Abstract
Ecological restoration aims to retrieve not only the structure but also the functionality of ecosystems. Frugivorous birds may play an important role in this process due to their efficiency in seed dispersal. Color perception in these animals is highly developed, and then the colors of fleshy fruits may provide important clues for choosing plant species for restoration plans. This study aims to integrate bird color preferences and restoration of degraded areas, with an objective to evaluate the potential attractiveness to birds by colored fruits. We carried out an experiment with 384 artificial fruits made of edible modeling clay with the following colors: black, blue, green and red, with 96 fruits of each color in six sites, including four restored areas and two second-growth forest fragments. We also tested the possible effect of light intensity on fruit consumption by color. A total of 120 (38.6%) were assumed to be consumed by birds, and the fruit consumption varied in response to the location and light incidence. Consumption of black and blue fruits was not related to site by chance. Notwithstanding, red and black fruits were consumed significantly more than any other colors, emphasizing bird preference to these colors, regardless of location. Enrichment with shade tolerant shrubs or forest species with black or red fruits may be an alternative way to manage established restorations. In recently established or new restorations, one may introduce pioneer shrubs or short-lived forest species which have blue fruits, but also those having black or red ones.
Keywords:
artificial fruits; Atlantic Forest; frugivory; ecological succession; color perception
Resumo
A restauração ecológica tem a finalidade de recuperar não apenas a estrutura, mas também a funcionalidade dos ecossistemas, e as aves frugívoras podem desempenhar um papel importante neste processo devido à sua eficiência na dispersão de sementes. Como a percepção da cor nestes animais é altamente desenvolvida, a cor dos frutos carnosos pode ser uma característica importante na escolha de espécies de plantas para os reflorestamentos. Este estudo tem como foco integrar a preferência de cor de frutos por aves e a recuperação de áreas degradadas, objetivando determinar a atratividade potencial de aves por frutos de cores diferentes. Foi realizado um experimento com 384 frutos artificiais feitos com massa de modelar comestível nas cores preta, azul, verde e vermelha, com um total de 96 frutos em cada cor em seis locais, incluindo quatro áreas restauradas e dois fragmentos de floresta secundária. Também foi testado o possível efeito da intensidade de luz sobre o consumo de frutos conforme as cores. Um total de 120 (38,6%) frutos foi considerado consumido pelas aves, e o consumo variou em resposta aos locais e incidência de luz. O consumo de frutos pretos e azuis foi significativamente relacionado com o local. Os frutos vermelhos e pretos foram significativamente mais consumidos do que as outras cores, enfatizando a preferência aves por essas cores, independentemente do local. O enriquecimento com espécies tolerantes à sombra com frutos pretos ou vermelhos pode ser uma alternativa para manejo de restaurações já estabelecidos; enquanto nos recentemente criados podem ser introduzidas espécies pioneiras ou florestais de vida curta com frutos azuis, pretos ou vermelhos.
Palavras-chave:
frutos artificiais; Mata Atlântica; frugivoria; sucessão ecológica; percepção de cores
1 Introduction
Humans have converted large areas of tropical, native vegetation into landscapes of mixed crops, pastureland, and frequently isolated remnants of native vegetation (Laurance and Bierregaard, 1997LAURANCE, W.F. and BIERREGAARD, R.O., 1997. Tropical forest remnants: ecology, management and conservation of fragmented communities. Chicago: University of Chicago Press. 632 p.; Steffen et al., 2011Steffen, W., Persson, Å., Deutsch, L., Zalasiewicz, J., Williams, M., Richardson, K., Crumley, C., Crutzen, P., Folke, C., Gordon, L., Molina, M., Ramanathan, V., Rockström, J., Scheffer, M., Schellnhuber, H.J. and Svedin, U., 2011. The Anthropocene: From Global Change to Planetary Stewardship. Ambio, vol. 40, no. 7, pp. 739-761. http://dx.doi.org/10.1007/s13280-011-0185-x. PMid:22338713.
http://dx.doi.org/10.1007/s13280-011-018...
). Such mosaics have led to an impoverishment in tropical biodiversity (Fahrig, 2003FAHRIG, L., 2003. Effects of habitat fragmentation on biodiversity. Annual Review of Ecology Evolution and Systematics, vol. 34, no. 1, pp. 487-515. http://dx.doi.org/10.1146/annurev.ecolsys.34.011802.132419.
http://dx.doi.org/10.1146/annurev.ecolsy...
) and losses of functionality and ecosystem services, as pest and diseases control and plant recruitment (Classen et al., 2014CLASSEN, A., PETERS, M.K., FERGER, S.W., HELBIG-BONITZ, M., SCHMACK, J.M., MAASSEN, G., SCHLEUNING, M., KALKO, E.K.V., BÖHNING-GAESE, K. and STEFFAN-DEWENTER, I., 2014. Complementary ecosystem services provided by pest predators and pollinators increase quantity and quality of coffee yields. Proceedings. Biological Sciences, vol. 281, no. 1779, pp. 1-7. http://dx.doi.org/10.1098/rspb.2013.3148. PMid:24500173.
http://dx.doi.org/10.1098/rspb.2013.3148...
; Gray and Lewis, 2014GRAY, C.L. and LEWIS, O.T., 2014. Do riparian forest fragments provide ecosystem services or disservices in surrounding oil palm plantations? Basic and Applied Ecology, vol. 15, no. 8, pp. 693-700. http://dx.doi.org/10.1016/j.baae.2014.09.009.
http://dx.doi.org/10.1016/j.baae.2014.09...
; Moleón et al., 2014MOLEÓN, M., SÁNCHEZ-ZAPATA, J.A., MARGALIDA, A., CARRETE, M., OWEN-SMITH, N. and DONÁZAR, J.A., 2014. Humans and Scavengers: the evolution of interactions and ecosystem services. Bioscience, vol. 64, no. 5, pp. 394-403. http://dx.doi.org/10.1093/biosci/biu034.
http://dx.doi.org/10.1093/biosci/biu034...
).
Ecological restoration aims to assist the recovery of a degraded ecosystem (SER, 2004SOCIETY FOR ECOLOGICAL RESTORATION – SER, 2004. [viewed 21 August 2015]. The SER primer on ecological restoration [online]. Washington: SER. Available from: http://www.ser.org/
http://www.ser.org/...
) within a functional perspective, allowing goals of increasing ecosystem sustainability and their services (Suding, 2011SUDING, K.N., 2011. Toward an era of restoration in ecology: successes, failures, and opportunities ahead. Annual Review of Ecology Evolution and Systematics, vol. 42, no. 1, pp. 465-487. http://dx.doi.org/10.1146/annurev-ecolsys-102710-145115.
http://dx.doi.org/10.1146/annurev-ecolsy...
; Stanturf et al., 2014STANTURF, J.A., PALIK, B.J. and DUMROESE, R.K., 2014. Contemporary forest restoration: a review emphasizing function. Forest Ecology and Management, vol. 331, pp. 292-323. http://dx.doi.org/10.1016/j.foreco.2014.07.029.
http://dx.doi.org/10.1016/j.foreco.2014....
). These processes may be accelerated by enhancing plant-animal networks (Piña-Rodrigues et al., 2009PIÑA-RODRIGUES, F.C.M., PIRATELLI, A.J., RUDGE, A.C., GONDIM, F.R., FREIRE, M. and CORREA, J.S., 2009. Mobile links in fragmented ecosystem: seed and birds dispersal approach towards Atlantic forest restoration and conservation. In: H. GAESE, J.C.T. ALBINO, J. WESENBERG and S. SCHLÜTER, eds. Biodiversity and land use systems in the fragmented Mata Atlântica of Rio de Janeiro. Göttingen: Cuvillier Verlag, pp. 313-360.). Plants and animals have multiple relationship levels, such as predation, pollination and seed dispersal (Menz et al., 2011MENZ, M.H.M., PHILLIPS, R.D., WINFREE, R., KREMEN, C., AIZEN, M.A., JOHNSON, S.D. and DIXON, K.W., 2011. Reconnecting plants and pollinators: challenges in the restoration of pollination mutualisms. Trends in Plant Science, vol. 16, no. 1, pp. 4-12. http://dx.doi.org/10.1016/j.tplants.2010.09.006. PMid:20980193.
http://dx.doi.org/10.1016/j.tplants.2010...
; Nuismer et al., 2013NUISMER, S.L., JORDANO, P. and BASCOMPTE, J., 2013. Co-evolution and the architecture of mutualistic networks. Evolution, vol. 67, no. 2, pp. 338-354. http://dx.doi.org/10.1111/j.1558-5646.2012.01801.x. PMid:23356608.
http://dx.doi.org/10.1111/j.1558-5646.20...
), and these interactions represent opportunities to establish a continuous regeneration, since animals may be considered as natural “sowers” and “planters” (Cole et al., 2010COLE, R.J., HOLL, K.D. and ZAHAWI, R.A., 2010. Seed rain under tree islands planted to restore degraded lands in a tropical agricultural landscape. Ecological Applications, vol. 20, no. 5, pp. 1255-1269. http://dx.doi.org/10.1890/09-0714.1. PMid:20666248.
http://dx.doi.org/10.1890/09-0714.1...
; McConkey et al., 2012MCCONKEY, K.R., PRASAD, S., CORLETT, R.T., CAMPOS-ARCEIZ, A., BRODIE, J.F., ROGERS, H. and SANTA-MARIA, L., 2012. Seed dispersal in changing landscapes. Biological Conservation, vol. 146, no. 1, pp. 1-13. http://dx.doi.org/10.1016/j.biocon.2011.09.018.
http://dx.doi.org/10.1016/j.biocon.2011....
). Likewise, the maintenance of species diversity is considered an important regulating ecosystem service (Isbell et al., 2011Isbell, F., Calcagno, V., Hector, A., Connolly, J., Harpole, W.S., Reich, P.B., Scherer-Lorenzen, M., Schmid, B., Tilman, D., van Ruijven, J., Weigelt, A., Wilsey, B.J., Zavaleta, E.S. and Loreau, M., 2011. High plant diversity is needed to maintain ecosystem services. Nature, vol. 477, no. 7363, pp. 199-202. http://dx.doi.org/10.1038/nature10282. PMid:21832994.
http://dx.doi.org/10.1038/nature10282...
).
Zoochory is the most common way of seed dispersal in tropical forests (Barcelos et al., 2012BARCELOS, A.O., PERÔNICO, C.P. and EUTRÓPIO, F.J., 2012. Color and odor of artificial fruit used to signal potential dispersers in the Atlantic forest in Brazil. Revista de Biologia Tropical, vol. 60, no. 2, pp. 925-931. PMid:23894956.; Gonçalves et al., 2015GONÇALVES, V.F., SILVA, A.M., BAESSE, C.Q. and MELO, C., 2015. Frugivory and potential of birds as dispersers of . Siparuna guianensisBrazilian Journal of Biology = Revista Brasileira de Biologia, vol. 75, no. 2, pp. 300-304. http://dx.doi.org/10.1590/1519-6984.11413. PMid:26132011.
http://dx.doi.org/10.1590/1519-6984.1141...
and references therein). Animal-dispersed fruits are usually fleshy berries or drupe, or dehiscent capsules that expose the seeds involved with an aril, which contains sources of carbohydrates and lipids (Fleming and John Kress, 2011FLEMING, T.H. and JOHN KRESS, W., 2011. A brief history of fruit and frugivores. Acta Oecologica, vol. 37, no. 6, pp. 521-530. http://dx.doi.org/10.1016/j.actao.2011.01.016.
http://dx.doi.org/10.1016/j.actao.2011.0...
).
Birds are the main frugivorous in the Neotropics and are efficient seed dispersers because they are very mobile and have high metabolism that requires constant energy consumption (Whelan et al., 2008WHELAN, C.J., WENNY, D.G. and MARQUIS, R.J., 2008. Ecosystem services provided by birds. Annals of the New York Academy of Sciences, vol. 1134, no. 1, pp. 25-60. http://dx.doi.org/10.1196/annals.1439.003. PMid:18566089.
http://dx.doi.org/10.1196/annals.1439.00...
; Gonçalves et al., 2015GONÇALVES, V.F., SILVA, A.M., BAESSE, C.Q. and MELO, C., 2015. Frugivory and potential of birds as dispersers of . Siparuna guianensisBrazilian Journal of Biology = Revista Brasileira de Biologia, vol. 75, no. 2, pp. 300-304. http://dx.doi.org/10.1590/1519-6984.11413. PMid:26132011.
http://dx.doi.org/10.1590/1519-6984.1141...
). They also show color sensitivity (Hart, 2001HART, N.S., 2001. The visual ecology of avian photoreceptors. Progress in Retinal and Eye Research, vol. 20, no. 5, pp. 675-703. http://dx.doi.org/10.1016/S1350-9462(01)00009-X. PMid:11470455.
http://dx.doi.org/10.1016/S1350-9462(01)...
) and well developed brain and vision, which allow for learning (Martin, 1993MARTIN, G.R., 1993. Producing the image. In: H.P. ZEIGLER and H.J. BISCHOF, eds. Vision brain, and behavior in birds. Cambridge: MIT Press. p. 5-24.). Color preferences and fidelity have been reported in previous studies (e.g. Puckey et al., 1996PUCKEY, H.L., LILL, A. and O’DOWD, D.J., 1996. Fruit color choices of captive silvereyes (). Zosterops lateralisThe Condor, vol. 98, no. 4, pp. 780-790. http://dx.doi.org/10.2307/1369858.
http://dx.doi.org/10.2307/1369858...
; Whitney, 2005WHITNEY, K.D., 2005. Linking frugivores to the dynamics of a fruit color polymorphism. American Journal of Botany, vol. 92, no. 5, pp. 859-867. http://dx.doi.org/10.3732/ajb.92.5.859. PMid:21652467.
http://dx.doi.org/10.3732/ajb.92.5.859...
); however, this may be transient and strongly depend upon the environment (Schmidt et al., 2004SCHMIDT, V., SCHAEFER, H.M. and WINKLER, H., 2004. Conspicuousness, not colour as foraging cue in plant-animal signaling. Oikos, vol. 106, no. 3, pp. 551-557. http://dx.doi.org/10.1111/j.0030-1299.2004.12769.x.
http://dx.doi.org/10.1111/j.0030-1299.20...
). Then, we may predict a non-random variation in fruit choice, based not only by colors but also due to the contrast that each color has in different background, which varies in areas having different luminosities.
Many frugivorous birds are able to use human-modified environments (such as crop fields and forest edges) and/or move across open areas and forest fragments (Gomes et al., 2008GOMES, L.G.L., OOSTRA, V., NIJMAN, V., CLEEF, A.M. and KAPPELLE, M., 2008. Tolerance of frugivorous birds to habitat disturbance in a tropical cloud forest. Biological Conservation, vol. 141, no. 3, pp. 860-871. http://dx.doi.org/10.1016/j.biocon.2008.01.007.
http://dx.doi.org/10.1016/j.biocon.2008....
), thus increasing seed dispersal along their route and acting as “mobile links” (Lundberg and Moberg, 2003LUNDBERG, J. and MOBERG, F., 2003. Mobile link organisms and ecosystem functioning: implications for ecosystem resilience and management. Ecosystems, vol. 6, no. 1, pp. 87-98. http://dx.doi.org/10.1007/s10021-002-0150-4.
http://dx.doi.org/10.1007/s10021-002-015...
; Piña-Rodrigues et al., 2009PIÑA-RODRIGUES, F.C.M., PIRATELLI, A.J., RUDGE, A.C., GONDIM, F.R., FREIRE, M. and CORREA, J.S., 2009. Mobile links in fragmented ecosystem: seed and birds dispersal approach towards Atlantic forest restoration and conservation. In: H. GAESE, J.C.T. ALBINO, J. WESENBERG and S. SCHLÜTER, eds. Biodiversity and land use systems in the fragmented Mata Atlântica of Rio de Janeiro. Göttingen: Cuvillier Verlag, pp. 313-360.). In this scenario, ecological restoration of degraded land also has the function of making this area more permeable and “bird-friendly”, reestablishing links among isolated forest remnants and allowing gene flow and increasing biological and functional diversity (Cavallero et al., 2012CAVALLERO, L., RAFFAELE, E. and AIZEN, M.A., 2012. Birds as mediators of passive restoration during early post-fire recovery. Biological Conservation, vol. 158, pp. 342-350. http://dx.doi.org/10.1016/j.biocon.2012.10.004.
http://dx.doi.org/10.1016/j.biocon.2012....
). Thus, if appropriate species are used in a given restored area, forest enrichment with attractive species may increase functional processes such as seed dispersal.
Therefore, the aim of this study was to integrate fruit color preference by birds and restoration of degraded areas, in order to evaluate the potential attractiveness of birds by colored fruits in different sites. Our premise is that birds are generally attracted and consume fruits that are more conspicuous, considering that the choice of fruit also depends on the environment and light intensities. We predict that in recently restored areas, fruits would be more detected and consumed due to the high luminosity of these open areas. Then we discuss the use of plant species whose fruits would be more attractive in each situation, which would increase seed dispersal and accelerate the process of ecological succession.
2 Material and Methods
2.1 Study area
We performed fieldwork near the city of Itu in the state of São Paulo, Southeastern Brazil (see Figure 1a) in a 526-ha area (lat 23°14’15.18”S; long 47°24’3.29”W). The regional predominant physiognomy is the seasonal semidecidual Atlantic Forest with a transition to Cerrado, which is characterized by its climatic seasonality (Veloso et al., 1991VELOSO, H.P., RANGEL-FILHO, A L.R. and LIMA, J.C.A., 1991. Classificação da vegetação brasileira adaptada a um sistema universal. Rio de Janeiro: IBGE. 124 p.). The climate is temperate humid with dry winters and hot summers. The average rainfall is 160mm for the rainy period and 56mm for dry season (Cepagri, 2015CENTRO DE PESQUISAS METEOROLÓGICAS E CLIMÁTICAS APLICADAS À AGRICULTURA – CEPAGRI, 2015 [viewed 20 February 2015]. Clima dos Municípios Paulistas [online]. Available from: http://www.cepagri.unicamp.br/outras-informacoes/clima-dos-municipios-paulistas.html
http://www.cepagri.unicamp.br/outras-inf...
).
(a) Location of the study area in the state of São Paulo, Brazil; (b) Location of the study area and schematic illustration of the sampling design used in the experiment on the preference of fruit color. F1 and F2 = forest fragments; RO1 and RO2 = restoration of 6 year-old; RN1 and RN2 = restoration of 3-year old).
The area is a 400 ha of abandoned pasture and croplands inserted in a restoration program (Martins, 2011MARTINS, A.F., 2011. Controle de gramíneas exóticas invasoras em área de restauração ecológica com plantio total, Floresta Estacional Semidecidual, Itu, SP. Piracicaba: Universidade de São Paulo. 112 p. Dissertação de Mestrado em Recursos Florestais.). We defined three habitat-types (recent, old-restored areas, and natural fragments), where we selected six study sites: two 3-year old areas (0.91 and 1.30-ha; from now RN1 and RN2), two 6-year-old restored sites (0.25 and 1.20-ha; from now RO1 and RO2) and two forest fragments with 9 and 23 ha (hereinafter F1 and F2). The study sites were mainly surrounded by pastures of Urochloa decumbensL. (Poaceae) (Figure 2).
The restorations were planted in 2005 (RO1 and RO2) and 2008 (RN1 and RN2), according to the “filling and diversity” methodology (Nave and Rodrigues, 2007NAVE, A.G. and RODRIGUES, R.R., 2007. Combination of species into filling and diversity groups as forest restoration methodology. In: R.R. RODRIGUES, S.V. MARTINS and S. GANDOLFI, orgs. High diversity forest restoration in degraded areas: methods and projects in Brazil. New York: Nova Science Publishers, pp. 103-126.). Fill species include those faster grow that provide shade to the others, and the “diversity” consists of those that increase the area diversity. The local seedling nursery produces 189 native tree species, mainly from initial (pioneers and early secondary) successional stages. About 49.2% of the species are abiotically dispersed and 50.8% of the species are animal-dispersed (Appendix A Appendix A Plant species available in the nursery or planted in the Centro de Experimentos Florestais, in the region of Itu, state of São Paulo, with colors of fruits/diasporas and dispersal syndrome (biotic or abiotic). Taxon Fruit/diaspore color Seed dispersal* Acacia caven Molina Brown Abiotic Acacia polyphylla DC. Black/Yellow Abiotic Aegiphila sellowiana Cham. Orange Biotic Albizia polyphylla E. Fourn. Brown Abiotic Allophylus edulis (A. St.-Hil., A. Juss. & Cambess.) Hieron. ex Niederl. Red Biotic Allophylus petiolulatus Radlk. Red Biotic Aloysia virgate (Ruiz & Pav.) Pers. White Abiotic Anadenanthera falcate (Benth.) Speg. Brown Abiotic Anadenanthera macrocarpa (Benth.) Brenan Brown Abiotic Anadenanthera peregrina (L.) Speg. Brown Abiotic Annona cacans Warm. Green Biotic Annona coriácea Mart. Green Biotic Apeiba tibourbou Aubl. Green Abiotic Aspidosperma parvifolium A.DC. Beige Abiotic Aspidosperma cylindrocarpon Müll. Arg. Brown Abiotic Aspidosperma ramiflorum Müll. Arg. Brown Abiotic Astronium graveolens Jacq. Brown Abiotic Balfourodendron riedelianum (Engl.) Engl. Yellow Abiotic Bastardiopsis densiflora (Hook. & Arn.) Hassl. Green Abiotic Bauhinia forficata Link Brown Abiotic Byrsonima sericea DC. Yellow Biotic Cabralea canjerana (Vell.) Mart. Red Biotic Calophyllum brasiliensis Camb. Green Biotic Campomanesia eugenioides (Cambess.) D. Legrand ex L.R. Landrum Green Biotic Campomanesia neriiflora (O. Berg) Nied. Green Biotic Campomanesia xanthocarpa Mart. Ex O. Berg Yellow Biotic Capsicodendron dinisii (Schwacke) Occhioni Red Biotic Cariniana estrellensis (Raddi) Kuntze Beige Abiotic Cariniana legalis (Mart.) Kuntze Beige Abiotic Casearia gossypiosperma Briq. Yellow/Green Biotic Casearia sylvestris Sw. Red/Black Biotic Cassia ferruginea (Schrad.) Schrader ex DC. Brown Abiotic Cassia leptophylla Vogel Brown Abiotic Cecropia hololeuca Miq. Brown Biotic Cecropia pachystachya Trécul Green Biotic Cedrela fissilis Vell. Brown Abiotic Cedrela odorata L. Brown Abiotic Ceiba speciosa (A. St.-Hil.) Ravenna Green Abiotic Centrolobium tomentosum Guillemin ex Benth. Brown Abiotic Chorisia glaziovii (Kuntze) E. Santos Green Abiotic Chorisia speciose A. St.-Hil. Green Abiotic Chrysophyllum gonocarpum (Mart. & Eichler ex Miq.) Engl. Yellow Biotic Citharexylum mirianthum Cham. Red Biotic Citharexylum solanaceum Cham. Orange Biotic Colubrina glandulosa Perkins Black Biotic Copaifera langsdorffii Desf. Orange/Black Biotic Cordia americana (L.) Gottschling & J.S. Mill. Brown Abiotic Cordia ecalyculata Vell. Red Biotic Cordia sellowiana Cham. Yellow Biotic Cordia superba Cham. White Biotic Cordia trichotoma (Vell.) Arráb. Ex Steud. Green Abiotic Couroupita guianensis Aubl. Yellow Biotic Coutarea hexandra (Jacq.) K. Schum. Green Abiotic Croton floribundus Spreng. Green Abiotic Croton urucurana Baill. Green Abiotic Cryptocarya aschersoniana Mez Yellow Biotic Cupania vernalis Cambess. Black/Red Biotic Curatella americana L. Red Biotic Cyclolobium vecchi A. Samp. Ex Hoehne Beige Abiotic Dendropanax cuneatum Decne. & Planch. Green Biotic Dictyoloma vandellianum A. Juss. Beige Abiotic Dilodendron bipinnatum Radlk. Black Biotic Diospyros inconstans Jacq. Purple Biotic Diplokeleba floribunda N.E. Br. Brown Abiotic Enterolobium contortisiliquum (Vell.) Morong Black Abiotic Enterolobium timbouva Mart. Black Abiotic Eriotheca gracilipes (K. Schum.) A. Robyns Green Abiotic Erythrina speciosa Andrews Brown Abiotic Erythrina crista-galli L. Brown Abiotic Erythrina falcate Benth. Brown Abiotic Erythrina velutina Willd. Green Abiotic Erythroxylum deciduum A. St.-Hil. Red Biotic Erythrina verna Vell. Brown Abiotic Esenbeckia leiocarpa Engl. Green Abiotic Eugenia brasiliensis Lam. Red/Black Biotic Eugenia cerasiflora Miq. Red Biotic Eugenia candolleana DC. Black Biotic Eugenia dysenterica DC. Yellow Biotic Eugenia glazioviana (Kiaersk.) D. Legrand Yellow Biotic Eugenia involucrata DC. Red/Black Biotic Eugenia luschnathiana (O. Berg) Klotzsch ex B.D. Jacks. Yellow Biotic Eugenia pyriformis Cambess. Yellow Biotic Eugenia uniflora L. Orange/Red Biotic Ficus enormis (Mart. Ex Miq.) Mart. Red/Purple Biotic Ficus guaranítica (Chodat) Green Biotic Ficus insipida Willd. Green Biotic Ficus luschnathiana (Miq.) Miq. Red/Purple Biotic Ficus obtusifolia Kunth Yellow/Orange Biotic Gallesia integrifólia (Spreng.) Harms Beige Abiotic Garcinia gardneriana (Planch. & Triana) Zappi Yellow Biotic Genipa Americana L. Green/Brown Biotic Gochnatia polymorpha (Less.) Cabrera White Abiotic Guapira graciliflora (Mart. Ex J.A. Schmidt) Lundell Black Biotic Guarea kunthiana A. Juss. Brown Biotic Guazuma ulmifolia Lam. Black Biotic Handroanthus chrysotrichus (Mart. ex A. DC.) Mattos Green Abiotic Handroanthus heptaphyllus (Vell.) Mattos Brown Abiotic Handroanthus impetiginosus (Mart. ex DC.) Mattos Brown Abiotic Heliocarpus popayanensis Kunth Beige Abiotic Hexachlamys edulis (O. Berg) Kausel & D. Legrand Yellow Biotic Hymenaea courbaril L. Green Biotic Inga laurina (Sw.) Willd. Green Biotic Inga marginata Willd. Green Biotic Inga uruguensis Hook. & Arn. Green Biotic Inga vera Willd. Green Biotic Jacaranda micranta Cham. Black Abiotic Jacaratia spinosa (Aubl.) A. DC. Yellow Biotic Lafoensia glyptocarpa Koehne Green Abiotic Lafoensia pacari A. St.-Hil. Brown Abiotic Leucochloron incuriale (Vell.) Barneby & J.W. Grimes Yellow Abiotic Lonchocarpus campestres Mart. ex Benth. Green Abiotic Lonchocarpus cultratus (Vell.) A.M.G. Azevedo & H.C. Lima Green Abiotic Lonchocarpus muehlbergianus Hassl. Brown Abiotic Luehea divaricata Mart. Green Abiotic Luehea grandiflora Mart. Green Abiotic Mabea fistulifera Mart. Green Abiotic Machaerium hirtum (Vell.) Stellfeld Brown Abiotic Machaerium stipitatum (DC.) Vogel Brown Abiotic Machaerium villosum Vogel Brown Abiotic Machaerium brasiliense Vogel Green Abiotic Maclura tinctoria (L.) D. Don ex Steud. Green Biotic Miconia cabucu Hoehne Yellow Biotic Mimosa bimucronata (DC.) Kuntze Brown Abiotic Mimosa scabrella Benth. Brown Abiotic Myracrodruon urundeuva Allemão Black Abiotic Myrciaria floribunda (H. West ex Willd.) O. Berg Red Biotic Myrciaria glazioviana (Kiaersk.) G.M. Barroso ex Sobral Yellow Biotic Myroxylon peruiferum L.f. Beige Abiotic Myrsine umbellata Mart. Black Biotic Nectandra megapotamica (Spreng.) Mez Black Biotic Ocotea puberula (Rich.) Nees Black/Red Biotic Ormosia arborea (Vell.) Harms Orange/Black Abiotic Parapiptadenia rígida (Benth.) Brenan Brown Abiotic Peltophorum dubium (Spreng.) Taub. Beige Abiotic Persea pyrifolia (D. Don) Spreng. Green Biotic Phytolacca dioica L. Yellow Abiotic Piptadenia gonoacantha (Mart.) J.F. Macbr. Green Abiotic Piptocarpha axillaris (Less.) Baker ** Abiotic Piptocarpha rotundifolia (Less.) Baker ** Abiotic Platypodium elegans Vogel Beige Abiotic Plinia edulis (Vell.) Sobral Yellow Biotic Poecilanthe parviflora Benth. Brown Abiotic Posoqueria acutifolia Mart. Yellow Abiotic Pouteria torta (Mart.) Radlk. Yellow Abiotic Prunus sellowii Koehne Purple Biotic Psidium cattleianum Sabine Yellow Biotic Psidium guajava L. Green/Red Biotic Psidium longipetiolatum D. Legrand Purple Biotic Psidium rufum DC. Green Biotic Psychotria carthagenensis Jacq. Red Biotic Pterocarpus violaceus Vogel Beige Abiotic Pterogyne nitens Tul. Beige Abiotic Rapanea ferrugínea (Ruiz & Pav.) Mez Black Biotic Rapanea gardneriana (A. DC.) Mez Black Biotic Rauvolfia sellowii Müll. Arg. Black Biotic Rhamnidium elaeocarpum Reissek Red Biotic Sapium glandulatum (Vell.) Pax Red Biotic Schefflera morototoni (Aubl.) Maguire, Steyerm. & Frodin Brown Biotic Schinus molle L. Red Biotic Schinus terebinthifolius Raddi Red Biotic Schizolobium parahyba (Vell.) S.F. Blake Beige Abiotic Seguieria langsdorffii Moq. Black Abiotic Senna alata (L.) Roxb. Black Abiotic Senna macranthera (DC. ex Collad.) H.S. Irwin & Barneby Black Abiotic Senna multijuga (Rich.) H.S. Irwin & Barneby Brown Biotic Senna pendula (Humb. & Bonpl. ex Willd.) H.S. Irwin & Barneby Green Abiotic Simira sampaiona (Standl.) Steyerm. Green Abiotic Solanum erianthum D. Don Yellow Biotic Solanum granuloso-leprosum Dunal ** Biotic Solanum lycocarpum A. St.-Hil. Green/Yellow Biotic Solanum pseudoquina A. St.-Hil. Yellow Biotic Sparattosperma leucanthum (Vell.) K. Schum. Beige Abiotic Strychnos brasiliensis (Spreng.) Mart. Yellow Biotic Styrax pohlii A. DC. Black Biotic Syagrus romanzoffiana (Cham.) Glassman Yellow Biotic Tabebuia avellanedae Lorentz ex Griseb. Green Abiotic Tabebuia ochracea A.H. Gentry Green Abiotic Tabebuia roseo alba (Ridl.) Sand. Green Abiotic Tabernaemontana hystrix Steud. Red Biotic Terminalia argentea Mart. Beige Abiotic Terminalia brasiliensis Spreng. Yellow Abiotic Trema micranta (L.) Blume Red Biotic Vantanea compacta (Schnizl.) Cuatrec. Yellow Biotic Vitex montevidensis Cham. Black Biotic Vochysia tucanorum Mart. Green Abiotic Xylosma glaberrima Sleumer ** Biotic Zanthoxylum caribaeum Lam. Purple Biotic Zanthoxylum rhoifolium Lam. Purple Biotic Zeyheria tuberculosa (Vell.) Bureau ex Verl. Brown Abiotic Source: *Resolução SMA - 8/2008 (São Paulo, 2008). ** unknown. ). Species were randomly planted in alternating rows of pioneers and non-pioneers species, keeping 2 x 3 m between rows. After three years, the dominant species were Schinus terebinthifolius Raddi, Cytharexyllum myrianthum Cham., Guazuma ulmifolia Lam., Machaerium nyctitans (Vell.) Benth, Luehea divaricata Mart. and Cedrela fissilis Vell.
2.2 Fruit color preference
We carried out an experiment in November 2011 with 384 artificial fruits made of odorless edible clay (Wennersten and Forsman, 2009WENNERSTEN, L. and FORSMAN, A., 2009. Does color polymorphism enhance survival of prey population? Proceedings of the Royal Society B, vol. 276, no. 1803, pp. 2187-2194. http://dx.doi.org/10.1098/rspb.2009.0252.
http://dx.doi.org/10.1098/rspb.2009.0252...
). We made 2-cm spherical fruits, dyed in either black, blue, green or red, with 96 fruits of each color. As the edible clay consisted of flour, butter and gelatin, we dyed the artificial fruits using food coloring.
These colors were selected because they are closer to those of naturally bird-dispersed fruits (Cazetta et al., 2009CAZETTA, E., SCHAEFER, H.M. and GALETTI, M., 2009. Why are fruits colorful? The relative importance of achromatic and chromatic contrasts for detection by birds. Evolutionary Ecology, vol. 23, no. 2, pp. 233-244. http://dx.doi.org/10.1007/s10682-007-9217-1.
http://dx.doi.org/10.1007/s10682-007-921...
) and this technique controls variables as the number and size of fruits and position in vegetation (Alves-Costa and Lopes, 2001ALVES-COSTA, P. and LOPES, A.V., 2001. Using artificial fruits to evaluate fruit selection by birds in the field. Biotropica, vol. 33, no. 4, pp. 713-717. http://dx.doi.org/10.1111/j.1744-7429.2001.tb00230.x.
http://dx.doi.org/10.1111/j.1744-7429.20...
). In each site we set four groups of four fruits (one of each color), from now on called ‘plots’ in 16 trees (chosen at random), hanging in branches at about 1.5m high with approximately one meter between them, totaling 64 fruits per site (see Figure 1b). We checked the experiment two times, once after 24 and again after 48 hours.
Fruits that were removed or that had beak marks were considered as “consumed” (see Figure 2). We disregard of our analysis those fruits that were dropped and/or damaged by ants and/or mammals. We did not replace either predated or bird-consumed fruits. If mammals are mainly guided by the sense of smell (Munger et al., 2009MUNGER, S.D., LEINDERS-ZUFALL, T. and ZUFALL, F., 2009. Subsystem organization of the Mammalian sense of smell. Annual Review of Physiology, vol. 71, no. 1, pp. 115-140. http://dx.doi.org/10.1146/annurev.physiol.70.113006.100608. PMid:18808328.
http://dx.doi.org/10.1146/annurev.physio...
), then they would prefer fruits having odor (Barcelos et al., 2012BARCELOS, A.O., PERÔNICO, C.P. and EUTRÓPIO, F.J., 2012. Color and odor of artificial fruit used to signal potential dispersers in the Atlantic forest in Brazil. Revista de Biologia Tropical, vol. 60, no. 2, pp. 925-931. PMid:23894956.). Furthermore, tropical fruits are thought to have a strong dichotomy of colors; fruits consumed by mammals are often orange, yellow or brown, while bird-dispersed fruits would be predominantly red or black (Willson and Whelan, 1990WILLSON, M. F. and WHELAN, C.J., 1990. The evolution of fruit color in fleshy-fruited plants. American Naturalist, vol. 136, no. 6, pp. 790-809. http://dx.doi.org/10.1086/285132.
http://dx.doi.org/10.1086/285132...
). Thus, this set of characteristics may support our decision to consider the removed fruits as consumed by birds.
We also tested the possible effect of light intensity on the fruit consumption by birds, assuming that the light intensity affect fruit conspicuousness (Schmidt et al., 2004SCHMIDT, V., SCHAEFER, H.M. and WINKLER, H., 2004. Conspicuousness, not colour as foraging cue in plant-animal signaling. Oikos, vol. 106, no. 3, pp. 551-557. http://dx.doi.org/10.1111/j.0030-1299.2004.12769.x.
http://dx.doi.org/10.1111/j.0030-1299.20...
). We measured each plot in the morning, choosing individual plants and taking photographs with the lens facing upward in the same place where the fruits were hung. Next, we calculated the luminosity (%) using the Adobe Photoshop CS5 software, following Engelbrecht and Herz (2001)ENGELBRECHT, B.M. and HERZ, H.M., 2001. Evaluation of different methods to estimate understorey light conditions in tropical forests. Journal of Tropical Ecology, vol. 17, no. 2, pp. 207-224. http://dx.doi.org/10.1017/S0266467401001146.
http://dx.doi.org/10.1017/S0266467401001...
with some adaptations. Each photo was converted to grayscale, dividing the image into two colors (black and white) and the percentage of white, which is equivalent to light intensity, was seen through the image histogram. In each area, we calculated the weighted average of the four plots.
2.3 Statistical analyses
The total fruit consumed (TFC) was calculated by adding the fruit consumed by color in the four plots at the six sites (n = 24). As the TFC did not show normality based on the Shapiro-Wilk Test (p<0.01), we transformed data using log (x+0.5), and log [(x+0.5)/100] to light intensity. We tested light intensity in the six sites using analysis of variance (AOV) followed by Tukey HSD to compare means, and a box-plot to assess the light homogeneity among them. Then, we performed a Spearman rank-correlation index using percentage of light intensity and mean of consumed fruits by plot in order to evaluate the relationship between light and color preference by birds; next, we carried out a Kruskall-Wallis One-way AOV and Dunn's all-pairwise comparisons to evaluate TFC by habitat-type.
We used a general analysis of variance (General-AOV) to check for the simultaneous effects of light incidence and fruit color consumption by site, with light as the covariate and colors as dependent variables (n= 4) and sites (n= 6) as a model statement. In order to compare means, we applied a pairwise comparison using LSD to report homogeneous sites by fruit color and T-paired for each color using the fruit consumption by plot. All statistical analyses were performed in Statistix 10.0 (Analytical Software, 2013ANALYTICAL SOFTWARE2013viewed 2 January 2015Statistix 8.0softwareAvailable from: http://www.statistix.com/free-trial/
http://www.statistix.com/free-trial/...
).
3 Results
A total of 73 (19%) of the 384 exposed fruits were found fallen (n=31) and/or were predated by mammals (n=27) and/or ants (n=15), and were not included in our analyses. From the 311 remaining fruits, 120 (38.6% of the total) were assumed to be consumed by birds (Table 1).
Study sites, light intensity (%) and total of fruit consumed by color near the city of Itu in the state of São Paulo, Brazil.
The incidence of light was heterogeneous within the study area; sites F1 and RN1 were the most homogeneous in terms of the plot´s light incidence, while RN2 and RO2 had the highest heterogeneity (as shown in Table 1; see Figure 3). Across sites, only F1 was different from the others, and probably due to this, the habitat-types diverge in light intensity (F= 5.74; p=0.0103). Although new and old restorations did not differ between themselves (new= 52.5±12.6%; old= 40.6±15.0%), the new-restorations were significantly different and more open than fragments (fragment= 25.5±14.3%).
Box plot - median and quartiles (quartile method interpolation) - for light intensity in six studied sites in the state of São Paulo, Brazil. F1 and F2 = forest fragments; RN1 and RN2 = restoration of 3-years old, and RO1 and RO2 = restoration of 6 years-old.
Only the general consumption of red fruits was slightly correlated (r= 0.59; p <0.05) to light intensity. Despite this, when we evaluate each site, the light did not influence fruit consumption of red (Fred= 0.96; p>0.05), probably due to the high variation of light between plots (see Figure 3). The light incidence also did not affect fruit consumption of the other colors (Fblack= 1.40; Fblue= 1.11; Fgreen= 1.02; p>0.05).
The habitat-types did not affect the overall consumption of fruits (TFC) (F= 0.11; p>0.05); and the variation within each site was higher than between them (F= 1.08; p< 0.05), suggesting that sites, not habitat-types, influenced fruit consumption. Indeed, fruit consumption was significantly higher in RN1 and differed across sites (Table 1). The two newer restorations (RN1 and RN2) differed in relation to fruit consumption, which did not occur when comparing the older restorations (RO1 and RO2).
The consumption of black and blue fruits was related significantly to sites, but not for red (F= 2.53; p> 0.05) or green (F= 2.19; p> 0.05). Notwithstanding, the red fruits were consumed significantly more than other colors regardless the site, with black being the only exception. However, the consumption of black and blue fruits differed between the two new-restorations and they were intensively pecked in RN1. Although black (31 fruits) and blue (25 fruits) did not differ in relation to the total amount of fruit consumed, only few black and none of the blue fruits were pecked by birds in the sites F1 and RN2.
4 Discussion
We found no influence of light exposition on fruit consumption by birds, even though this may affect color conspicuousness (e.g. Cazetta et al., 2009CAZETTA, E., SCHAEFER, H.M. and GALETTI, M., 2009. Why are fruits colorful? The relative importance of achromatic and chromatic contrasts for detection by birds. Evolutionary Ecology, vol. 23, no. 2, pp. 233-244. http://dx.doi.org/10.1007/s10682-007-9217-1.
http://dx.doi.org/10.1007/s10682-007-921...
). This is probably due to the light heterogeneity within each site. This heterogeneity in the recovered sites is probably a consequence of the filling and diversity methodology, which mix species with wider and sparser canopies used to foster sucessional processes (Rodrigues et al., 2009RODRIGUES, R.R., BRANCALION, P.H.S. and ISERNHAEN, I., 2009. Pacto pela restauração da mata atlântica: referencial dos conceitos e ações de restauração florestal. São Paulo: LERF/ESALQ. 264 p.).
Species composition and arrangement affected light heterogeneity only for new restorations, that also differed in fruit consumption. This suggests that fruit consumption by birds may be more affected by sites mainly in their early stages. Confirming that, in the forest fragments fruit consumption was not affected, and the spatial heterogeneity of light incidence may be explained both by the expected stratification in understories of semidecidual forests, and by their relatively small size (see study area) and the consequent degradation process.
In general, we observed a higher consumption of blue and black fruits in the restored areas than in the fragments, and the consumption of red and green were site-independent (Table 1). Color conspicuousness may be relative and influenced by factors such as the type of environment and luminosity (Arruda et al., 2008ARRUDA, R.D., RODRIGUES, J. and IZZO, T.J., 2008. Rapid assessment of fruit-color selection by birds using artificial fruits at local scale in Central Amazonia. Acta Amazonica, vol. 38, no. 2, pp. 291-296. http://dx.doi.org/10.1590/S0044-59672008000200011.
http://dx.doi.org/10.1590/S0044-59672008...
), and the contrast between the fruit and the foliage in the background (Schmidt et al., 2004SCHMIDT, V., SCHAEFER, H.M. and WINKLER, H., 2004. Conspicuousness, not colour as foraging cue in plant-animal signaling. Oikos, vol. 106, no. 3, pp. 551-557. http://dx.doi.org/10.1111/j.0030-1299.2004.12769.x.
http://dx.doi.org/10.1111/j.0030-1299.20...
; Cazetta et al., 2009CAZETTA, E., SCHAEFER, H.M. and GALETTI, M., 2009. Why are fruits colorful? The relative importance of achromatic and chromatic contrasts for detection by birds. Evolutionary Ecology, vol. 23, no. 2, pp. 233-244. http://dx.doi.org/10.1007/s10682-007-9217-1.
http://dx.doi.org/10.1007/s10682-007-921...
). Thus, different colors may be more or be less conspicuous depending on the conditions of a given area. Galetti et al. (2003)GALETTI, M., ALVES-COSTA, C.P. and CAZETTA, E., 2003. Effects of forest fragmentation, anthropogenic edges and fruit colour on the consumption of ornithocoric fruits. Biological Conservation, vol. 111, no. 2, pp. 269-273. http://dx.doi.org/10.1016/S0006-3207(02)00299-9.
http://dx.doi.org/10.1016/S0006-3207(02)...
observed a strong trend towards a higher consumption of red and black fruits in relation to white ones in large fragments, whereas this difference was less pronounced in smaller and more fragmented areas.
Our study is consistent with the premise that red and black fruit displays are an evolutionary trait associated with the reported preference of tropical birds to these colors (e.g. Wheelwright and Janson, 1985WHEELWRIGHT, N.T. and JANSON, C.H., 1985. Colors of fruit displays of bird-dispersed plants in two tropical forests. American Naturalist, vol. 126, no. 6, pp. 777-799. http://dx.doi.org/10.1086/284453.
http://dx.doi.org/10.1086/284453...
). For black and blue fruits there was a potential site preference by birds to these fruit colors, independent of habitat type.
In our restored areas few species had black (n=22; ~11%) or red (n=22; ~11%) fruits, while none were blue, and about 93 (~49%) species were unattractive to birds (mainly wind-dispersed) (see Appendix A
Appendix A
Plant species available in the nursery or planted in the Centro de Experimentos Florestais, in the region of Itu, state of São Paulo, with colors of fruits/diasporas and dispersal syndrome (biotic or abiotic).
Taxon
Fruit/diaspore color
Seed dispersal*
Acacia caven Molina
Brown
Abiotic
Acacia polyphylla DC.
Black/Yellow
Abiotic
Aegiphila sellowiana Cham.
Orange
Biotic
Albizia polyphylla E. Fourn.
Brown
Abiotic
Allophylus edulis (A. St.-Hil., A. Juss. & Cambess.) Hieron. ex Niederl.
Red
Biotic
Allophylus petiolulatus Radlk.
Red
Biotic
Aloysia virgate (Ruiz & Pav.) Pers.
White
Abiotic
Anadenanthera falcate (Benth.) Speg.
Brown
Abiotic
Anadenanthera macrocarpa (Benth.) Brenan
Brown
Abiotic
Anadenanthera peregrina (L.) Speg.
Brown
Abiotic
Annona cacans Warm.
Green
Biotic
Annona coriácea Mart.
Green
Biotic
Apeiba tibourbou Aubl.
Green
Abiotic
Aspidosperma parvifolium A.DC.
Beige
Abiotic
Aspidosperma cylindrocarpon Müll. Arg.
Brown
Abiotic
Aspidosperma ramiflorum Müll. Arg.
Brown
Abiotic
Astronium graveolens Jacq.
Brown
Abiotic
Balfourodendron riedelianum (Engl.) Engl.
Yellow
Abiotic
Bastardiopsis densiflora (Hook. & Arn.) Hassl.
Green
Abiotic
Bauhinia forficata Link
Brown
Abiotic
Byrsonima sericea DC.
Yellow
Biotic
Cabralea canjerana (Vell.) Mart.
Red
Biotic
Calophyllum brasiliensis Camb.
Green
Biotic
Campomanesia eugenioides (Cambess.) D. Legrand ex L.R. Landrum
Green
Biotic
Campomanesia neriiflora (O. Berg) Nied.
Green
Biotic
Campomanesia xanthocarpa Mart. Ex O. Berg
Yellow
Biotic
Capsicodendron dinisii (Schwacke) Occhioni
Red
Biotic
Cariniana estrellensis (Raddi) Kuntze
Beige
Abiotic
Cariniana legalis (Mart.) Kuntze
Beige
Abiotic
Casearia gossypiosperma Briq.
Yellow/Green
Biotic
Casearia sylvestris Sw.
Red/Black
Biotic
Cassia ferruginea (Schrad.) Schrader ex DC.
Brown
Abiotic
Cassia leptophylla Vogel
Brown
Abiotic
Cecropia hololeuca Miq.
Brown
Biotic
Cecropia pachystachya Trécul
Green
Biotic
Cedrela fissilis Vell.
Brown
Abiotic
Cedrela odorata L.
Brown
Abiotic
Ceiba speciosa (A. St.-Hil.) Ravenna
Green
Abiotic
Centrolobium tomentosum Guillemin ex Benth.
Brown
Abiotic
Chorisia glaziovii (Kuntze) E. Santos
Green
Abiotic
Chorisia speciose A. St.-Hil.
Green
Abiotic
Chrysophyllum gonocarpum (Mart. & Eichler ex Miq.) Engl.
Yellow
Biotic
Citharexylum mirianthum Cham.
Red
Biotic
Citharexylum solanaceum Cham.
Orange
Biotic
Colubrina glandulosa Perkins
Black
Biotic
Copaifera langsdorffii Desf.
Orange/Black
Biotic
Cordia americana (L.) Gottschling & J.S. Mill.
Brown
Abiotic
Cordia ecalyculata Vell.
Red
Biotic
Cordia sellowiana Cham.
Yellow
Biotic
Cordia superba Cham.
White
Biotic
Cordia trichotoma (Vell.) Arráb. Ex Steud.
Green
Abiotic
Couroupita guianensis Aubl.
Yellow
Biotic
Coutarea hexandra (Jacq.) K. Schum.
Green
Abiotic
Croton floribundus Spreng.
Green
Abiotic
Croton urucurana Baill.
Green
Abiotic
Cryptocarya aschersoniana Mez
Yellow
Biotic
Cupania vernalis Cambess.
Black/Red
Biotic
Curatella americana L.
Red
Biotic
Cyclolobium vecchi A. Samp. Ex Hoehne
Beige
Abiotic
Dendropanax cuneatum Decne. & Planch.
Green
Biotic
Dictyoloma vandellianum A. Juss.
Beige
Abiotic
Dilodendron bipinnatum Radlk.
Black
Biotic
Diospyros inconstans Jacq.
Purple
Biotic
Diplokeleba floribunda N.E. Br.
Brown
Abiotic
Enterolobium contortisiliquum (Vell.) Morong
Black
Abiotic
Enterolobium timbouva Mart.
Black
Abiotic
Eriotheca gracilipes (K. Schum.) A. Robyns
Green
Abiotic
Erythrina speciosa Andrews
Brown
Abiotic
Erythrina crista-galli L.
Brown
Abiotic
Erythrina falcate Benth.
Brown
Abiotic
Erythrina velutina Willd.
Green
Abiotic
Erythroxylum deciduum A. St.-Hil.
Red
Biotic
Erythrina verna Vell.
Brown
Abiotic
Esenbeckia leiocarpa Engl.
Green
Abiotic
Eugenia brasiliensis Lam.
Red/Black
Biotic
Eugenia cerasiflora Miq.
Red
Biotic
Eugenia candolleana DC.
Black
Biotic
Eugenia dysenterica DC.
Yellow
Biotic
Eugenia glazioviana (Kiaersk.) D. Legrand
Yellow
Biotic
Eugenia involucrata DC.
Red/Black
Biotic
Eugenia luschnathiana (O. Berg) Klotzsch ex B.D. Jacks.
Yellow
Biotic
Eugenia pyriformis Cambess.
Yellow
Biotic
Eugenia uniflora L.
Orange/Red
Biotic
Ficus enormis (Mart. Ex Miq.) Mart.
Red/Purple
Biotic
Ficus guaranítica (Chodat)
Green
Biotic
Ficus insipida Willd.
Green
Biotic
Ficus luschnathiana (Miq.) Miq.
Red/Purple
Biotic
Ficus obtusifolia Kunth
Yellow/Orange
Biotic
Gallesia integrifólia (Spreng.) Harms
Beige
Abiotic
Garcinia gardneriana (Planch. & Triana) Zappi
Yellow
Biotic
Genipa Americana L.
Green/Brown
Biotic
Gochnatia polymorpha (Less.) Cabrera
White
Abiotic
Guapira graciliflora (Mart. Ex J.A. Schmidt) Lundell
Black
Biotic
Guarea kunthiana A. Juss.
Brown
Biotic
Guazuma ulmifolia Lam.
Black
Biotic
Handroanthus chrysotrichus (Mart. ex A. DC.) Mattos
Green
Abiotic
Handroanthus heptaphyllus (Vell.) Mattos
Brown
Abiotic
Handroanthus impetiginosus (Mart. ex DC.) Mattos
Brown
Abiotic
Heliocarpus popayanensis Kunth
Beige
Abiotic
Hexachlamys edulis (O. Berg) Kausel & D. Legrand
Yellow
Biotic
Hymenaea courbaril L.
Green
Biotic
Inga laurina (Sw.) Willd.
Green
Biotic
Inga marginata Willd.
Green
Biotic
Inga uruguensis Hook. & Arn.
Green
Biotic
Inga vera Willd.
Green
Biotic
Jacaranda micranta Cham.
Black
Abiotic
Jacaratia spinosa (Aubl.) A. DC.
Yellow
Biotic
Lafoensia glyptocarpa Koehne
Green
Abiotic
Lafoensia pacari A. St.-Hil.
Brown
Abiotic
Leucochloron incuriale (Vell.) Barneby & J.W. Grimes
Yellow
Abiotic
Lonchocarpus campestres Mart. ex Benth.
Green
Abiotic
Lonchocarpus cultratus (Vell.) A.M.G. Azevedo & H.C. Lima
Green
Abiotic
Lonchocarpus muehlbergianus Hassl.
Brown
Abiotic
Luehea divaricata Mart.
Green
Abiotic
Luehea grandiflora Mart.
Green
Abiotic
Mabea fistulifera Mart.
Green
Abiotic
Machaerium hirtum (Vell.) Stellfeld
Brown
Abiotic
Machaerium stipitatum (DC.) Vogel
Brown
Abiotic
Machaerium villosum Vogel
Brown
Abiotic
Machaerium brasiliense Vogel
Green
Abiotic
Maclura tinctoria (L.) D. Don ex Steud.
Green
Biotic
Miconia cabucu Hoehne
Yellow
Biotic
Mimosa bimucronata (DC.) Kuntze
Brown
Abiotic
Mimosa scabrella Benth.
Brown
Abiotic
Myracrodruon urundeuva Allemão
Black
Abiotic
Myrciaria floribunda (H. West ex Willd.) O. Berg
Red
Biotic
Myrciaria glazioviana (Kiaersk.) G.M. Barroso ex Sobral
Yellow
Biotic
Myroxylon peruiferum L.f.
Beige
Abiotic
Myrsine umbellata Mart.
Black
Biotic
Nectandra megapotamica (Spreng.) Mez
Black
Biotic
Ocotea puberula (Rich.) Nees
Black/Red
Biotic
Ormosia arborea (Vell.) Harms
Orange/Black
Abiotic
Parapiptadenia rígida (Benth.) Brenan
Brown
Abiotic
Peltophorum dubium (Spreng.) Taub.
Beige
Abiotic
Persea pyrifolia (D. Don) Spreng.
Green
Biotic
Phytolacca dioica L.
Yellow
Abiotic
Piptadenia gonoacantha (Mart.) J.F. Macbr.
Green
Abiotic
Piptocarpha axillaris (Less.) Baker
**
Abiotic
Piptocarpha rotundifolia (Less.) Baker
**
Abiotic
Platypodium elegans Vogel
Beige
Abiotic
Plinia edulis (Vell.) Sobral
Yellow
Biotic
Poecilanthe parviflora Benth.
Brown
Abiotic
Posoqueria acutifolia Mart.
Yellow
Abiotic
Pouteria torta (Mart.) Radlk.
Yellow
Abiotic
Prunus sellowii Koehne
Purple
Biotic
Psidium cattleianum Sabine
Yellow
Biotic
Psidium guajava L.
Green/Red
Biotic
Psidium longipetiolatum D. Legrand
Purple
Biotic
Psidium rufum DC.
Green
Biotic
Psychotria carthagenensis Jacq.
Red
Biotic
Pterocarpus violaceus Vogel
Beige
Abiotic
Pterogyne nitens Tul.
Beige
Abiotic
Rapanea ferrugínea (Ruiz & Pav.) Mez
Black
Biotic
Rapanea gardneriana (A. DC.) Mez
Black
Biotic
Rauvolfia sellowii Müll. Arg.
Black
Biotic
Rhamnidium elaeocarpum Reissek
Red
Biotic
Sapium glandulatum (Vell.) Pax
Red
Biotic
Schefflera morototoni (Aubl.) Maguire, Steyerm. & Frodin
Brown
Biotic
Schinus molle L.
Red
Biotic
Schinus terebinthifolius Raddi
Red
Biotic
Schizolobium parahyba (Vell.) S.F. Blake
Beige
Abiotic
Seguieria langsdorffii Moq.
Black
Abiotic
Senna alata (L.) Roxb.
Black
Abiotic
Senna macranthera (DC. ex Collad.) H.S. Irwin & Barneby
Black
Abiotic
Senna multijuga (Rich.) H.S. Irwin & Barneby
Brown
Biotic
Senna pendula (Humb. & Bonpl. ex Willd.) H.S. Irwin & Barneby
Green
Abiotic
Simira sampaiona (Standl.) Steyerm.
Green
Abiotic
Solanum erianthum D. Don
Yellow
Biotic
Solanum granuloso-leprosum Dunal
**
Biotic
Solanum lycocarpum A. St.-Hil.
Green/Yellow
Biotic
Solanum pseudoquina A. St.-Hil.
Yellow
Biotic
Sparattosperma leucanthum (Vell.) K. Schum.
Beige
Abiotic
Strychnos brasiliensis (Spreng.) Mart.
Yellow
Biotic
Styrax pohlii A. DC.
Black
Biotic
Syagrus romanzoffiana (Cham.) Glassman
Yellow
Biotic
Tabebuia avellanedae Lorentz ex Griseb.
Green
Abiotic
Tabebuia ochracea A.H. Gentry
Green
Abiotic
Tabebuia roseo alba (Ridl.) Sand.
Green
Abiotic
Tabernaemontana hystrix Steud.
Red
Biotic
Terminalia argentea Mart.
Beige
Abiotic
Terminalia brasiliensis Spreng.
Yellow
Abiotic
Trema micranta (L.) Blume
Red
Biotic
Vantanea compacta (Schnizl.) Cuatrec.
Yellow
Biotic
Vitex montevidensis Cham.
Black
Biotic
Vochysia tucanorum Mart.
Green
Abiotic
Xylosma glaberrima Sleumer
**
Biotic
Zanthoxylum caribaeum Lam.
Purple
Biotic
Zanthoxylum rhoifolium Lam.
Purple
Biotic
Zeyheria tuberculosa (Vell.) Bureau ex Verl.
Brown
Abiotic
Source: *Resolução SMA - 8/2008 (São Paulo, 2008).
**
unknown.
), which are diverging to tropical forests, where red and black fruits represent 50~70% of all fleshy fruits (Wheelwright and Janson, 1985WHEELWRIGHT, N.T. and JANSON, C.H., 1985. Colors of fruit displays of bird-dispersed plants in two tropical forests. American Naturalist, vol. 126, no. 6, pp. 777-799. http://dx.doi.org/10.1086/284453.
http://dx.doi.org/10.1086/284453...
).
In restored areas, animal seed dispersion is an ecosystem ecological functionality that is expected to be recovered and managed (SER, 2002SOCIETY FOR ECOLOGICAL RESTORATION – SER, 2002. SER primer on ecological restoration. Washington: SER. 16 p.). For attracting birds, an appropriate species selection and management of the area is required. Adaptive management is a challenge for restorers as it depends on research and science as key elements for restoration decisions (Failing et al., 2013FAILING, L., GREGORY, R. and HIGGINS, P., 2013. Science, uncertainty, and values in ecological restoration: a case study in structured decision-making and adaptive management. Restoration Ecology, vol. 21, no. 4, pp. 422-430. http://dx.doi.org/10.1111/j.1526-100X.2012.00919.x.
http://dx.doi.org/10.1111/j.1526-100X.20...
), and interference in a restoration process is necessary to establish objectives and to adjust future management actions (LoSchiavo et al., 2013LOSCHIAVO, A.J., BEST, R.G., BURNS, R.E., GRAY, S., HARWELL, M.C., HINES, E.B., MCLEAN, A.R., ST. CLAIR, T., TRAXLER, S. and VEARIL, J.W., 2013. Lessons learned from the first decade of adaptive management in comprehensive Everglades restoration. Ecology and Society, vol. 18, no. 4, pp. 70. http://dx.doi.org/10.5751/ES-06065-180470.
http://dx.doi.org/10.5751/ES-06065-18047...
).
In our study, new restored sites were potentially more attractive to birds than fragments, especially for blue and black fruits, suggesting that plant species selection needs to consider these fruit colors. The re-establishment of ecosystem functionality and services is one of the most important goals in restoration ecology and often exhibits divergent and unpredictable pathways (Chazdon, 2008CHAZDON, R.L., 2008. Beyond deforestation: restoring forests and ecosystem services on degraded lands. Science, vol. 320, no. 5882, pp. 1458-1460. http://dx.doi.org/10.1126/science.1155365. PMid:18556551.
http://dx.doi.org/10.1126/science.115536...
). Enrichment with shade tolerant shrubs or forest species with black and/or red fruits may be an alternative way to manage established restorations. On the other hand, in recently established or new restorations, the introduction of pioneer shrubs or short-lived forest species having blue fruits would be more appropriate, but also those having black or red ones might be considered.
Adaptive practices may be used to manage forest restoration, by selecting pioneers with blue (e.g. Psychotria suterella Müll. Arg. and Miconia affinis DC) or black (e.g. Myrsine coriacea (Sw.) R.Br. ex Roem. & Schult. and Dendropanax cuneatus (DC.) Decne. & Planch.) fruits and secondary or climax species with more conspicuous fruits such as red (e.g. Cabralea canjerana (Vell.) Mart. and Cordia ecalyculata Vell.) or black (e.g. Cupania vernalis Cambess. and Nectandra megapotamica (Spreng.) Mez).
Our results suggest that fruit color should be taken into account when selecting the species to be used in reforestation programs, whether planting or enrichment. This could speed up the process of ecological succession and optimize the recovery of degraded areas.
Appendix A Plant species available in the nursery or planted in the Centro de Experimentos Florestais, in the region of Itu, state of São Paulo, with colors of fruits/diasporas and dispersal syndrome (biotic or abiotic).
Taxon | Fruit/diaspore color | Seed dispersal* | |
---|---|---|---|
Acacia caven Molina | Brown | Abiotic | |
Acacia polyphylla DC. | Black/Yellow | Abiotic | |
Aegiphila sellowiana Cham. | Orange | Biotic | |
Albizia polyphylla E. Fourn. | Brown | Abiotic | |
Allophylus edulis (A. St.-Hil., A. Juss. & Cambess.) Hieron. ex Niederl. | Red | Biotic | |
Allophylus petiolulatus Radlk. | Red | Biotic | |
Aloysia virgate (Ruiz & Pav.) Pers. | White | Abiotic | |
Anadenanthera falcate (Benth.) Speg. | Brown | Abiotic | |
Anadenanthera macrocarpa (Benth.) Brenan | Brown | Abiotic | |
Anadenanthera peregrina (L.) Speg. | Brown | Abiotic | |
Annona cacans Warm. | Green | Biotic | |
Annona coriácea Mart. | Green | Biotic | |
Apeiba tibourbou Aubl. | Green | Abiotic | |
Aspidosperma parvifolium A.DC. | Beige | Abiotic | |
Aspidosperma cylindrocarpon Müll. Arg. | Brown | Abiotic | |
Aspidosperma ramiflorum Müll. Arg. | Brown | Abiotic | |
Astronium graveolens Jacq. | Brown | Abiotic | |
Balfourodendron riedelianum (Engl.) Engl. | Yellow | Abiotic | |
Bastardiopsis densiflora (Hook. & Arn.) Hassl. | Green | Abiotic | |
Bauhinia forficata Link | Brown | Abiotic | |
Byrsonima sericea DC. | Yellow | Biotic | |
Cabralea canjerana (Vell.) Mart. | Red | Biotic | |
Calophyllum brasiliensis Camb. | Green | Biotic | |
Campomanesia eugenioides (Cambess.) D. Legrand ex L.R. Landrum | Green | Biotic | |
Campomanesia neriiflora (O. Berg) Nied. | Green | Biotic | |
Campomanesia xanthocarpa Mart. Ex O. Berg | Yellow | Biotic | |
Capsicodendron dinisii (Schwacke) Occhioni | Red | Biotic | |
Cariniana estrellensis (Raddi) Kuntze | Beige | Abiotic | |
Cariniana legalis (Mart.) Kuntze | Beige | Abiotic | |
Casearia gossypiosperma Briq. | Yellow/Green | Biotic | |
Casearia sylvestris Sw. | Red/Black | Biotic | |
Cassia ferruginea (Schrad.) Schrader ex DC. | Brown | Abiotic | |
Cassia leptophylla Vogel | Brown | Abiotic | |
Cecropia hololeuca Miq. | Brown | Biotic | |
Cecropia pachystachya Trécul | Green | Biotic | |
Cedrela fissilis Vell. | Brown | Abiotic | |
Cedrela odorata L. | Brown | Abiotic | |
Ceiba speciosa (A. St.-Hil.) Ravenna | Green | Abiotic | |
Centrolobium tomentosum Guillemin ex Benth. | Brown | Abiotic | |
Chorisia glaziovii (Kuntze) E. Santos | Green | Abiotic | |
Chorisia speciose A. St.-Hil. | Green | Abiotic | |
Chrysophyllum gonocarpum (Mart. & Eichler ex Miq.) Engl. | Yellow | Biotic | |
Citharexylum mirianthum Cham. | Red | Biotic | |
Citharexylum solanaceum Cham. | Orange | Biotic | |
Colubrina glandulosa Perkins | Black | Biotic | |
Copaifera langsdorffii Desf. | Orange/Black | Biotic | |
Cordia americana (L.) Gottschling & J.S. Mill. | Brown | Abiotic | |
Cordia ecalyculata Vell. | Red | Biotic | |
Cordia sellowiana Cham. | Yellow | Biotic | |
Cordia superba Cham. | White | Biotic | |
Cordia trichotoma (Vell.) Arráb. Ex Steud. | Green | Abiotic | |
Couroupita guianensis Aubl. | Yellow | Biotic | |
Coutarea hexandra (Jacq.) K. Schum. | Green | Abiotic | |
Croton floribundus Spreng. | Green | Abiotic | |
Croton urucurana Baill. | Green | Abiotic | |
Cryptocarya aschersoniana Mez | Yellow | Biotic | |
Cupania vernalis Cambess. | Black/Red | Biotic | |
Curatella americana L. | Red | Biotic | |
Cyclolobium vecchi A. Samp. Ex Hoehne | Beige | Abiotic | |
Dendropanax cuneatum Decne. & Planch. | Green | Biotic | |
Dictyoloma vandellianum A. Juss. | Beige | Abiotic | |
Dilodendron bipinnatum Radlk. | Black | Biotic | |
Diospyros inconstans Jacq. | Purple | Biotic | |
Diplokeleba floribunda N.E. Br. | Brown | Abiotic | |
Enterolobium contortisiliquum (Vell.) Morong | Black | Abiotic | |
Enterolobium timbouva Mart. | Black | Abiotic | |
Eriotheca gracilipes (K. Schum.) A. Robyns | Green | Abiotic | |
Erythrina speciosa Andrews | Brown | Abiotic | |
Erythrina crista-galli L. | Brown | Abiotic | |
Erythrina falcate Benth. | Brown | Abiotic | |
Erythrina velutina Willd. | Green | Abiotic | |
Erythroxylum deciduum A. St.-Hil. | Red | Biotic | |
Erythrina verna Vell. | Brown | Abiotic | |
Esenbeckia leiocarpa Engl. | Green | Abiotic | |
Eugenia brasiliensis Lam. | Red/Black | Biotic | |
Eugenia cerasiflora Miq. | Red | Biotic | |
Eugenia candolleana DC. | Black | Biotic | |
Eugenia dysenterica DC. | Yellow | Biotic | |
Eugenia glazioviana (Kiaersk.) D. Legrand | Yellow | Biotic | |
Eugenia involucrata DC. | Red/Black | Biotic | |
Eugenia luschnathiana (O. Berg) Klotzsch ex B.D. Jacks. | Yellow | Biotic | |
Eugenia pyriformis Cambess. | Yellow | Biotic | |
Eugenia uniflora L. | Orange/Red | Biotic | |
Ficus enormis (Mart. Ex Miq.) Mart. | Red/Purple | Biotic | |
Ficus guaranítica (Chodat) | Green | Biotic | |
Ficus insipida Willd. | Green | Biotic | |
Ficus luschnathiana (Miq.) Miq. | Red/Purple | Biotic | |
Ficus obtusifolia Kunth | Yellow/Orange | Biotic | |
Gallesia integrifólia (Spreng.) Harms | Beige | Abiotic | |
Garcinia gardneriana (Planch. & Triana) Zappi | Yellow | Biotic | |
Genipa Americana L. | Green/Brown | Biotic | |
Gochnatia polymorpha (Less.) Cabrera | White | Abiotic | |
Guapira graciliflora (Mart. Ex J.A. Schmidt) Lundell | Black | Biotic | |
Guarea kunthiana A. Juss. | Brown | Biotic | |
Guazuma ulmifolia Lam. | Black | Biotic | |
Handroanthus chrysotrichus (Mart. ex A. DC.) Mattos | Green | Abiotic | |
Handroanthus heptaphyllus (Vell.) Mattos | Brown | Abiotic | |
Handroanthus impetiginosus (Mart. ex DC.) Mattos | Brown | Abiotic | |
Heliocarpus popayanensis Kunth | Beige | Abiotic | |
Hexachlamys edulis (O. Berg) Kausel & D. Legrand | Yellow | Biotic | |
Hymenaea courbaril L. | Green | Biotic | |
Inga laurina (Sw.) Willd. | Green | Biotic | |
Inga marginata Willd. | Green | Biotic | |
Inga uruguensis Hook. & Arn. | Green | Biotic | |
Inga vera Willd. | Green | Biotic | |
Jacaranda micranta Cham. | Black | Abiotic | |
Jacaratia spinosa (Aubl.) A. DC. | Yellow | Biotic | |
Lafoensia glyptocarpa Koehne | Green | Abiotic | |
Lafoensia pacari A. St.-Hil. | Brown | Abiotic | |
Leucochloron incuriale (Vell.) Barneby & J.W. Grimes | Yellow | Abiotic | |
Lonchocarpus campestres Mart. ex Benth. | Green | Abiotic | |
Lonchocarpus cultratus (Vell.) A.M.G. Azevedo & H.C. Lima | Green | Abiotic | |
Lonchocarpus muehlbergianus Hassl. | Brown | Abiotic | |
Luehea divaricata Mart. | Green | Abiotic | |
Luehea grandiflora Mart. | Green | Abiotic | |
Mabea fistulifera Mart. | Green | Abiotic | |
Machaerium hirtum (Vell.) Stellfeld | Brown | Abiotic | |
Machaerium stipitatum (DC.) Vogel | Brown | Abiotic | |
Machaerium villosum Vogel | Brown | Abiotic | |
Machaerium brasiliense Vogel | Green | Abiotic | |
Maclura tinctoria (L.) D. Don ex Steud. | Green | Biotic | |
Miconia cabucu Hoehne | Yellow | Biotic | |
Mimosa bimucronata (DC.) Kuntze | Brown | Abiotic | |
Mimosa scabrella Benth. | Brown | Abiotic | |
Myracrodruon urundeuva Allemão | Black | Abiotic | |
Myrciaria floribunda (H. West ex Willd.) O. Berg | Red | Biotic | |
Myrciaria glazioviana (Kiaersk.) G.M. Barroso ex Sobral | Yellow | Biotic | |
Myroxylon peruiferum L.f. | Beige | Abiotic | |
Myrsine umbellata Mart. | Black | Biotic | |
Nectandra megapotamica (Spreng.) Mez | Black | Biotic | |
Ocotea puberula (Rich.) Nees | Black/Red | Biotic | |
Ormosia arborea (Vell.) Harms | Orange/Black | Abiotic | |
Parapiptadenia rígida (Benth.) Brenan | Brown | Abiotic | |
Peltophorum dubium (Spreng.) Taub. | Beige | Abiotic | |
Persea pyrifolia (D. Don) Spreng. | Green | Biotic | |
Phytolacca dioica L. | Yellow | Abiotic | |
Piptadenia gonoacantha (Mart.) J.F. Macbr. | Green | Abiotic | |
Piptocarpha axillaris (Less.) Baker | ** ** unknown. | Abiotic | |
Piptocarpha rotundifolia (Less.) Baker | ** ** unknown. | Abiotic | |
Platypodium elegans Vogel | Beige | Abiotic | |
Plinia edulis (Vell.) Sobral | Yellow | Biotic | |
Poecilanthe parviflora Benth. | Brown | Abiotic | |
Posoqueria acutifolia Mart. | Yellow | Abiotic | |
Pouteria torta (Mart.) Radlk. | Yellow | Abiotic | |
Prunus sellowii Koehne | Purple | Biotic | |
Psidium cattleianum Sabine | Yellow | Biotic | |
Psidium guajava L. | Green/Red | Biotic | |
Psidium longipetiolatum D. Legrand | Purple | Biotic | |
Psidium rufum DC. | Green | Biotic | |
Psychotria carthagenensis Jacq. | Red | Biotic | |
Pterocarpus violaceus Vogel | Beige | Abiotic | |
Pterogyne nitens Tul. | Beige | Abiotic | |
Rapanea ferrugínea (Ruiz & Pav.) Mez | Black | Biotic | |
Rapanea gardneriana (A. DC.) Mez | Black | Biotic | |
Rauvolfia sellowii Müll. Arg. | Black | Biotic | |
Rhamnidium elaeocarpum Reissek | Red | Biotic | |
Sapium glandulatum (Vell.) Pax | Red | Biotic | |
Schefflera morototoni (Aubl.) Maguire, Steyerm. & Frodin | Brown | Biotic | |
Schinus molle L. | Red | Biotic | |
Schinus terebinthifolius Raddi | Red | Biotic | |
Schizolobium parahyba (Vell.) S.F. Blake | Beige | Abiotic | |
Seguieria langsdorffii Moq. | Black | Abiotic | |
Senna alata (L.) Roxb. | Black | Abiotic | |
Senna macranthera (DC. ex Collad.) H.S. Irwin & Barneby | Black | Abiotic | |
Senna multijuga (Rich.) H.S. Irwin & Barneby | Brown | Biotic | |
Senna pendula (Humb. & Bonpl. ex Willd.) H.S. Irwin & Barneby | Green | Abiotic | |
Simira sampaiona (Standl.) Steyerm. | Green | Abiotic | |
Solanum erianthum D. Don | Yellow | Biotic | |
Solanum granuloso-leprosum Dunal | ** ** unknown. | Biotic | |
Solanum lycocarpum A. St.-Hil. | Green/Yellow | Biotic | |
Solanum pseudoquina A. St.-Hil. | Yellow | Biotic | |
Sparattosperma leucanthum (Vell.) K. Schum. | Beige | Abiotic | |
Strychnos brasiliensis (Spreng.) Mart. | Yellow | Biotic | |
Styrax pohlii A. DC. | Black | Biotic | |
Syagrus romanzoffiana (Cham.) Glassman | Yellow | Biotic | |
Tabebuia avellanedae Lorentz ex Griseb. | Green | Abiotic | |
Tabebuia ochracea A.H. Gentry | Green | Abiotic | |
Tabebuia roseo alba (Ridl.) Sand. | Green | Abiotic | |
Tabernaemontana hystrix Steud. | Red | Biotic | |
Terminalia argentea Mart. | Beige | Abiotic | |
Terminalia brasiliensis Spreng. | Yellow | Abiotic | |
Trema micranta (L.) Blume | Red | Biotic | |
Vantanea compacta (Schnizl.) Cuatrec. | Yellow | Biotic | |
Vitex montevidensis Cham. | Black | Biotic | |
Vochysia tucanorum Mart. | Green | Abiotic | |
Xylosma glaberrima Sleumer | ** ** unknown. | Biotic | |
Zanthoxylum caribaeum Lam. | Purple | Biotic | |
Zanthoxylum rhoifolium Lam. | Purple | Biotic | |
Zeyheria tuberculosa (Vell.) Bureau ex Verl. | Brown | Abiotic |
http://www.cetesb.sp.gov.br/licenciament... ).
Acknowledgements
We thank Aretha Medina and all the staff of Centro de Experimentos Florestais de Itu/SOS Mata Atlântica, for their support during the fieldwork. We also thank Mariana de Castro, Marina Maximiano and Leandro Moraes for their help in the field, Fiorella F. M. Capelo for suggestions of some species having blue fruits and two anonymous referees for their revisions, which have significantly improved this manuscript.
-
(With 3 figures)
References
- ALVES-COSTA, P. and LOPES, A.V., 2001. Using artificial fruits to evaluate fruit selection by birds in the field. Biotropica, vol. 33, no. 4, pp. 713-717. http://dx.doi.org/10.1111/j.1744-7429.2001.tb00230.x
» http://dx.doi.org/10.1111/j.1744-7429.2001.tb00230.x - ANALYTICAL SOFTWARE2013viewed 2 January 2015Statistix 8.0softwareAvailable from: http://www.statistix.com/free-trial/
» http://www.statistix.com/free-trial/ - ARRUDA, R.D., RODRIGUES, J. and IZZO, T.J., 2008. Rapid assessment of fruit-color selection by birds using artificial fruits at local scale in Central Amazonia. Acta Amazonica, vol. 38, no. 2, pp. 291-296. http://dx.doi.org/10.1590/S0044-59672008000200011
» http://dx.doi.org/10.1590/S0044-59672008000200011 - BARCELOS, A.O., PERÔNICO, C.P. and EUTRÓPIO, F.J., 2012. Color and odor of artificial fruit used to signal potential dispersers in the Atlantic forest in Brazil. Revista de Biologia Tropical, vol. 60, no. 2, pp. 925-931. PMid:23894956.
- CAVALLERO, L., RAFFAELE, E. and AIZEN, M.A., 2012. Birds as mediators of passive restoration during early post-fire recovery. Biological Conservation, vol. 158, pp. 342-350. http://dx.doi.org/10.1016/j.biocon.2012.10.004
» http://dx.doi.org/10.1016/j.biocon.2012.10.004 - CAZETTA, E., SCHAEFER, H.M. and GALETTI, M., 2009. Why are fruits colorful? The relative importance of achromatic and chromatic contrasts for detection by birds. Evolutionary Ecology, vol. 23, no. 2, pp. 233-244. http://dx.doi.org/10.1007/s10682-007-9217-1
» http://dx.doi.org/10.1007/s10682-007-9217-1 - CENTRO DE PESQUISAS METEOROLÓGICAS E CLIMÁTICAS APLICADAS À AGRICULTURA – CEPAGRI, 2015 [viewed 20 February 2015]. Clima dos Municípios Paulistas [online]. Available from: http://www.cepagri.unicamp.br/outras-informacoes/clima-dos-municipios-paulistas.html
» http://www.cepagri.unicamp.br/outras-informacoes/clima-dos-municipios-paulistas.html - CHAZDON, R.L., 2008. Beyond deforestation: restoring forests and ecosystem services on degraded lands. Science, vol. 320, no. 5882, pp. 1458-1460. http://dx.doi.org/10.1126/science.1155365 PMid:18556551.
» http://dx.doi.org/10.1126/science.1155365 - CLASSEN, A., PETERS, M.K., FERGER, S.W., HELBIG-BONITZ, M., SCHMACK, J.M., MAASSEN, G., SCHLEUNING, M., KALKO, E.K.V., BÖHNING-GAESE, K. and STEFFAN-DEWENTER, I., 2014. Complementary ecosystem services provided by pest predators and pollinators increase quantity and quality of coffee yields. Proceedings. Biological Sciences, vol. 281, no. 1779, pp. 1-7. http://dx.doi.org/10.1098/rspb.2013.3148 PMid:24500173.
» http://dx.doi.org/10.1098/rspb.2013.3148 - COLE, R.J., HOLL, K.D. and ZAHAWI, R.A., 2010. Seed rain under tree islands planted to restore degraded lands in a tropical agricultural landscape. Ecological Applications, vol. 20, no. 5, pp. 1255-1269. http://dx.doi.org/10.1890/09-0714.1 PMid:20666248.
» http://dx.doi.org/10.1890/09-0714.1 - ENGELBRECHT, B.M. and HERZ, H.M., 2001. Evaluation of different methods to estimate understorey light conditions in tropical forests. Journal of Tropical Ecology, vol. 17, no. 2, pp. 207-224. http://dx.doi.org/10.1017/S0266467401001146
» http://dx.doi.org/10.1017/S0266467401001146 - FAHRIG, L., 2003. Effects of habitat fragmentation on biodiversity. Annual Review of Ecology Evolution and Systematics, vol. 34, no. 1, pp. 487-515. http://dx.doi.org/10.1146/annurev.ecolsys.34.011802.132419
» http://dx.doi.org/10.1146/annurev.ecolsys.34.011802.132419 - FAILING, L., GREGORY, R. and HIGGINS, P., 2013. Science, uncertainty, and values in ecological restoration: a case study in structured decision-making and adaptive management. Restoration Ecology, vol. 21, no. 4, pp. 422-430. http://dx.doi.org/10.1111/j.1526-100X.2012.00919.x
» http://dx.doi.org/10.1111/j.1526-100X.2012.00919.x - FLEMING, T.H. and JOHN KRESS, W., 2011. A brief history of fruit and frugivores. Acta Oecologica, vol. 37, no. 6, pp. 521-530. http://dx.doi.org/10.1016/j.actao.2011.01.016
» http://dx.doi.org/10.1016/j.actao.2011.01.016 - GALETTI, M., ALVES-COSTA, C.P. and CAZETTA, E., 2003. Effects of forest fragmentation, anthropogenic edges and fruit colour on the consumption of ornithocoric fruits. Biological Conservation, vol. 111, no. 2, pp. 269-273. http://dx.doi.org/10.1016/S0006-3207(02)00299-9
» http://dx.doi.org/10.1016/S0006-3207(02)00299-9 - GOMES, L.G.L., OOSTRA, V., NIJMAN, V., CLEEF, A.M. and KAPPELLE, M., 2008. Tolerance of frugivorous birds to habitat disturbance in a tropical cloud forest. Biological Conservation, vol. 141, no. 3, pp. 860-871. http://dx.doi.org/10.1016/j.biocon.2008.01.007
» http://dx.doi.org/10.1016/j.biocon.2008.01.007 - GONÇALVES, V.F., SILVA, A.M., BAESSE, C.Q. and MELO, C., 2015. Frugivory and potential of birds as dispersers of . Siparuna guianensisBrazilian Journal of Biology = Revista Brasileira de Biologia, vol. 75, no. 2, pp. 300-304. http://dx.doi.org/10.1590/1519-6984.11413 PMid:26132011.
» http://dx.doi.org/10.1590/1519-6984.11413 - GRAY, C.L. and LEWIS, O.T., 2014. Do riparian forest fragments provide ecosystem services or disservices in surrounding oil palm plantations? Basic and Applied Ecology, vol. 15, no. 8, pp. 693-700. http://dx.doi.org/10.1016/j.baae.2014.09.009
» http://dx.doi.org/10.1016/j.baae.2014.09.009 - HART, N.S., 2001. The visual ecology of avian photoreceptors. Progress in Retinal and Eye Research, vol. 20, no. 5, pp. 675-703. http://dx.doi.org/10.1016/S1350-9462(01)00009-X PMid:11470455.
» http://dx.doi.org/10.1016/S1350-9462(01)00009-X - Isbell, F., Calcagno, V., Hector, A., Connolly, J., Harpole, W.S., Reich, P.B., Scherer-Lorenzen, M., Schmid, B., Tilman, D., van Ruijven, J., Weigelt, A., Wilsey, B.J., Zavaleta, E.S. and Loreau, M., 2011. High plant diversity is needed to maintain ecosystem services. Nature, vol. 477, no. 7363, pp. 199-202. http://dx.doi.org/10.1038/nature10282 PMid:21832994.
» http://dx.doi.org/10.1038/nature10282 - LAURANCE, W.F. and BIERREGAARD, R.O., 1997. Tropical forest remnants: ecology, management and conservation of fragmented communities. Chicago: University of Chicago Press. 632 p.
- LOSCHIAVO, A.J., BEST, R.G., BURNS, R.E., GRAY, S., HARWELL, M.C., HINES, E.B., MCLEAN, A.R., ST. CLAIR, T., TRAXLER, S. and VEARIL, J.W., 2013. Lessons learned from the first decade of adaptive management in comprehensive Everglades restoration. Ecology and Society, vol. 18, no. 4, pp. 70. http://dx.doi.org/10.5751/ES-06065-180470
» http://dx.doi.org/10.5751/ES-06065-180470 - LUNDBERG, J. and MOBERG, F., 2003. Mobile link organisms and ecosystem functioning: implications for ecosystem resilience and management. Ecosystems, vol. 6, no. 1, pp. 87-98. http://dx.doi.org/10.1007/s10021-002-0150-4
» http://dx.doi.org/10.1007/s10021-002-0150-4 - MARTIN, G.R., 1993. Producing the image. In: H.P. ZEIGLER and H.J. BISCHOF, eds. Vision brain, and behavior in birds. Cambridge: MIT Press. p. 5-24.
- MARTINS, A.F., 2011. Controle de gramíneas exóticas invasoras em área de restauração ecológica com plantio total, Floresta Estacional Semidecidual, Itu, SP. Piracicaba: Universidade de São Paulo. 112 p. Dissertação de Mestrado em Recursos Florestais.
- MCCONKEY, K.R., PRASAD, S., CORLETT, R.T., CAMPOS-ARCEIZ, A., BRODIE, J.F., ROGERS, H. and SANTA-MARIA, L., 2012. Seed dispersal in changing landscapes. Biological Conservation, vol. 146, no. 1, pp. 1-13. http://dx.doi.org/10.1016/j.biocon.2011.09.018
» http://dx.doi.org/10.1016/j.biocon.2011.09.018 - MENZ, M.H.M., PHILLIPS, R.D., WINFREE, R., KREMEN, C., AIZEN, M.A., JOHNSON, S.D. and DIXON, K.W., 2011. Reconnecting plants and pollinators: challenges in the restoration of pollination mutualisms. Trends in Plant Science, vol. 16, no. 1, pp. 4-12. http://dx.doi.org/10.1016/j.tplants.2010.09.006 PMid:20980193.
» http://dx.doi.org/10.1016/j.tplants.2010.09.006 - MOLEÓN, M., SÁNCHEZ-ZAPATA, J.A., MARGALIDA, A., CARRETE, M., OWEN-SMITH, N. and DONÁZAR, J.A., 2014. Humans and Scavengers: the evolution of interactions and ecosystem services. Bioscience, vol. 64, no. 5, pp. 394-403. http://dx.doi.org/10.1093/biosci/biu034
» http://dx.doi.org/10.1093/biosci/biu034 - MUNGER, S.D., LEINDERS-ZUFALL, T. and ZUFALL, F., 2009. Subsystem organization of the Mammalian sense of smell. Annual Review of Physiology, vol. 71, no. 1, pp. 115-140. http://dx.doi.org/10.1146/annurev.physiol.70.113006.100608 PMid:18808328.
» http://dx.doi.org/10.1146/annurev.physiol.70.113006.100608 - NAVE, A.G. and RODRIGUES, R.R., 2007. Combination of species into filling and diversity groups as forest restoration methodology. In: R.R. RODRIGUES, S.V. MARTINS and S. GANDOLFI, orgs. High diversity forest restoration in degraded areas: methods and projects in Brazil. New York: Nova Science Publishers, pp. 103-126.
- NUISMER, S.L., JORDANO, P. and BASCOMPTE, J., 2013. Co-evolution and the architecture of mutualistic networks. Evolution, vol. 67, no. 2, pp. 338-354. http://dx.doi.org/10.1111/j.1558-5646.2012.01801.x PMid:23356608.
» http://dx.doi.org/10.1111/j.1558-5646.2012.01801.x - PIÑA-RODRIGUES, F.C.M., PIRATELLI, A.J., RUDGE, A.C., GONDIM, F.R., FREIRE, M. and CORREA, J.S., 2009. Mobile links in fragmented ecosystem: seed and birds dispersal approach towards Atlantic forest restoration and conservation. In: H. GAESE, J.C.T. ALBINO, J. WESENBERG and S. SCHLÜTER, eds. Biodiversity and land use systems in the fragmented Mata Atlântica of Rio de Janeiro. Göttingen: Cuvillier Verlag, pp. 313-360.
- PUCKEY, H.L., LILL, A. and O’DOWD, D.J., 1996. Fruit color choices of captive silvereyes (). Zosterops lateralisThe Condor, vol. 98, no. 4, pp. 780-790. http://dx.doi.org/10.2307/1369858
» http://dx.doi.org/10.2307/1369858 - RODRIGUES, R.R., BRANCALION, P.H.S. and ISERNHAEN, I., 2009. Pacto pela restauração da mata atlântica: referencial dos conceitos e ações de restauração florestal. São Paulo: LERF/ESALQ. 264 p.
- SÃO PAULO. Governo do Estado. Secretaria do Meio Ambiente – SMA, 2008. [viewed 20 February 2015]. Resolução SMA - 8, de 31-1-2008. Fixa a orientação para o reflorestamento heterogêneo de áreas degradadas e dá providências correlatas [online]. São Paulo: Secretaria do Meio Ambiente. Available from: http://www.cetesb.sp.gov.br/licenciamento/documentos/2008_Res_SMA_08.pdf
» http://www.cetesb.sp.gov.br/licenciamento/documentos/2008_Res_SMA_08.pdf - SCHMIDT, V., SCHAEFER, H.M. and WINKLER, H., 2004. Conspicuousness, not colour as foraging cue in plant-animal signaling. Oikos, vol. 106, no. 3, pp. 551-557. http://dx.doi.org/10.1111/j.0030-1299.2004.12769.x
» http://dx.doi.org/10.1111/j.0030-1299.2004.12769.x - SOCIETY FOR ECOLOGICAL RESTORATION – SER, 2002. SER primer on ecological restoration. Washington: SER. 16 p.
- SOCIETY FOR ECOLOGICAL RESTORATION – SER, 2004. [viewed 21 August 2015]. The SER primer on ecological restoration [online]. Washington: SER. Available from: http://www.ser.org/
» http://www.ser.org/ - STANTURF, J.A., PALIK, B.J. and DUMROESE, R.K., 2014. Contemporary forest restoration: a review emphasizing function. Forest Ecology and Management, vol. 331, pp. 292-323. http://dx.doi.org/10.1016/j.foreco.2014.07.029
» http://dx.doi.org/10.1016/j.foreco.2014.07.029 - Steffen, W., Persson, Å., Deutsch, L., Zalasiewicz, J., Williams, M., Richardson, K., Crumley, C., Crutzen, P., Folke, C., Gordon, L., Molina, M., Ramanathan, V., Rockström, J., Scheffer, M., Schellnhuber, H.J. and Svedin, U., 2011. The Anthropocene: From Global Change to Planetary Stewardship. Ambio, vol. 40, no. 7, pp. 739-761. http://dx.doi.org/10.1007/s13280-011-0185-x PMid:22338713.
» http://dx.doi.org/10.1007/s13280-011-0185-x - SUDING, K.N., 2011. Toward an era of restoration in ecology: successes, failures, and opportunities ahead. Annual Review of Ecology Evolution and Systematics, vol. 42, no. 1, pp. 465-487. http://dx.doi.org/10.1146/annurev-ecolsys-102710-145115
» http://dx.doi.org/10.1146/annurev-ecolsys-102710-145115 - VELOSO, H.P., RANGEL-FILHO, A L.R. and LIMA, J.C.A., 1991. Classificação da vegetação brasileira adaptada a um sistema universal. Rio de Janeiro: IBGE. 124 p.
- WENNERSTEN, L. and FORSMAN, A., 2009. Does color polymorphism enhance survival of prey population? Proceedings of the Royal Society B, vol. 276, no. 1803, pp. 2187-2194. http://dx.doi.org/10.1098/rspb.2009.0252
» http://dx.doi.org/10.1098/rspb.2009.0252 - WHEELWRIGHT, N.T. and JANSON, C.H., 1985. Colors of fruit displays of bird-dispersed plants in two tropical forests. American Naturalist, vol. 126, no. 6, pp. 777-799. http://dx.doi.org/10.1086/284453
» http://dx.doi.org/10.1086/284453 - WHELAN, C.J., WENNY, D.G. and MARQUIS, R.J., 2008. Ecosystem services provided by birds. Annals of the New York Academy of Sciences, vol. 1134, no. 1, pp. 25-60. http://dx.doi.org/10.1196/annals.1439.003 PMid:18566089.
» http://dx.doi.org/10.1196/annals.1439.003 - WHITNEY, K.D., 2005. Linking frugivores to the dynamics of a fruit color polymorphism. American Journal of Botany, vol. 92, no. 5, pp. 859-867. http://dx.doi.org/10.3732/ajb.92.5.859 PMid:21652467.
» http://dx.doi.org/10.3732/ajb.92.5.859 - WILLSON, M. F. and WHELAN, C.J., 1990. The evolution of fruit color in fleshy-fruited plants. American Naturalist, vol. 136, no. 6, pp. 790-809. http://dx.doi.org/10.1086/285132
» http://dx.doi.org/10.1086/285132
Publication Dates
-
Publication in this collection
06 May 2016 -
Date of issue
Oct-Dec 2016
History
-
Received
26 Mar 2015 -
Accepted
01 Oct 2015