Impact on fruit removal and seed predation of a secondary metabolite, emodin, in Rhamnus alaternus fruit pulp

Abstract

There are two contradictory approaches to explaining the presence of secondary metabolites in ripe fruits. One holds that they evolved toward enhancing dispersal success (adaptive approach); the other claims that they evolved primarily to deter herbivores from eating leaves and seeds and that their presence in ripe fruits is a byproduct of that function (non‐adaptive approach). We tested the validity of three hypotheses of the adaptive approach that explain the presence of secondary metabolites in ripe fruits. We explored the current function of a secondary metabolite, emodin, in Mediterranean buckthorn (Rhamnus alaternus, Rhamnaceae) fruits by relating intraspecific variation and seasonal patterns of concentration to fruit removal and seed damage and by conducting feeding trials with captive birds presented artificial fruits that varied in emodin concentration. The concentration of emodin in the pulp of 10–13 Rhamnus plants from the same population was determined by HPLC every month during two fruiting seasons. Fruit removal by birds and seed predation by invertebrates and microbes were determined for the same plants. Emodin concentration rose during the first stages of ripening, reaching a peak before the fruits were ripe, and then decreased to a minimum when the fruits were ripe. No significant correlation between emodin concentration and ripe fruit removal rate among trees was observed in the first year, whereas in the second year the correlation was positive and significant. Thus, the impact of emodin on fruit selection varied between years, suggesting that emodin concentration does not solely govern fruit selection. A significant negative correlation was found in the first year between emodin concentration and seed predation during the first fruiting month. The yellow‐vented bulbul (Pycnonotus xanthopygos), a seed dispersing bird, distinguished between artificial foods that differed in emodin concentration (control, 0.001% and 0.002%), always preferring the lower concentration. In contrast, house sparrows, (Passer domesticus), a seed predator, did not detect such differences in emodin concentration but did distinguish between control foods and food with 0.005% and 0.001% emodin. We suggest that emodin has an ecological role, preventing seed predation by invertebrates and microbes without decreasing fruit removal by avian dispersers.

Unripe red fruits may be aposematic

“…This concentration decreases to 2.5 ± 0.9 ppm in ripe black fruits. 75 Similar fruit color change also occurs in R. lycioides L., in R. punctata Boiss., and probably also in other Rhamnus species.…”

“…It has been demonstrated for the Old World's Rhamnus alaternus and R. lycioides (R. palaestinus) and for the New World's R. cathartica that bird species do not consume unripe red fruits. 75,86,87 Emodin is the predominant secondary metabolite in Rhamnus fruits and recently it has been demonstrated that birds and small mammals are unable to detoxify high concentrations of emodin efficiently. 88 There are good indications for considerable predispersal seed predation in R. alaternus, 89 which may trigger the evolution of defense.…”

Short communication. Insecticidal activity of different extracts of Rhamnus dispermus (Rhamnaceae) against peach trunk aphid, Pterochloroides persicae (Homoptera: Lachnidae)

“…Abu-Darwish (2000) isolated and identified 11 compounds from barks of R. This study aimed to test the insecticidal activity of R. dispermus against the PTA, since it has been shown that Rhamnus spp. may contain compounds that act as botanical pesticides, such as emodin (Trial and Dimond, 1979, Singh et al, 1992, Tsahar, 2001Izhaki, 2002) Bark of R. dispermus was collected from AshShoubak, Jordan. Its botanical identification was confirmed by Dr. Talal Abu Rjae, at the University of Jordan, who keeps voucher specimens in his laboratory.…”

Effects of nicotine on the digestive performance of nectar-feeding birds reflect their relative tolerance to this alkaloid

“…Murray et al (1994) found that fruits of the family Solanaceae contained laxative chemicals that reduced seed retention time, while in contrast glycoalkaloids had a significant constipative effect on cedar waxwings Bombycilla cedrorum, increasing seed retention time (Wahaj et al 1998). Emodin, an anthraquinine present in fruits of the family Rhamnaceae, was found to increase gut retention time and food assimilation of yellow-vented bulbuls Pycnonotus xanthopygos (Tsahar et al 2002;Tsahar et al 2003); thus, the naturally low emodin concentration in fruits increases digestibility for these frugivorous birds (Tsahar et al 2003). …”