Conservation Biology (1990)

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1 Conservation Biology (1990)

2 Selective defaunation creates a new selective force for evolution: a sequel to Rodolfo Dirzo Mauro Galetti Departamento de Ecologia São Paulo State University - Rio Claro, São Paulo, Brazil mgaletti@rc.unesp.br

3 We live in a zoologically impoverished world, from which all the hugest, and fiercest, and strangest forms have recently disappeared Alfred Russell Wallace (1876)

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7 World diversity of mammals 199 evaluated (35% in risk) DD= 110 species 8 species 14 species 40 species species 19 species World= 21% of species at risk Schipper et al Chiarello et al. 2008

8 Relative importance, in rank order, of ecological predictors of mammalian extinction risk. Davidson A D et al. PNAS 2009;106: by National Academy of Sciences

9 % Species Major Threats Habitat lossfragmentation Poaching Persecution Chiarello et al. 2008

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11 The scale of defaunation Killed animals/year Peres, 2000, Fa et al. 2002

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13 Proportion Hunting affects selectively the game species Nobre, 2007

14 Densidade (Ind/km2) Abundance of mammals in the continuous Serra do Mar 30 x Nobre & Galetti, unpubl. data

15 1 What s the status of large mammals in the largest continuous Atlantic Forest? >4.000 km sampling 13 Continuous Protected Areas

16 Mammal density (Ind/km2) Density of mammals: Amazon x Atlantic forest , Atlantic forest Amazon ,00 75,04 63,96 62,40 56, ,68 18,65 14,33 11,12 10,89 8,92 5,69 3, x 9.5x Galetti et al. 2009, Haugaasen & Peres 2005

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20 The role of mammals in promoting diversity Trampling Pollination Herbivory Seed dispersal Seed predation 30% of trees in the Atlantic forest

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22 Non defaunated forest Predation Competition or Interference Predation

23 Highly Defaunated forests Predation

24 Abundance/Ecological Rol Expected changes in mammal communities in relation to perturbation None Moderate High Perturbation intensity Wright, 2003

25 Trade-offs between rodent and large mammal abundance in Africa Saccostomus mearnsi McCauley et al. 2006

26 eves, 2010 Parque Estadual Serra do Mar Núcleo Santa Virgínia 2 sites= 15 km

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28 Mammal abundance Base Itamambuca Base Vargem Grande Tayassu pecari Callithrix aurita Cebus nigritus Sciurus aestuans Tapirus terrestris Alouatta guariba Nasua nasua Puma concolor Cuniculus paca Leopardus wiedii Leopardus pardalis Pecari tajacu Puma yagouaroundi Dasyprocta leporina (aff.) Cerdocyon thous Leopardus tigrinus Dasypus novemcinctus Tamandua tetradactyla Didelphis aurita Eira barbara Hydrochoerus hydrochaeris Canis lupus familiaris Número de registros Número de registro por espécie de mamíferos (transectos lineares + armadilhas fotográficas) para as bases Itamambuca e Vargem Grande, bases de pesquisa do Núcleo Santa Virgínia Parque Estadual da Serra do Mar. Rocha-Mendes & Galetti, unpubl.

29 Sampling Small Mammals Live-trap 2700 live-traps/night/site Pitfall 720 pitfall-traps/night/site

30 Abundance of marsupials 6 5 Marsupials No-defaunated Defaunated livetrap pitfall

31 Abundance of rodents Rodents 25 No-defaunated Defaunated livetrap pitfall

32 Alternative hypothesis Snake abundance Rejected Mesopredator abundance Rejected Resource limitation (fruits/insects) Rejected Microhabitat limitation - Rejected

33 A forest with too many rodents, may have high seed predation

34 Palmito, Euterpe edulis Dominant and keystone species in the AF Fruits consumed by more than 47 bird species Harvested for palm heart

35 defaunated sites X 3 non-defaunated sites 5 1

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37 Richness of Seed Predators in Nondefaunated forests

38 Richness of Seed Predators in Defaunated forests

39 Number of seeds predated/day Higher seed predation in defaunated forests Number of Predations per day GLM ~ Poisson distribution F value=10.59; P= ** Df= 1,138 Effect magnitude: 6.33 higher Defaunated Non-defaunated

40 Proportion Rodents were the major Proportion seed predator of predated in defaunated forests Defaunated Birds Large rodents Small rodents Ungulates Non-defaunated

41 Conclusion 1 Peccaries exerts a top down effects on rodent populations Peccaries-free forest have higher seed predation due to rodent overabundance

42 What about seed dispersal? We collected about 1400 hours of focal observation in 15 populations of Euterpe edulis. Each area was classified as defaunated if toucans were absent.

43 15 populations (6 defaunated x 9 non defaunated) -Frugivory and seed dispersal -Seed size variation -Demography and spatial distribution

44 The extinction of palmito dispersers affects more largegaped birds

45 Regurgitate 12 Regurgitate 3 Defecate 4 Predate 10 Drop Drop Regurgitate Predate Regurgitate Defecate Phylogeny of species of birds that eat Euterpe edulis fruits in nondefaunated forests

46 Regurgitate 1 Regurgitate 1 Defecate 0 Predate 10 Drop Drop Defecate Phylogeny of species of birds that eat Euterpe edulis fruits in defaunated forests

47 Impact of losing large Pollination birds Seed dispersal Non-defaunated area Long distance dispersal Dispersal effectiveness Fruit choice Defaunated area

48 Defaunation selects for small gaped birds GLM, F1,10=5.5, P=0.041

49 2.5x 380 g 7x 55 g Larger seed disperser in non-defaunated site Larger seed disperser in defaunated site

50 Rottweiler Pug 50 kg 7 kg

51 Large-gaped birds eat larger seeds than small-gaped birds

52 Seed size eaten by different frugivores GLM, F6,390=25.5, P<0.0001

53 Seed size eaten by different frugivores GLM, F6,390=25.5, P<0.0001

54 Palmito seeds need to be dispersed by birds that regurgitate them

55 Probability of seed germination per disperser type Survival analysis, F1,3=65.64, P=0.0001

56 Therefore, large seeds are not dispersed in defaunated forests

57 Pecked by birds (not dispersed) Regurgitated (dispersed)

58 Probability of seed dispersal in defaunated sites decline with seed size Defaunated Nondefaunate d Binary GLM, Site/Size: 2 [4] = 153.6, df = 5, P < 0.001

59 The populations of defaunated sites have smaller seeds

60 Comparing seed size among populations with same soil, climate, forest type Fragments Continuous

61 Comparison of seed size between pair populations Nested GLM, F2,1594=211, P<0.0001

62 seeds 13 populations 13

63 Alternative hypothesis Geographical distance (Rejected) Tree age (size and DBH) (Rejected) Rainfall (Rejected) Latitude (Rejected) Soils (Rejected) Trade-off between fruit crop and seed size (Rejected) Founder effect (Rejected)

64 Rapid phenotypic changes can explain seed shrinkage in palmitos

65 Response to selection (Rt) R t 1 h 2 (d f d t ) Heritability Mean seed size in non-defaunated population Mean seed size in defaunated sites (Selected by small frugivores) Generation time in Euterpe = 18.7 years

66 Predicted seed size after bird defaunation Continuous forests h2=0.2 h2=0.3 Fragmented forests h2=0.2 h2=0.3

67 How old are these fragments?

68 Between 1821 e 1824, several sugar cane and coffee farms were established. Rio Claro: The Plantation System. Warren Dean. Fragments ~190 years (10 generations)

69 Long term consequences of defaunation under a Global change scenario

70 The importance of having larger seeds Larger seeds means more reserve Bigger seedlings (vigor) Can be partially predated Can have less predators May be able to cope with global change scenarios

71 Take home messages 1.Defaunation will create new ecological constraints to plant populations (increasing seed predation, seed limitation). 2.Defaunation will create new selective force for evolution 3.Defaunation can drive rapid evolutionary changes on key phenotypic traits in plants

72 It is not the strongest of the species that survives, nor the most intelligent that survives. It is the one that is the most adaptable to change. Charles Darwin

73 Palmito gang

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