Reduced Impact Logging and its Effects on the Pollination of

Amazonian Trees

Amazônia OrientalAmazônia OrientalUnB

Márcia Motta MauésEmbrapa Eastern Amazon9th International Pollination SymposiumAmes, Iowa – June 24-28th, 2007

Tropical ForestsTropical Forests•• Ecosystems with highest biodiversity on Earth, comprisingEcosystems with highest biodiversity on Earth, comprising

20%20% toto 40%40% of known animal and plant species;of known animal and plant species;

•• Amazon ForestAmazon Forest ≈ 4.1 millions km4.1 millions km22 →→ 449% of the Brazilian 9% of the Brazilian territory => biggest extent of continuous tropical forestterritory => biggest extent of continuous tropical forest

In the last 30 years, the Amazon Biome In the last 30 years, the Amazon Biome lost almost 17% of its forest cover lost almost 17% of its forest cover ≈≈

700,000 km700,000 km22 ((LentiniLentini, 2005), 2005)

Major drivers of deforestation:Major drivers of deforestation:

Pollination biology X FragmentationPollination biology X Fragmentation• Most tropical trees occurs in low densitylow density, are crosscross--

pollinatedpollinated by animals (mainly bees, beetles, butterflies, moths, flies, wasps, bats and birds), presenting complex selfself--incompatibilityincompatibility systems;

• Fragmentation ↓↓ nº of adult (reproductive) trees =>=>effective number of pollen donors, ↓↓ pollen amount and quality, and might be associated with ↓↓ in abundance and composition of pollinators (gene flow agents);

•• ↓↓ of adult trees density may affect seed dispersal, ↓↓ gene pool ↑↑ progeny deletery effects, due to ↑↑ of inbreeding.

Main GoalMain Goal::

• Evaluate the effects of Reduced Impact Logging (RIL) on the pollen flow of five timber trees, as well as the frequency and composition of pollinator groups under two situations: non-logged forest (NLF) and logged forest (LF)

SpeciesSpecies:• Jacaranda copaia (parapará) Bignoniaceae• Dipteryx odorata (cumaru) Leg-Papilionoideae• Carapa guianensis (andiroba) Meliaceae• Symphonia globulifera (anani) Clusiaceae• Bagassa guianensis (tatajuba) Moraceae

TapajTapajóóss National Forest:National Forest:“An area with native

species forest cover, with purposes of sustainable and multiple use of its natural resources, as well as scientific research, with emphasis on methods of sustainable logging”

VegetationVegetation: : Dense rain forest;LocationLocation:east-central Amazon;AreaArea ≈ 550.000 ha;

Climatic conditions:Climatic conditions: 600–3.000mm of rainfall per year (annual average precipitation 2.000mm) =>=> severe drought during El Niño episodes

Study siteStudy site••500 ha500 ha plot plot →→ Intensive Study Plot (ISPISP) Dendrogene Project, within an area of the Management of Tapajós Forest for Sustainable IndustrialTimber Production;••Reduced Impact Logging (RIL)Reduced Impact Logging (RIL): Nov/1999 to Dec/2003;

•• Phenological patternsPhenological patterns:: Gentry (1974) and Newstron et al. (1994a, b);•• Floral biologyFloral biology →→ flower morphology, SEM of pollen & reproductive

organs, floral resources & rewards (nectar, pollen, etc), pollen/ovule ratio, osmophores, stigma & pollen biology;

•• Reproductive systemReproductive system →→ controlled pollination (field and lab), pollen germination & pollen tube growth under fluorescence (incompatibility incompatibility site site identification);

•• Pollination systemPollination system: survey (capture) and/or photographic register of flower visitors, identification of legitimate and illegitimate pollinatorslegitimate and illegitimate pollinators;

Material & MethodsMaterial & Methods

Pollen deposition analysis on the stigmaPollen deposition analysis on the stigma:• At least six trees/species in non-logged forest (NLF) and logged forest (LF):

– Jacaranda copaia (pistils: 350350 NLF, 450450 LF)– Dipteryx odorata (pistils : 330330 NLF, 390390 LF)– Carapa guianensis (pistils : 232232 NLF, 199199 LF)– Symphonia globulifera (pistils : 500500 NLF, 300300 LF)– Bagassa guianensis (pistils : 460460 NLF, 600600 LF)

3,811 analyzed pistils3,811 analyzed pistils

• Pistil analysis under fluorescencefluorescence for pollen counting: average number of pollen grains deposited per sample stigma => pollen deposition rate pollen deposition rate -- PDRPDR, and percentage of pistil fertilization => % of pollen tube growth% of pollen tube growth and ovule's ovule's fertilizationfertilization;

Frequency and composition of 9 visitors/pollinators groups:Frequency and composition of 9 visitors/pollinators groups:

• Duration and frequency of visits (15 min/hour, 6 work hours)• Visitation rate

1. Small to medium bodied bees; 2. Large bodied bees;3. Wasps;4. Dipterans;5. Lepidopterans; 6. Coleopterans;7. Passerines (perching birds);8. Hummingbirds; 9. Other birds

Infrastructure to canopy accessInfrastructure to canopy access

Jacaranda Jacaranda copaiacopaia (parapar(paraparáá))

Hermaphroditic Hermaphroditic lilac flowers;

Annual intermediary floweringAnnual intermediary flowering, synchronous, cornucopia, Sep/Nov;

MediumMedium sized humid pollen grains (≈ 22x 25.3 µm).

Pollinators/visitorsPollinators/visitors: 61 spp. =>=> mainly bees (Centris, Eulaema, Bombus, Euglossa, Eufriesea, Epicharis, Augochloropsis, Trigona, Tetragona ) ((melitophilymelitophily)); medium to long flight rangemedium to long flight range; occasional pollinatorsoccasional pollinators: butterflies & moths (Hesperidae, Nymphalidae), beetles (Cnemida, Macraspis), hummingbirds (Florisuga, Glaucis, Hylocharis, Thalurania)

Reproductive system allogamous allogamous –– late acting selflate acting self--incompatibility (LSI)incompatibility (LSI)

DipteryxDipteryx odorataodorata (cumaru)(cumaru)

Hermaphroditic Hermaphroditic pinkish aromatic flowers;

SubSub--annual extended floweringannual extended flowering, synchronous, multiple-bang/episodic, 2x/year;

MediumMedium sized humid pollen grains (≈ 25.8 x 28.6 µm).

Pollinators/visitorsPollinators/visitors: 45 spp. => bees (Bombus, Centris, Epicharis, Eulaema, Eufriesea, Partamona e Trigona), butterflies & moths (Hesperidae, Nymphalidae), beetles (Cnemida, Macraspis), hummingbirds (Florisuga, Glaucis, Hylocharis, Thalurania) ((entomophilyentomophily)); medium to long flight rangemedium to long flight range

Reproductive system allogamous allogamous –– late acting selflate acting self--incompatibility (LSI)incompatibility (LSI)

CarapaCarapa guianensisguianensis (andiroba)(andiroba)

MonoeciousMonoecious: ♀ & ♂ flowers on the same tree (inflorescence);

Annual extended floweringAnnual extended flowering, asynchronous, multiple-bang, > intensity Set/Apr;

MediumMedium sized humid pollen grains (≈ 26 x 25.5 µm).

PollinatorsPollinators: < 20 spp. stingless bees and small butterflies (short flight rangeshort flight range) => Riodinidae, Lycaenidae e Meliponina ((entomophilyentomophily));

Reproductive system allogamous allogamous –– sporophiticsporophitic selfself--incompatibility (SSI)incompatibility (SSI)

SymphoniaSymphonia globuliferaglobulifera (anani)(anani)

Hermaphroditic Hermaphroditic reddish flowers;

SubSub--annual extended floweringannual extended flowering, synchronous, multiple-bang/episodic, 3x/year;

LargeLarge sized humid pollen grains, with sticky substance outside (≈ 44.3 µm).

PollinatorsPollinators: 21 spp. of birds (Thraupidae, Icteridae, Trochilidae, Picidae, Ramphastidae, Psittacidae) =>=> mainly passerines ((ornitophilyornitophily)); long flight rangelong flight range

Reproductive system allogamous allogamous –– sporophiticsporophitic selsel--incompatibility (SSI)incompatibility (SSI)

•Cyanerpes caeruleus & C. cyaneus•Dacnis cayana•Chlorophanes spiza•Hemithraupis guira•Lamprospiza melanoleuca•Psarocolius viridis•Tachyphonus cristatus•Tangara punctata & T. velia•Anthracothorax nigricollis•Celeus grammicus•Melanerpes cruentatus

BagassaBagassa guianensisguianensis(tatajuba)(tatajuba)

DioeciousDioecious, globose pistillate inflorescences & spicate staminate inflorescences;Simple flowers, without petals or sepals;Annual intermediary floweringAnnual intermediary flowering, synchronous, cornucopiaVery smallsmall dry pollen grains (≈ 5 x 7 µm);Obligate allogamousObligate allogamous

Pistillate and staminate flowers were visited by thrips (Pistillate and staminate flowers were visited by thrips (Thysanoptera)

Anemophily evidencesAnemophily evidences:•Emergent tree →→ crown above the forest canopy;• Flowering in dry period, hundreds of simple flowers/inflorescence;•Pending staminate inflorescences, large amounts of small dry pollen grains;•Pistillate inflorescences with hundreds of filiform stigmas, exposed for 2 weeks;•Absence of floral attractants;•Low incidence and diversity of biotic agents

Anemophilous syndrome + insects (thrips) = ambophily ambophily => long distance pollen long distance pollen dispersaldispersal

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Low Impact Logging (LIL) versus Pollen Deposition Rate (PDR):Low Impact Logging (LIL) versus Pollen Deposition Rate (PDR):• Pollen deposition rate was different between the two logging treatments (NLF & LF);• PDR of D. odorata was significantly > in LF (F1, 11 = 4,96; p = 0,05), whereas S.

globulifera showed opposite response →→ lower PDR in LF (F1,13 = 4,59; p = 0,05)

Pollen deposition rate of Jacaranda copaia(Jc), Dipteryx odorata(Do), Carapaguianensis (Cg), Symphoniaglobulifera (Sg) and Bagassa guianensis(Bg) in non-logged (NLF) and logged forest (LF) at the Tapajós National Forest, Brazil. * denotes (p < 0.05)

Percentage of Pistil Fertilization (PFP):Percentage of Pistil Fertilization (PFP):• Concerning PPF, over all species it was significantly lower in LF than in NLF (F1,4 =

5.74; p = 0.018), but single species analyses were not significant, with ↑↑ for C. guianensis and B. guianensis and ↓↓ for J. copaia and D. odorata. No difference was detected for S. globulifera.

Percentage od pistil fertilization of Jacaranda copaia (Jc), Dipteryx odorata (Do), Carapa guianensis(Cg), Symphoniaglobulifera (Sg) and Bagassa guianensis(Bg) in non-logged (NLF) and logged forest (LF) at the Tapajós National Forest, Brazil.

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• J. copaia and D. odorata flowers attracted the same group of visitors, with minor differences at the species level;

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s mall bees large bees w as ps f lies leps beetles hummingbirdspollina tors groups

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• S. globulifera flowers were visited by three groups of birds;

Symphonia globulifera

All five studied species are allogamousallogamous, thus dependent on pollination vectors to successfully reproduce by means of proper pollen transfer among trees;RIL changedchanged the pollen deposition ratepollen deposition rate as well as the initial fruit developmentinitial fruit development, evaluated by the % of pollen germination and ovule fertilization;All the species showed ≠ in the composition of pollinators groups under both logging treatments, which was more conspicuous in D. odorata;Considering the maintenance of reproductive processes, RIL could affect mainly species with reduced mobility pollinators, asynchronous/irregular reduced mobility pollinators, asynchronous/irregular flowering cycles and low population densityflowering cycles and low population density;Changes on the pollinators frequency and composition of tropical trees might affect the pollination efficiencypollination efficiency;RIL, despite lower visual impacts on the forest, affects pollination dynamics, changing the composition of pollinator groups, as well as the pollination and fertilization of surviving trees

The complex integration between reproductive biology of woody

trees and forest management: are we improving?

The processes driving plant-animal interactions in tropical forest ecosystems are very complex and diversified;

Forest management practices, even Reduced Impact Logging, do not consider specific reproductive needs of plant species, applying the same rules for all the species (disregarding differences on the pollination biology);

Information about the reproductive processes of these plants could help the implementation of forest management practices regardingtheir specificities, thus considering their needs to maintain the reproductive success of remnant trees in logged forest areas.

The preservation of ecosystems services in the Amazon The preservation of ecosystems services in the Amazon biome, including biome, including pollinationpollination and its diversity of and its diversity of pollen pollen vectorsvectors, relies on conservation strategies and , relies on conservation strategies and rational rational

use of the local biodiversityuse of the local biodiversity

ThanksThanks !!