Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent...

59
QuickTime™ and a decompressor are needed to see this picture. Perda de biodiversidade e doencas infecciosas Kevin D. Lafferty U.S. Geological Survey

Transcript of Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent...

Page 1: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

QuickTime™ and a decompressor

are needed to see this picture.

Perda de biodiversidade e

doencas infecciosas

Kevin D. Lafferty

U.S. Geological Survey

Page 2: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Como o stress ambiental afeta doencas?

Page 3: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Parasite

Eutroph-

ication

Thermal

effluent

Pulp-mill

effluent Crude oil

Industrial

effluent

Sewage-

sludge

Acid

precipitation Disturbance

Heavy

metals

Ciliophora + + + +Nematoda

+ + +/- + -/+ = +/-Monogenea

+ +/- -/+ + +/- = - -Other groups

+ +/- + - - = = - +Cestoda

+ = -/+ + - - -Acanthocephala

+ +/- - - - + -Digenea

+ - -/+ - -/+ -/+ - - -

Diverse responses of parasites to stress

Lafferty 1997 Parasitology Today

Respostas variadas de parasitas ao stress

Page 4: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Parasite

Eutroph-

ication

Thermal

effluent

Pulp-mill

effluent Crude oil

Industrial

effluent

Sewage-

sludge

Acid

precipitation Disturbance

Heavy

metals

Ciliophora + + + +Nematoda

+ + +/- + -/+ = +/-Monogenea

+ +/- -/+ + +/- = - -Other groups

+ +/- + - - = = - +Cestoda

+ = -/+ + - - -Acanthocephala

+ +/- - - - + -Digenea

+ - -/+ - -/+ -/+ - - -

Diverse responses of parasites to stress

Lafferty 1997 Parasitology Today

Respostas variadas de parasitas ao stress

Page 5: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Parasite

Eutroph-

ication

Thermal

effluent

Pulp-mill

effluent Crude oil

Industrial

effluent

Sewage-

sludge

Acid

precipitation Disturbance

Heavy

metals

Ciliophora + + + +Nematoda

+ + +/- + -/+ = +/-Monogenea

+ +/- -/+ + +/- = - -Other groups

+ +/- + - - = = - +Cestoda

+ = -/+ + - - -Acanthocephala

+ +/- - - - + -Digenea

+ - -/+ - -/+ -/+ - - -

Diverse responses of parasites to stress

Lafferty 1997 Parasitology Today

Respostas variadas de parasitas ao stress

Page 6: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Population impact of disease versus stress

NO DISEASE

DISEASE

Par

asi

te m

ort

alit

y,

(a +

u +

m +

a)

Susceptibility, (- q)

Slope = K

Lafferty and Holt 2003 Ecol Lett

Impacto da doenca ou stress na populacao

Page 7: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Population impact of disease versus stress

NO DISEASE

DISEASE

Par

asi

te m

ort

alit

y,

(a +

u +

m +

a)

Susceptibility, (- q)

Slope = K

Lafferty and Holt 2003 Ecol Lett

Impacto da doenca ou stress na populacao

Page 8: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Population impact of disease versus stress

NO DISEASE

DISEASE

Para

site

mort

alit

y, (a

+ u

+ m

+ a

)

Susceptibility, (- q)

Lafferty and Holt 2003 Ecol Lett

Impacto da doenca ou stress na populacao

Page 9: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Population impact of disease versus stress

NO DISEASE

DISEASE

Para

site

mort

alit

y, (a

+ u

+ m

+ a

)

Susceptibility, (- q)

Slope = K

Lafferty and Holt 2003 Ecol Lett

Impacto da doenca ou stress na populacao

Page 10: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Population impact of disease versus stress

NO DISEASE

DISEASE

Para

site

mort

alit

y, (a

+ u

+ m

+ a

)

Susceptibility, (- q)

Lafferty and Holt 2003 Ecol Lett

Impacto da doenca ou stress na populacao

Page 11: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Has disease increased or

decreased in the ocean?As doencas estao aumentando

no oceano?

Page 12: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

% disease by host taxa. All wild, no duplicatesPorcentagem de doenca por tipo de hospedeiro. Todos Selvagens,

sem duplicacoes

Page 13: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Ward and Lafferty 2004 PLoS

% p

ubli

cati

ons

on d

isea

se

Sea Turtles

Publication Date

Tartarugas marinhas

% P

ub

lica

co

es e

m d

oe

nca

Data de publicacao

Page 14: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Ward and Lafferty 2004 PLoS

% p

ubli

cati

ons

on

dis

ease

Publication Date

% P

ub

lica

co

es e

m d

oe

nca

Data de publicacao

Page 15: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Ward and Lafferty 2004 PLoS

% p

ubli

cati

ons

on d

isea

se

Publication Date

Marine Mammals

% P

ub

lica

co

es e

m d

oe

nca

Data de publicacao

Mamiferos marinhos

Page 16: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

% p

ubli

cati

ons

on d

isea

se

Publication Date

Echinoderms

% P

ub

lica

co

es e

m d

oe

nca

Data de publicacao

Equinodermos

Page 17: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Lafferty et al 2004 Ecol. Appl.

Populacoes densas sofrem mais doencas

Page 18: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Lafferty et al 2004 Ecol. Appl.

Lobsters

Urchins

Algae

Disease

No Fishing Fishing

Lagostas

Ourico do mar

Alga

Doenca

pesca proibida, pesca permitida

Page 19: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Ward and Lafferty 2004 PLoS

% p

ubli

cati

ons

on d

isea

se

Publication Date

Mollusca%

Pu

blic

aco

es e

m d

oe

nca

Data de publicacao

moluscos

Page 20: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Torchin, Lafferty et al 2003, Nature

Livrando-se de inimigos naturais(26 taxa)

0

2

4

6

8

10

12

14

16

18

Introduced Native

Pa

rasite

sp

ecie

s

transferred

colonized

Page 21: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Ward and Lafferty 2004 PLoS

% p

ubli

cati

ons

on d

isea

se

Publication Date

Peixes

% P

ub

lica

co

es e

m d

oe

nca

Data de publicacao

Page 22: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Amundsen and Kristoffersen. 1990, Can J. Fish 68:1187-1192

Cestodas em Peixes (Norway)

Antes

0

20

40

60

80

100

120

140

160

180

200

1 2 3 4 5 6 7 8

Fish length

Num

ber

of

fish c

aught

infected uninfected

um

ero

de p

eix

es c

ole

tados

Comprimento do peixe

Page 23: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Amundsen and Kristoffersen. 1990, Can J. Fish 68:1187-1192

Cestodas em Peixes (Norway)

Antes Depois de pescaria intensa

0

20

40

60

80

100

120

140

160

180

200

1 2 3 4 5 6 7 8

Fish length

Num

ber

of

fish c

aught

infected uninfected

0

20

40

60

80

100

120

140

160

180

200

1 2 3 4 5 6 7 8

Fish lengthN

um

ber

of

fish c

aught

infected uninfected

um

ero

de p

eix

es c

ole

tados

Comprimento do peixe

um

ero

de p

eix

es c

ole

tados

Comprimento do peixe

Page 24: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Ransom A. Myers andハBoris WormNature 423, 280-283

Diminuicao global de peixes

Page 25: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

QuickTime™ and a decompressor

are needed to see this picture.

Quic

kT

ime

™ a

nd a

deco

mp

resso

ra

re n

ee

de

d to

se

e th

is p

ictu

re.

QuickTime™ and a decompressor

are needed to see this picture.

Sandin et al. 2008 PLoS1

Kiritim

ati Tabuaera

n P

alm

yra

K

ingm

an

Recifes de coral e pescaria

Page 26: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

QuickTime™ and a decompressor

are needed to see this picture.

Page 27: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

QuickTime™ and a decompressor

are needed to see this picture.

Page 28: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

QuickTime™ and a decompressor

are needed to see this picture.

Page 29: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

QuickTime™ and a decompressor

are needed to see this picture.

Page 30: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

QuickTime™ and a decompressor

are needed to see this picture.

Page 31: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

QuickTime™ and aH.264 decompressor

are needed to see this picture.

Page 32: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

QuickTime™ and a decompressor

are needed to see this picture.

Page 33: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

QuickTime™ and a decompressor

are needed to see this picture.

Page 34: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

QuickTime™ and a decompressor

are needed to see this picture.

Page 35: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

QuickTime™ and a decompressor

are needed to see this picture.

Page 36: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

QuickTime™ and a decompressor

are needed to see this picture.

Page 37: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

QuickTime™ and a decompressor

are needed to see this picture.

Page 38: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

QuickTime™ and a decompressor

are needed to see this picture.

Page 39: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Palmyra Atoll Natl. Wildlife Refuge

Parasitos em peixes

Page 40: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

0

5

10

15

20

25

P. arcatus A. nigricans P. dickii C. margaritifer L. bohar

Host Species

Jackn

ife p

arasit

e s

pecie

s/ f

ish

specie

s (

+/-

95

%)

Kirimati

Palmyra

Comunidades de parasitas sao mais diversas no atol

protegido do que no atol com pescaria

QuickTime™ and a decompressor

are needed to see this picture.

Lafferty et al. 2008 EcoHealth

Page 41: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

0

10

20

30

40

50

60

70

80

90

P. arcatus A. nigricans P. dickii C. margaritifer L. bohar

Host species

Pre

vale

nce o

f shark

tap

ew

orm

s (

+/- 9

5%

CL)

Kiritimati

Palmyra

Pre

vale

ncia

de t

enia

s d

e t

ubaro

es

Especie de hospedeirro

Page 42: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Teia alimentar com parasitos (amarelo)

Lafferty et al. 06 PNAS

Page 43: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Teia alimentar com parasitos (amarelo)

Page 44: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Teia alimentar com parasitos (amarelo)

Page 45: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

0

5

10

15

20

25

30

35

40

45

0 10 20 30 40 50 60 70 80

Free-living richness

Para

sit

e r

ich

ness

Extincao secundaria de parasitos com o

desmanchamento da teia alimentae

Lafferty et al. 09 Phil transRoy Soc

Page 46: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals
Page 47: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Sequencia temporal, video

•5 sec/min, 12 hrs/day, 14 days = 2000 clips

QuickTime™ and aYUV420 codec decompressor

are needed to see this picture.

Page 48: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Div

ers

ida

de

de

esp

ecie

s d

e tre

ma

tod

os

Diversidade de especies de aves

Div

ers

ida

de

de

esp

ecie

s d

e tre

ma

tod

os

Diversidade de especies de aves

Page 49: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Huspeni and Lafferty 2004. Ecological Applications

Div

ers

ida

de

me

dia

de

esp

ecie

s d

e tre

ma

tod

os

Controle

Impacto

Page 50: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

• Stress may increase or decrease disease

• Stress pode aumentar ou diminuir parasitas

• Increased susceptibility, increased parasite mortality, reduced host density

• Susceptibilidade aumentada, mortalidade de parasitas aumentada, densidade do hospedeiro diminuida

• Diseases have increased and decreased

• Doencas tem aumentado e diminuidoFishing reduces disease

• Pescaria diminui doencas

• Host diversity begets parasite diversity

• Diversidade de hospedeiro controla a diversidade de parasitas

Conclusions

Page 51: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Dawson et al. 2005 Phys Ecol.

Field Experiment: haematophagous flies and

tree swallows.

Page 52: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Dawson et al. 2005 Phys Ecol.

Field Experiment: haematophagous flies and

tree swallows.

Page 53: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

0

0.02

0.04

0.06

0.08

0.1

22 24 26 28 30 32 34

Path

ogen d

evelo

pm

ent ra

te

Louis et al. 1986

Rickettsia in Crickets

Page 54: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Temperature response

Climate projection

Martens et al. 1995

Page 55: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Hypothetical temperature-transmission relationships

Martens et al. 1997 Climate Change ** Tree 18 34-350 (2003)

Page 56: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Process-based model for

changes in malaria

Thomas et al. 2004

Present

Contraction

Expansion

2025 2055 2085

Page 57: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Peterson and Shaw 2003, IJP

Projection to 2050 (change)

Sandflies

(Lutzomyia spp)Leishmaniasis vector

Contraction

Expansion

Page 58: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Covariates

Page 59: Kevin D. Lafferty U.S. Geological Surveyfapesp.br/eventos/2009/11/biota/lafferty.pdf · effluent Crude oil Industrial effluent Sewage-sludge Acid precipitation Disturbance Heavy metals

Land-use change and malaria reduction in Britain

Kuhn et al. 2003 PNAS