Cyanide two-step: Fruits lead and seeds follow in the chemical phenology of a subtropical cherry.
Cyanide, in the form of cyanogenic glycosides (cyanide bound to a sugar molecule), is typically present in the vegetative tissues, fruits, and seeds of species in the genus Prunus (family Rosaceae), and might defend seeds against predation (Levin, 1976; Swain et al., 1992; Haque and Bradbury, 2002). Cyanide is thus a likely candidate for defense of the unripe fruit in this genus. Cyanogenic glycosides liberate cyanide when the cyanide molecule is enzymatically cleaved from the sugar molecule (Swain et al., 1992). In Prunus, enzymes associated with this activity include amygdalin hydrolase, prunasin hydrolase, and mandelonitrile lyase (Swain et al., 1992). Functionally cyanogenic tissues liberate cyanide when the tissue is disrupted, allowing cyanogenic glycosides to interact with cyanide-cleaving enzymes. Thus, a tissue that contains cyanogenic glycosides, but lacks cyanide-cleaving enzymes, is functionally acyanogenic. Cyanogenic glycosides are typically present in fruit tissue of Prunus species. Though the unripe fruit of some Prunus species is cyanogenic, many lack the necessary enzymes to release cyanide from tissues of their unripe fruits, rendering them acyanogenic and precluding any defensive function in fruit tissue (Machel and Dorsett, 1970; Nahrstedt, 1970; Swain et al. 1992; Sanchez-Perez et al., 2012).
Fruits of many Prunus species ripen quickly, with those fruits initiated in spring being fully ripe by midsummer. The reproductive phenology of the laurel cherry (Prunus caroliniana) stands in sharp contrast to its north-temperate congeners. In this species flowering occurs in the early spring, and fruit ripening does not occur until new flowers are produced the following year. Thus, laurel cherry presents year-old ripe fruit along with new flowers each spring. This extended fruit maturation period amplifies the risk of premature fruit removal or seed predation relative to its fast-developing congeners. Given this extended period of vulnerability, we suspected that unripe laurel cherry fruit might be chemically defended from damage or premature removal by way of cyanogenicity of the unripe fruit. Our goal was to determine whether laurel cherry was divergent from the majority of its congeners or conformed to the pattern of fruit and seed chemistry typical for the genus.
We collected unripe (firm and green) and ripe (soft and black) fruits and seeds from laurel cherry growing in riparian forest along the Colorado River at University of Texas Brackenridge Field Laboratory in Austin, Texas, in spring of 2013 and 2014; and we assayed fruit and seed tissues for cyanide. We macerated the entirety of each tissue for each sample in 5-mL distilled water, strained and collected the resulting liquid, and used a Quantofix[R] cyanide test kit (Reference number: 91318; Macherey-Nagel GmbH & Co, Duren, Germany) to measure cyanide concentrations. This kit worked through addition of chloramine T, pyridine, and phosphate buffers to a liquid sample. We then applied this solution to a test strip containing a barbituric acid derivative (H. Medollo, CTL Scientific, pers. comm.), which changed color in response to presence of cyanide. We compared the color on the strip with a color scale provided with the kit (similar to pH test strips) categorizing tissues into 0-, 1-, 3-, 10-, or 30mg cyanide per L concentrations.
Unripe fruits liberated cyanide after damage, whereas seeds in these fruits did not (Fig. 1). We found an inverse pattern in ripe fruits and seeds, with ripe fruit failing to liberate cyanide, whereas ripe seeds were approximately half as cyanogenic as unripe fruit (Fig. 1).
[FIGURE 1 OMITTED]
Laurel cherry's exceptionally long fruit-maturation period likely necessitates long-term protection of its fruits, which might be provided via the observed cyanogenicity. Though more detailed study of the chemical and seed dispersal ecology of laurel cherry is necessary to discern whether fruit cyanogenicity holds any functional significance for the species, we pose the hypothesis that cyanogenicity in developing laurel cherry fruits serves as a defense against premature removal and insect or bird damage, facilitating exceptionally long fruit-maturation period of the laurel cherry.
We began this study after observing that flocks of American robins (Turdus migratorius) and cedar waxwings (Bombycilla cedrorum) left behind seemingly ripe fruit after visiting patches of laurel cherry for days. It was unclear why the fruit was left behind by flocks capable of fully stripping large fruit crops in other species such as the Ashe juniper (Juniperus ashei). We suggest that there may be a lag between color transition and loss of cyanogenicity, and that this may influence fruit removal rates.
Though slower fruit removal may at first appear disadvantageous because of the potential opportunity cost via reduced quantity of dispersal in a given period of time, it may in fact result in a higher quality dispersal pattern overall. The broader the area over which an individual's seeds are dispersed (the seed shadow), the higher the success rate for that seed crop (Janzen, 1970, 1971; Connell, 1971; Howe and Miriti, 2000). However, seed rain tends to follow a leptokurtic distribution, with the majority of seeds deposited near the parent plant (Janzen, 1971; Ward and Paton, 2007). When a large flock of birds strips the entire fruit crop from a stand in a short time period, the seed shadow for those plants is limited to the area that the flock covers within a given gut-retention-time window. Though this may be a large area, the seed shadow that would be created by visitation of multiple flocks, separated in time, is likely to be much larger because of stochastic variation in flock movements. Thus, mechanisms that effectively slow the release of seeds from a parent plant may improve the overall quality of seed dispersal.
The balance of potential opportunity cost to the benefit of a potentially larger seed shadow would thus be context-dependent--if visitation by frugivores is high, then a slowrelease mechanism might be more beneficial; whereas if visitation is low, then simultaneous release might be favored. The study of pollen dispersal has produced similar predictions. In many zoochorous pollination systems, the benefit of broader pollen dispersal via visitation by more individual pollinators must be weighed against the potential opportunity cost of incomplete pollen removal. Ecological modeling of such systems suggests that high visitation should favor gradual release of pollen (Harder and Thomson, 1989; Harder, 1990). Indeed, pollen release timing is facultative in some plant species with respect to visitation frequency (Harder, 1990). Though the mechanisms would not be comparable, it is conceivable that some plants exhibit analogous facultative control over fruit ripening in response to removal frequency by frugivores. Investigation of such phenomena would require controlled fruit-removal experiments with careful tracking of the onset of transition to mature fruit color and the loss of cyanogenic properties.
Our observations suggest that a closer look at other plants with comparable patterns of lag between flowering and fruiting seasons, as described by Croat (1978), could uncover similar metabolic dances between fruits, seeds, dispersers, and seed predators. Seasonal patterns of seed disperser and seed predator abundance and behavior are likely to underlie such chemo-phenology patterns.
The authors would like to acknowledge the Brackenridge Field Laboratory, the University of Texas field ecology course, and the Ari Yehiel Blattstein Endowed Presidential Scholarship for their support of this study through the undergraduate research opportunities provided to J. Heiling. The authors would also like to thank J. Trout-Haney for translation of Nahrstedt (1970) from the original German.
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Submitted 18 August 2015.
Acceptance recommended by Associate Editor, James Moore, 23 December 2015.
Jacob M. Heiling *, Lawrence E. Gilbert
Brackenridge Field Laboratory and Department of Integrative Biology, University of Texas at Austin, Austin, TX 78703 (JMH, LEG)
Department of Biological Sciences, Dartmouth College, Hanover, NH 03755 (JMH)
Present address of JMH: Department of Applied Ecology, North Carolina State University, Raleigh, NC 27695
* Correspondent: firstname.lastname@example.org
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|Author:||Heiling, Jacob M.; Gilbert, Lawrence E.|
|Date:||Mar 1, 2016|
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