Intraspecific directed deterrence by the mustard oil bomb in a desert plant

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Plant secondary metabolites (SMs) acting as defensive chemicals in reproductive organs such as fruit tissues play roles in both mutualistic and antagonistic interactions between plants and seed dispersers/predators [1–5]. The directed-deterrence
  Current Biology 22 , 1–3, July 10, 2012 ª 2012 Elsevier Ltd All rights reserved DOI 10.1016/j.cub.2012.04.051 ReportIntraspecific Directed Deterrenceby the Mustard Oil Bombin a Desert Plant Michal Samuni-Blank, 1, *Ido Izhaki, 2 M. Denise Dearing, 3 Yoram Gerchman, 4 Beny Trabelcy, 4 Alon Lotan, 2 William H. Karasov, 5 and Zeev Arad 1 1 Department of Biology, Technion–Israel Institute of Technology, Haifa 32000, Israel 2 Department of Evolutionary and Environmental Biology,University of Haifa, Haifa 31905, Israel 3 Department of Biology, University of Utah, Salt Lake City,UT 84112, USA  4 Department of Biology and Environment, University of Haifaat Oranim, Tivon 36006, Israel 5 Department of Forest and Wildlife Ecology, University of Wisconsin–Madison, Madison, WI 53706, USA  SummaryPlant secondary metabolites (SMs) acting as defensivechemicals in reproductive organs such as fruit tissues playroles in both mutualistic and antagonistic interactionsbetween plants and seed dispersers/predators [1–5]. Thedirected-deterrence hypothesis states that SMs in ripe fruitsdeter seed predators but have little or no effect on seeddispersers [6].Indeed,studies havedemonstratedthatbirdsare able to cope with fruit SMs whereas rodents are deterredby them [1, 7]. However, this mechanism was only demon-strated at the class level, i.e., between birds and mammals,based on differences in the vanilloid receptors [7]. Here wepresent experimental and behavioral data demonstratingthe use of the broad-range, class-independent ‘‘mustard oilbomb’’ mechanism in Ochradenus baccatus  fruits to forcea behavioral change at an ecological timescale, convertingrodents from seed predators to seed dispersers. This isachieved by a unique compartmentalization of the mustardoil bomb, causing activation of the system only upon seedand pulp coconsumption, encouraging seed dispersal viaseed spitting by rodents. Our findings demonstrate thepower of SMs to shift the animal-plant relationship frompredation to mutualism and provide support for thedirected-deterrence hypothesis at the intraspecific level, inaddition to the interspecific level.Results and Discussion Glucosinolates (GLSs) are secondary metabolites (SMs) thatare found in many plant species in the order Brassicales,including members of the Brassicaceae and Resedaceaefamilies [8]. Generally, intact GLSs are harmless; however,when plant tissue is mechanically damaged, released myrosi-nases hydrolyze the GLSs, producing mainly thiocyanates,isothiocyanates, and/or nitriles [8, 9]. These compoundshavebeenshowntoinducetoxicologicalandpharmacologicaleffects on various organisms [9–12]. We examined ripe fruitsfrom a wild population of  Ochradenus baccatus from southernIsrael for presence of GLSs. Ochradenus baccatus (Resedaceae) is a Saharo-Sindiandesert plant. Unlike most desert plants, it produces fleshyfruits with a high water and sugar content consumed bya wide variety of vertebrates [13, 14]. The fruit pulp is rich incarbohydrates (85.1% 6 0.4% dry mass; all values aremeans 6 SE) but low in nitrogen (2.6% 6 0.09% dry mass),whereas the seeds are rich in protein (25% 6 0.09% drymass). Each stem carries tens of fruits arranged in clusters( Figure 1C). The fruits are white berries, each w 4 mm in diam-eter (56.8 6 3.9 mg fresh mass) and containing an average of 9.4 (  6 0.5, n = 100 fruits) small black (viable) or white (inviable)seeds (average seed fresh mass 0.7 6 0.03 mg, n = 40 fruits). O. baccatus organs (roots, leaves, stems, and fruit pulp)were found to be rich in GLSs. Moreover, in the fruits of  O. baccatus , we found a compartmentalization between theGLSs, found only in the pulp ( Figure 1 A), and myrosinaseenzyme, found only in the seeds ( Figure 1B). The interactionof the myrosinase and GLSs during seed consumption hydro-lyzes harmless GLSs in the pulp into toxic compounds,a mechanism known as the ‘‘mustard oil bomb’’ ( Figure 1C).This activation of GLSs could deter seed predators but wouldnot affect seed dispersers because they are not likely todamage the seeds and thus release the enzyme.We tested the interaction between O. baccatus and Acomyscahirinus ( Figure2 A),anocturnal,predominantlyseed-predat-ingmuridrodent[15],insitu.Usingday/nightmotion-activatedcameras, we documented multiple events of  A. cahirinus climbing on O. baccatus bushes (n = 3 individuals;MovieS1 A) and carrying an entire fruit cluster away from the parentplant (n = 3 individuals;Movie S1B). Moreover, we docu-mented A. cahirinus consuming the fruits on the groundbetween the rocks (‘‘rocky crevices’’; 8 distinct individuals,20 fruits per individual per session on average) and orallyexpelling O. baccatus seeds in the process ( Movie S1C).When fruits were placed overnight in 90 mm Petri dishes inrocky crevices (n = 8 sites) or under  O. baccatus bushes (n =22 bushes), more seeds were left intact in the rocky crevicescompared to under the bushes (25.7% 6 14.0% versus6.2% 6 2.7%; Mann-Whitney U = 44.5, p < 0.05), further evidence that fruits are more likely to be moved away fromthe parent plant. These are conservatively low bounds of uneaten seeds, because we counted only seeds remaininginside the small dishes, and the video recordings showedthat A. cahirinus may handle fruits away from the dish. Inter-estingly,rockycrevices mayalsoprovide favorableconditionsfor establishment of seedlings by blocking radiation andincreasing humidity, factors which often limit plant growth inthe desert ecosystem [14, 16]. Furthermore, compared toseeds dispersed by birds, seeds dispersed by A. cahirinus are more likely to remain in the wadi, which is a primary condi-tionfor  O.baccatus germinationsuccess[14].Seedscollectedfrom the field that had been orally expelled by A. cahirinus germinated successfully in the laboratory (100% of all viable,black-colored seeds [n = 22] germinated). In laboratoryexperiments, 21 of 23 naive A. cahirinus individuals presentedwith whole fruits ate the pulp but left 73.8% 6 7.7% of theseeds intact, by either dropping the seeds or spitting them( Figure 2 A;Movie S2 ). The germination rate of these seeds * CURBIO 9572 Please cite this article in press as: Samuni-Blank et al., Intraspecific Directed Deterrence by the Mustard Oil Bomb in a Desert Plant,Current Biology (2012), doi:10.1016/j.cub.2012.04.051  (83.1%, n=65 seeds treatedby n=10  A. cahirinus individuals)did not differ from seeds that had been manually separatedfrom the pulp by the experimenter (90.3%, n = 31 seeds;Z = 2 1.32, p = 0.18). The fruit-eating strategy of seed spittingimproved germination by more than 2-fold compared to thereported germination rate of seeds within intact fruit [13, 14].Otherrodents,i.e.,  Acomysrussatus (n=4;Figure2B;Movie S3 ) and Sekeetamys calurus (n = 1;Figure 2C), were alsoobserved spitting the seeds while consuming O. baccatus fruits in the field, suggesting that this behavior is not limitedto one species. Although seed dispersal via seed spittinghas been shown in other mammalian taxa [17, 18], the presentstudy is to our knowledge the first documentation in rodents,which are usually highly specialized granivores [19–21].To examine the role of GLSs in modifying the behavior of   A. cahirinus , we presented captive naive A. cahirinus (n = 21)with whole fruits containing seeds that had undergone treat-ment to deactivate myrosinase. In this experiment, less than20% of the seeds were left intact by the rodents, comparedtomorethan73%foruntreatedseedswithnaturalmyrosinaseactivity (Mann-Whitney U = 46.5, p < 0.001). Thus, when facedwith a ‘‘disarmed’’ mustard oil bomb, Acomys behaved asa seed predator. To further examine the effects of consump-tion of different parts of the fruit, we performed feeding trialsin which we monitored body mass of rodents fed for 4 dayson one of five possible treatments (n = 8 individuals per treat-ment). Treatments 1 (pulp and seeds mashed together) and 2(purifiedGLSsmashedwithseeds)containedallthenecessarycomponents to generate the mustard oil bomb, whereas theother treatments contained only some of the components.Only treatment 1 had a significant negative effect on thebodymassof   A.cahirinus ( Figure3 ).Treatment2alsoresultedin decreased body mass, although not significantly, relative tocontrols (treatments 3–5), probably because the pulp, whichwasmissingintreatment2,providesanoptimalchemicalenvi-ronment for the myrosinase enzyme activity.The mustard oil bomb is well established for its role in pre-venting herbivory [8, 12]. Generally, GLSs are found in allplant organs, and their concentration may vary betweenorgans as well as between individuals of the same species([22]; A.L. and I.I., unpublished data). The myrosinase enzymeis stored in cells separated from GLSs, presumably to avoidautotoxic effects [8, 22]. Some herbivores utilize this separa-tion to avoid the mustard oil bomb. For example, green peachaphids, Myzus persicae , consume phloem containing GLSswhile leaving the cells containing myrosinase that surroundit intact [8, 23]. Here we demonstrate a new role for thismechanism in ripe fruits: a generalistic, species-independent,seed-dispersal-promoting mechanism resulting in an unusualrelationship between a plant and a predominantly seed-predating rodent. We found that the granivorous rodent Figure 1. Compartmentalization of Glucosinolates and the MyrosinaseEnzyme in Fruits of  Ochradenus baccatus (A) Glucosinolate (GLS) concentration in pulp (n = 8) and seeds (n = 8). Datain (A) and (B) are presented as means 6 SE.(B) Myrosinase activity in pulp (n = 8) and seeds (n = 8).(C) Upon mechanical injury to seeds, GLSs are activated (hydrolyzed) bythe enzyme myrosinase, producing toxic components [8, 9].Figure 2. Three Rodent Species Spitting Intact Seeds of  Ochradenus baccatus during Fruit Consumption(A) Captive Acomys cahirinus (seeMovie S2 ).(B) Wild Acomys russatus (seeMovie S3 ).(C) Wild Sekeetamys calurus . Current Biology Vol 22 No 132 CURBIO 9572 Please cite this article in press as: Samuni-Blank et al., Intraspecific Directed Deterrence by the Mustard Oil Bomb in a Desert Plant,Current Biology (2012), doi:10.1016/j.cub.2012.04.051   A. cahirinus circumvents the activation of GLSs found in O. baccatus fruits by spitting viable seeds, thus becominga seed disperser. When the mustard oil bomb was disarmedby inactivation of the myrosinase enzyme, the rodent returnedto its typical behavior as a seed predator. When offered dietscontaining a GLS-myrosinase combination, A. cahirinus werenegativelyimpacted.Nosucheffectwasevidentwhenfeedingon GLSs, on seeds (containing myrosinase), or on pulp withseeds containing deactivated myrosinase. Given the impor-tance of  O . baccatus as a keystone species in the desertecosystem [13], this mustard oil bomb mechanism and theability of  A. cahirinus to alter its behavior with respect toSMs in the fruits illustrates the flexibility of symbiotic relation-ships within an ecological timescale. Moreover, our findingssuggest an intraspecies, in addition to interspecies, variationof the directed-deterrence hypothesis: SMs in ripe fruits deter individuals if they act as seed predators but have no sucheffect on individuals of the same species acting as seeddispersers. Our results suggest that SMs in ripe fruits playa deeper role in plant fitness by shaping plant-animal interac-tions much more than previously assumed. Supplemental Information SupplementalInformationincludesSupplementalExperimentalProceduresand three movies can be found with this article online atdoi:10.1016/j.cub.2012.04.051. Acknowledgments  All experimental protocols were approved by the Committee of AnimalExperimentation of the University of Haifa (permit number 096/08). We aregrateful to M. Reichelt from the Max Planck Institute for Chemical Ecologyfor his help in developing the GLS quantification protocol and to themembers of the Oranim College animal house staff, particularly N. Dainov,N. Sheena, and N. Keshales, for their help with animal maintenance. Wealso thank the Israel Nature and Parks Authority, N. Taube, U. Hilberger,L. Samuni, V. Demartsev, A. Weinstein, and especially M. Blank for their help with field work. We are also grateful to L.J. Douglas, T. Keasar, S.Lev-Yadun, K.C. Burns, and an anonymous referee for their usefulcomments on previous versions of this paper. Support for this study wasavailable through grants from the United States-Israel Binational ScienceFoundation (2006043), the Israel Science Foundation (189/08), and theMiddle East Regional Cooperation Program (TA-MOU-08-M28-013).Received: April 11, 2012Revised: April 23, 2012 Accepted: April 24, 2012Published online: June 14, 2012 References 1. Tewksbury, J.J., and Nabhan, G.P. (2001). Seed dispersal. Directeddeterrence by capsaicin in chilies. Nature 412 , 403–404.2. Cipollini, M.L., and Levey, D.J. (1997). Why are some fruits toxic?Glycoalkaloids in Solanum and fruit choice by vertebrates. Ecology 78 , 782–798.3. Foley, W.J., and Moore, B.D. (2005). Plant secondary metabolites andvertebrate herbivores—from physiological regulation to ecosystemfunction. Curr. Opin. Plant Biol. 8 , 430–435.4. Levey, D.J., and Cipollini, M.L. (1998). A glycoalkaloid in ripe fruit detersconsumption by cedar waxwings. Auk 115 , 359–367.5. Herrera, C.M. (1982). 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Intraspecific Directed Deterrence 3 CURBIO 9572 Please cite this article in press as: Samuni-Blank et al., Intraspecific Directed Deterrence by the Mustard Oil Bomb in a Desert Plant,Current Biology (2012), doi:10.1016/j.cub.2012.04.051
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