its distance from the mother plant.

3. Scale-dependent frugivory in a desert ecosystem.

   Seed dispersal is a process with important ecological implications at the population and community levels. Fleshy-fruited plants are usually dispersed by an array of frugivores, differing in the effectiveness of dispersal service they provide to the plant.

   A disperser's effectiveness is its contribution to the plant's future reproduction, and therefore to its fitness, in comparison with all other dispersers. Comparison of dispersal effectiveness includes two main components: the quantity of dispersed seeds, and the quality of dispersal provided to each seed. This quality is a function of the effect of passage through the disperser's digestive track on seed germination and of the dispersal distances and deposition site suitability for establishment.

   This project focused on dispersal of the shrub Ochradenus baccatus, which is common throughout the deserts of Israel. Although fleshy-fruited plants are relatively uncommon in desert ecosystems, they are disproportionately important as a source of water, sugars and nutrients for a variety of frugivores, including mammals, reptiles and birds. Among the main dispersers of O. baccatus are two resident bird species: Tristram's grackle (Onychognathus tristramii) and yellow vented bulbul (Pycnonotus xanthopygos). The goal of this study was to compare the dispersal effectiveness between those species, and to examine whether this effectiveness and its components were scale dependent. The hypothesis was that the two species differ in their dispersal effectiveness, mainly as an outcome of a body size difference. The grackle is bigger than the bulbul; it was therefore expected to have longer gut retention times and bigger home ranges, resulting in a higher dispersal effectiveness at greater spatial scales.

   Video photography at the study site in the lower part of Wadi Rahaf showed minor differences between the two species in the quantity of seeds that they dispersed (10.7±4.0 and 9.4±1.9 fruits/day*shrub, by grackles and bulbuls, respectively, mean ± SE). In two sets of laboratory experiments, both species were shown to have a similar positive effect on the probability of germination, as compared to control seeds within intact fruits, mainly due to the effect pulp removal (+31%±3.3% vs. +29%±3.6%), regardless the major difference in their gut retention times (mean: 2.01±1.3h vs. 0.52±0.21h; max: 6.5h vs. 2.2h, respectively). As expected from the differences in their body size, the two species differed markedly in the spatial scale of their movements, measured at small scales (10-200m) by a laser range finder and at large scales (1-10km) by radio telemetry. Grackles performed longer daily flights, and used a larger home range than bulbuls (9.3±2.4 km/day and 1142± 283 ha vs. 2.3± 0.4km/day and 66±21 ha).

   Predicting dispersal distances with a simple mechanistic model suggests that the two avian dispersers switch roles as a function of spatial scale. The majority of the seeds dispersed at shorter distances at both scales were transported by the bulbuls; they are probably responsible for most of the seed dispersal within the wadi. In contrast, grackles are exclusively responsible for dispersal at larger spatial scales larger, up to few km, connecting populations in adjacent wadies. These results reveal a fundamental limitation of the dispersal effectiveness concept, and stress the need for elaborating it by incorporating the effect of dispersal by vectors functioning in various scales.

4. Review of fleshy-fruited plants and frugivores in desert ecosystems

   A traditional emphasis on the rarity of fleshy fruit in deserts has contributed to a paucity of information about the importance of frugivory in desert systems. We compared the Ochrodenus baccatus frugivory system to that of the New World interaction between chilies (Capsicum annuum ) and their dispersers, and more generally synthesized information on desert frugivory and its ecological significance. We found ample evidence that frugivory plays an important role in the ecology of deserts, generating a particularly high degree of spatial structure in fleshy-fruited species. This spatial structure in fruiting species may itself be a general emergent property of xeric systems that exerts a great deal of influence on frugivore behavior, creating positive feedbacks and a yet higher degree of resource aggregation. Thus, fleshy-fruited species found in arid environments may be disproportionately important ecologically, since they provide precious resources for a wide diversity of animals, and the increased activity of animals in the vicinity of fleshy-fruited desert plants can generate islands of productivity, structuring both plant and animal communities. The patterns of aggregation and the potential effects on animals are not unique to xeric systems, but the relative simplicity of desert ecosystems makes these patterns easier to study, thus providing unique opportunities to gain insight into major unanswered questions in the study of seed dispersal ecology. A review of these phenomena suggested nine avenues in which future research would be particularly valuable:

   • Is there such thing as a "desert fruit"?
   • Do desert systems favour directed dispersal?
   • Do fruiting "hotspots" determine seed fate?
   • Are deserts ideal systems for studying disperser movement and contagion?
   • Are super-abundant fleshy-fruited species in deserts keystone species?
   • Are desert systems ideal for estimating total dispersal kernels?
   • Is the temporal dimension of seed dispersal more important in desert systems?
   • Are fleshy fruit more persistent in deserts than other habitats?
   • Does the patchy nature of the desert vegetation and the contagious dispersal by frugivores result in a more readily invaded and perturbed system, or is it more resilient?

Outcome

Articles in Journals

Holden, C. 2006. "Inching toward movement ecology." Science: 313:779+782.

Nathan, R. 2006. "Long-distance dispersal of plants"Science. 313:786-788.

Buckley, Y. M., S. Anderson, C. P. Cattarall, R. T. Corlett, T. Engel, C. R. Gosper, R. Nathan, D. M. Richardson, M. Setter, O. Spiegel, G. Vivan-Smith, F. A. Voigt, J. E. S. Weir, and D. A. Westcott. 2006. “Management of plant invasions mediated by frugivore interactions.” Journal of Applied Ecology (In Press).

Spiegel, O., and R. Nathan. “Dispersal effectiveness depends on spatial scale: a desert plant dispersed by two avian frugivores.” Journal of Ecology . (In Review)

Bohrer, G., R. Nathan, and S. Volis. 2005. “Effects of long-distance dispersal for metapopulation survival and genetic structure at ecological time and spatial scales.” Journal of Ecology 93:1029-1040.

Nathan, R. 2005. “Long-distance dispersal research: building a network of yellow brick roads.” Diversity and Distributions 11:125-130.

Nathan, R., and G. G. Katul. 2005. “Foliage shedding in deciduous forests lifts up long-distance seed dispersal by wind.” Proceedings of the National Academy of Sciences of the United States of America 102:8251-8256.

Trakhtenbrot, A., R. Nathan, G. Perry, and D. M. Richardson. 2005. “The importance of long-distance dispersal in biodiversity conservation.” Diversity and Distributions 11:173-181.

Nathan, R., and R. Casagrandi. 2004. “A simple mechanistic model of seed dispersal, predation and plant establishment: Janzen-Connell and beyond.” Journal of Ecology 92:733-746.

Book Chapters

Bronstein, J.L., I. Izhaki, R. Nathan, J. Tewksbury, O. Speigel, A. Lotan, and O. Altstein. 2006. Fleshy-fruited plants and frugivores in desert ecosystems. In: Seed Dispersal: Theory and its Application in a Changing World, eds. A. Dennis, R. Green, E. Schupp, and D. Westcott. CAB International Publishing, Wallingford, Oxfordshire, UK (In Press).

Nathan, R. Total dispersal kernels and the evaluation of diversity and similarity in complex dispersal systems, In Seed Dispersal: Theory and its Application in a Changing World, eds. A. J. Dennis, R. J. Green, E. W. Schupp, and D. A. Westcott. CAB International, Wallingford, UK. (In Review)

M.S. Theses

Altstein, O. 2004. Seed dispersal of a flashy fruited desert shrub by birds: the influence of the disperser behavior, the transition through the digestive system and the spatial structure of the site on the seed dispersion pattern. M.Sc. Thesis. Dept. of Life Sciences, Ben-Gurion University of the Negev, Israel.

Lotan A. 2005. The impact of environmental conditions on the morphology, nutritional value and secondary metabolites in Ochradenus baccatus fruits. M.Sc. Thesis, University of Haifa, Israel.

Spiegel, O. 2006. Scale-dependent frugivory in a desert ecosystem. Department of Evolution, Systematics and Ecology, M.Sc. Thesis. The Hebrew University of Jerusalem, Israel.

Presentations

Nathan, R. 2006. Total dispersal kernels and the evaluation of diversity and similarity in complex dispersal systems. Modeling Approaches in Biodiversity Research(International Workshop); 19-23 March 2006, Sede Boqer, Israel. (oral presentation)

Spiegel, O. and R. Nathan. 2006. Dispersal effectiveness as a function of spatial scale in a fleshy fruited desert plant (Ochradenus baccatus) dispersed by two avian frugivores (Onychognathus tristramii, Pycnonotus xanthopygos). The 42nd Annual Meeting of the Zoological Society of Israel. The Hebrew University of Jerusalem, Rehovot, Israel. (oral presentation)

Lotan, A. and I. Izhaki. 2005. The impact of environmental conditions on fruit nutritional value of a desert plant (Ochradenus baccatus). Frugivores and Seed Dispersal, 4 th International Symposium/Workshop. Brisbane, Australia. (oral presentation)

Spiegel, O. and R. Nathan. 2005. Dispersal effectiveness as a function of spatial scale in a fleshy-fruited desert plant dispersed by two avian frugivores. CARESS 2005: The 5th Annual Conference on Active Research by Environmental Science Students. Weizmann Institute, Rehovot, Israel, 30 May 2005. (poster presentation)

Spiegel, O. and R Nathan. 2005. Dispersal effectiveness as a function of spatial scale in a fleshy fruited desert plant dispersed by two avian frugivores. Frugivores and Seed Dispersal, 4th International Symposium/Workshop. Brisbane, Australia. (poster and oral presentation)

Spiegel, O., S. Ben-Yosef, and R. Nathan. 2004. Digestion by Tristram's grackles (Onychognathus tristramii) enhance germination of Ochradenus baccatus seeds. The 41st Annual Meeting of the Zoological Society of Israel. Haifa University, Israel. 12 December 2004. (oral presentation)

Funding