AOBPreview published online on August 27, 2008
Annals of Botany, doi:10.1093/aob/mcn153
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Parthenocarpy and Seed Predation by Insects in Bursera morelensis
1 FES Iztacala UNAM, Laboratorio de Ecología UBIPRO, Av. De los Barrios 1, Los Reyes Iztacala, Tlalnepantla, Edo. México, CP 54090, México
2 Facultad de Ciencias UNAM, Laboratorio de Desarrollo en Plantas, Circuito Exterior s/n, Ciudad Universitaria, Avenida Universidad 3000, CP 04510, México
* For correspondence. E-mail coro{at}servidor.unam.mx
Received: 26 May 2008 Returned for revision: 18 June 2008 Accepted: 10 July 2008
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Background and Aims: While parthenocarpy (meaning the production of fruits without seeds) may limit fecundity in many plants, its function is not clear; it has been proposed, however, that it might be associated with a strategy to avoid seed predation. Bursera morelensis is a dioecious endemic plant that produces fruits with and without seeds, and its fruits are parasitized by insects. Its reproductive system is not well described and no published evidence of parthenocarpy exists for the species. The purpose of this work was to describe the breeding system of B. morelensis and its relationship to seed predation by insects.
Methods: The breeding system was described using pollination experiments, verifying the presence of parthenocarpic fruits and apomictic seeds. Reproductive structures from flower buds to mature fruits were quantified. For fruits, an anatomical and histological characterization was made. The number of fruits in which seeds had been predated by insects was correlated with parthenocarpic fruit production.
Key Results: The major abortion of reproductive structures occurred during fruit set. The results discard the formation of apomictic seeds. Flowers that were not pollinated formed parthenocarpic fruits and these could be distinguished during early developmental stages. In parthenocarpic fruits in the first stages of development, an unusual spread of internal walls of the ovary occurred invading the locule and preventing ovule development. Unlike fruits with seeds, parthenocarpic fruits do not have calcium oxalate crystals in the ovary wall. Both fruit types can be separated in the field at fruit maturity by the presence of dehiscence, complete in seeded and partial in parthenocarpic fruits. Trees with more parthenocarpic fruits had more parasitized fruits.
Conclusions: This is the first time the anatomy of parthenocarpic fruits in Burseraceae has been described. Parthenocarpic fruits in B. morelensis might function as a deceit strategy for insect seed predators as they are unprotected both chemically and mechanically by the absence of calcium oxalate crystals.
Key words: Parthenocarpy, Bursera morelensis, predation, seeds, insects, breeding system, calcium oxalate crystals
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Seed development is one of the key processes in angiosperm reproduction (Yadegari and Drews, 2004; Berger et al., 2006). The abortion of flowers, fruits and seeds is a physiological process in which plants can fit progeny levels according to resource availability avoiding predator-damaged seeds or genetically deficient ones (Janzen, 1971, 1977; Sorensen, 1982; Stephenson and Bertin, 1983; Evenari, 1984).
All species of the genus Bursera (Burseraceae) have seeds covered by a pseudoaril that has a colour contrasting with surrounding vegetation (Rzedowsky et al., 2004, 2005). These seeds possess all the features to be bird dispersed (Howe and Westley, 1988). Several studies have stressed the importance of seed dispersion of Bursera by birds (Scott and Martin, 1984; Trainer and Hill, 1984; Bates, 1992; Greenberg et al., 1993; 1995; Poulin et al., 1994; Grant and Grant, 1996; Ortiz-Pulido et al., 1999; Ortiz-Pulido and Rico-Gray, 2000; Graham, 2002; Stevenson et al., 2005) and other vertebrates (Clark and Clark, 1981; Evans, 1989; Stevenson, 2000; Stevenson et al., 2000). The genus has more than 100 species of trees and shrubs inhabiting tropical dry forests (Espinosa et al., 2006). Development of fruits and seeds in the genus are almost unknown except for Srivastava (1968) and Cortes (1998). Cortes (1998) described the production of apomictic seeds in Bursera medranoana, while Srivastava (1968) and Cortes (1998) reported that the development of ovules with respect to the ovary in B. delpechiana and B. medranoana suffered a delay giving the impression of a fruit without seed. The presence of parthenocarpic fruits has been reported for B. fagaroides and B. morelensis (Verdú and García-Fayos, 1998).
The production of parthenocarpic fruits has been regarded as a defensive strategy to lower predation probabilities of viable seeds (Zangerl et al., 1991; Traveset, 1993a, b; Ziv and Bronstein, 1996; Fuentes and Schupp, 1998; Verdú and García-Fayos, 1998, 2001). Insects lay eggs into fruits when ovules are still immature without knowing if the fruit will bear seeds. When fruits become mature only those larvae in fruits with seeds can survive (Scurlock et al., 1982; Coetzee and Giliomee, 1987; Jordano, 1989, 1990; Niwa and Overhulser, 1992; Mustart et al., 1995; Verdú and García-Fayos, 1998). Traveset (1993a) found a negative correlation between the number of parthenocarpic fruits in Pistacia terebinthus and the number of wasp-damaged seeds, suggesting that empty fruits can serve to lower predation risks. Ziv and Bronstein (1996) showed that moths avoid infertile seeds by flying away from trees where they find them thus reducing the impact on viable seeds. Zangerl et al. (1991) reported that butterfly larvae (Depressaria pastinacella) preferred the parthenocarpic fruits of Pastinaca sativa (Umbelliferae) due to the lower content of furanocoumarins (toxin) compared with seeded fruits.
The purpose of the present work was to determine the breeding system of Bursera morelensis, describing pollination and fruiting ecology, and following the maturation of seeds and fruits from the anatomic and histological perspective to determine the presence of parthenocarpic fruits or apomictic seeds in the plant, and its relationship with seed predation by insects.
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MATERIALS AND METHODS |
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Study site
The study site was located near Barranca de Muchil in San Rafael Coxcatlán, in the southeast portion of the Tehuacan Valley, Puebla, México (18°12' and 18°14'N; 97°07' and 97°09'W), at 1000 m a.s.l. and has a dry climate with summer rains (Fernández, 1999). Mean annual temperature is 25 °C and mean annual rainfall 394·6 mm, with a dry season from November to May and a rainy season from June to October (Valiente, 1991). It is an alluvial fan where the predominant vegetation is tropical deciduous forest with 57 species of angiosperms reported (Fernández, 1999). It has a high soil diversity (Medina, 2000) resulting in the formation of different vegetal associations: the ‘Fouquerial’ dominated by Fouqueria formosa Kunt, the ‘Cuajiotal’ dominated by Bursera morelensis Ramírez, the ‘Chiotillal’ dominated by Escontria chiotilla (Weber) Rose and ‘Cardonal’ dominated by Pachycereus weberi (Coulter) Buxb. (Ríos-Casanova et al., 2004).
Species studied
Bursera morelensis is a dioecious tree endemic to Mexico. Male flowers are produced in paniculated or inflorescent racemes while female flowers can be solitary, in pairs or in short paniculates. Female flowers have non-functional anthers. Fruits are trivalvated ovoid (5–8 mm long; 4–6 mm wide). Seeds are covered by a yellow pseudoaril (Rzedowski et al., 2005). The tree was used to produce matches and now is used locally for live-fences (Reyes et al., 2004). It also has medicinal properties (Jolad, 1977). It is distributed in the tropical dry forests of the Mexican states of Guerrero, Morelos, Puebla and Oaxaca (Reyes et al., 2004; Becerra, 2005).
Breeding system
Phenology was described by monthly visits to the study area from May 2005 to May 2007. Forty individuals were observed and flowers, fruits and leaf production was followed.
The breeding system was determined using six trees, where three branches were randomly chosen for each treatment; in each branch ten inflorescences were chosen for each pollination treatment (10 inflorescences x 3 branches x 3 treatments x 6 trees). The total number of inflorescences used was 540 and total flowers was 5930. The experiment was carried out in May 2006 and was followed until January 2007, and was done separately from the phenological observations. The number of fruits formed after pollination, number of full-grown fruits, and fruits with and without seed was registered in each treatment. All fruits produced in the experiment were collected and dissected. Three pollination treatments were applied.
- Open pollination (control treatment: n = 2013 flowers). Inflorescences were marked and the number of flowers available counted. Flowers were exposed to biotic pollinators and abiotic factors. When they were dry, they were covered with mosquito mesh to avoid fruit loss.
- Manual pollination (n = 1992 flowers). Flower buds were enclosed before anthesis. Flowers were hand-pollinated using pollen from 12 male trees. Each female flower received pollen from three different male trees. Flowers were enclosed after pollination and fruit production was monitored.
- Pollination exclusion (n = 1925 flowers). Flower buds were enclosed with fine mosquito mesh and flowers left open were enclosed for the duration of their lives. Fruit production was followed.
Fruit development
Of the fruits formed in May 2005 and May 2006, 50 fruits were collected from 14 randomly chosen plants of Bursera morelensis in April 2006 and in April 2007, respectively, 11 months after flowering when they reached full size and maturity. Fruits collected in this part were independent of those of the pollination experiment. Total dimensions (width and length in millimetres), weight (dry and fresh in grams), colour and presence of odour (Berlanga, 1991; Martínez, 1996) were measured. External features were measured using an electronic caliper with a resolution of 0·01 mm. Fresh weight was measured using an analytical balance while the dry weight was obtained using a dryer to 70 °C until the sample reached a constant weight. Fruit type was noted (with or without seed).
Monthly collections of different stages of fruit formation were carried out to follow fruit development using anatomical techniques (López et al., 2005). Fifty fruits each month were collected between June 2006 and February 2007 from three randomly chosen trees. Fruits were collected and fixed in FAA (formol : acetic acid : 96 % ethanol : water, 1 : 0·5 : 5 : 3·5) and transported to the laboratory where they were embedded in paraffin and stained with safranin–fast green. Also collected were flowers which were embedded in LR-White and stained with toluidine blue. Fruits were dissected to describe all developmental stages. Fruits were classified according to their characteristics. Parts of the fruits were dried to critical point, coated with gold and observed under the scanning electron microscope (SEM).
Insect seed predation
The proportion of damaged seeds was determined, collecting 50 fruits from 23 randomly chosen trees. Fruits were dissected and classified as fruits with or without seeds and damaged or undamaged. Insect-damaged fruits were those containing eggs or larvae inside or those presenting a hole by which the insect abandoned the fruit after hatching. The proportion of damaged and empty fruits was calculated and a correlation between variables was carried out.
To identify parasitic insects, 70 fruits were collected, isolated inside plastic bags and placed in total darkness until fruit maturation and the insects hatched. The insects were collected and preserved in 70 % alcohol for further identification by a specialist. To determine the timing of infection, 50 fruits were collected monthly from three randomly chosen trees and dissected to search for eggs or larvae. Fruits were collected in April 2007 when the fruits produced in May 2006 were maturing.
Data analysis
To analyse the breeding system, an ANOVA with arcsine square root-transformed data was used. Fruit size variation among fruit types was analysed using a one-way ANOVA. Correlations were carried out to test the relationship between crop size, number of parasitized fruits and parthenocarpic fruits. All analyses were done using SPSS (SPSS, 2003) and XLSTAT (Addinsoft, 2007).
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RESULTS |
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Phenology and breeding system
Flowering in B. morelensis was synchronic and occurred in the two observed years 1 week following the first rains (third week of May 2005 and second week of May 2006). Male buds formed earlier than female buds and anthesis followed the same pattern. Male flowers lasted between 5 d and 7 d while female flowers lasted between 3 d and 4 d. Pollination was completed by bees (Apis mellifera).
Anthers were present in the female flowers of B. morelensis but they were not developed and did not produce pollen.
Flowering lasted 2 weeks and after that immature fruits could be seen in trees. Immature fruits were green and reached their full size (7–8 mm) in 1 week. Maturation time was between 7 and 8 months with a maximum of 11 months (Table 1). Fruits became red when maturing.
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Pollination experiments showed that there were two important times of fruit loss, the first from flower to fruit (fruit set) and the second between fruit set and maturation (Fig. 1). In the open pollination treatments, 63·59 ± 17·31 % of the flowers formed fruits (n = 2013 flowers) and 46·62 ± 21·18 % of these reached full size. Most of those fruits had seeds (42·47 ± 21·47 %) while the others had no seeds but presented two different types of tissues inside (2·23 ± 2·77 %). Hand-pollinated treatments resulted in 59·34 ± 16·97 % of fruit set (n = 1992 flowers) and 38·91 ± 14·60% of full-sized fruits formed. Almost all these fruits formed seeds with only 2·73 ± 1·89 % being seedless. In pollen-exclusion treatments only 2·26 ± 4·01 % of fruit set (n = 1925 flowers), and of these only 1·54 ± 2·99 % grew to full size and none contained seeds. The plant is self-incompatible and no pollen limitation is occurring (Fig. 1).
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Fruit development
Overall, four different fruit types in Bursera morelensis were found (Fig. 2 and Table 2; n = 700 fruits). Fruit size was not different either in the total length or width, nor for fresh or dry weight (P > 0·05).
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Type 1 fruit was red in colour and had three lines of dehiscence. Fruit opened completely separating three valves through these lines. The pseudoarile was orange surrounding the seed coat completely. The seed coat was formed completely, and the seed itself was trigonous measuring 5·7 ± 0·7 mm in length and 5 ± 0·3 mm in width. Seed colour was grey dotted with black.
Type II fruits were also red, with the three dehiscence lines but, when ripening, dehiscence was incomplete in 100 % of cases. From a total of 280 type II fruits, only 191 were opened by one valve (68·2 %), 78 opened by two valves (27·85 %) and 11 (3·92 %) presented dehiscence in at least one valve but this was never complete. In the areas without dehiscence, the pseudoarile was not formed; in the areas with dehiscence the pseudoarile was orange. When some part of the seed with pseudoarile became exposed the exocarp dehydrated and the pseudoarile became brown. Seed measurements were 5·4 ± 0·6 mm in length and 4·8 ± 0·5 mm in width. Seeds were white dotted with black spots. The seed coat was not completely formed and presented two types of tissue: one hard and white with the other soft and translucent. The only way to separate fruits of type I and II in the tree was by observing valve dehiscence.
Fruit types III and IV were similar. They were green to red depending on maturation stage. Fruit tissues were not differentiated and no dehiscence formed. Type III presented one to two ovules and type IV presented a tissue instead of ovules in the locules.
Inside type III fruits three locules, each bearing two ovules, were found. When the fruit was growing (approx. 4–5 mm in diameter) only one locule persisted with one of the two ovules being aborted and the other developing into a seed. Usually, there was one seed per fruit. The ovary walls were well defined (Fig. 3). Inside type IV fruits all the locules were occupied by tissue with obliterated locules, ovary walls were diffuse, and ovules had either degenerated or were absent (Fig. 3). Type IV fruits represented parthenocarpic fruits and could be differentiated under a microscope from the first month after blooming.
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In type III fruits, ovary layers showed a different arrangement than type IV fruit (Fig. 4). The tissue found filling the locule in type IV fruits was formed by cells from endocarp and mesocarp (Becerril, 2004) that grew into the locule squashing the ovule (Fig. 4).
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In the seeded fruits (type III) the mesocarp and endocarp were formed by cells with relatively thick walls and calcium oxalate crystals. In the parthenocarpic fruits, cells were larger with thin walls and calcium oxalate crystals were absent (n = 21 fruits randomly chosen) (Fig. 5).
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Type III fruit had small ovules that remained small for 5–8 months, after which they reached full size when they dehisced and were ready for seed dispersal. Type III fruits were classified as such when immature; however, upon reaching full size they became type I (Figs 3 and 6). Similarly, type IV fruit represented the immature phases of type II.
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The outermost layer that protected the seed was a tissue derived from the endocarp. In the seeded fruits it was a continuous layer that protected the seed, but in the parthenocarpic fruits the layer was incomplete.
Insect seed predation
Of the fruits examined, 79·15 ± 2·79 % (range 43·6–98·2 %) presented seeds, 17·6 ± 2·2 % (range 1·75–45·45 %) were parthenocarpic and 3·05 ± 0·89 % (range 0–18 %) were parthenocarpic and parasitized by flies of the family Cecidomyiidae (Diptera) and wasps of the superfamily Chalcidoidea (Himenoptera; n = 1150 fruits, 23 trees, 50 fruits per tree). Insects began laying eggs on fruits in the seventh month of fruit development. Dissected fruits for the observation of fruit development showed also that insects visit the fruits in the seven month of development. It was not possible to determine hatching time. Only one larva per fruit was recorded and only in parthenocarpic fruits. Parasitized fruits could be easily recognized because the puncture that the insect made to insert eggs in fruits was full of resin forming a white scar. Of the 280 parthenocarpic fruits dissected 62 were parasitized, while of the 870 fruits with seeds examined none was parasitized. A negative and significant correlation between the percentage of damaged fruits and the percentage of parthenocarpic fruits in a tree was found (r2 = –0·71, d.f. = 22, P < 0·05; Fig. 7).
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DISCUSSION |
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Breeding system
Flowering of B. morelensis occurred after the first summer rains in May. Flowering synchrony can be a strategy to avoid competition for pollinators (Frankie et al., 1974). This phenological pattern has been reported for several species of the tropical dry forests such as Plumeria rubra and Guazuma ulmifolia (Borchert et al., 2004). The delay of female flower maturation related to male flowers is a frequent pattern between dioecious trees (Lloyd and Webb, 1977; Obeso, 1996), and has been related to the higher energetic costs of female related to male plants (Lovett-Doust and Lovett-Doust, 1988).
Fruit set reported here for B. morelensis was similar to values reported by Jordano (1988) in the three pollination treatments and slightly lower that those reported by Verdú and García-Fayos (1998) for P. lentiscus. Fruit production is limited by pollen availability as shown by the high abortion rate of enclosed flowers as stated by other authors (Jordano, 1988; Verdú and García-Fayos, 1998; Bañuelos and Obeso, 2005). Pollination can be affected by the number of pollinators available, number of visits and distance between trees of different sex in dioecious species (Pascarella, 1996; Bañuelos and Obeso, 2003; de Jong et al., 2005). Abortion can also be a consequence of environmental scarcity of resources, seeds being genetically deficient or seed predation and damage (Janzen, 1971, 1977; Stephenson, 1981; Aker, 1982; Ehrlén, 1991; Bañuelos and Obeso, 2005).
Seeds produced by B. morelensis clearly had a sexual origin. This if often related to the maintenance of high variability in the population that can ensure adaptation in the long term (Muller, 1964; Michod and Levin, 1988; Kondrashov, 1994; Hurst and Peck, 1996; Doncaster et al., 2000; Maynard-Smith and Szathmáry, 2001; Rice and Chippindale, 2001).
Fruit description and development
Parthenocarpic fruits in B. morelensis can be recognized and separated from seeded fruits in trees when maturation has finished because of the incomplete dehiscence of the valves; however, during the long period in which fruit are immature, these two types cannot be distinguished as is the case in many other angiosperms (Jordano, 1988; Traveset, 1993b; Fuentes, 1995).
There are many reports of plants producing parthenocarpic fruits but most of them involve an induced phenomena to produce seedless fruits for commercial purposes (Varoquaux et al., 2000; Ampomah-Dwamena et al., 2002; Zohary, 2004). In species where parthenocarpy is believed to exist naturally, there are no complete anatomical descriptions of fruit development. In P. lentiscus, parthenocarpic fruits presented only remnants of the funicule without any trace of embryos (Jordano, 1988), and in P. terebinthus the fruits presented remnants of both funicule and ovules (Traveset, 1993a). In B. morelensis traces of funicule and ovule were observed but a huge spread of probably mesocarp and endocarp was also found. This suggests that different factors (environmental, genetic, physiological) may promote the production of parthenocarpic fruits in the different species studied (Gillaspy et al., 1993).
Parthenocarpy can originate by several factors both internal and external. Sources of external factors include scarcity of resources (Bertin, 1995; Jang and Sheen, 1997; Sato et al., 2001), thermal stress (Sato et al., 2001, 2002; Higashiyama et al., 2003; Young et al., 2004), hydric stress (Gay et al., 1987) and damages in the reproductive organs (Galil and Eisikowitch, 1971; Solomon, 1980). Internal causes include changes in hormone concentration (Nitsch, 1950; Gillaspy et al., 1993; Azcon-Bieto and Talon, 2000; Fos et al., 2003), polyploidy and errors in gene expression (Mazzucato et al., 1998, 2003; Varoquaux et al., 2000; Ampomah-Dwamena et al., 2002; Carmi et al., 2003; Zohari, 2004).
Parthenocarpy and insect seed predation
Seed predation registered for Bursera morelensis (3·05 ± 0·89 %) was lower than that registered in other parthenocarpic species such as Olea europaea (18 % ± 8·8 %; Jordano, 1987), Pastinaca sativa (14·4 %; Zangerl et al., 1991), Pistacia lentiscus (0·4–2·9 %; Jordano, 1989; Verdú and García-Fayos, 1998) and P. terebinthus (9 %; Traveset, 1993a). This could probably be related to the presence of resins that characterize Bursera and decrease survivorship and growth rates in some larvae (Becerra, 1994). It is probable that insects have evolved some mechanism enabling them to parasitize Bursera fruits, with smaller survivorship and growth rates, such as that described for beetles feeding on leaves of Bursera (Becerra and Venable, 1990; Becerra, 1994; Evans et al., 2000). According to Traveset (1993a), it is possible that insects can differentiate between fruits with and without ovules while inserting the ovipositor. If this is true, the growth of soft tissue inside parthenocarpic fruits of B. morelensis might serve to deceive parasitizing insects.
The pollination experiment showed that 2 % of the fruits produced were parthenocarpic and without parasites, nevertheless when the number of parasitized fruits was determined it was found that approx. 20 % of the fruits were parthenocarpic and 3 % had insects. In the pollination experiment, fruits were protected by the bags preventing the entrance of insects, while in the other experiment the fruits developed without protection. The presence of parasites and the increase in the number of parthenocarpic fruits could suggest that insects could be one of the factors that promote the formation of parthenocarpic fruits as indicated by Galil and Eisikowitch (1971) and Solomon (1980), although further studies are necessary to investigate it.
Parthenocarpy has been proposed to be related to seed predation in Pastinaca sativa (Zangerl et al., 1991). The hardness of the fruit wall depends on the internal layer of mesocarp, which is full of crystals of calcium oxalate, and the lignified endocarp. In parthenocarpic fruit when the mesocarp spreads and the cell became more elonged, the endocarp gets fragmented forming unprotected sites. The presence of crystals has been regarded as a defence against seed predation (Franceschi and Horner, 1980; Sunell and Healey, 1985; Perera et al., 1990; Ward et al., 1997; Webb, 1999; Molano-Flores, 2001; Ruiz et al., 2002). The production of calcium oxalate crystals is a specialized process analogous to bone formation in animals (Webb, 1999). These crystals are produced as a way of metabolizing harmful elements such as oxalic acid (Franceschi and Horner, 1980; Carvalhâo, 1997), and serve to store calcium, minimizing the amount of calcium in circulation but maintaining calcium available for tissue formation (Franceschi and Horner, 1980; Tilton and Hornet, 1980; Volk et al., 2002). Crystals provide reinforcement, giving additional strength to the tissues (Franceschi and Horner, 1980; Fink, 1991; Webb, 1999), and minimize predation (Molano-Flores, 2001). Chemically they are considered as irritating compounds that reduce palatability and for some insects are toxic (Smith, 1989). Absence of insects in the fruits with crystals of calcium oxalate of B. morelensis suggests that the plant can produce fruits armed mechanically and chemically to ensure seed development as well as unprotected seedless fruits as a deceit low-cost strategy to reduce the probability of seed predation as suggested by Lee et al. (1991), and enhance an attraction unit for seed dispersers (Traveset, 1993a; Fuentes, 1995; Fuentes and Schupp, 1998; Verdú and García-Fayos, 1998). Nevertheless more studies are needed to assess the effect of the presence of calcium oxalate crystals on parasitization and survival rates of insects (Smith, 1989; Zangerl et al., 1991; Molano-Flores, 2001).
Parthenocarpy was reported previously for B. morelensis and B. fagaroides by Verdú and García Fayos (1998), and during the present work this type of fruit was observed in B. aptera, B. schlechtendalli and B. submoniliformis. Recently, Bonfil et al. (2007) reported parthenocarpy in B. grandifolia, B. bipinnata, B. lancifolia, B. copallifera, B. glabrifolia and B. bicolor. This suggests that parthenocarpy is a widespread phenomenon in the genus Bursera but more studies are needed to demonstrate this. This adds weight to the proposal of Verdú and García-Fayos (1998) that parthenocarpy was present in a common ancestor of the families Anacardiaceae and Burseraceae, and this character was positively selected for some reason and remains today. Although the original function of parthenocarpy is still unknown, presently it is proposed that parthenocarpic fruits can enhance attraction to seed dispersers and lower the individual probability of a seeded fruit being parasitized (Zangerl et al., 1991; Traveset, 1993a, b; Fuentes, 1995; Ziv and Bronstein, 1996; Fuentes and Schupp, 1998; Verdú and García-Fayos, 1998; M. F. Ramos-Ordoñez, unpubl. res.).
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ACKNOWLEDGEMENTS |
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We thank the following: Dra. Silvia Espinosa and M. en C. Anabel Bieler of the laboratories of Microscopía Electrónica de Barrido and Microcine, Facultad de Ciencias UNAM, for help with photographs; R. Wong and M. Pérez-Pacheco for assistance with the anatomical techniques; N. Zea, JL. Peña-Ramírez, L. Baños-Van Dick and M. Sánchez-Matias for assistance in the field; Dr Vicente Hernández Ortiz, Instituto de Ecología A.C. for insect identification; and Amy E. McAndrews for revising an earlier version of the manuscript. Financial support was provided by DGAPA-PAPIIT No. IN207305 and CONABIO DT006 projects to M.C.A., CONACyT research scholarship to M.F.R.-O. This work is part of the PhD thesis of M.F.R.-O. of the Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México.
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LITERATURE CITED |
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Addinsoft. (2007) XLSTAT version 2007·8·04. http://www.xlstat.com. Accessed 31 March 2008.
Aker CL. Regulation of flower, fruit and seed production by a monocarpic perennial. Yucca whipplei. Journal of Ecology (1982) 70:357–372.
Ampomah-Dwamena C, Morris BA, Sutherland P, Veit B, Yao J. Down-regulation of TM29, a tomato SEPALLATA homolog, causes parthenocarpic fruit development and floral reversion. Plant Physiology (2002) 130:605–617.
Azcon-Bieto J, Talón M. Fundamentos de fisiología vegetal (2000) Madrid: McGraw Hill Interamericana.
Bañuelos MJ, Obeso JR. Maternal provisioning, sibling rivalry and seed mass variability in the dioecious shrub Rhamnus alpinus. Evolutionary Ecology (2003) 17:19–31.[CrossRef][Web of Science]
Bañuelos MJ, Obeso JR. How is fruit production regulated in the dioecious fleshy-fruited shrub Rhamnus alpinus? Basic and Applied Ecology (2005) 6:249–259.[CrossRef][Web of Science]
Bates JM. Frugivory on Bursera microphylla (Burseraceae) by wintering Gray Vireos (Vireo vicinior, Vireonidae) in the coastal deserts of Sonora, Mexico. Southwestern Naturalist (1992) 37:252–258.[CrossRef]
Becerra JX. Squirt-gun defense in Bursera and the chrysomelid counterploy. Ecology (1994) 75:1991–1996.[CrossRef][Web of Science]
Becerra JX. Timing the origin and expansion of the Mexican tropical dry forest. Proceedings of the National Academy of Sciences of the USA (2005) 102:10919–10923.
Becerra JX, Venable DL. Rapid-terpene-bath and ‘squirt-gun’ defense in Bursera schlechtendalii and the counterploy of chrysomelid beetles. Biotropica (1990) 22:320–323.[CrossRef][Web of Science]
Becerril CF. Morfología y anatomía del fruto de dos especies del género Bursera Jack. ex L. Sección Bursera (Burseraceae). (2004) Universidad Nacional Autónoma de México. Tesis de Licenciatura.
Berger F, Grini PE, Schnittger A. Endosperm: an integrator of seed growth and development. Current Opinion in Plant Biology (2006) 9:664–670.[CrossRef][Web of Science][Medline]
Berlanga H. Las aves frugívoras de Chamela, Jalisco, su recurso vegetal y su papel en la dispersión de semillas (1991) Universidad Nacional Autónoma de México. Tesis de Licenciatura.
Bertin N. Competition for assimilates and fruit position affect fruit set in indeterminate greenhouse tomato. Annals of Botany (1995) 75:55–65.[CrossRef]
Bonfil C, Cajero I, Castellanos C, Healy E, Evans R. Germinación y propagación vegetativa de diversas especies del género Bursera. (2007) URL: http://www.socbot.org.mx/Congresos/XVII/Resumenes%20Congreso.pdf. Last successful access 23 November 2007.
Borchert R, Meyer SA, Felger RS, Porter-Bolland L. Environmental control of flowering periodicity in Costa Rican and Mexican tropical dry forests. Global Ecology and Biogeography (2004) 13:409–425.[CrossRef][Web of Science]
Carmi N, Salts Y, Dedicova B, Shabtai S, Barg R. Induction of parthenocarpy in tomato via specific expression of the rolB gene in the ovary. Planta (2003) 217:726–735.[CrossRef][Web of Science][Medline]
Carvalhâo F. El bitter pit de las manzanas, desarrollo y control. Fruticultura Profesional (1997) 86:12–20.
Clark DA, Clark DB. Effects of seed dispersal by animals on the regeneration of Bursera graveolens (Burseraceae) on Santa Fe Island, Galapagos. Oecologia (1981) 49:73–75.[CrossRef][Web of Science]
Coetzee JH, Giliomee JH. Seed predation and survival in the infructescences of Protea repens (Proteaceae). The South African Journal of Botany (1987) 53:61–64.
Cortes A. Biología reproductiva de Bursera medranoana Rzedowski & Ortiz (Burseraceae), una especie de origen híbrido. (1998) Universidad Nacional Autónoma de México. Tesis de Licenciatura.
Doncaster CP, Pound GE, Cox SJ. The ecological cost of sex. Nature (2000) 404:281–285.[CrossRef][Web of Science][Medline]
Ehrlén J. Why do plants produce surplus flowers? A reserve-ovary model. The American Naturalist (1991) 138:918–933.[CrossRef]
Espinosa D, Llorente J, Morrone JJ. Historical biogeographical patterns of the species of Bursera (Burseraceae) and their taxonomic implications. Journal of Biogeography (2006) 33:1945–1958.[CrossRef][Web of Science]
Evans MA. Ecology and removal of introduced rhesus monkeys: Desecho Island National Wildlife. Puerto Rico Health Sciences Journal (1989) 8:139–156.[Medline]
Evans PH, Becerra JX, Venable DL, Bowers WS. Chemical analysis of squirt-gun defense in Bursera and counterdefense by chrysomelid beetles. Journal of Chemical Ecology (2000) 26:745–754.[CrossRef][Web of Science]
Evenari M. Seed physiology: from ovule to maturing seed. Botanical Review (1984) 50:143–170.[CrossRef]
Fernández N. Análisis de la dinámica de comunidades vegetales con relación a la evolución del paisaje en la zona semiárida de Coxcatlán, Puebla. Caso: Abanico aluvial de la Barranca del Muchil. (1999) Universidad Nacional Autónoma de México. MSc Thesis.
Fink S. The micromorphological distribution of bound calcium in needles of Norway spruce Picea abies (L.) Karst. New Phythologist (1991) 119:33–40.[CrossRef]
Fos M, Proaño K, Alabadí D, Nuez F, Carbonell J, García-Martínez JL. Polyamine metabolism is altered in unpollinated parthenocarpic pat-2 tomato ovaries. Plant Physiology (2003) 131:359–366.
Franceschi VR, Horner HT. Calcium oxalate crystals in plants. Botanical Review (1980) 46:361–427.[CrossRef]
Frankie GW, Baker KG, Opler PA. Comparative phenological studies of trees in tropical wet and dry forest in the lowlands of Costa Rica. Journal of Ecology (1974) 62:881–919.[CrossRef][Web of Science]
Fuentes M. The effect of unripe fruits on ripe fruit removal by birds in Pistacia terebinthus: flag or handicap? Oecologia (1995) 101:55–58.[CrossRef][Web of Science]
Fuentes M, Schupp E. Empty seeds reduce seed predation by birds in Juniperus osteosperma. Evolutionary Ecology. (1998) 12:823–827.
Galil J, Eisikowitch D. Studies on mutualistic symbiosis between syconia and sycophilous wasp in monoecious figs. New Phytology (1971) 70:773–787.[CrossRef]
Gay G, Kerhoas C, Dumas C. Quality of a stress-sensitive Cucurbita pepo L. pollen. Planta (1987) 171:82–87.[CrossRef][Web of Science]
Gillaspy G, Ben-David H, Gruissem W. Fruits: a developmental perspective. The Plant Cell (1993) 5:1439–1451.
Graham C. Use of fruiting trees by birds in continuous forest and riparian forest remnants in Los Tuxtlas, Veracruz, Mexico. Biotropica (2002) 34:589–597.[Web of Science]
Grant BR, Grant PR. High survival of Darwin's finch hybrids: effects of beak morphology and diets. Ecology (1996) 77:500–509.[CrossRef][Web of Science]
Greenberg R, Niven DK, Hopp S, Boone C. Frugivory and coexistence in a resident and a migratory vireo on the Yucatan Peninsula. The Condor (1993) 95:990–999.[CrossRef]
Greenberg R, Foster MS, Marquez-Valdelamar L. The role of the white-eyed vireo in the dispersal of Bursera fruit on the Yucatan Peninsula. Journal of Tropical Ecology (1995) 11:619–639.[Web of Science]
Higashiyama T, Kuroiwa H, Kuroiwa T. Pollen-tube guidance: beacons from the female gametophyte. Current Opinion in Plant Biology (2003) 6:36–41.[CrossRef][Web of Science][Medline]
Howe H, Westley LC. Ecological relationships of plants and animals (1988) Oxford: Oxford University Press.
Hurst LD, Peck JR. Recent advances in understanding of the evolution and maintenance of sex. Trends in Ecology and Evolution (1996) 11:46–52.[CrossRef]
Jang JC, Sheen J. Sugar sensing in higher plants. Trends in Plant Science (1997) 2:208–214.[CrossRef][Web of Science]
Janzen D. Seed predation by animals. Annual Review in Ecology and Systematics (1971) 2:465–492.[CrossRef]
Janzen D. A note on optimal mate selection in plants. American Naturalist (1977) 111:365–371.[CrossRef][Web of Science]
Jolad SD, Wiedhopf RM, Cole JR. Cyto toxic agents from Bursera morelensis Burseraceae deoxy podophyllo toxin and a new lignan 5 demethoxydeoxy podophyllo toxin. Journal of Pharmaceutical Sciences (1977) 66:892–893.[CrossRef][Web of Science][Medline]
de Jong TJ, Batenburg JC, Klinkhamer PGL. Distance-dependent pollen limitation of seed set in some insect-pollinated dioecious plants. Acta Oecologica (2005) 28:331–335.[CrossRef]
Jordano P. Avian fruit removal: effects of fruit variation, crop size, and insect damage. Ecology (1987) 68:1711–1723.[CrossRef][Web of Science]
Jordano P. Polinización y variabilidad de la producción de semillas en Pistacia lentiscus L. (Anacardiaceae). Anales del Jardin Botanico de Madrid (1988) 45:213–231.
Jordano P. Pre-dispersal biology of Pistacia lentiscus (Anacardiaceae): cummulative effects on seed removal by birds. Oikos (1989) 55:375–386.[CrossRef][Web of Science]
Jordano P. Utilización de los frutos de Pistacia lentiscus (Anacardiaceae) por el verderón común (Carduelis chloris). In: Actas I Congreso Nacional de Etología—Arias de Reyna L, Recuerda P, Redondo T, eds. (1990) Cajasur, Córdoba, Spain. 145–153.
Kondrashov AS. Muller's ratchet under epistatic selection. Genetics (1994) 136:1469–1473.[Abstract]
Lee WG, Grubb PJ, Wilson JB. Patterns of resource allocation in fleshy fruits of nine European tall-shrub species. Oikos (1991) 61:307–315.[CrossRef][Web of Science]
Lloyd DG, Webb CJ. Secondary sex characters in plants. Botanical Review (1977) 43:177–216.[CrossRef]
López CML, Márquez J, Murguía G. Técnicas para el estudio del desarrollo en angiospermas (2005) 2nd edn. Mexico City: Universidad Nacional Autónoma de México.
Lovett-Doust J, Lovett-Doust L. Modules of production in a dioecious clonal shrub. Rhus typhina. Ecology (1988) 69:741–750.
Martínez GR. Remoción post-dispersión de semillas y frutos por mamíferos en diferentes grados de perturbación antropogénica de la selva alta perenifolia en la región de Los Tuxtlas, Ver (1996) Universidad Nacional Autónoma de México. PhD Thesis.
Maynard-Smith J, Szathmáry E. Ocho hitos de la evolución: del origen de la vida a la aparición del lenguaje (2001) Barcelona: Tusquets Editores. Colección Metatemas.
Mazzucato A, Olimpieri I, Ciampolini F, Cresti M, Soressi GP. A defective pollen-pistil interaction contributes to hamper seed set in the parthenocarpic fruit tomato mutant. Sexual Plant Reproduction (2003) 16:157–164.[CrossRef][Web of Science]
Mazzucato A, Taddei AR, Soressi GP. The parthenocarpic fruit (pat) mutant of tomato (Lycopersicon esculentum Mill.) sets seedless fruits and has aberrant anther and ovule development. Development (1998) 125:107–114.[Abstract]
Medina JS. Determinación del vigor reproductivo de Stenocereus stellatus (Cactaceae) a lo largo de una cronosecuencia edáfica en un abanico aluvial en Coxcatlán, Valle de Tehuacán. (2000) Universidad Nacional Autónoma de México. Tesis de Licenciatura.
Menges E. The application of minimum viable population theory to plants. In: Genetics and conservation of rare plants—Falk DA, Holsinger KE, eds. (1991) New York, NY: Oxford University Press. 45–61.
Michod RE, Levin BR. The evolution of sex (1988) Sunderland, MA: Sinauer.
Molano-Flores B. Herbivory and concentrations affect calcium oxalate crystal formation in leaves of Sida (Malvaceae). Annals of Botany (2001) 88:387–391.
Müller HJ. The relation of recombination to mutational advance. Mutation Research (1964) 1:2–9.[Web of Science]
Mustart PJ, Cowling RM, Wright MG. Clustering of fertile seeds in infructescences of serotinous Protea species: an anti-predation mechanism? African Journal of Ecology (1995) 33:224–229.[CrossRef][Web of Science]
Nitsch JP. Growth and morphogenensis of the strawberry as related to auxin. American Journal of Botany (1950) 37:211–215.[CrossRef][Web of Science]
Niwa CG, Overhulser DL. Oviposition and development of Megastigmus spermotrophus (Hymenoptera: Torymidae) in unfertilized Douglas-fir seed. Journal of Economical Entomology (1992) 85:2323–2328.
Obeso JR. Fruit and seed production in European holly, Ilex aquifolium L. (Aquifoliaceae). Anales del Jardin Botanico de Madrid (1996) 54:533–539.
Ortiz-Pulido R, Rico-Gray V. The effect of spatio-temporal variation in understanding the fruit crop size hypothesis. Oikos (2000) 93:523–528.
Ortiz-Pulido R, Laborde J, Guevara S. Frugivoría por aves en un paisaje fragmentado: consecuencias en la disponibilidad de semillas. Biotropica (1999) 32:473–488.[Web of Science]
Pascarella JB. Reproductive ecology of Picramnia pentrandra (Picramniaceae) in South Florida. Caribbean Journal of Science (1996) 32:99–104.
Perera CO, Hallett IC, Nguyen TT, Charles JC. Calcium oxalate crystals: the irritant factor in kiwifruit. Journal of Food Science (1990) 55:1066–1069.[CrossRef][Web of Science]
Poulin B, Lefebvre G, McNeil R. Diets of land birds from northeastern Venezuela. The Condor (1994) 96:354–361.[CrossRef]
Reyes SJ, Brachet C, Pérez J, Gutiérrez de la Rosa A. Cactáceas y otras plantas nativas de la Cañada Cuicatlán, Oaxaca (2004) Cuicatlán A. C. México: Universidad Nacional Autónoma de México; CONABIO. Comisión Federal de Electricidad; Sociedad Mexicana de Cactología.
Rice WR, Chippindale AK. Sexual recombination and the power of natural selection. Science (2001) 294:555–557.
Ríos-Casanova L, Valiente-Banuet A, Rico-Gray V. Las hormigas del Valle de Tehuacán (Hymenoptera: Formicidae): una comparación con otras zonas áridas de México. Acta Zoológica Mexicana (n.s.) (2004) 20:37–54.
Ruiz N, Ward D, Saltz D. Calcium oxalate crystals in leaves of Pancratium sickenbergeri: constitutive or induced defence? Functional Ecology (2002) 16:99–105.[CrossRef]
Rzedowski J, Medina R, Calderón G. Las especies de Bursera (Burseraceae) en la cuenca superior del Río Papaloapan (México). Acta Botánica Mexicana (2004) 66:23–151.
Rzedowski J, Medina R, Calderón G. Inventario del conocimiento taxonómico, así como de la diversidad y del endemismo regionales de las especies mexicanas de Bursera (Burseraceae). Acta Botánica Mexicana (2005) 70:85–111.
Sato S, Peet MM, Gardner RG. Formation of parthenocarpic fruit, undeveloped flowers and aborted flowers in tomato under moderately elevated temperatures. Scientia Horticulturae (2001) 90:243–254.[CrossRef]
Sato S, Peet MM, Thomas JF. Determining critical pre- and post-anthesis periods and physiological processes in Lycopersicon esculentum Mill. Journal of Experimental Botany (2002) 53:1187–1195. exposed to moderately elevated temperatures.
Scott PE, Martin RF. Avian consumers of Bursera, Ficus, and Ehretia fruit in Yucatan. Biotropica (1984) 16:319–323.[CrossRef][Web of Science]
Scurlock JH, Mitchell RG, Ching KK. Insects and other factors affecting noble for seed production at two sites in Oregon. Northwest Science (1982) 56:101–107.
Smith C. Plant resistance to insects. (1989) Hoboken, NJ: John Wiley & Sons.
Solomon BP. Frumenta nundinella (Lepidoptera: Gelechiidae): life history and induction of host parthenocarpy. Environmental Entomology (1980) 9:821–825.[Web of Science]
Sorensen FC. The roles of polyembryony and embryo viability in the genetic system of conifers. Evolution (1982) 36:725–733.[CrossRef][Web of Science]
Souza RCOS, Marquete O. Miconia tristis Spring e Miconia doriana Cogn. (Melastomataceae): anatomia do eixo vegetativo e folha. Rodriguésia (2000) 51:133–142.
Lucek LE. SPSS. SPSS version 12·0·0. SPSS 12 Data analysis basics (2003) Northern Illinois University Information Technology Services.
Srivastava GN. Male and female gametophytes and development of the seeds in Bursera delpechiana Poiss. Journal of Indian Botanical Society (1968) 47:53–59.
Stephenson AG. Flower and fruit abortion: proximate causes and ultimate functions. Annual Review of Ecology and Systematics (1981) 12:253–279.[CrossRef][Web of Science]
Stephenson AG, Bertin RI. Male competition, female choice, and sexual selection in plants. In: Pollination biology—Real L, ed. (1983) New York, NY: Academic Press. 109–149.
Stevenson PR. Seed dispersal by woolly monkeys (Lagothrix lagothricha) at Tinigua National Park, Colombia: dispersal distance, germination rates, and dispersal quantity. American Journal of Primatology (2000) 50:275–289.[CrossRef][Web of Science][Medline]
Stevenson PR, Quiñones MJ, Castellanos MC. Guía de Frutos de los Bosques del Río Duda, La Macarena, Colombia. (2000) Asociación para La Defensa de La Macarena-IUCN (The Netherlands), Santafé de Bogotá.
Stevenson PR, Link A, Ramírez BH. Frugivory and seed fate in Bursera inversa (Burseraceae) at Tinigua Park, Colombia: implications for primate conservation. Biotropica (2005) 37:431–438.[CrossRef][Web of Science]
Sunell LA, Healey PL. Distribution of calcium oxalate crystal idioblasts in leaves of taro (Colocasia esculenta). American Journal of Botany (1985) 72:1854–1860.[CrossRef][Web of Science]
Tilton VR, Horner HT Jr. Calcium oxalate raphide crystals and crystalliferous idioblasts in the carpels of Ornithogalum caudatum. Annals of Botany (1980) 46:533–539.
Trainer JM, Hill TC. Avian methods of feeding on Bursera simaruba (Burseraceae) fruits in Panama. The Auk (1984) 101:193–195.
Traveset A. Deceptive fruits reduce insect seed predation in Pistacia terebinthus L. Evolutionary Ecology (1993) a 7:357–361.[CrossRef][Web of Science]
Traveset A. Weak interactions between avian and insect frugivores: the case of Pistacia terebinthus L. (Anacardiaceae). Vegetatio 107/108 (1993) b 191–203.
Valiente BL. Patrones de precipitación en el Valle semiárido de Tehuacán, Puebla, México (1991) Universidad Nacional Autónoma de México. PhD Thesis.
Varoquaux F, Blanvillain R, Delseny M, Gallois P. Less is better: new approaches for seedless fruit production. Trends in Biotechnology (2000) 18:233–242.[CrossRef][Web of Science][Medline]
Verdú M, García-Fayos P. Ecological causes, function, and evolution of abortion and parthenocarpy in Pistacia lentiscus (Anacardiaceae). Canadian Journal of Botany (1998) 76:134–141.[CrossRef]
Verdú M, García-Fayos P. The effect of deceptive fruits on predispersal seed predation by birds in Pistacia lentiscus. Plant Ecology. (2000) 156:245–248.
Volk GM, Lynch-Holm VJ, Kostman TA, Goss LJ, Franceschi VR. The role of druse and raphide calcium oxalate crystals in tissue calcium regulation in Pistia stratiotes leaves. Plant Biology (2002) 4:34–45.[CrossRef]
Ward D, Spiegel M, Saltz D. Gazelle herbivory and interpopulation differences in calcium oxalate content of leaves of a desert lily. Journal of Chemical Ecology (1997) 23:333–346.[CrossRef][Web of Science]
Webb MA. Cell-mediated crystallization of calcium oxalate in plants. The Plant Cell (1999) 11:751–761.
Yadegari R, Drews GN. Female gametophyte development. The Plant Cell (2004) 16:S133–S141.
Young LW, Wilen RW, Bonham-Smith PC. High temperature stress of Brassica napus during flowering reduces micro- and megagametophyte fertility, induces fruit abortion, and disrupts seed production. Journal of Experimental Botany (2004) 55:485–495.
Zangerl AR, Berenbaum MR, Nitao JK. Parthenocarpic fruits in wild parsnip: decoy defence against a specialist herbivore. Evolutionary Ecology (1991) 5:136–145.[CrossRef][Web of Science]
Ziv Y, Bronstein JL. Infertile seeds of Yucca schottii: a beneficial role for the plant in the yucca-yucca moth mutualism? Evolutionary Ecology (1996) 10:63–76.[CrossRef][Web of Science]
Zohary D. Unconscious selection and the evolution of domesticated plants. Economic Botany (2004) 58:5–10.[CrossRef][Web of Science]
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