DISEASE ECOLOGY IN MULTI-HOST SYSTEMS
AT WILDLIFE/LIVESTOCK INTERFACES
CONCEPTS AND APPLICATIONS
CARON, A., GAIDET, N., CAPPELLE, J., MIGUEL, E., CORNELIS, D., GROSBOIS, V., DE
GARINE-WICHATITKSY, M.
Presented to ILRI at an open seminar on the 10th
of June 2015, Nairobi

GENERAL CONTEXT:
AFRICAN SOCIO-ECOSYSTEMS
• Arid & Semi-arid ecosystems
• Coexistence of People & Nature
• Development & Biodiversity Conservation
• Emerging & neglected diseases

Wildlife/Livestock/Human interface

Pathogen
transmission

CONCEPTS IN DISEASE
ECOLOGY
• Reservoir
• Maintenance host
• Target Host
Haydon et al. 2002, Ashford 1997, 2003
M T
Maintenance
Host
Target
Host
Spillover
Spillback
Critical Population Size
Susceptibility, Replicate, Excrete
Inter-species Contact Patterns

CONCEPTS IN DISEASE
ECOLOGY
M T
Spillover
To prevent and control disease…
1. Host control
2. Contact control
e.g. vaccination or culling

ECOLOGY OF BUFFALO - CATTLE INTERACTIONS
IMPLICATIONS FOR DISEASE TRANSMISSION
AT WILDLIFE/LIVESTOCK INTERFACES IN TFCAS
CARON, A., DE GARINE-WICHATITSKY, M., MIGUEL, E., GROSBOIS, V., FOGGIN, C., HOFMEYR,
M. CORNELIS, D.
An example of contact patterns at W/L interface
& Implications

TRANSFRONTIER CONSERVATION AREAS

GLTFCA & KAZA TFCA

EXAMPLE: BOVINE TB SPREAD IN THE GREAT
LIMPOPO TFCA
de Garine-Wichatitsky et al. 2010, Kock et al. 2014

DISEASE BURDEN AT THE WILDLIFE/
LIVESTOCK INTERFACE IN THE GLTFCA
Unfenced Interface
Malipati Pesvi
Buffalo Cattle Cattle
bTB
(SCITT)
NA 1.03%
2/195, 0.0-2.4
1.68%
3/179, 0.0-3.6
FMD
SAT 1 92.1%
35/38, 87.7-96.5
7.1%
5/70, 4.1-10.2
NA
SAT 2 68.4%
26/38, 60.9-75.9
1.4%
1/70, 0.0-2.8
NA
SAT 3 65.8%
25/38, 58.1-73.5
2.9%
2/70, 0.1-4.8
NA
Subtotal 94.7%
36/38, 91.1-98.3
10.0%
7/70, 6.4-13.6
NA
Br 0.0% 9.6% 16.0%
(RBT & c-ELISA) 0/38, <7.8 55/575, 7.2-12.0 84/526, 12.8-19.1
RVF 5.3% 18.3% NA
(I-ELISA) 2/38, 0.0-12.5 13/71, 9.2-27.4
Th
IFA 3.7%
1/27, 0.0-11.0
3.2%
1(3)/31, 0.0-9.5
42.5%
17(5)/40, 27.0-58.0
RT-PCR 88.2%
15/17, 72.4-100.0
NA NA
LSD 0.0% 52.2% NA
(VNT) 0/21, <14.1 35/67, 40.2-64.3
!
Caron et al. 2013

OBJECTIVE: FREQUENCY AND INTENSITY OF
CONTACTS BETWEEN CATTLE AN BUFFALO
AT DIFFERENT WILDLIFE/LIVESTOCK INTERFACES
IN TFCAS

PROTOCOL Material(&Methods(
(
• Regular(blood(sampling(in(ca6le(and(opportunis7c(in(buffaloes(
Communal(area(
• 45(GPS(collars(on(ca2le((
(1/herd)((
GPS(point(every(hour(
Na>onal(parks(
• 68(GPS(collars((on(buffalos((
(3/herd)((
GPS(point(every(hour(
2009(2008( 2011(2010( 2013(
12B/12C(
GNP(
6B/6C(
GNP(
12B/6C(
Crook(
20B/12C(
Crook(
18B/9C(
KNP(
Regular blood sampling in cattle populations and
opportunistic buffaloes

2 INTERFACES IN THE GLTFCA

LIMPOPO RIVER ADULT FEMALES
Adult female HR: localised ratios
Transboundary populations
No use of Sengwe corridor
Buffalo population connectivity: none

INTERFACE BETWEEN BUFFALO & CATTLE
Cattle GPS point
Buffalo Home Range

DEFINITION OF CONTACTS BETWEEN BUFFALO
& CATTLE —> E.G. FMD
Space & time window
for Foot and Mouth Disease :
0-15d & 0-300m
So a contact occurs when a cattle position is recorded within 300
m of the buffalo position less than 15 days after the buffalos
position recording

IDENTIFYING CONTACTS
Cattle Home Range
Buffalo Home Range
Buffalo/Cattle contact

RELATIONSHIP BETWEEN CONTACT & FMD
INCIDENCE IN CATTLE
0
0,1
0,2
0,3
0,4
0,5
0,6
0,7
0 0,5 1 1,5 2 2,5 3 3,5 4 4,5 5 5,5 6 6,5 7 7,5 8 8,5 9
Predicted
serological
incidence
log(number
of
contacts)
[herd&period
specific]
Estimated
serological
incidence
rate
over
4
month
periods
as
a
function
of
contact
rate
0→1/(0→1+0→0)
329
transitions/164
individuals/32
herds
Miguel et al. 2013

MODEL CAN BE ADAPTED TO OTHER
PATHOGENS
Contact definition:
• Can be adapted to different
pathogens:
• bTB
• Tick-borne diseases…
Different contact pattern
according to pathogen
chosen
de Garine-Wichatitsky et al. in prep

NEW PROTOCOL IN OCTOBER 2013
Adult female -> localised HR
Adult male -> 2 tries -> 2 failures
Young female hypothesis: n=19; between 2.5 and 4.5 years
Caron et al., Revision EID

SPEEDY, RARE AND SEASONAL PATTERN?
Caron et al., Revision EID

IMPLICATION FOR BUFFALO ECOLOGY &
CONSERVATION
Ecology of the African buffalo
• Outbreeding behavior during rainy season
A case or not for the Sengwe Corridor?
Redefinition of the W/L interface?
• Not restrained to land-use boundaries
• Relevance of boundaries of the GLTFCA

IMPLICATION FOR DISEASE MANAGEMENT
Clear and strong hypothesis to explain the spread of bTB
from KNP to GNP
Measuring intensity and frequency of contacts?
• Who is migrating? How? How often?
How do we manage such « new » interface?
• E.g. FMD surveillance & control

BRIDGE HOSTS, A MISSING LINK IN DISEASE
ECOLOGY IN MULTI-HOST SYSTEMS
IMPLICATIONS FOR AIV ECOLOGY AT WILD/
DOMESTIC BIRD INTERFACE IN SOUTHERN AFRICA
CARON, A., CAPPELLE, J., CUMMING, G.S, MUNDAVA, J., GROSBOIS, V., DE GARINE-
WICHATITSKY, M., GAIDET, N.
An example of Conceptual Development
& Implications

CONCEPTS IN DISEASE
ECOLOGY
M T
Contact
Transmission
B
Bridge Host
Caron et al. 2015
So far,
not properly defined

BRIDGE HOST PROPERTIES
• Contact with the maintenance host/community
• Contact with the target population
• Susceptible, able to replicate & excrete the pathogen
= Host competence (excep. mechanic transmission)
B
Bridge Host Caron et al. 2015

MAINTENANCE - BRIDGE - TARGET SYSTEMS
Adapted from Haydon et al. 2002 Caron et al. 2015

AVIAN INFLUENZA VIRUSES
AT WILD/DOMESTIC BIRD INTERFACE
IN AFRICA

AIV IN WILD BIRDS IN AFRICA
• Target population = domestic poultry
• Anseriforms (duck sp.) are known to be the
maintenance host for LPAI worldwide
• In Africa, since 2006, results indicate similar role of
ducks in LPAI epidemiology (Caron et al. 2011, Cumming et al. 2011,
Gaidet et al. 2012, etc.)

HOW TO IDENTIFY BRIDGE HOST
FOR AIV?
B
Bridge Host
Contact with ducks
Contact with poultry
AIV competence

TOOLS AT DISPOSAL
Host competence Host contacts Resources
Method Receptivity Replication Excretion
Contact/
Maintenanc
Contact/
Target
Experimental
Infection
xxx xxx xxx xxx
Risk Analysis x x x
Serological
investigation
x x x xx
Virological
investigation
xx xx xx xx xx
Telemetry
study
xxx xxx xxx
Bird ringing
and
xx x x
Bird counts xx xx x
Molecular
epidemiology
xx xx xx xx xx xxx
Need a combination of techniques (Epidemiology + Ecology)
Caron et al. 2015

STUDY SITE

Wild bird
community
MODEL
Intensive Poultry Backyard poultry
Ostrich farms
Waterfowl
community
Bird count
B
B
Caron et al. 2009, 2010

SHARED COMMUNITY OF WILD BIRDS
BETWEEN COMPARTMENTS
Caron et al. 2014

INTERACTIONS WERE DOMINATED BY A
FEW SPECIES
Caron et al. 2014

SUSCEPTIBILITY OF POTENTIAL BRIDGE
SPECIES IN LITERATURE
Red-billed quelea (Quelea quelea)
• potential H5N1 spreader (Breithaupt et al. 2010)
• positive for LPAI in Mali (Cappelle, pers. obs.)
Barn swallow (Hirunda rustica)
• positive for LPAI in Europe (Grosenova et al. 2008; Mizakova et al. 2008)
• positive for LPAI in Zambia and Zimbabwe (Caron, pers. obs.)
Cattle egret (Bulbucus ibis)
• positive for LPAI in Northern America (Squires et al. 2008)

SAMPLING OF POTENTIAL BRIDGE HOSTS
N=# AIV# NCD# WNV#
Red$billed(
Quelea(
206( 2(0.97%)( 15(7.28%)( 6((2.91%)(
Barn(
swallow(
133( 4(3.00%)( 8(6.02%)( 2(1.50%)(
CaAle(
egret(
166( 0(0.00%)( 1(0.60%)( 0(0.00%)(
Bridge Hosts
For AIV
B
B
Caron et al. 2014
Adapted protocol
Timely for interactions

IMPLICATIONS FOR AIV MANAGEMENT
Control contacts between bridge
and target populations
• Control on-farm wild bird
attractors (food/water)
• Control building roosting
site (swallow)
• Efficient quelea control
(pest)
Intervention targeted at specific
species & during period when
interactions are high

CONCLUSION
Disease ecology at Wildlife/Livestock interface
Combined ecology and epidemiology sciences
Approach using « Epidemiological Functions »
• Maintenance function (maintenance host)
• Transmission function (maintenance, bridge
hosts)
Caron et al. 2012, 2014, 2015

E.G. EBOLA
Bats Human
Bat
sp. 1
Bat
sp. 2 Bat
sp. 3
Bushmeat
Hunting
Others???
Antelopes
Pigs
Dogs
Apes
???
???
???
???
de Garine-Wichatitsky et al. in prep

E.G. FMD
Buffalo CattleDirect contacts
Fences?
Impala
Kudu
???
???
Goats
de Garine-Wichatitsky et al. in prep

TAKE HOME MESSAGE
Functional approaches
applied to disease
transmission
They need integrating more
Ecology & Epidemiology
e.g. EID: Pathogen hunting is
important —> but working on
transmission dynamics is as
much important

WHAT’S NEXT? ON-GOING?
Other epidemiological functions (amplification, dilution)?
(de Garine-Wichatitsky et al. in prep)
Include the animal/human interface (social science,
economic aspects) (de Garine-Wichatitsky et al. 2012)
How to predict infectious transmission (EID)?
• Community of shared pathogens
• Rodent-borne diseases-based networks at rodent/human interfaces: transmission
ecology in heterogeneous landscapes in Southeast Asia (Bordes et al. in prep)
• Patho-indicator of transmission (e.g. Commensal Escherichia coli
populations)
• Escherichia coli populations sharing and antibiotic resistance gradient at a buffalo/
cattle interface in southern Africa (Mercat et al. Revision, AEM)

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http://www.researchgate.net/profile/Alexandre_Caron

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IMPLICATIONS FOR AIV IN WILD BIRDS
More than just Anseriformes &
Charadriiformes in AIV ecology
Other orders & species play an important
role
• depending on ecosystem
• species ecology
Redefine wild bird surveillance for AIV
• Not blind sampling
• More eco-epidemiological
approaches
Caron et al. 2012
Caron et al. in prep