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Abundance of frugivorous birds and richness of fruit resource: is there a temporal relationship? PDF

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Caldasia 22(1): 93-107 ABUNOANCE OF FRUGIVOROUS BIROS ANO RICHNESS OF FRUIT RESOURCE: IS THERE A TEMPORAL RELATIONSHIP? R. ORTIZ-PULlDO Departamento de Ecología Vegetal, Instituto de Ecología, A.C., Apartado 63, Xalapa, Veracruz, 91000, México. [email protected] Abstraet Itisbelievedthat theabundance offrugivorous birdsinalandscape isrelated to the fruit supply ineach vegetation type. Although some evidence for this relationship exists atthe birdcommunity level, it hasseldom beendemonstrated infrugivorous bird species that inhabit different vegetation types or succesional gradients in a landscape. Inthis study, Iassessedthe temporal relationships between the abun- danceof individual frugivorous birdspeciesandthe richness offruiting ornithocho- rous plant species in different, contiguous vegetation types in a neotropical landscape. Monthly variation in abundance of each frugivorous bird species cannot beexplained bythe richnessoffruiting ornithochorous plant speciesineach vegetation type. Ifound only two positive correlations out of apossible 42 (four- teen bird species inthree vegetation tvpes), which could easily bedue to chanceo Instudies ofthis type, it ispossibleto obtain different results ifthe variables areab- solute abundance offruit (e.g., numberofripefruits inanarea)orrichness orabun- dance of specific plant species eaten by each bird species assessed, instead of richness of fruiting ornithochorous plant species by vegetation type. Keywords: Frugivorous birds, landscape, ornithochorous plants, vegetation type. Resumen Secreequelaabundancia delasavesfrugívoras endiferentes parches deunpaisa- jeestárelacionada con lariquezadelrecursofruto. Aunque existe evidencia anivel decomunidad, estarelación pocasveceshasidoprobadacuantitativamente anivel deespecie paraaves frugívoras quehabitan diferentes tipos devegetación oeta- passucesionales enunpaisaje. Enestetrabajo evalué, enunpaisajeneotropical, la relación mensualentre abundancia deespeciesdeavesfrugívoras y riquezadelre- cursofruto endiferentes tipos devegetación contiguos. Laabundancia mensualde cadaespeciedeavefrugívora nosepuedeexplicar enfunción delariquezadelas especiesdeplantas ornitócoras enfruto portipo devegetación. Sóloencontré dos correlaciones positivas delas42 realizadas(catorce especiesdeavesportres tipos devegetación), locual bienpodríaserresultado delazar. Enestudios deeste tipo esposible queseobtenga otro resultado alconsiderar variables como laabundan- ciaabsoluta delrecurso fruto (v. gr., número defrutos maduros disponibles enun área)olariqueza oabundancia delasespeciesespecíficas delasque sealimenta cada especie de ave, envez de lariqueza del recurso por detipo de vegetación. Palabrasclave: Avesfrugívoras, paisaje,plantasornitócoras, tipo devegetación. 94 Caldasia Vol. 22, No. 1,2000 Introduction ornithocorous plant species in each vegetation type. The abundance of frugivorous birds is hypothe- sized to be positively related to the supply of fruit resources (Karr 1976, Wheelwright 1983, Blake Study Site &Loiselle 1991, Loiselle &Blake 1991, Levey & Field work was carried out atthe Centro de Inves- Stiles 1992). This relationship has been found to tigaciones Costeras La Mancha (CICOLMA), 10- exist between communities of frugivorous birds cated in the central coastal plain of Veracruz, and the abundance of ripe fruit inparticular vege- Mexico (19° 36' N, 96° 22' W; 100m aboye sea tation types, but ithas been found in few particu- level). The mean annual temperature is22.9° C, lar frugivorous bird species within those maximum extreme 33.3° C and minimum ex- communities (e.g., Loiselle & Blake 1991, Rey treme 12.1° C. Annual precipitation varies be- 1995, Herrera 1998). Oftwo different studies ina tween 900-1800 mm, with a dry season between tropical rain forests in Costa Rica, there is evi- October and May (Moreno-Casasola 1982, Blain dence that abundance of acommunity of frugivo- 1988). rous birds is correlated on both spatial and temporal scales with the abundance of fruit re- Two hundred and sixty-three bird species have sources within different vegetation types (Levey been recorded at CICOLMA (Ortiz-Pulido et al. 1988, Loiselle & Blake 1991). 1995, Ortiz-Pulido et al. inpress), and another 35 species that have not yet been reported in the re- If bird abundance is related to fruit abundance serve itself are known from the surrounding re- within a vegetation type at the community level, gion (López-Portillo et al. 1993, Alvarez 1994). then one would expect that abundance of individ- Birds that feed on invertebrates are the most com- ual bird species within that community is also re- mon in this area (84% ofthe species) while 36% lated to other measures of fruit abundance as of species feed on fruits and 35% inelude verte- richness ofornithochorous plants. Several studies brates in their diet (Ortiz-Pulido et al. 1995). have examined the presence or abundance ofpar- ticular frugivorous bird species inrelation to fruit Inthis reserve there are more than 70plant species availability indifferent vegetation types inaland- whose fruits have ornithochorous characteristics scape (e.g., Davies 1945, Wheelwright 1983, (e.g., red, black or purple skin with aril or pulp, Murray 1988, Herrera 1985), but few of these sensu Van der Pijl 1972 and Howe & Westley studies quantified the relationship (e.g., Loiselle 1988) but birds are known to eat the fruits of only &Blake 1993, Rey 1995, Herrera 1998; seeHutto 33of these (Ortiz-Pulido 1994). These plants are 1990, Jordano 1992 for reviews). Lack of quanti- found in seven vegetation types (sensu Novelo tative studies may be because this relationship be- 1978): shrubs on sand dunes, pastures with iso- tween individual species and fruit does notexist or lated standing trees, tropical dry forest, man- because such a relationship is difficult to detect. groves, tropical deciduous forest, flooded forest, and field crops. This study was limited tothe first In this study, I addressed the hypothesis that three of these -shrubs, pastures, and dry forest- monthly number of individuals of each frugivo- because they comprise the largest part ofthevege- rous bird species (abundance) is related to tation in CICOLMA (except for mangrove). Fru- monthly richness of ornithochorous plant species. givorous birds cross the vegetation boundaries To test this hypothesis, I determined monthly regularly such that abundance patterns of these abundance of cornmon frugivorous bird species birds could reflect potential habitat quality inhabiting three different vegetation types within (Ortiz-Pulido 1997, Ortiz-Pulido et al. in press). the Gulf of Mexico coastal region and compared Over this landscape on a community level, rich- bird abundance in relation to monthly richness of 95 Ortiz-Pulido: Bird-fruit temporal relations ness of frugivorous birds and ornithochorous teristics (sensu Howe & Westley 1988) that 1saw plants are related onamonthly basis (Ortiz-Pulido being eaten bybirds. The systematic method used et al. in press). to detect these plants (census and focal observa- tions) and an estimate of missing frugivorous- ornithochorous interactions in each vegetation Methods type (between 0-20%, depending on the analysis To assess the abundance of cornmon frugivorous used) can be checked elsewhere (Ortiz-Pulido bird species, 1walked one transect inone patch of 1994, Ortiz-Pulido etal. inpress). For each plant each of the three vegetation types, three or four collected, I recorded the date, vegetation type, times per month, from April1992 toMarch 1993. and exact collecting site. Individual plants were Each transect was approximately 1000mlong and deposited and identified inHerbarium ofthe Insti- I walked at constant speed for a duration of one tuto de Ecologia, A.C., Xalapa, Veracruz hour twenty minutes. The three vegetation types (XAL). Scientific names are reported following were surveyed once per day, changing order on Sosa & Gómez-Pompa (1994). I considered the consecutive days, starting from sunrise to 11:00 monthly total number of plant species with ripe hours, following Emlen's suggestions (1971, fruit in a vegetation type as the ornithochorous 1977). Survey effort was similar for each vegeta- monthly richness of this vegetation. tion type -about 44km were walked ineach vege- To determine the monthly relationship in each tation type each year. For each bird or group of vegetation type between abundance of each bird birds seen, I recorded species, number of indi- species and richness of ornithochorous plants, I viduals, and perpendicular distance to the tran- performed Spearman rank correlations (r.), Idid sect. 1did not register flying birds and excluded not test to detect temporal autocorrelation of the rainy or windy days. In order to reduce bias be- two assessed variables (Verdú y García-Fayos cause of different detectability in each vegetation 1994) because the result did not merit it (see be- type (e.g., in grassland a bird Canbe seen up to low). Tests of temporal autocorrelation must be 500 maway but indry forest rarely further than 20 done when significant correlations are found. m), Ialso excluded every bird observed more than 20 m from me. Iconsidered abird species to be common ifIrecorded it40or more times, and fru- Results givorous ifIsaw iteating fruits during this study. I recorded fourteen common frugivorous bird Iconsidered the total number of monthly records species in 180 hours of field work. All occurred ofeach bird species inavegetation type asameas- inallthree vegetation types. In shrubs Irecorded ure of the monthly abundance of each species in 321 frugivorous birds, inpastures 300, and indry this particular vegetation. The monthly richness forest 461. Monthly number of records by bird reported here takes into account only the common species are shown inAppendix 1. Golden-fronted frugivorous species; the monthly richness of the Woodpecker (Melanerpes aurifrons) and Social bird community isdifferent and can be found else- Flycatcher (Myiozetetes similis) were the most where (Ortiz-Pulido 1994). Scientific and com- cornmon species in all vegetation types. AIso mon names are reported following AOU (1998) cornmon in shrubs were Northern Mockingbird and status and feeding guild following Ortiz- (Mimus polyglottos), in pastures Melodious Pulido et al. (1995). Blackbird (Dives dives), and in dry forest Brown To determine the monthly richness of ornitho- Jay (Cyanocorax morio), Montezuna Oropendola chorous plant species with ripe fruit, I collected, (Psarocolius moniezumai, Black-headed Trogon ineach transect (20 mtoeach side), the plant spe- (Trogon melanocephalus), and Scissor-tailed Fly- cies with ripe fruits with ornithochorous charac- catcher (Tyrannus forficatus). In shrubs I re- 96 Caldasia Vol. 22. No. 1.2000 corded an average of 6.3 ± 0.7 bird species per frugivorous bird species and sorne measure of month, in pastures 5.1 ± 0.5, and in dry forest fruit availability (Wheelwright 1983, Rey 1995, 7.0 ± 0.8. Bird diversity was highest in shrubs in Herrera 1998). However, two of these studies April and August (nine species), in pastures in treated the same species, Sylvia atricapilla of September (eight species) and indry forest inFeb- Eurasia, thus prec1uding broader conc1usions. Of ruary, March, and May (ten species). five similar studies conducted at the community level, two found no relationship between abun- I collected 77 plant species with ornithochorous dance offrugivorous birds and richness of fruiting characteristics. I recorded 27 species with ripe ornithochorous plants (Levey 1988, Herrera fruits in shrubs, 18in pastures and 60 in dry for- 1998), one found that a relationship did exist est. Months in which each plant species was re- (Blake & Loiselle 1991, Loiselle & Blake 1991), corded are found in Appendix 2. On average 7 ± while the lasttwo assumed it,but didnottest itsta- 1.1 species had ripe fruits inshrubs during anyone tistically (Thompson & Willson 1979, Wong month, 3 ± 0.4 in pastures, and 11 ± 0.6 in dry 1986). forest. Months with higher richness were Febru- ary and November in shrubs (twelve species), It could be argued that richness of fruiting plants May (five) in pastures, and August (fourteen) in isnot the best variable touse, as itprevents detec- dry forest. tion of other kinds of relationships between the two groups of organisms, but it is not c1ear what Two combinations, out of42 tested, ofabundance other variables would be more suitable (see Hutto ofparticular frugivorous bird species and richness 1990). For example, when abundance of indi- of fruiting ornithochorous plants species, showed viduals in a cornmunity of frugivorous birds was significant correlations. Northern Mockingbird examined for correlation with the abundance of was significantIy related to fruit species richness fruiting ornithochorous plants, no c1ear relation- in shrub habitat (rs = 0.84, P < 0.001) as was ship was found. In two different studies (Levey Golden-fronted Woodpecker in pastures (rs = 1988, Loiselle & Blake 1991) where the abun- 0.60, P <0.05). Any other data processing (e.g., dance ofthree offour frugivorous groups were re- dephasíng data series one or two months earlier, lated toabundance of ripe ornithochorous fruits in or taking into account only plant species whose three vegetation types, less than 22% of the com- fruits are reported as ingested by birds in these binations tested were significantly correlated. In landscapes) gave a similar result (i.e., zero or another study Loiselle & Blake (1993) obtained a three significant correlations among the 42 com- similar result (13% ofpositive significant correla- binations). tions) when they looked for a relationship be- tween the abundance of five frugivorous bird species and three fruiting plant species eaten by Discussion these birds. However, when they tried to find a Monthly abundance of the most cornmon frugivo- correlation between each bird and plant species rous birds species inhabiting the vegetation types studied, they found O.(X}3%of significant correla- studied cannot be explained as a function of the tions. Something similar was found by Herrera richness of fruiting ornithochorous plant species (1998), who detected only one significant corre1a- within a vegetation type. In this study, only two tion out of 112made between Mediterranean bird bird species showed significant correlations with and plant species. At the community level, it is richness of fruiting plants, and these correlations possible that abundance of bird species may be can be explained by chanceo To the best of my better related to the absolute number of fruits knowledge, only three studies have reported sig- available inavegetation type than other variables. nificant correlations between the abundance of The results obtained by Loiselle & Blake (1991) Ortiz-Pulido: Bird-fruittemporal relations 97 and Blake & Loiselle (1991), where three or four 42 combinations tested), where apositive signifi- of nine correlations were significant, and those of cant correlation was found can be explained as a Verdú & García-Fayos (1994), where only one result of chanceo Even though my results are correlation was significant, support this possibil- based on a tiny sample size (one transect walked ity. For individual bird species, this possibility three or four times by month in each vegetation remains to be tested at the landscape level more type), myconc1usions are supported bythe lack of broadly, i.e., considering different vegetation pattems found in other studies. types. Itisalso possible that arelationship may be found between individual bird species and fruiting Acknowledgements omithochorous plants if the abundance of plant species ingested by a particular bird species is Ithank J. Laborde for training infield work meth- considered, ashad been proved for Turdus phi/o- odology, V. Rico-Gray, J. Galindo, M. Carvallo, melos (Rey 1995), Sylvia atricapilla (Rey 1995, E. Paul, B. Loiselle and D. Levey for suggestions Herrera 1998), and, partially, for Pharomachrus onearly drafts ofthis manuscript, S.Guevara, the mocinno (Wheelwright 1983). However, this re- Departamento de Ecología Vegetal del Instituto lationship remains generally unexplored, possibly de Ecología, A.e. (Proyect 902-16), and CONA- because of a lack of knowledge about the natural CyT for financial and material support during history of many frugivorous-omithochorous sys- field work. I wrote this manuscript while I was tems (Blake et al. 1990). supported by a doctoral study credit-grant from CONACyT (# 9352171). I appreciate the im- Inaddition totheother altematives mentioned, the provements made in English usage by Ellen Paul lack ofobserved pattems with this set ofbird spe- through the Association of Field Omithologists' cies may reflect their ability to use altemative program of editorial assistance. food sources. None ofthe species listed inAppen- dix 1,even the Olive-throated Parakeet (Aratinga nana), are strictIy frugivorous in the zone (Ortiz- Pulido et al. 1995, Ortiz-Pulido, unpublished data). The lack ofpattems may reflect the need to Literature cited include all food resources used by the bird spe- cies. In other words, a more general hypothesis ÁLVAREZA,. A. 1994. Distribución espacio-tem- may be true, i.e., food resources explain bird poral de una comunidad de aves de playa abundance, but the pattem was not detected be- (aves: Charadriiformes) en una franja costera cause 1used only fruit resources as the predictor del Municipio de Ursulo Galván, Veracruz. variable. In the zone tbe studied frugivorous bird Bachelor Thesis. Facultad de Biología, Uni- versidad Veracruzana, Xalapa, Veracruz, species eat the fruits of three to twelve plant specíes (x =6.8), and ten of these bird species are México. AOU (AMERICANORNITHOLOGISTU'sNION).1998. included amung thetwelve most frugivorous birds Check-list of North American Birds, 6th in this landscape (Ortiz-Pulido et al. in press). edition. ABen Press, Lawrence, KS, U.S.A. Inthis study, the evidence did not support the hy- BLAIN,D. 1988. Factors affecting the early stages pothesis of a positive relationship between the of regeneration of three tropical tree species abundance of particular frugivorous bird species inaseasonal forest, Veracruz, Mexico. M. SC. and the richness of fruiting omithochorous plants Thesis. York University, North York, Ontario, within three vegetation types. Rare cases (two of Canada. 98 Caldasia Vol. 22, No. 1,2000 BLAKE,1.G., B. A. LmSELLE,T.C. MOERMONDD,. availability and movement patterns in 1.LEVEY,&1.S. DENSLOW1.990. Quantifying neotropical landbirds. American Naturalist abundance of fruits for birds in tropical 140:447-476. habitats. Studies inAvian Biology 13:73-79. LOISELLEB, A. & 1. G. BLAKE.1991. Temporal BLAKE,1.G. &B. A. LmsELLE.1991. Variation in variation in birds and fruits along an resource abundance affects capture rates of elevational gradient inCosta Rica. Ecology 72: birds in three lowland habitats in Costa Rica. 180-193. Auk 108: 114-130. LmsELLE,B A. & J. G. BLAKE.1993. Spatial DAVIES,D.E. 1945. The annual cycle of plants, distribution ofunderstory Iruit-eatíng birds and mosquitos, birds, and mammals in two fruiting plants in a neotropical lowland wet Brazilian forests. Ecological Monographs 15: forest. Vegetatio 107/108: 177-189. 243-295. LÓPEz-PoRTILLO1,,T.PuLIDO,G.VÁZQUEZP, Mo- EMLEN,1. T. 1971. Population densities of birds RENO-CASASOLPA.,ZAMORAF,. GONZÁLEZ&, derived from transectcounts. Auk 88:323-342. E. RUELAS.1993. Impacto ambiental de la EMLEN1,.T. 1977.Estimating breeding season bird ampliación de la carretera Cardel-Veracruz, densities from transect counts. Auk 95: 455- Unpublished Report, Maquinaria deVeracruz, 468. Gobierno del Estado deVeracruz, México. HERRERA, C. M. 1985. Habitat-consumer interactions in frugivorous birds. Pages 341- MORENO-CASASOLPA.,1982. Ecología de la vege- 365 in: M.L. Cody, (ed.). Habitat selection in tación de dunas costeras: factores físicos. birds. Academic Press, New York. Biótica (México) 7:577-602. HERRERAC, . M. 1998. Long-term dynamics of MURRAYK,.G. 1988. Avian seed dispersal ofthree Mediterranean frugivorous birds and fleshy neotropical gap-dependent plants. Ecological fruits: a 12-year study.Ecological Monographs Monographs 58: 271-298. 68: 511-538. NOVELOR,.A. 1978. Lavegetación en la Estación HOWE,H. F. & L. C. WESTLEY.1988. Ecological Biológica El Morro de La Mancha, Veracruz. relationships of plants and animals. Oxford Biótica (México) 3:9-23. University Press. Oxford. ORTIZ-PULIOOR., 1994. Frugivoría ydispersión de HUTTOR, . L. 1990. Measuring the availability of semillas por aves en La Mancha. Veracruz. food resources. Studies in Avian Biology 13: Bachelor Thesis. Facultad deBiología, Univer- 20-28. sidadVeracruzana, Xalapa, Veracruz, México. JORDANOp., 1992. Fruits and frugivory. Pages 105- ORTIZ-PULIDOR,. 1997. Actividades frugívoras de 156 in:M.Fenner (ed.). Seeds: the ecology of Tyrannus forficatus en unmosaico de vegeta- regeneration in plant communities. C.A.B. ción durante la migración. Ornitología International. Wallingford, England. Neotropical8: 237-239. KARR1, R. 1976.Seasonality, resource availability, and community diversity in tropical bird ORTIZ-PULIDOR,., H.GÓMEZDESILVAF,.GONZÁLEZ- communities. American Naturalist 110: 973- GARCfA,& A, ALvAREZ.1995. Avifauna del 994. Centro de Investigaciones La Mancha, LEVEY,D. J. 1988. Spatial and temporal variation Veracruz, México. Acta Zoológica Mexicana in Costa Rican fruit and fruit-eating bird (nueva serie) 66: 87-118. abundance. Ecological Monographs 58: 435- ORTIZ-PULIDOR,., 1. LABORDE&, S. GUEVARAIn. 455. press. Frugivoría por aves en unpaisaje frag- LEVEY,D. & F. G. STILES.1992. Evolutionary mentado: consecuencias en la dispersión de precursors oflong-distance migration: resource semillas. Biotropica. 99 Ortiz-Pulido: Bird-fruK temporal relations REy, P.J. 1995. Spatio-temporal variation in fruit VANDERPIJL,L. 1972. 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Recibido ellO defebrero de 1999. versuin final aceptada el25 de octubre de 1999. 100 CaldasiaVol. 22, No. 1,2000 APPENDIX 1.Number of frugivorous birds registered per species per month inthree vegetation types inCICOLMA, Veracruz, Mex. MONTH A M J J A S O N D F M VEGETATION TYPE SHRUBS SPECIES Columba flavirostris 5 4 2 2 Aratinga nana 2 2 4 Tyrannus forficatus 2 Trogon melanocephalus Melanerpes aurifrons 6 6 3 3 6 2 4 Pitangus sulphuratus 5 2 4 7 5 Myiozetetes similis 5 8 3 7 2 27 11 19 7 Tityra semifasciata 2 5 3 Cyanocorax morio 2 3 2 3 Mimus polyglottos 22 6 9 8 3 Dives dives 2 3 11 4 4 lcterus gularis 2 7 2 3 lcterus galbula 9 15 2 Psarocolius montezuma 3 Register \month 23 O 16 21 37 33 18 73 23 39 16 22 Species \month 9 O 5 5 9 7 6 8 6 8 4 8 VEGETATION TYPE PASTURES SPECIES Columba flavirostris 3 4 3 Aratinga nana 2 6 9 2 2 Tyrannus [orficatus 26 2 Trogon melanocephalus Melanerpes aurifrons 4 6 4 7 9 5 3 2 4 6 Pitangus sulphuratus 2 2 Myiozetetes similis 11 11 6 11 4 4 2 Tityra semifasciata Cyanocorax morio 4 10 7 Ortiz-Pulido: Bird-fruit temporal relations 101 APPENDIX 1.Continued. MONTH A M J J A S O N D J F M Mimus polyglottos Dives dives 11 6 7 5 15 9 Icterus gularis 7 20 Icterus galbula 10 Psarocolius montezuma 5 2 2 2 Register \month 51 37 23 31 21 57 17 15 13 15 12 8 Species \month 7 6 6 6 5 8 4 4 3 5 5 2 VEGETATION TYPE DRYFOREST SPECIES Columba flavirostris 10 7 Aratinga nana 2 4 14 7 Tyrannusforjicatus 37 Trogon melanocephalus 6 3 2 7 17 Melanerpes aurifrons 3 9 9 7 2 2 5 8 14 7 Pitangus sulphuratus 4 3 3 3 5 2 Myiozetetes similis 3 9 6 18 2 4 Tityra semifasciata 5 3 3 4 7 3 Cyanocorax morio 3 17 7 3 3 5 4 11 8 Mimus polyglottos Dives dives 8 5 2 2 3 2 Icterus gularis 2 2 2 1cterus galbula 3 5 Psarocolius monteruma 10 4 5 3 35 17 Register \month 83 45 35 O 14 18 23 20 12 48 96 67 Species \month 8 10 7 O 5 8 7 7 4 8 10 10 102 Caldasia Vol. 22, No. 1,2000 APPENDIX 2. Plant species with omithocorous characteristics fruiting inthree vegetation types per month inCICOLMA, Veracruz, Mexico. MONTH A M A S O N D J F M VEGETATION TYPE SHRUBS SPECIES Achatocarpus nigricans Annona glabra Bromelia pinguin Brosimun alicastrum Bursera [agaroides x x Bursera simaruba x x x x Cactaceae sp. 1 Capparis baducca Casearia corymbosa x Celastraceae sp. 1 x Celtis caudata x x x x Chioccoca alba x x x x x x Chiococca coriaceae Clethra mexicana Coceoloba barbadensis x x Cojoba arborea Coniza sp. 1 x x x Cupanea dentata Cytharexylum hexangulare Dendropanax arboreus Desmopsis sp. 1 x x Diospyros verae-crucis Erithroxylum havanense Eugenia acapulcensis Euphobiaceae sp. 1 Ficus cotinifolia Ficus obtusifolia x Guetarda elliptica Hyperbaena mexicana Jacquinia sp. 1 Karwinskia humboldtiana x Lantana camara x x x x x Malpighia glabra x x x x Manilkara rapote Nectandra coriaceae x Oleaceae-Olacaceae sp. 1 Opuntia stricta x x x x x x x x x Passiflora sp. 1 x x Paullinia sp. 1 x

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