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2Centro de Investigación Científica de Yucatán, A.C., A.P. 87, Cordemex 97310, Mérida, Yucatán, México; and 3Instituto de Ecología, Universidad Nacional Autónoma de México, A. P. 70-275, México, D.F. 04510, México
Received for publication June 26, 1998. Accepted for publication November 16, 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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30% of the flowers and >70% of the capsules of A. aurantiaca showed herbivore damage, but its impact changed depending on the type of forest habitat. Flower and fruit herbivores caused more damage in closed forest than in gaps, and this difference was even bigger under the insecticide treatment. Insecticide effectiveness varied depending on the type of forest patch. The highest herbivore impact on seeds was found in the mature forest without insecticide treatment, where most seeds were destroyed. The percentages of seed damage reported here show that predispersal predation is limiting seedling recruitment, especially in mature forest. Other possible explanations might be differences in insect composition, densities, and behavior between gaps and mature forest.
Key Words: Acanthaceae • Aphelandra aurantiaca • florivory • herbivory • insect exclusion • Los Tuxtlas rainforest • México • seedling recruitment
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, 1976
; Heithaus, Stashko, and Anderson, 1982
; Louda, 1982a
, b
; Horvitz and Schemske, 1984
, 1994
; Brody, 1992
; Louda and Potvin, 1995
). Therefore, seed reduction by insects clearly has the potential of imposing a limit on plant recruitment and affecting population dynamics. Although a wide variety of plants experience a great amount of predispersal damage, experimental data that evaluate the importance of different factors which limit seed production are still sparse (Louda and Potvin, 1995
).
Spatial and temporal heterogeneity in the communities of herbivores and seed predators affect demographic parameters of plants. In two tropical understory species, seed predators were important factors explaining differences among stands in the proportion of seeds present at the time of seed dispersal (Heithaus, Stashko, and Anderson, 1982
; Horvitz and Schemske, 1984
).
The opening of a gap in the canopy of tropical rainforests provokes changes in the microenvironment that have an impact on different life cycle stages of plant species (Whitmore, 1975
; Martínez-Ramos, 1985
; Horvitz and Schemske, 1986
, 1995
). Flower, fruit, and seed production as well as the number of reproductive individuals differ between gaps and mature forest. Differences in the amount of resources as well as differences in biotic interactions have been cited as contributing factors (Piñero and Sarukhán, 1982
; Levey, 1988
; Martínez-Ramos, Sarukhán, and Piñero, 1988
; Horvitz and Schemske, 1994
).
Although the number of herb species in the rainforest understory is small (Smith, 1987
), this growth form is an important component of ground cover. Understory herbs complete their life cycle in an environment where light is a limited resource. Some authors have emphasized that understory herbs, which persist in shade, require long periods of vegetative growth to obtain sufficient resources for sexual reproduction (Smith, 1987
; Mulkey, Wright, and Smith, 1993
). Under these conditions the allocation of resources to reproduction is expected to be particularly efficient. One way to achieve it is by avoiding losses such as those caused by insect consumption. There is evidence of higher concentrations of secondary defense compounds in leaves of individuals growing in gaps compared to those under mature forest (Coley, 1983
; Coley, Bryant, and Chapin, 1985
), but there is no information on this aspect for reproductive tissue.
Environmental heterogeneity generated by gap openings has an impact on the demography of the rainforest understory herb Aphelandra aurantiaca (Acanthaceae). A reproductive individual growing in a gap produces, on average, almost twice the ovules produced in mature forest (Calvo-Irabién, 1997
). If differences in the number of recruited seedlings were due only to these fecundity differences, one would expect twice the number of seedlings in gaps compared to closed forest. Nevertheless, the ratio of recruited seedlings per reproductive individual is 1:17 in mature forests vs. gaps (Calvo-Irabién, 1997
). Germination percentages were not significantly different between gaps and mature forest (Calvo-Irabién, 1989
), so predispersal predation seems to be a plausible explanation for the observed recruitment differences between gaps and mature forest. The objective of this work was to evaluate the extent to which damage to flowers, fruits, and seeds in A. aurantiaca reduces the number of seeds available for seedling establishment.
The present study had three purposes: (1) to describe and quantify flower, fruit, and seed predation in A. aurantiaca under natural conditions, (2) to assess the influence of habitat variation, due to gap opening, on predispersal insect predation, and (3) to evaluate experimentally, by insecticide application, the effect of herbivore exclusion on fruit and seed damage under gaps and mature forest.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, Ibarra-Manríquez and Sinaca-Colin (1987)
, Dirzo and Miranda (1991)
, and González-Soriano, Dirzo, and Vogt (1997)
.
Aphelandra aurantiaca is an abundant understory herb, widespread in the regeneration mosaic of the rainforest. It is among the five dominant herb species in the Los Tuxtlas understory. A. aurantiaca has protogynous, hermaphroditic tubular flowers (between five and 45 flowers) arranged in a spike with big flower bracts (Wasshausen, 1975
). Flowers mature asynchronously from top to bottom. Flowers are yellow as buds and red-orange when opened and are exposed to pollinators for 1–3 d. On the 2nd and 3rd d the corolla and reproductive structures are less turgid and the colors are less bright (Islas-Luna, 1995
). The flowers produce an average of 10.14 ± 1.0 µL of nectar, with a mean sugar concentration of 19.24 ± 0.89% (Islas-Luna, unpublished data). Flowers are self-compatible and pollinated by the hummingbird Phaetornis superciliosus, bumble bees, and butterflies (Toledo, 1975
; Islas-Luna, 1995
). The fruit is an ovoid capsule with a constant number of four seeds (2–4.5 mm diameter). Seed dispersal is ballistic. At the Los Tuxtlas rainforest reserve, individuals flower from September through February with a peak in December. Fruit maturation takes 1 mo. Approximately 2 mo later, seeds are dispersed during the dry season, starting in March. Germination takes place mainly during June and July (Calvo-Irabién, 1997
).
Flower and fruit damage under natural conditions in gaps and mature forest
To describe the magnitude and variability in the mean percentage of damaged flowers and fruits we systematically sampled inflorescences and immature and fully developed infructescences (prior to seed dispersal) of this understory herb. The effect of habitat on predispersal damage was evaluated with collections of inflorescences and infructescences in treefall gaps (sensu Brokaw, 1982
) and in mature forest (forest patches with at least 30 yr since gap opening). A. aurantiaca usually produces one inflorescence per reproductive individual, therefore each sample consisted of at least 25 individuals in gaps and 25 in mature forest. Immediately after collection inflorescences were carefully dissected and three flower-age categories were defined: young flower bud (yellow), mature flower bud (orange-yellow), and opened flower (red-orange) (Fig. 1). Flowers were considered damaged when either reproductive structures (stigma and/or stamens) or corolla, or both, showed any sign of herbivory, regardless of the amount of damage. Preliminary statistical comparisons for each flower category indicated no effect of inflorescence age (inflorescences were classified as young, mature, and old based on the proportions of young, mature, and old flowers) on average percentage of damage, either in gaps or mature forest (ANOVA tests, all P values 
0.05; data not shown). Therefore, we pooled the data from different-age inflorescences. Statistical differences between gaps and mature forests in the percentage of damaged flowers per inflorescence were analyzed using t tests.
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). We have no measure of the number of infructescences totally destroyed by predispersal herbivores, so our estimate of damage under natural conditions is probably an underestimate.
Insecticide application experiment
A field experiment was designed to quantify an insect's effect on the ovary-seed transition and its variation between forest habitats. Twelve forest sites were selected, six in gaps and six in mature forest. In these sites, we tagged all reproductive A. aurantiaca individuals presenting an undamaged inflorescence bud. For both gaps and mature forest, three sites were randomly selected as controls; in the other three, inflorescence buds were sprayed with insecticide dissolved in water at the recommended rate. We used Nuvacron® (dimethyl phosphate of 3-hydroxy-N-methyl-cis crotonamide: Novartis, México, D.F., México), a contact and systemic insecticide. Inflorescences were sprayed every 5 d until the end of the experiment (1 mo). In order to reduce variation in ovule development due to pollination, we sampled 5–10 mature flower buds and removed the stamens before pollen was liberated. Manual pollinations were then performed using pollen from flowers of other individuals. In each infructescence, these pollinated flowers were marked with red nail polish on the bract. The infructescences of all individuals were checked every 5 d, and treatment effectiveness was assessed at the end of the fruiting period. When capsules were fully developed, but prior to dispersal, infructescences were collected. In contrast to the technique used for evaluating natural damage, this methodology allowed us to quantify those infructescences that were fully destroyed by herbivores during infructescence development. Immediately after collection, mature infructescences were carefully dissected in the laboratory. Fruits were categorized as previously described. Additionally, capsules were opened and seeds were categorized as undamaged, damaged, and aborted or partially developed. The effect of forest habitat and insecticide application on the mean percentage of damaged fruits per infructescence was analyzed using a two-way ANOVA. Post hoc multiple comparisons among means were performed using Tukey's test (Sokal and Rohlf, 1995
).
For all statistical analyses, data were arcsine transformed to improve normality and meet the criterion of equal variances within groups (Sokal and Rohlf, 1995
). All parametric tests were performed on transformed data.
While dissecting inflorescences and infructescences, the insects in or on flowers, immature and mature capsules, and seeds were collected and preserved in 70% ethanol for later determination. In some cases, the type of damage caused by insects was determined by field observation.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Herbivore damage in different flower parts was not randomly distributed (
2 = 62.7; df = 4, P < 0.05). Flowers with a damaged corolla, pistil, and stamens were more frequent. For young buds, damage in the corolla and reproductive structures was higher than expected, while for opened flowers only damaged corollas were more abundant compared with other flower stages (Table 1). Predation on reproductive structures due to flower herbivory has a direct impact on loss of reproductive potential.
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After fertilization, fruit damage by herbivores can occur at different times during the development of the ovary into a capsule. The mean percentage of damage in A. aurantiaca capsules was significantly affected by infructescence age (F1,132 = 62.1, P = 0.0001). There was no significant difference in the proportion of damaged capsules between mature forest and gaps (F1,132 = 1.34, P = 0.25). Likewise, the interaction of these two factors was nonsignificant (F1,132 = 0.06, P = 0.80). More than 40% of the total developing ovaries were attacked by herbivores in immature infructescences (Fig. 2a, b). Abortion was another cause of fruit loss. Herbivore damage was higher in immature than in fully developed capsules, where <5% of the capsules showed signs of herbivory (Fig. 2a, b).
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Insecticide application experiment
The mean percentage of damaged fruits per infructescence was significantly affected by the type of forest patch (F1,355 = 52.81, P < 0.0001) and by the application of insecticide (F1,355 = 36.55, P < 0.0001). The interaction of these two factors was also significant (F1,355 = 14.06, P = 0.0001). In the control, >70% of the capsules in an infructescence showed herbivore damage (Fig. 3). This result is higher than those reported from infructescence collections in different forest sites under natural conditions (Fig. 2). In contrast with the results obtained from unmanipulated infructescences (see above), with the application of insecticide the type of forest habitat did show a small significant effect on the mean percentage of damaged fruits per infructescence. This difference in results was likely due to the different methodologies used for evaluating herbivore damage. Under natural conditions samples were taken at different times, while for the insecticide treatment flowers were hand pollinated and a cohort of flowers was followed, which gives more control over the quantification of the losses due to herbivory.
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Relative variation in the percentage of damaged capsules at the individual level was highest in gaps with insecticide (CV = 137%), where one-half of the individuals showed undamaged capsules and 25% had infructescences with all the capsules damaged. In contrast, herbivores destroyed all the capsules in most plant infructescences in the mature forest plots without insecticide treatment (CV = 38%; Fig. 3).
As a consequence of total capsule damage and additional herbivory of seeds in undamaged capsules, the mean percentage of damaged seeds per infructescence was higher than the percentage of damaged capsules. The highest herbivore impact on seeds was found in the mature forest without insecticide treatment, where most seeds were destroyed (99.7 ± 10.5%). Gaps with insecticide showed the lowest mean percentage of damaged seeds (48.3 ± 4.2%). Intermediate levels of predispersal herbivory were found in gaps without insecticide (80.0 ± 8.7%) and mature forest with insecticide (86.9 ± 9.6%). Similar to what was found for capsule damage, insecticide effectiveness on seed damage was different depending on the forest habitat. In gaps, herbivore exclusion decreased seed damage by 40%, while in the mature forest this decrease was 13%.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Augspurger, 1984
; Levey, 1988
; Horvitz and Schemske, 1994
). In this study we showed that predispersal damage in A. aurantiaca is high, but its impact changed depending on the type of forest habitat. Flower and fruit herbivores caused more damage in closed forest than in gaps, and this difference was even bigger with insecticide application. One possible explanation is that due to a higher amount of light in gaps and under a smaller load of insects because of insecticide application, individual plants growing in gaps will have a better chance of compensating for herbivore damage or avoiding herbivory by higher concentrations of chemical defenses, than plants growing in mature forest (McKey, 1974
, 1979
; Coley, 1983
; Bazzaz, 1984
; Coley, Bryant, and Chapin, 1985
). Other possible explanations might be related with differences in insect composition, densities, and behavior between gaps and closed forest.
The impact of predispersal predation on ovule losses starts in flowers. Approximately 30% of the flowers in A. aurantiaca were damaged, and at least half of these flowers had damaged pistils. Flower damage in A. aurantiaca was intermediate compared with that reported for other herbaceous species. The flowers of two Acanthaceae species (Aphelandra golfodulcensis and Justicia aurea) showed damage in 40% of pistils and stamens (McDade and Kinsman, 1980
). Flower herbivory was seen in 59.4% of Bauhinia ungulata flowers in a tropical moist forest in Costa Rica. Flowers suffered more than one type of damage, with most of the damage being internal; 22.8% of opened flowers had the pistil destroyed and 9.8% of the flowers had other types of external damage (Heithaus, Stashko, and Anderson, 1982
). Beattie, Breedlove, and Ehrlich (1973)
found <4.7% of the flowers damaged in Frasera speciosa, a perennial understory herb of temperate forests, while in this same forest, Lupinus amplus, another herb with the same habit, had between 50 and 79% of the flowers damaged by butterfly larvae (Breedlove and Ehrlich, 1968
).
In A. aurantiaca, the highest probability of insect damage was found in the capsules of immature infructescences, probably due to the tenderness of the capsule in this stage and/or its higher moisture content. Once the capsule is fully developed, it takes 1–2 wk for it to harden (personal observation), and it has been shown that tissue tenderness is important for herbivory (Janzen, 1971
, 1976
; Evans, Smith, and Gendron, 1989
; Warren, 1989
; Lalonde and Roitberg, 1992
; Greig, 1993
). However, in other studies the proportion of seeds lost to predators was higher in mature than in immature pods (Heithaus, Stashko, and Anderson, 1982
).
Although most of the ovule losses found during ovary development were caused by herbivory, a certain percentage (between 10 and 25%) of the ovules aborted. There can be a variety of causes for abortion in plants, including herbivore damage, the genetic quality of the offspring, limiting resources, and inadequate pollination (Stephenson, 1981
; Shivanna, 1982
; McDade, 1985
; Warren, 1989
; Martin and Lee, 1993
). Elucidation of these mechanisms in A. aurantiaca will require further study.
There was a high variation in the mean percentage of damaged fruits among individuals, and other factors than those considered in this study, such as genotype, differential distribution, and behavior of herbivores, and differences in abundance and distribution of flowering plants (Janzen, 1971
, 1975
; Augspurger, 1980
, 1981
; Auld, 1986
) might also have influenced the loss of potential ovules in the predispersal phase.
Predispersal predation of capsules and seeds of A. aurantiaca was high, with >75% of them lost due to herbivore damage. This result agrees with other studies. Heithaus, Stashko, and Anderson (1982)
found that in Bahuinia ungulata the proportion of seeds lost to predators was 27.7%, and herbivores destroyed 6.9% of the ovules while they were still developing. Half of the capsules of Bartsia alpina, a perennial arctic-alpine herb, were attacked by insects (Molau, Eriksen, and Knudsen, 1989
). Green and Palmbald (1975)
found that 58.0–88.9% of seeds were destroyed in two prairie species of herbaceous perennial legumes. In Baptista australis, a long-lived prairie perennial, 65–100% of the seeds were infested by herbivores (Evans, Smith, and Gendron, 1989
).
When insecticide was applied, there was a significant reduction in the average percentage of damaged fruits and seeds in gaps (40%) but not in the mature forest (12%). To our knowledge, no other studies have compared insect damage between different rainforest habitats. Compared with other studies the insecticide was not too effective in excluding herbivores. Louda and Potvin (1995)
found that insecticide decreased the total amount of undamaged seeds by 170–310% for Cirsium canescens a perennial prairie herbaceous species. Horvitz and Schemske (1984)
found that for the rainforest understory herb Calathea ovandensis, the exclusion of Diptera larvae increased mean seed production by 33–66%, depending on the presence of ants. For two species of Haplopappus, Louda (1982a
, 1983)
found increases of 53 and 60% in the percentage of seeds produced. At Los Tuxtlas rainforest, insecticide effectiveness might be reduced by the heavy and frequent rains that occur during the flowering and fruiting period of A. aurantiaca. Other studies have reported a poor effect of insecticide application on excluding insects, and in some cases, it even increases insect abundance or the most aggressive herbivores are not excluded (Waloff and Richards, 1977
).
On an annual basis, A. aurantiaca rarely produces a mean of more than a hundred potential ovules (83.7 ± 13.4 ovules in gaps and 48.3 ± 0.8 ovules in mature forest; Calvo-Irabién, 1989
), so the percentages of seed damage reported here (80% for gaps and 99.7% in mature forest) show that predispersal predation is limiting recruitment, especially in mature forest. Based on the present results, seedling density for this species is expected to be 20 times higher in gaps than in mature forest, a figure close to that observed under natural conditions in the Los Tuxtlas understory. These results show that herbivores consuming flowers, fruits, and seeds have an important impact on the abundance and spatial distribution of A. aurantiaca in the forest understory.
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FOOTNOTES |
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4 Author for correspondence (e-mail: lumali@cicy.cicy.mx).
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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and mature forest sites 