Spatial and temporal distribution of floral resources used ...ijprb.com/vol 12 (1)/3.pdf · B Y T I O E I C L O O G S I S E T H S T Angiosperms sustain most of the planet’s nutrient

The International Journal of Plant Reproductive Biology 12(1) Jan., 2020, pp.11-24

DOI 10.14787/ijprb.2020 12.1.

Spatial and temporal distribution of floral resources used by pollinators in a semi-deciduous seasonal forest

1 *Erika Ramos Ono , Adriano Valentin-Silva and Elza Guimarães .

1

São Paulo State University, Rua Prof. Dr. Antonio Celso Wagner Zanin, s/n, 18618-689, 2

Botucatu, São Paulo, Brazil; Department of Botany, Institute of Biosciences, UNESP – São Paulo State University, Rua Prof. Dr. Antonio Celso Wagner Zanin, s/n, 18618-689,

Botucatu, São Paulo, Brazil.

*e-mail: [email protected]

Received :

ABSTRACT

Keywords :

1 2

Graduate Program of Biological Sciences (Botany), Institute of Biosciences, UNESP –

08.10.2019; Revised: 09.12.2019; Accepted and Published online: 15. 12. 2019

Pollination is a fundamental process in the life cycle of many plant species because it is related to the maintenance of new generations and consequent perpetuation of most of the species. Flowers are the organs related to the sexual reproduction of angiosperms, and most species are pollinated by animals, which visit flowers in search of resources that are essential to their survival. We aimed to evaluate the spatial and temporal supply of floral resources associated with the maintenance of the pollinator community in the forest remnants of the Botanical Garden of the Institute of Biosciences (BG/IB), located in Botucatu, state of São Paulo, Brazil. In order to describe the floral resources available to pollinators, we used a floristic survey and we obtained information about the type of habit, floral resources, pollinators, and flowering period of each plant species in specialized websites, books and papers. Of the 207 listed species, we obtained data for 136 (65.7%) species. Nectar was the resource most frequently found in species of all habits, being present in 77 species, followed by pollen (32), nectar/pollen (20), and oil (two). We separated plant species into nine groups based on pollination vectors. Bees predominated as pollinators in all plant habits. We recorded two flowering peaks in the community, one in the transition months between the rainy and dry season (March/April) and the other in the transition months between dry and rainy season (October/November). The melittophilous species were the majority in the study area (70%) and its flowering pattern coincided with that observed for the community. For species pollinated by bats and beetles, it was not possible to identify an annual distribution pattern due to the low number of representatives in the study area. Thus, most pollination vectors seem to be supplied by floral resources throughout the year at BG/IBB.

Floral resources, flowering, nectar, phenology, pollen, pollination syndromes.

EPR R OT DN UAL CP T IF VEO BYT I OEI L

C O

O G

S I SE TH ST

Angiosperms sustain most of the planet’s nutrient and Mostly, pollinators visit flowers for food, especially energy cycles through the production of food used by a large nectar and, less commonly, pollen (Willmer 2011). Resins are number of herbivorous animals; in addition, about one third used as nest building material (Armbruster 1984) and oils of the crop products used in human consumption depend generally serve as food for larvae because they are more directly on animal pollination (Willmer 2011). Biotic energetic than nectar and are used to coat nests (Alves-dos-pollination is more common in the tropics (Ollerton et al. Santos et al. 2007). There is still no complete understanding of 2011); it is usually more effective than anemophily or the function of fragrances, but possibly there is a relationship hydrophily (Willmer 2011), and may be an important factor in with the reproductive functions of animals that collect them the diversification of some animal and plant groups (Ollerton (Endress 1994), primarily male Euglossini bees (Farias and et al. 2011). Martins 2013, Eltz et al. 2015). In general, each pollinator

Several attributes contribute to the attraction of floral group looks for one or more types of resource in flowers, for visitors; these characteristics may be related to the plant, such example animals such as lepidoptera (butterflies and moths), as distribution, number and location of flowers (Murawski some bird species (usually hummingbirds in the New World), 1987), or to the flowers features, such as color, symmetry, and some bat species search for nectar in the flowers as the shape and size (Willmer 2011). These traits are called main source of energy intake (Endress 1994). Wasps search secondary attractants and are responsible for stimulating only for nectar, flies usually collect nectar and pollen, while visits. The primary attractants are those by which the bees are a more diverse group in the use of floral resources, as pollinator finds the flower and their resources, which most of they collect pollen, nectar, oils, resins, and even fragrances the times are essential to its survival, such as nectar, pollen, or (Endress 1994). Beetles, on the other hand, are a different other less common resources as oils, resins, fragrances, group that can look for pollen, floral parts for food, and can use mating places or shelters (Faegri and van der Pijl 1979). the flower as a shelter and place for mating (Gottsberger

2012). Normally, flowers pollinated only by abiotic vectors do most recent and have covered the entire area of BG/IB. Among not have primary or secondary attractants (Guimarães and all species, we removed from the list those that were exotic.Machado 2011). Survey of species information—Based on specialized

Studies on the relationship between plants and their websites (Flora do Brasil, Flora de Santa Catarina), books pollinators can be fundamental in understanding the structure (Flora fanerogâmica do estado de São Paulo vols. 1-8, Flora and organization of communities (Bawa et al. 1985). Studies ilustrada catarinense), and papers, we collected information regarding pollination biology in tropical seasonal forests about the plant species habit and characteristics of their generally focus on one or a few plant species (e.g. Lenza and flowers, such as color, size, and shape. After the completion of Oliveira 2005, Lima and Vieira 2006), or even on a set of this stage, we consulted the BOTU herbarium collection, species of a particular pollination syndrome (e.g. Araújo et al. which has material collected at the BG/IB since the 1980s, to 2013), addressing aspects related to both pollinators and identify the flowering periods of the species, as well as to flowering phenology, but see Tunes et al. (2017). Phenological complement the information on floral traits. We also obtained studies, which help in understanding the temporal patterns information on flowering phenology in the study of Galhego of floral resource distribution, including all plant species (1998), which was performed at BG/IB, and in phenological present in a community are uncommon. We have only around studies conducted in other areas of semi-deciduous seasonal 30% of studies conducted in Central and South America, with forest in Brazil.predominance of tree species and prioritizing areas of tropical We identified pollinators from literature data, but for rainforests (Morellato et al. 2013). plant species that did not have published information we used

In tropical seasonal forests, flowering has a seasonal the observed floral attributes to frame the species in a pattern, usually showing peaks in the dry season or in the pollination syndrome following Faegri and van der Pijl (1979) transition from dry to rainy season (Morellato et al. 2013). and Endress (1994). Thus, we separated the plant species into Thus, there may be seasonality in the supply of floral resources nine groups of pollination vectors: bats, bees, beetles, that are used by different pollinators throughout the year. In butterflies, flies, hummingbirds, moths (sitting-moth and addition, tropical seasonal forests are vertically stratified, hawkmoth), wasps, and wind. We identified the type of showing two well defined layers, the canopy (composed by resource present in the flowers of each species from data trees) and the understory (composed by shrubs and published in papers; when this was not possible we considered herbaceous species), which are connected by a continuous the information available for another species of the same midstory (Lopes et al. 2014). Thus, besides the temporal genus.variation in the supply of floral resources, there may also be a We analyze the data together on two levels. 1) Spatial spatial influence due to a vertical stratification in the resources distribution: we separated plant species by habit of plant availability related to the habit of the plant species (Silva et al. species presenting each type of floral resource and by group of 2012). Given the importance of floral resources in maintaining pollination vector. 2) Temporal distribution: we analyzed the the plant-pollinator relationship, we aimed to evaluate the flowering phenology of the species in order to identify the spatial and temporal supply of these resources associated with supply of resources for each group of pollination vector the maintenance of the pollinator community in the remnants throughout the year.of a semi-deciduous seasonal forest.

RESULTS AND DISCUSSIONMATERIAL AND METHODS

We recorded 207 native plant species from Brazil, Study area and studied species—We conducted the study at belonging to the Atlantic Forest Domain, in which semi-the Botanical Garden of the Institute of Bioscience (BG/IB), deciduous seasonal forest (SSF) is included according to located in Botucatu (22°53’11'’S; 48°29’55'’W), state of São Oliveira-Filho and Fontes (2000). From these, we found Paulo, Brazil. The BG/IB consists of fragments with information regarding pollinators, flowering in SSF, and type secondary vegetation of semi-deciduous seasonal forest of floral resource for 136 species (Appendix) belonging to 47 (Veloso et al. 1991), with about 20 ha of area, which have been families, which corresponds to 65.7% of the species occurring preserved for over 45 years. The climate in Botucatu, in BG/IB. according to the Köppen classification, is Cfa, hot climate Regarding the resources available, of the 136 species with rain in the summer, drought in the winter and warmest recorded, we disregarded in this analysis six species that were month average temperature above 22°C (Alvarez et al. 2013). exclusively anemophilous. Nectar was the most frequent

In order to know the resources available to pollinators in resource, present as the only floral resource in 77 species, the study area, we used floristic lists carried out in the being absent mainly in species of families that secrete resin Botanical Garden between 2003 and 2006 (Bignotto 2005, (Clusiaceae), in species of families in which buzz pollination Santos 2007), whose exsiccates are deposited in the BOTU is frequent and pollen is the main resource (Commelinaceae, Herbarium. These surveys were chosen because they are the Fabaceae, and Solanaceae), and in those families with species

12 The International Journal of Plant Reproductive Biology 12(1) Jan., 2020, pp.11-24

that secrete oils (Malpighiaceae). Pollen was the second most flowering peaks coincide, respectively, with the end and common resource (32 species). We registered 20 species that beginning of the rainy season in the Botucatu region (Cunha had both nectar and pollen as floral resources and oil was and Martins 2009). Water availability is an important factor present in only two species, both from Malpighiaceae family. associated with the modulation of plant phenological We did not find studies conducted in SSF areas with this type responses (van Schaik et al. 1993).of analysis. However, our results were similar to those Most of the recorded species were pollinated by bees (95 observed by Araújo et al. (2009) in a remnant of rainforest in species), followed by butterflies (23), hummingbirds (17), northeastern Brazil. moths (15), flies (15), wind (nine), wasps (seven), bats (four),

Among the 136 species analyzed, 34 were trees (or and beetles (four). Of this total, 40 species were pollinated by treelets), 56 were shrubs (or subshrubs), 22 were herbs, and 24 two or more vectors, which corresponded to 29.4% of the were climbers (Appendix). In all types of plant habit there was

a predominance of nectar as a resource. Oil was present in one evaluated species. The predominance of species pollinated by tree and one climber species (Table 1). Bees predominated as insects, mainly by bees (70% of species), was also observed in pollinators in all plant habits (Fig. 1), similar to that observed

other areas of SSF in the state of São Paulo (Kinoshita et al. in another SSF fragment in the state of São Paulo (Kinoshita et 2006, Yamamoto et al. 2007). The large amount of species al. 2006). The absence of a kind of pollination vector in a

particular habit is related to floral and pollinator attributes. For belonging to Asteraceae, Melastomataceae, and Solanaceae example, we observed chiropterophily only in tree and shrub (accounting for almost 30% of the total of species), which species (Fig. 1), as these animals usually visit plants with

have bees as their main pollinators, contributes to this result. large, resistant flowers that are positioned outside the foliage The least representative groups recorded in our study were (Vieira and Fonseca 2014).bats and beetles, with 3% of species each, a result similar to those obtained by Morellato (1991) and Yamamoto et al. (2007).

From the analysis of the distribution of flowering periods of the species according to the groups of pollination vectors (Fig. 3), it was possible to observe for bees, butterflies and flies the existence of two peaks with higher number of species flowering, one in March and one in October, which coincided with the end and beginning of the rainy season, respectively.

Some pollinators preferentially forage in the lower strata The distribution of the flowering period of bee pollinated of vegetation, such as hummingbirds (Rocca and Sazima species was similar to the distribution described by Morellato 2007), which used few floral resources of tree species (Fig. 1). (1991). In addition, the BG/IB melittophilous species According to Rocca and Sazima (2007), long-billed presented the same flowering pattern observed in the whole hummingbirds visit long corolla flowers in the understory, community, which can be explained by the species richness while short-billed hummingbirds visit short corolla flowers of this group, recorded in 31 of the 47 families in the study usually in the canopy. Despite this, most groups of pollination area.vectors can forage in species of all types of habits (Fig. 1). Regarding hummingbirds, there was little variation These results suggest that species of different habits can throughout the year, with only a reduction in the number of flourish at different periods throughout the year (Stranguetti species flowering in December (Fig. 3). In the study of Abreu and Ranga 1997), forming a vertical mosaic of floral and Vieira (2004), in a SSF in the state of Minas Gerais, a resources availability (Silva et al. 2012), contributing to the greater number of species flowering was found in the rainy maintenance of pollinators. season, although the resource supply was continuous

In fact, flowering occurred throughout the year in the throughout the year as well as in the forest fragments of community (Fig. 2), as observed in other areas of SSF in the BG/IB. This constant supply pattern is important as it enables state of São Paulo (Morellato et al. 1989, Stranguetti and the hummingbirds to meet their energy needs throughout their Ranga 1997). Nevertheless, we recorded two peaks in the life cycle (Piacentini 2006). For months, we found a single number of flowering species: the first in March-April and the peak at the end of the rainy season (April; Fig. 3). For the other second in October-November (Fig. 2), similar to the findings groups, the low number of recorded species made it difficult to of Yamamoto et al. (2007). Each of these peaks can be related visualize a pattern.to different plant habits. Mikich and Silva (2001) observed, in Most pollination vectors, including bees, butterflies, SSF areas in the state of Paraná, that tree and shrub species flies, hummingbirds, moths, and wasps, find floral resources flower mainly at the beginning of the rainy season while (nectar and pollen) throughout the year in BG/IB due to the herbaceous species at the end of this season. These periods of distribution of flowering periods of plant species, that creates

Table 1 – Distribution of floral resources according to the type of plant habit.

Type of habitat Nectar Pollen Nectar/Pollen Oil

Tree 17 6 10 1

Shrub 31 18 5 0

Herb 12 7 1 0

Climber 17 1 4 1

2019 13Spatial and temporal distribution of floral resources used by pollinators in a semi-deciduous seasonal forest


Fig. 2 – Flowering of the 136 analyzed species occurring in the Botanical Garden of Institute of Bioscience, Botucatu, state of São Paulo, Brazil.

Fig. 1 – Distribution of groups of pollination vectors according to the type of plant habit.

Fig. 3 – Flowering periods separating plants according to groups of pollination vector.

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Appendix – Information on species occurring in the Botanical Garden of Institute of Bioscience, Botucatu, state of São Paulo, Brazil. N = nectar, O = oil, P = pollen; BA = bats, BE = bees, BT = beetles, BU = butterflies, FL = flies, HU = humminbirds, MO = moths, WA = wasps, WI = wind.

Family Species Habitat Floral Ref. Polinator Ref. Flowering Ref.Resource

Acanthaceae Justicia brasiliana Roth shrub N 51 HU 76 Jan-May, Oct 120

Ruellia brevifolia (Pohl) C.Ezcurra shrub N 9 BU, HU 121 Jan-Jul, Oct-Dec 78

Anacardiaceae Tapirira guianensis Aubl. tree N 48, 90 BE 37 Oct-Dec 61

Apocynaceae Forsteronia rufa Müll.Arg. climber N 74 BE, MO - Dec 90

Prestonia coalita (Vell.) Woodson climber N 74, 90 BE 55 Jan-Apr, Dec 56

Temnadenia violacea (Vell.) Miers climber N 74 BE, HU - Nov H

Apocynaceae Asclepias curassavica L. shrub N 142 BU 59,146 Feb-Dec 120

Araliaceae Dendropanax cuneatus (DC.) tree N 109, 90 BE, FL 107, 109 Mar-May 87Decne. & Planch.

Asteraceae Piptocarpha axillaris (Less.) Baker shrub N 90 BE, MO - Jul-Aug H

Mikania cordifolia (L.f.) Willd. climber N, P 20, 88 BE, MO - Apr-May 70

Gochnatia polymorpha (Less.) Cabrera tree N. P 90, 143 BE, MO - Nov-Dec 70

Gochnatia barrosoae Caberra shrub N, P 103, 143 BE, MO - Apr, Jul-Aug, Nov H

Galinsoga quadriradiata Ruiz & Pav. herb N 7 BE, MO - May H


Calea pinnatifida (R.Br.) Less. shrub N 90 BE, BU - Sep-Nov 120

Bidens brasiliensis Sherff herb N, P 90 BE, BU - Mar-May 90

Baccharis dracunculifolia DC. shrub N, P 103, 88 BE 37 Jan-May, Oct 120

Ambrosia polystachya DC. shrub P 20 BE, BU - Jan, Oct-Nov H

Senecio brasiliensis (Spreng.) Less. herb N 20 BE, BU - Jul, Sep-Nov 120

Tilesia baccata (L.f.) Pruski shrub N 52 BE 52 Jan-Mar, Nov-Dec 52

Elephantopus mollis Kunth herb N 20 BE, BU - Feb-Jul, Oct 120

Achyrocline satureioides (Lam.) DC. herb N 58 MO, WA - Mar-Jun 70

Chromolaena laevigata (Lam.) shrub N 29 BE, BU - Mar HR.M.King & H.Rob.

Vernonanthura phosphorica (Vell.) H.Rob. shrub N 116,8 BE 37 May-Jun H

Chromolaena maximilianii (Schrad. ex DC.) shrub N 29 BE, BU - Dec HR.M.King & H.Rob.

Blainvillea dichotoma (Murray) Stewart herb P 20 BE, BU - May H

Dasyphyllum brasiliense (Spreng.) Cabrera shrub N 90 BE - Mar-Jun, Aug-Sep 120

Mikania hirsutissima DC. climber N, P 42, 88 BE 42 Aug-Sep 42

Cyrtocymura scorpioides (Lam.) H.Rob. climber N, P 20, 86 BE, BU - Jul-Oct H

Heterocondylus alatus (Vell.) R.M.King shrub N 29 BE, BU - Jul H & H.Rob.

Vernonanthura discolor (Spreng.) H.Rob. tree N 8 BE - Oct H

Begoniaceae Begonia cucullata Willd. herb P 145 BE 145 Jan-Mar, Sep-Dec 120

Bignoniaceae Adenocalymma bracteatum (Cham.) DC. climber N 50,90 BE 5 Apr-Dec 41

Anemopaegma chamberlaynii (Sims) climber N 33, 90 BE 33 Jan-Aug, Nov-Dec 41Bureau & K.Schum.

Fridericia pulchella (Cham.) L.G.Lohmann climber N 50 HU - Sep-Nov H

Fridericia speciosa Mart. climber N 50, 90 HU 22, 119 Jan-Apr 22

Fridericia samydoides (Cham.) climber N 50, 90 BE 41 Feb-Apr, 148 L.G.Lohmann Oct-Dec

Mansoa difficilis (Cham.) Bureau climber N 50, 90 HU - Jul-Nov 120& K.Schum.

Pyrostegia venusta (Ker Gawl.) Miers climber N 50, 90 HU 22,119,37 May-Aug 70

Tanaecium pyramidatum (Rich.) climber N 50 BE, HU - Nov 61L.G.Lohmann

Zeyheria montana Mart. tree N 9 HU 17 May-Jun 114

Boraginaceae Cordia superba Cham. tree N 1 BU 43 Jun, Dec H

Bromeliaceae Tillandsia tricholepsis Baker herb N 30 BU, HU - Sep H

Tillandsia aeranthos (Loisel.) L.B.Sm. herb N 30 HU - Sep H

Tillandsia mallemontti Glaz. ex Mez herb N 30 HU - Jan H

Cannabaceae Trema micrantha (L.) Blume shrub 131, 90 WI 112 Jan-May, Aug-Dec 120

Clusiaceae Clusia criuva Cambess. shrub P 30, 31 BT 31 Jan H

Commelinaceae Tripogandra diuretica (Mart.) Handlos herb P 46 BE - Feb-Apr, Jul 120

Dichorisandra thyrsiflora J.C.Mikan herb P 46 BE - Jan-Mar, Nov-Dec 87

Convulvulaceae Ipomoea cairica (L.) Sweet climber N 81, 90 BE 82, 81 Mar-Apr 90

Merremia macrocalyx (Ruiz & Pav.) climber N 108, 90 BE 108 May 70 O'Donell

Erythroxilaceae Erythroxylum cuneifolium (Mart.) shrub P 126 BE - Sep-Oct 70O.E.Schulz

Euphorbiaceae Croton floribundus Spreng. tree N, P 109, 90 FL, WI 102 Oct-Dec 102

Actinostemon klotzschii (Didr.) Pax shrub P BE 73 Jul-Aug 66

Fabaceae Bauhinia brevipes Vogel shrub N 9 BA 91 Oct H

Bauhinia forficata Link tree N 92, 90 MO 92 Jan-May, Oct 120

Bauhinia longifolia (Bong.) Steud. shrub N 130 BA 130 Jan-Apr 83

Bauhinia holophylla (Bong.) Steud. shrub N 91, 90 BA 44, 130 Jan-Apr 83

Copaifera langsdorffii Desf. tree N 57, 90 BE 34, 57 Jan-Feb, Dec 61

Senna pendula (Humb.& Bonpl.ex Willd.) shrub P 18 BE - Apr H H.S.Irwin & Barneby

Senna splendida (Vogel) shrub P 18 BE 12 Mar-May 83H.S.Irwin & Barneby

Stryphnodendron adstringens (Mart.) shrub N 47 BE 98 Mar, Oct HCoville

Stylosanthes viscosa ( L.) Sw. shrub N 20 BE 110 Apr H

Machaerium villosum Vogel tree N, P 90 BE - Oct-Nov 61

Inga vera Willd. tree N, P 9, 18 MO 35 Jun-Oct 83

Erythrina speciosa Andrews tree N 85, 1 HU 22 May-Aug 22

Dalbergia frutescens (Vell.) Britton tree N, P 90 BE 147 Feb-Mar, Nov-Dec 120

Crotalaria micans Link shrub N 45, 18 BE 139 Apr, Nov-Dec H

Macroptilium atropurpureum climber N 138 BE 138 Aug H(Sessé & Moc. ex DC.) Urb.

Platypodium elegans Vogel tree N 103, 90 BE - Oct-Dec 90

Lauraceae Nectandra grandiflora Nees tree N, P 143 BT, WA - Aug 61

Lythraceae Lafoensia pacari A.St.-Hil. tree N 126, 1 BA 118 Nov-Dec H

Malpighiaceae Niedenzuella acutifolia (Cav.) climber O 140 BE - Feb-Apr HW.R.Anderson

Byrsonima intermedia A.Juss. tree P, O 103, 6 BE 94 Jan, Nov H

Malvaceae Guazuma ulmifolia Lam. tree N 54 FL 141 Mar, Oct-Nov 61

Triumfetta semitriloba Jacq. shrub N 25 BE 25 Mar-May 26

Melastomataceae Miconia sellowiana Naudin shrub N, P 80 BE, FL 80 Sep-Oct 61

Miconia chamissois Naudin shrub P 126 BE 122 Aug H

Miconia stenostachya DC. shrub P 126 BE 15 Sep, Nov H

Miconia theizans (Bonpl.) Cogn. shrub N, P 80 BE, BU, 80 Oct-Dec 19FL, WA

Miconia latecrenata (DC.) Naudin shrub P 126 BE 65 Mar-Oct 132

Leandra purpurascens (DC.) Cogn. shrub P 126 BE - Jul H

Rhynchanthera dichotoma (Desr.) DC. shrub P 126 BE 68 Jan H

Tibouchina gracilis (Bonpl.) Cogn. shrub P 126 BE 56 Nov-Dec 70

Tibouchina stenocarpa tree P 126 BE 65 Jul-Aug 70(Schrank & Mart. ex DC.) Cogn.

Meliaceae Cabralea canjerana (Vell.) Mart. tree N, P 75, 143 BE 37 Oct 61

Guarea guidonia (L.) Sleumer tree N 75 MO 111 Jan-Mar, Dec 132

Moraceae Ficus guaranitica Chodat tree P 71 WA 104 Jan-Dec 87,105

Myrtaceae Syzygium jambos (L.) Alston tree N 126 BE - Jul H

Myrcia venulosa DC. tree N 126 BE - Sep H

Onagraceae Ludwigia elegans (Cambess.) H.Hara shrub N 21 BE 62, 63, 64 Apr, Aug, Oct H

Orchidaceae Habenaria parviflora Lindl. herb N 123 FL, MO 123 Feb-Apr 100

Mesadenella cuspidata (Lindl.) Garay herb N 23 BE 124, 23 Jan-May 144

Oeceoclades maculata (Lindl.) Lindl. herb N 3 BU 3 Mar-Apr 100

Lophiaris pumila (Lindl.) Braem herb N 101 BE 101 Sep-Oct 101


Passifloraceae Passiflora alata Curtis climber N 77 BE 77, 135, Jan-Jun 77136, 60

Peraceae Pera glabrata (Schott) Poepp. ex Baill. shrub P 90 BE, FL, 39 Apr 70WA

Piperaceae Piper frutescens C. DC. shrub P 38,16 FL - Oct-Dec H

Piper gaudichaudianum Kunth shrub P 38, 16 BE, FL, 38 Jan-Mar, Dec 133 WI

Poaceae Andropogon bicornis L. herb 126 WI - Mar-Apr H

Portulacaceae Talinum paniculatum (Jacq.) Gaertn. herb P 134 BE 134 Feb-Mar, Nov-Dec 120

Primulaceae Myrsine parvifolia A. DC. shrub 4 WI 4 May H

Myrsine guianensis (Aubl.) Kuntze tree 4 WI - Apr-Jul 14

Proteaceae Roupala montana Aubl. shrub N 103 MO 37 Apr H

Ranunculacaceae Clematis dioica L. climber N 79 WI 73 Apr-May 90

Rosaceae Prunus myrtifolia (L.) Urb. tree N, P 53 BE 147 Jul-Aug H

Rubiaceae Cordiera concolor (Cham.) Kuntze shrub N 103 MO 147 Apr-May 70

Chiococca alba (L.) Hitchc. shrub N 106 BE, FL - Jan 90

Coccocypselum lanceolatum herb N 72 BE, HU - Jul H(Ruiz & Pav.) Pers.

Guettarda viburnoides Cham. & Schltdl. shrub N 11 MO - Dec 70

Manettia gracilis Cham. & Schltdl. climber N 72 HU 22 Mar-Jul 22

Palicourea marcgravii A.St.-Hil. shrub N 28 HU 28 Jan, Nov H

Psychotria carthagenensis Jacq. shrub N 69 BE 27 Feb-Nov 120

Psychotria hoffmannseggiana shrub N 24 BE, WA 129 Jan, Dec 96(Willd. ex Schult.) Müll.Arg.

Psychotria vellosiana Benth. shrub N 24 BE, BU 147 Jan, Sep-Nov H

Rutaceae Esenbeckia febrifuga (A.St.-Hil.) tree N, P 126, 90 BE 73 Oct-Dec 90A. Juss. ex Mart.

Esenbeckia grandiflora Mart. shrub N 126 FL 147 Jan-Feb, Dec 61

Salicaceae Casearia sylvestris Sw. shrub N, P 90, 143 FL 37 Jul-Nov 120

Sapindaceae Allophylus edulis (A.St.-Hil. et al.) tree N, P 125, 143 BE - Oct-Nov 61 Hieron. ex Niederl.

Serjania caracasana (Jacq.) Willd. climber N, P 125, 90 BE 73 Mar-Jun 90

Cupania vernalis Cambess. tree N 125, 143 BE 49 Jul-Oct 61

Solanaceae Acnistus arborescens (L.) Schltdl. shrub N 20 BE, BU, 127, 137 Mar-Apr, HFL, HU, Jun, SepWA

Cestrum mariquitense Kunth shrub P 40 BE 73 Jun 70

Solanum americanum Mill. herb P 90 BE 58 Mar, Nov-Dec 58,70

Solanum granulosoleprosum Dunal tree P 90 BE 67,99 Jan-Jun, Oct-Dec 87

Solanum didymum Dunal shrub P 90 BE 93 Feb-Apr, Aug-Nov H

Solanum lycocarpum A.St.-Hil. tree P 89 BE 95 Nov H

Solanum paniculatum L. shrub P 90, 2 BE 53 Oct H

Solanum variabile Mart. tree P 10 BE 10 Mar, May, Aug-Sep H

Smilacaceae Smilax elastica Griseb. climber N 90 BT, FL - Jun-Jul 90

Styracaceae Styrax camporum Pohl tree N 103 BE 117 Jul 70

Trigoniaceae Trigonia nivea Cambess. climber N, P 126, 90 BE, FL - Mar H

Urticaceae Urtica dioica L. herb 128 WI 128 Jun H

Verbenaceae Lantana camara L. shrub N 59 BU 13, 84 Jan-May, Aug-Nov 120


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