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Keywords:

  • Atlantic forest;
  • conservation biology;
  • Ficus;
  • forest regeneration;
  • frugivory;
  • fruit bats;
  • Phyllostomidae;
  • Piper;
  • restoration ecology;
  • seed dispersal

ABSTRACT

  1. Top of page
  2. ABSTRACTRESUMO
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGMENTS
  7. LITERATURE CITED

Previous tests with essential oils from ripe chiropterochoric fruits suggested they can be used to attract and capture fruit-eating bats inside forest remnants. Here we evaluated the efficiency of these oils to attract frugivorous bats to open areas. We performed field tests with artificial fruits impregnated with essential oils of the genera Piper or Ficus that were attached to two groups of mist-nets set 50 m outside the border of a forest remnant. One group of artificial fruits received the corresponding oil isolated through hydrodistillation and the other received water only. Fruits with oils attracted significantly more fruit-eating bats, especially Artibeus lituratus that regularly crosses open habitats to reach other forest remnants. The highly significant attraction of A. lituratus by the oil of Piper was unexpected, since this bat is a specialist on Ficus fruits. We hypothesize that in habitats with no fruit available it is possible to attract frugivorous bats with the odor of several ripe fruit species. Furthermore, we verified that almost half of the individuals captured defecated seeds, indicating that the oils also attract recently fed bats, even when their preferred food is available nearby. This technique potentially may increase seed rain at specific locations, being particularly promising to restoration projects.

RESUMO

Estudos anteriores realizados com óleos essenciais extraídos de frutos quiropterocóricos maduros sugerem que estes podem ser utilizados para atrair e capturar morcegos frugívoros no interior de remanescentes florestais. No presente trabalho nós avaliamos a eficiência destes óleos na atração de morcegos frugívoros para áreas abertas por meio de testes com dois grupos de redes-de-neblina instaladas a 50 m de distância de um fragmento florestal. Todas as redes receberam um fruto artificial (gêneros Piper ou Ficus) em sua porção mediana, mas apenas um dos grupos recebeu o óleo correspondente isolado por hidrodestilação; o outro recebeu somente água destilada. Os frutos com óleo atraíram significativamente mais morcegos frugívoros, especialmente Artibeus lituratus. A atração altamente significativa desta espécie pelo óleo de Piper foi inesperada, considerando que este morcego é especialista em frutos de Ficus. Conseqüentemente, nós sugerimos que em hábitats com nenhum fruto disponível é possível atrair morcegos frugívoros com o odor de diversas espécies de frutos maduros. Além disso, quase a metade dos morcegos capturados defecou sementes, indicando que os óleos também atraem indivíduos que se alimentaram recentemente, até mesmo quando seu alimento preferencial encontra-se disponível nas proximidades. Esta técnica tem o potencial de incrementar a chuva de sementes em locais específicos, sendo particularmente promissora para projetos de restauração florestal.

Fruit consumption and seed dispersal through bat feces are fundamental for the reproductive success of the consumed plants, the maintenance of forests, and the recovery of degraded areas (Fleming & Sosa 1994, Garcia et al. 2000). Through seed dispersal bats influence the structure of the vegetation of the plant species they consume and disperse (Fleming & Heithaus 1981). Such service is favored by the rapid passage of seeds through the gut of frugivorous bats (approximately 30 min for some species) (Fleming 1988), as well as the large distances that bats often travel, visiting different habitats and sites in a single night (e.g., Fleming 1988, Estrada & Coates-Estrada 2002, Bernard & Fenton 2003).

In the Neotropical region fruit-eating bats belong to the Family Phyllostomidae, which has 160 species (Simmons 2005) with high capacity of environmental perception. The importance of odor in the location of food resources by phyllostomid bats has been cited in the literature since the middle of the twentieth century (e.g., Mann 1951, van der Pijl 1957, Fleming 1988). Some authors (Rieger & Jacob 1988, Thies et al. 1998, Mikich et al. 2003, Korine & Kalko 2005) have shown that olfaction was the primary sense employed by some species to detect and/or locate ripe fruits. In addition, Mikich et al. (2003) verified that it was possible to attract Carollia perspicillata (short-tailed fruit bat) using just the essential oil isolated from ripe fruits of Piper gaudichaudianum Kunth (Piperaceae).

The fruit-eating bats of the genera Artibeus, Carollia and Sturnira exhibit a strong preference for a restricted group of chiropterochoric fruits. According to previous studies (e.g., Bonaccorso 1979, Fleming 1985, Palmerim et al. 1989, Handley et al. 1991, Kalko et al. 1996, Iudica & Bonaccorso 1997, Wendeln et al. 2000), Artibeus lituratus (great fruit-eating bat) prefers fruits of Ficus spp., while Carollia perspicillata prefers those of Piper spp., and Sturnira lilium (little yellow-shouldered bat) those of Solanum spp. Such preferences were also observed in the study area (Mikich 2002).

Based on the results obtained by Mikich et al. (2003), the use of the essential oils of these fruit species has the potential to attract fruit-eating bats to open or degraded forest areas, improving seed rain from bat feces and, consequently, accelerating plant succession. In this study we present the results of field tests designed to measure the efficiency of essential oils in the attraction of fruit-eating bats to agricultural fields surrounding Atlantic Forest habitat islands in southern Brazil.

METHODS

  1. Top of page
  2. ABSTRACTRESUMO
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGMENTS
  7. LITERATURE CITED

Study area.— We conducted this study in an agricultural field (corn and soybean) located next to the Parque Estadual Vila Rica do Espírito Santo (PEVR) (23°55′ S −51°57′ W), Fênix, Paraná state, Southern Brazil. The PEVR is a small (354 ha) Atlantic Forest isolate limited by cultivated fields and two large rivers, the Ivaí and the Corumbataí. The relief is smooth and the mean altitude is 330 m; climate is Cfa (classification after Koeppen) with annual mean temperatures between 16°C and 29°C (ITCF 1987, Mikich & Oliveira 2003). Annual rainfall ranges between 1400 and 1500 mm, mostly concentrated between December and March (Mikich & Oliveira 2003).

At present, the study region, which was once covered by continuous forest, holds few forest isolates up to 800 ha surrounded by extensive areas of agriculture (especially corn and soybean) and degraded riparian forests. The limits of the PEVR with the cultivated areas that surround it are very abrupt, with no buffer zone, and the fields themselves lack bushes or trees. Detailed descriptions of our study area and its plant species, including phenological data, can be found in Mikich and Silva (2001) and Mikich and Oliveira (2003).

Plant species and phenology.— The family Piperaceae (pepper family) has six genera and approximately 2000 species distributed both in the tropical and subtropical regions (Judd et al. 1999). Pepper plants of the pantropical genus Piper are shrubs or small trees relatively common as pioneer species in regeneration areas, but they also occur in forest understory, edges, and gaps (Fleming 1988, Thies et al. 1998). Piper fruits are typically chiropterochorous: they exhibit strong odor and dull color, are presented beyond the foliage (van der Pijl 1957, Yuncker 1972), and some species ripen in late afternoon (Thies et al. 1998, Thies & Kalko 2004, S.B.M. pers. obs.). In the PEVR the genus Piper has nine species distributed along roads, trails, forest interior, and edges. Piper gaudichaudianum, one of the most abundant species in this preserve, has curved fruits measuring 100 × 6 mm, holding up to 2000 seeds of 1.0 × 0.8 mm. It has two annual peaks of fruit availability, the most intense one between November and February (wet season) and the other between May and July (dry season) (Mikich & Silva 2001). Piper crassinervium, less abundant in the study area, has fruits measuring 100 × 10 mm, containing up to 3000 seeds of 1.3 × 1.5 mm. It also exhibits two annual peaks of fruit production, the first between March and May (beginning of the dry season), and the other between September and November (beginning of the wet season) (Mikich & Silva 2001).

The genus Ficus exhibits intrapopulation as well as intertree asynchronous flowering and fruiting, yet there is strong intratree synchronous flowering and fruiting, which produces a large fruit crop over a brief period of time (Morrison 1978, Janzen 1979, Cosson et al. 1999, Wendeln et al. 2000). According to Mikich and Silva (2001) there are six Ficus species in the PEVR, all low to medium density forest trees. Ficus insipida is one of the more common fig species in the study region. It has fruits measuring 24 × 23 mm, containing 100 to 300 seeds of 2.1 × 1.4 mm each. Fruits of this and/or other fig species are available all year round in the study region (Mikich & Silva 2001).

Essential oil isolation.— We collected ripe chiropterochoric fruits in the PEVR, isolated the essential oils through hydrodistillation using a modified Clevenger for 4 h, and stored the oils in freezed vials until the field tests. We used the essential oils of Piper gaudichaudianum in September 2002, October 2002 and January 2003, P. crassinervium in July 2002, and F. insipida in August 2002 and April 2003. The oils were always diluted in distilled water (approximately 17.5 mg/ml), and different species were used according to their availability in the laboratory.

Field experiment.— We employed ten mist-nets set 50 m away from the forest edge and parallel to it to evaluate the efficiency of the essential oils in the attraction of fruit-eating bats to open areas outside a forest remnant (PEVR). The nets were grouped into two sets of five, with 50 m between the sets, in order to verify whether the application of the oil in one set would produce a significant (χ2 test, df = 1) higher capture of fruit-eating bats. To avoid bias, each night a different set of mist-nets received the oil.

We shaped artificial fruits of the plant species tested in green foam and put one in the midpoint of each net. All nets, in both sets, received one artificial fruit but the fruits were impregnated with the corresponding essential oil in only one set; fruits of the other set were impregnated with distilled water only.

Since all mist-nets had an artificial fruit as a visual cue, we were able to measure the effect of odor alone in the capture of bats. We opened the nets (12 × 2.5 m, 60 mm mesh) at sunset, checked them every 15 min, and closed them after 6 h of exposure. We performed the tests in July (one night), August (two), September (two) and October 2002 (three), plus January (one) and April 2003 (three), totaling 12 nights of test or 21600 m2.h (Straube & Bianconi 2002) of capture area. This capture schedule (months and number of nights) was determined by the availability of intercrop bare soil (we were not able to work when crops were mature), as well as climatic conditions since rain probably interferes with the oil efficiency. Consequently we conducted no test during rainy nights.

All captured bats were identified to species and had the net set recorded. Individuals were kept inside cotton bags for at least 2 h to collect fecal samples. Each sample was examined for seeds, which were isolated and identified based on a reference collection of the study area (Mikich 2001, 2002).

RESULTS

  1. Top of page
  2. ABSTRACTRESUMO
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGMENTS
  7. LITERATURE CITED

We had captured 112 frugivorous bats belonging to six species: Artibeus lituratus, A. jamaicensis, A. fimbriatus, Sturnira lilium, Carollia perspicillata, and Chiroderma villosum. All species except for A. lituratus (n= 102, 91% of all captures) were represented by few individuals (Table 1), thus preventing analysis of data for each species separately. All bat taxa, however, had higher capture rates in nets with oils. When all species were pooled, 79 fruit-eating bats were captured in nets with oil, while nets without oil captured only 33 (χ2= 18.89, P < 0.0001).

Table 1. Number of frugivorous bats captured during field tests with essential oils of chiropterochoric fruits performed between July 2002 and April 2003 in a cultivated field next to the Parque Estadual Vila Rica do Espírito Santo, Parana state, Brazil.
Bat speciesPlant species
Piper gaudichaudianumP. crassinerviumFicus insipidaTotal
With oilWithout oilWith oilWithout oilWith oilWithout oil
Artibeus lituratus287114223102
Artibeus jamaicensis 1000 1 0  2
Artibeus fimbriatus 0000 1 1  2
Sturnira lilium 0021 0 0  3
Carollia perspicillata 1000 1 0  2
Chiroderma villosum 0000 1 0  1
Total307324624112

For A. lituratus, we performed a specific analysis of the tests with Ficus insipida and Piper gaudichaudianum (number of captured individuals 65 and 35, respectively). Of the 65 A. lituratus captured during the tests with F. insipida, 42 (65%) were captured in nets with oil and 23 (35%) in nets without oil, indicating a significant (χ2= 5.55, P= 0.0184) preference for the former. Moreover, of the 35 individuals captured with P. gaudichaudianum essential oil, 28 (80%) were captured in nets with oil and only seven in nets without it (χ2= 12.60, P= 0.0004). Therefore, the use of essential oils of chiropterochoric fruits increased bat capture rate.

Forty-seven out of the 102 A. lituratus captured during the tests defecated one or more seeds (up to 100) inside the cotton bags. Seven (58%) of the 12 fecal samples from bats captured during the tests with the essential oil of P. gaudichaudianum contained seeds of Ficus spp. (Ficus insipida, F. glaba Vell. or F. luschnathiana Miq.), four samples (33%) contained seeds of Cecropia glaziouii Sneth., and one (9%) of Maclura tinctoria (L) D. Don ex Steud. Consumption of Ficus seeds by A. lituratus was also observed during the tests with F. insipida oil, since 25 (71%) out of 35 fecal samples examined had seeds of Ficus spp. (Ficus insipida or F. guaranitica), five (14%) had seeds of Maclura tinctoria, three (9%) of Cecropia pachystachya Trécul, and two (6%) of Piper sp. (Piper hispidum Sw. or P. gaudichaudianum).

DISCUSSION

  1. Top of page
  2. ABSTRACTRESUMO
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGMENTS
  7. LITERATURE CITED

Although the use of the essential oils had produced differential capture rates, the highly significant attraction exhibited by P. gaudichaudianum oil upon A. lituratus was not expected since Piper spp. are not the preferred food item of this bat genus. Furthermore, when the essential oil of P. gaudichaudianum was previously used in tests performed within the PEVR (see Mikich et al. 2003), 67 Artibeus spp. were captured but exhibited no positive response to the oil. Therefore, we believe that in habitats with no zoochoric fruit available, as in the agricultural land that surrounds the PEVR, fruit-eating bats are attracted by the odor of several fruit species, and not just preferred fruits. Inside the forest remnants, due to the higher diversity of chiropterochoric fruit, bats may be more selective with regard to food. An alternative explanation would be a temporary unavailability of Ficus fruits within the PEVR when the three tests with P. gaudichaudianum oil were performed. Analysis of fecal samples of A. lituratus captured during the tests with P. gaudichaudianum, however, revealed that most samples contained seeds of three of the six Ficus species that exist in the PEVR. Additionally, high levels of fig consumption by A. lituratus observed during the tests with the oil of F. insipida proved that one or more species of Ficus were available during the tests. The presence of seeds in the fecal samples of bats captured during the tests with the oils of chiropterochoric fruit species indicates that recently fed bats are attracted by such baits, making the proposed technique potentially effective in forest restoration programs.

Because fig production is asynchronous within populations and, in our study region, trees occur at low density in different forest fragments (Mikich & Silva 2001), we believe that the high number of the fig specialist (A. lituratus) captured in the cultivated field was associated with a foraging pattern that included frequent movements within and between forest fragments. The results obtained for Carollia perspicillata by Bianconi (2003), who conducted a bat-banding program in this region, revealed that this species has small feeding areas, probably in response to the abundance of preferred food items, like Piper spp. (Mikich & Silva 2001), inside the forest isolates. Such behavior could explain why few C. perspicillata were captured during the field tests, despite this species being common in the study region.

Although the tests were performed inside an agricultural field only 50 m away from a forest border, we believe the results may also be valid for larger distances since bats (especially larger species such as Artibeus spp.) frequently move between forest fragments (Cosson et al. 1999, Estrada & Coates-Estrada 2002, Bianconi et al. 2004). Preliminary results from other trials suggest that the oils attract bats even when applied as far as 700 m away from the forest.

The essential oils of chiropterochoric fruit species can be used to attract frugivorous bats to specific locations within an altered matrix, especially those species that often cross open areas to reach other forest isolates in the search of food and other resources. This finding could significantly increase the qualitative and quantitative seed rain within these habitats. Foraging bats attracted by the odor of a supposed food source (essential oil) would spend some time flying around the odor source, increasing the probability of defecating in the vicinity (considering that seed passage is relatively fast and that recently fed bats are attracted by the essential oils). Consequently, the proposed technique has potential use for the restoration of degraded forests within agricultural or pasture land, where the seed bank is usually poor. Future isolation of the active ingredients will allow the wide use of the proposed technique in forest restoration programs.

ACKNOWLEDGMENTS

  1. Top of page
  2. ABSTRACTRESUMO
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGMENTS
  7. LITERATURE CITED

We thank Mater Natura—Instituto de Estudos Ambientais and Fundo Estadual do Meio Ambiente for providing financial support to conduct these experiments; Instituto Ambiental do Paraná and Mr. A. Santiago Lago for permitting the development of this study in their properties; and F. Rocha-Mendes, C. E. Conte, J. Ricetti, and R. A. Machado for helping in the field work. We also thank two anonymous reviewers and Elisabeth Kalko for criticisms and suggestions on earlier drafts. The authors declare that the experiments comply with the current Brazilian laws.

LITERATURE CITED

  1. Top of page
  2. ABSTRACTRESUMO
  3. METHODS
  4. RESULTS
  5. DISCUSSION
  6. ACKNOWLEDGMENTS
  7. LITERATURE CITED
  • Bernard, E., and M. B. Fenton. 2003. Bat mobility and roosts in a fragmented landscape in central Amazonia, Brazil. Biotropica 35 (2): 262277.
  • Bianconi, G. V. 2003. Diversidade e deslocamentos de morcegos (Mammalia, Chiroptera) em remanescentes florestais do noroeste do Paraná, Brasil. Master thesis. Universidade Estadual Paulista , São José do Rio Preto .
  • Bianconi, G. V., S. B. Mikich, and W. A. Pedro. 2004. Diversidade de morcegos (Mammalia, Chiroptera) em remanescentes florestais do município de Fênix, noroeste do Paraná, Brasil. Rev. Bras. Zool. 21 (4): 943954.
  • Bonaccorso, F. J. 1979. Foraging and reproductive ecology in a panamanian bat community. Bull. Fla. State Mus. Biol. Sci. 24 (4): 359408.
  • Cosson, J., J. Pons, and D. Masson. 1999. Effects of forest fragmentation on frugivorous and nectarivorous bats in French Guiana. J. Trop. Ecol. 15: 515534.
  • Estrada, A., and R. Coates-Estrada. 2002. Bats in continuous forests?, forest fragments and in a agricultural mosaic habitat-island at Los Tuxtlas, Mexico. Biol. Conserv. 103: 237245.
  • Fleming, T. H. 1985. Coexistence of five sympatric Piper (Piperaceae) species in a tropical dry forest. Ecology 66 (3): 688700.
  • Fleming, T. H. 1988. The short-tailed fruit bat: A study in plant-animal interactions. University Chicago Press, Chicago .
  • Fleming, T. H., and E. R. Heithaus. 1981. Frugivorous bats, seed shadows and the structure of tropical forests. Biotropica 13 (Supplement): 4553.
  • Fleming, T. H., and V. J. Sosa. 1994. Effects of nectarivorous and frugivorous mammals on reproductive success of plants. J. Mammal. 75 (4): 845851.
  • Garcia, Q. S., J. L. P. Rezende, and L. M. S. Aguiar. 2000. Seed dispersal by bats in a disturbed area of Southeastern Brazil. Rev. Biol. Trop. 48 (1): 125128.
  • Handley, C. O. Jr ., A. L. Gardner, and D. E. Wilson. 1991. Food habits. In C. O.HandleyJr., D. E.Wilson, and A. L.Gardner (Eds.). Demography and natural history of the common fruit bat, Artibeus jamaicensis, on Barro Colorado Island, Panamá, pp. 141146. Smithson. Contrib. Zool. 511, Smithsonian Institution Press, Washington , D.C.
  • ITCF (Instituto de Terras, Cartografia e Florestas). 1987. Plano de manejo do Parque Estadual de Vila Rica do Espírito Santo, Fênix, PR. ITCF, Curitiba , Paraná .
  • Iudica, C. A., and F. J. Bonaccorso. 1997. Feeding of the bat, Sturnira lilium, on fruits of Solanum riparium influences dispersal of this pionner tree in forests of northwestern Argentina. Stud. Neotrop. Fauna & Environm. 32: 46.
  • Janzen, D. H. 1979. How to be a fig. Annu. Rev. Ecol. Syst. 10: 1351.
  • Judd, W. S., C. S. Campbell, E. A. Kellog, and P. F. Stevens. 1999. Plant systematics: a phylogenetic approach. Sinauer Associates Inc., Sunderland , MA .
  • Kalko, E. K. V., E. A. Herre, and C. O. Handley. 1996. The relation of fig fruit syndromes to fruit-eating bats in the New and Old World tropics. J. Biogeogr. 23: 565576.
  • Korine, C., and E. K. V. Kalko. 2005. Fruit detection and discrimination by small fruit-eating bats (Phyllostomidae): Echolocation call design and olfaction. Behav. Ecol. Sociobiol. 59: 1223.
  • Mann, G. 1951. Esquema ecologico de selva, sabana y cordillera em Bolívia. Universidad de Chile, Santiago .
  • Mikich, S. B. 2001. Frugivoria e dispersão de sementes em uma pequena reserva isolada do Estado do Paraná, Brasil. PhD thesis. Universidade Federal do Paraná , Curitiba .
  • Mikich, S. B. 2002. A dieta dos morcegos frugívoros (Mammalia, Chiroptera, Phyllostomidae) de um pequeno remanescente de Floresta Estacional Semidecidual do sul do Brasil. Rev. Bras. Zool. 19 (1): 239249.
  • Mikich, S. B. and S. M. Silva. 2001. Composição florística e fenologia das espécies zoocóricas de remanescentes de Floresta Estacional Semidecidual no centro-oeste do Paraná, Brasil. Acta Bot. Bras. 15 (1): 89113.
  • Mikich, S. B., and K. L. De Oliveira. 2003. Revisão do Plano de Manejo do Parque Estadual Vila Rica do Espírito Santo. Mater Natura/FNMA, Curitiba .
  • Mikich, G. V., Bianconi, B. H. L. N. S. Maia, and S. D. Teixeira. 2003. Attraction of the fruit-eating bat Carollia perspicillata to Piper gaudichaudianum essential oil. J. Chem. Ecol. 29 (10): 23792383.
  • Morrison, D. W. 1978. Influence of habitat on the foranging distances of the fruit bat, Artibeus jamaicensis. J. Mammal. 59 (3): 622624.
  • Palmerim, J. M., D. L. Gorchov, and S. Stoleson. 1989. Trophic structure of a neotropical frugivore community: Is there competition between birds and bats? Oecologia 79: 403411.
  • Rieger, J. M., and E. M. Jakob. 1988. The use of olfaction in food location by frugivorous bats. Biotropica 20 (2): 161164.
  • Simmons, N. B. 2005. Order Chiroptera. In D. E.Wilson and D. M.Reeder (Eds.). Mammal species of the world: A taxonomic and geographic reference, 3rd edition. Johns Hopkins University Press, Baltimore , Maryland .
  • Straube, F. C., and G. V. Bianconi. 2002. Sobre a grandeza e a unidade utilizada para estimar esforço de captura com utilização de redes-de-neblina. Chiropt , Neotrop . 8 (1–2): 150152.
  • Thies, W., E. K. V. Kalko, and H. U. Schnitzler. 1998. The roles of echolocation and olfaction in two Neotropical fruit-eating bats, Carollia perspicillata and C. castanea, feeding on Piper. Behav. Ecol. Sociobiol. 42 (6): 397409.
  • Thies, W., E. K. V. Kalko, and E. K. V. Kalko. 2004. Phenology of neotropical pepper plants (Piperaceae) and their association with their main dispersers, two short-tailed fruit bats, Carollia perspicillata and C. castanea (Phyllostomidae). Oikos 104: 362376.
  • Van Der Pijl, L. 1957. The dispersal of plants by bats (chiropterochory). Acta Bot. Neerl. 6: 291315.
  • Wendeln, M. C., J. R. Runkle, and E. K. V. Kalko. 2000. Nutritional values of 14 fig species and bat feeding preferences in Panama. Biotropica 32 (3): 489501.
  • Yuncker, T. G. 1972. The Piperaceae of Brazil I. Piper. Hoehnea 2: 19366.