Conservation Biology (1990)

Selective defaunation creates a new

selective force for evolution: a sequel to

Rodolfo DirzoMauro Galetti

Departamento de Ecologia

São Paulo State University - Rio Claro, São Paulo,

Brazil

mgaletti@rc.unesp.br

We live in a zoologically

impoverished world, from which

all the hugest, and fiercest, and

strangest forms have recently

disappeared…

Alfred Russell Wallace (1876)

World diversity of mammals

40 species

11 species

19 species

14 species

653

199 evaluated (35% in risk)

World= 21% of species at risk

Schipper et al. 2008

8 species

DD= 110 species

Chiarello et al. 2008

Relative importance, in rank order, of ecological predictors of mammalian extinction risk.

Davidson A D et al. PNAS 2009;106:10702-10705

©2009 by National Academy of Sciences

Major Threats

% S

pecie

s

Chiarello et al. 2008

Habitat lossFragmentation Poaching Persecution

The scale of defaunation

Killed animals/yearPeres, 2000, Fa et al. 2002

Hunting affects selectively the game

species

Nobre, 2007

Pro

po

rtio

n

Abundance of mammals in the

continuous Serra do Mar

Nobre & Galetti, unpubl. data

30 x

De

nsid

ade

(In

d/k

m2

)

1

34

2

5

6

7

8 910

111213

>4.000 km sampling

13 Continuous Protected Areas

What’s the status of large mammals in

the largest continuous Atlantic Forest?

Density of mammals: Amazon x Atlantic forest

278,78

75,04

63,96 62,4056,56

19,68 18,6514,33

11,12 10,89 8,925,69 3,66

270

229

200

164

142 140

126

111106,00

0

50

100

150

200

250

300

1 2 3 4 5 6 7 8 9 10 11 12 13

Mam

mal de

nsity (

Ind

/km

2)

Galetti et al. 2009,

Haugaasen & Peres 2005

3x 9.5x

Amazon

Atlantic forest

The role of mammals in promoting diversity

Pollination

Seed dispersal

Seed predation

Herbivory

Trampling

30% of trees

in the

Atlantic

forest

Predation

Competition or Interference

Non defaunated forest

Predation

Predation

Highly Defaunated forests

None Moderate High

Perturbation intensity

Ab

un

da

nce

/Eco

log

ica

l R

ol

Expected changes in mammal communities

in relation to perturbation

Wright, 2003

Trade-offs between rodent and

large mammal abundance in Africa

Saccostomus mearnsi

McCauley et al. 2006

Parque Estadual Serra do Mar

Núcleo Santa Virgínia

2 sites= 15 km

Neves, 2010

30 25 20 15 10 5 0 5 10 15 20 25 30 35 40 45

Canis lupus familiaris

Hydrochoerus hydrochaeris

Eira barbara

Didelphis aurita

Tamandua tetradactyla

Dasypus novemcinctus

Leopardus tigrinus

Cerdocyon thous

Dasyprocta leporina (aff.)

Puma yagouaroundi

Pecari tajacu

Leopardus pardalis

Leopardus wiedii

Cuniculus paca

Puma concolor

Nasua nasua

Alouatta guariba

Tapirus terrestris

Sciurus aestuans

Cebus nigritus

Callithrix aurita

Tayassu pecari

Número de registros

Base Itamambuca Base Vargem Grande

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.

Mammal abundance

Sampling Small Mammals

Live-trap

2700 live-traps/night/site

Pitfall

720 pitfall-traps/night/site

Marsupials

Abundance o

f m

ars

upia

ls

livetrap pitfall

0

1

2

3

4

5

6No-defaunated

Defaunated

Rodents

Abundance o

f ro

dents

livetrap pitfall

0

5

10

15

20

25No-defaunated

Defaunated

Alternative hypothesis

• Snake abundance – Rejected

• Mesopredator abundance – Rejected

• Resource limitation (fruits/insects) – Rejected

• Microhabitat limitation - Rejected

A forest with too many

rodents, may have high

seed predation

Palmito, Euterpe edulis

Dominant and keystone species in the AF

Fruits consumed by more than 47 bird

species

Harvested for palm heart

1

34

2

5

4 defaunated sites

X

3 non-defaunated sites

Richness of Seed Predators in Non-

defaunated forests

Richness of Seed Predators in

Defaunated forests

Defaunated Non-defaunated

0.0

0.5

1.0

1.5

2.0

2.5

3.0

Number of Predations per day

GLM ~ Poisson distribution

F value=10.59; P= 0.0014 **

Df= 1,138

Effect magnitude: 6.33 higher

Nu

mbe

r o

f se

eds p

red

ate

d/d

ay

Higher seed predation in defaunated forests

Proportion of predated

Pro

po

rtio

n

0.0

0.2

0.4

0.6

0.8

1.0

Defaunated Non-defaunated

BirdsLarge rodents

Small rodentsUngulates

Rodents were the major seed predator in defaunated forests

Conclusion 1

• Peccaries exerts a top down effects on

rodent populations

• Peccaries-free forest have higher seed

predation due to rodent overabundance

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.

15 populations (6 defaunated x 9 non defaunated)

-Frugivory and seed dispersal

-Seed size variation

-Demography and spatial distribution

The extinction of

palmito dispersers

affects more large-

gaped birds

Regurgitate

Regurgitate

Regurgitate

Defecate

Predate

Drop

12 Regurgitate

3 Defecate

4 Predate

10 Drop

Phylogeny of species of birds that eat Euterpe edulis fruits in non-

defaunated forests

Regurgitate

Defecate

Drop

1 Regurgitate

1 Defecate

0 Predate

10 Drop

Phylogeny of species of birds that eat Euterpe edulis fruits in

defaunated forests

Impact of losing large

birdsPollination Seed dispersal

Non-defaunated area

Defaunated area

Long distance dispersal

Dispersal effectiveness

Fruit choice

Defaunation selects for small gaped birds

GLM, F1,10=5.5, P=0.041

380 g 55 g7x

2.5x

Larger seed disperser

in non-defaunated

site

Larger seed

disperser in

defaunated site

Rottweiler Pug

50 kg 7 kg

Large-gaped birds eat

larger seeds than

small-gaped birds

Seed size eaten by different frugivores

GLM, F6,390=25.5, P<0.0001

Seed size eaten by different frugivores

GLM, F6,390=25.5, P<0.0001

Palmito seeds need to

be dispersed by birds

that regurgitate them

Probability of seed germination per disperser type

Survival analysis, F1,3=65.64, P=0.0001

Therefore, large seeds

are not dispersed in

defaunated forests

Regurgitated

(dispersed)

Pecked by birds

(not dispersed)

Defaunated

Non-

defaunate

d

Binary GLM, Site/Size: 2[4] =

153.6, df = 5, P < 0.001

Probability of seed dispersal in defaunated sites decline

with seed size

The populations of

defaunated sites have

smaller seeds

Fragments

Continuous

Comparing seed size among populations with

same soil, climate, forest type

Nested GLM, F2,1594=211, P<0.0001

Comparison of seed size between pair populations

1

1

2

3

4

5

6

7

8

9

10

11

12

13

23

45

136

7 8

9

11

12

8418 seeds

13

populations

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)

Rapid phenotypic

changes can explain

seed shrinkage in

palmitos

Response to selection (Rt)

Heritability 0.2

0.3

Mean seed size in defaunated sites

(Selected by small frugivores)

Mean seed size in

non-defaunated

population

Generation time in Euterpe = 18.7 years

Rt1 h2(d f dt )

h2=0.3h2=0.2

Continuous forests

Fragmented forests

Predicted seed size after bird defaunation

h2=0.3

h2=0.2

How old are these

fragments?

Fragments

~190 years

(10 generations)

“Between 1821 e 1824, several sugar cane and coffee farms were established.” Rio Claro: The Plantation System. Warren Dean.

Long term consequences

of defaunation under a

Global change scenario

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

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

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

Palmito gang