UnB Amazônia Oriental

Reduced Impact Logging and its Effects on the Pollination of Amazonian Trees

Márcia Motta Maués Embrapa Eastern Amazon 9th International Pollination Symposium Ames, Iowa – June 24-28th, 2007 TropicalTropical ForestsForests

•• EcosystemsEcosystems withwith highesthighest biodiversitybiodiversity onon Earth,Earth, comprisingcomprising 20%20% toto 40%40% ofof knownknown animalanimal andand plantplant species;species;

•• AmazonAmazon ForestForest ≈ 4.14.1 millionsmillions kmkm2 →→ 449%9% ofof thethe BrazilianBrazilian territoryterritory =>=> biggestbiggest extentextent ofof continuouscontinuous tropicaltropical forestforest

InIn thethe lastlast 3030 years,years, thethe AmazonAmazon BiomeBiome lostlost almostalmost 17%17% ofof itsits forestforest covercover ≈≈ 700,000700,000 kmkm2 ((LentiniLentini,, 2005)2005) MajorMajor driversdrivers ofof deforestation:deforestation: PollinationPollination biologybiology XX FragmentationFragmentation • Most tropical trees occurs in lowlow densitydensity, 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. MainMain GoalGoal:

• 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 NationalNational Forest:Forest: ƒ “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” ƒƒVegetationVegetation:: Dense rain forest; ƒƒLocationLocation:east-central Amazon; ƒ AreaArea ≈ 550.000 ha; ƒƒClimaticClimatic conditions:conditions: 600– 3.000mm of rainfall per year (annual average precipitation 2.000mm) =>=> severe drought during El Niño episodes StudyStudy sitesite •500 ha plot → Intensive Study Plot (ISP) Dendrogene Project, within an area of the Management of Tapajós Forest for Sustainable Industrial Timber Production; •Reduced Impact Logging (RIL): Nov/1999 to Dec/2003; MaterialMaterial && MethodsMethods

•• PhenologicalPhenological patternspatterns:: Gentry (1974) and Newstron et al. (1994a, b); •• FloralFloral biologybiology →→ flower morphology, SEM of pollen & reproductive organs, floral resources & rewards (nectar, pollen, etc), pollen/ovule ratio, osmophores, stigma & pollen biology; •• ReproductiveReproductive systemsystem →→ controlled pollination (field and lab), pollen germination & pollen tube growth under fluorescence (incompatibilityincompatibility sitesite identification); •• PollinationPollination systemsystem: survey (capture) and/or photographic register of flower visitors, identification of legitimatelegitimate andand illegitimateillegitimate pollinatorspollinators; PollenPollen depositiondeposition analysisanalysis onon thethe stigmastigma: • At least six trees/species in non-logged forest (NLF) and logged forest (LF): – Jacaranda copaia (pistils: 350 NLF, 450 LF) – Dipteryx odorata (pistils : 330 NLF, 390 LF) – Carapa guianensis (pistils : 232 NLF, 199 LF) – Symphonia globulifera (pistils : 500 NLF, 300 LF) – Bagassa guianensis (pistils : 460 NLF, 600 LF)

3,811 analyzed pistils

• Pistil analysis under fluorescence for pollen counting: average number of pollen grains deposited per sample stigma => pollen deposition rate - PDR, and percentage of pistil fertilization => % of pollen tube growth and ovule's fertilization; 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 InfrastructureInfrastructure toto canopycanopy accessaccess JacarandaJacaranda copaiacopaia (parapar(paraparáá)) Hermaphroditic lilac flowers; Annual intermediary flowering, synchronous, cornucopia, Sep/Nov; Medium sized humid pollen grains (≈ 22x 25.3 µm). Pollinators/visitors: 61 spp. => mainly bees (Centris, Eulaema, Bombus, Euglossa, Eufriesea, Epicharis, Augochloropsis, Trigona, Tetragona ) (melitophily); medium to long flight range; occasional pollinators: butterflies & moths (Hesperidae, Nymphalidae), beetles (Cnemida, Macraspis), hummingbirds (Florisuga, Glaucis, Hylocharis, Thalurania) Reproductive system allogamous – latelate actingacting selfself-incompatibilityincompatibility (LSI)(LSI)

DipteryxDipteryx odorataodorata (cumaru)(cumaru) Hermaphroditic pinkish aromatic flowers; Sub-annual extended flowering, synchronous, multiple-bang/episodic, 2x/year; Medium sized humid pollen grains (≈ 25.8 x 28.6 µm). Pollinators/visitors: 45 spp. => bees (Bombus, Centris, Epicharis, Eulaema, Eufriesea, Partamona e Trigona), butterflies & moths (Hesperidae, Nymphalidae), beetles (Cnemida, Macraspis), hummingbirds (Florisuga, Glaucis, Hylocharis, Thalurania) (entomophily); medium to long flight range Reproductive system allogamous – latelate actingacting selfself-incompatibilityincompatibility (LSI)(LSI)

CarapaCarapa guianensisguianensis (andiroba)(andiroba) Monoecious: ♀ & ♂ flowers on the same tree (inflorescence); Annual extended flowering, asynchronous, multiple-bang, > intensity Set/Apr; Medium sized humid pollen grains (≈ 26 x 25.5 µm). Pollinators: < 20 spp. stingless bees and small butterflies (short flight range) => Riodinidae, Lycaenidae e Meliponina (entomophily); Reproductive system allogamous – sporophitic self-incompatibilityincompatibility (SSI)(SSI)

SymphoniaSymphonia globuliferaglobulifera (anani)(anani) Hermaphroditic reddish flowers; Sub-annual extended flowering, synchronous, multiple-bang/episodic, 3x/year; Large sized humid pollen grains, with sticky substance outside (≈ 44.3 µm). Pollinators: 21 spp. of birds (Thraupidae, Icteridae, Trochilidae, Picidae, Ramphastidae, Psittacidae) => mainly passerines (ornitophily); longlong flightflight rangerange Reproductive system allogamous – sporophitic sel-incompatibilityincompatibility (SSI)(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) Dioecious, globose pistillate inflorescences & spicate staminate inflorescences; Simple flowers, without petals or sepals; Annual intermediary flowering, synchronous, cornucopia Very small dry pollen grains (≈ 5 x 7 µm); Obligate allogamous

Pistillate and staminate flowers were visited by thrips (Thysanoptera)

Anemophily 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 => longlong distancedistance pollenpollen dispersal

Low ImpactLogging(LIL) versusPollenDepositionRate(PDR): •PDR depositionratewas differentbetweenthetwologging treatments(NLF&LF); Pollen of• Low ImpactLogging(LIL) versusPollenDepositionRate(PDR): globulifera Pollen deposition rate 10 20 30 40 0 D. odorata cD gS Bg Sg Cg Do Jc showed oppositeresponse

was significantly>inLF(F NLF Tree species cD gS Bg Sg Cg Do Jc → → * lower PDRinLF(F

1, 11 * = 4,96; LF p = 0,05),whereas denotes ( Forest, Brazil. * National Tapajós forest (LF) atthe (NLF) andlogged (Bg) innon-logged guianensis Bagassa globulifera Symphonia guianensis (Do), Carapa odorata (Jc), Dipteryx of Jacarandacopaia Pollen depositionrate 1,13 = 4,59; p < 0.05) (Cg), (Sg) and p = 0,05) S. 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), Symphonia globulifera (Sg) and Bagassa guianensis (Bg) in non-logged (NLF) and logged forest (LF) at the Tapajós National Forest, Brazil. • J. copaia and D. odorata flowers attracted the same group of visitors, with minor differences at the species level;

100 non-logged logged

80

s Jacaranda copaia 60

40 % of visit % of

20

0 small bees large bees w asps flies leps beetles hummingbirds pollinators groups

50,0 non-logged logged

40,0 Dipteryx odorata s 30,0

20,0 % of visit

10,0

0,0 large bees small bees w asps flies leps beetles hummingbirds pollinators groups • S. globulifera flowers were visited by three groups of birds;

non-logged logged 70

60 Symphonia globulifera 50 s 40

30 % of visit 20

10

0 passerines hummingbirds other birds pollinators groups All five studied species are allogamous, thus dependent on pollination vectors to successfully reproduce by means of proper pollen transfer among trees; RIL changed the pollen deposition rate as well as the initialinitial fruitfruit developmentdevelopment, 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 flowering cycles and lowlow populationpopulation densitydensity; Changes on the pollinators frequency and composition of tropical trees might affect the pollination 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 regarding their specificities, thus considering their needs to maintain the reproductive success of remnant trees in logged forest areas.

TheThe preservationpreservation ofof ecosystemsecosystems servicesservices inin thethe AmazonAmazon biome,biome, includingincluding pollinationpollination andand itsits diversitydiversity ofof pollenpollen vectorsvectors,, reliesrelies onon conservationconservation strategiesstrategies andand rationalrational useuse ofof thethe locallocal biodiversitybiodiversity ThanksThanks!!