1. Ecology
  2. Epidemiology and Global Health
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Ecological multiplex interactions determine the role of species for parasite spread amplification

  1. Massimo Stella
  2. Sanja Selakovic
  3. Alberto Antonioni
  4. Cecilia S Andreazzi  Is a corresponding author
  1. University of Southampton, United Kingdom
  2. Utrecht University, Netherlands
  3. University College London, United Kingdom
  4. Universidad Carlos III de Madrid, Spain
  5. University of Zaragoza, Spain
  6. Fundação Oswaldo Cruz, Brazil
Research Article
Cite this article as: eLife 2018;7:e32814 doi: 10.7554/eLife.32814
11 figures, 4 tables and 1 additional file

Figures

Visual representation of our ecological multiplex network model.

The background colouring on the right panels indicates that elements such as bushes, trees, grass and water areas are not present in the spatial embedding of the ecomultiplex model, where only the spatial network structure among close animal groups is considered.

https://doi.org/10.7554/eLife.32814.003
Single layer interactions and multiplex cartographies of Canastra and Pantanal biomes.

(a) and (b) Food web layer and vectorial layer in Canastra (left) and Pantanal (right) biomes. Predators are highlighted in blue, preys in orange and the vectors in green. Interactions involving the insect are highlighted in red. Interactions involving other species are reported for completeness in blue. (c–f): Multiplex cartography of the Canastra ecomultiplex network with 10% (c) and 25% (e) of total groups as vectors. Multiplex cartography of the Pantanal ecomultiplex network with 10% (d) and 25% (f) of total groups as vectors. The red line separates hub nodes, i.e. the most connected nodes within the 95th percentile of the total degree distribution. The cartography highlights the average trends of species: blue for predators, orange for preys, and green for vectors. As evident from (a–e), vectors have higher total degree in the ecosystem and tend to distribute more equally their links across both the multiplex layers than all other species. Vectors are therefore pivotal in the ecosystem.

https://doi.org/10.7554/eLife.32814.004
Immunisation strategies for the Canastra (top) and Pantanal (bottom) ecosystems when the vector frequency is 0.1 (left) and 0.25 (right).

The infection time increase plotted on the y-axis is defined in Immunisation Strategies (Methods and Materials). An increase of +0.3 indicates that the infection time in a given immunisation scenario was 30% higher than in the reference case of random immunisation.

https://doi.org/10.7554/eLife.32814.005
Difference in performances of the best immunisation strategy (hemoculture - Highest 3) when another top predator in the ecosystem (not interacting with the vector in the vectorial layer) is immunised instead of Leopardus pardalis (hemoculture - H 3 No Leopardus).

The other top predator is the maned wolf (Chrysocyon brachiurus).

https://doi.org/10.7554/eLife.32814.006
Appendix 1—figure 1
Interaction matrix includes trophic (predator-prey, blue squares) and vectorial (vector-host, green squares) interactions in Canastra area.
https://doi.org/10.7554/eLife.32814.010
Appendix 1—figure 2
Interaction matrix includes trophic (predator-prey, blue squares) and vectorial (vector-host, green squares) interactions in Pantanal area.
https://doi.org/10.7554/eLife.32814.011
Appendix 3—figure 1
In general home ranges Hi for different animal groups of the same species can overlap (e.g.

see the red overlapping area Ω on the left). Hence, not all the energy available in the home range can sustain the biomass of the animal groups as some resources must be shared and competition can occur. We therefore approximate the total energy effectively available from the overlapping home ranges with the energy coming from non-overlapping effective home ranges Hi, which allow to approximate the total biomass for species i. Effective home ranges Hi have radius r equal to half the distance between animal groups. .

https://doi.org/10.7554/eLife.32814.016
Appendix 5—figure 1
Scheme on which species are immunised as animal groups in the ecomultiplex network in the different immunisation strategies presented in the main text.

The average frequency, serology and hematology of the animal groups immunised in each strategy are presented as well. Error margins indicate standard deviations.

https://doi.org/10.7554/eLife.32814.019
Appendix 7—figure 1
Infection time increases in Canastra for immunisation strategies that are not reported in the main text.

Visual comparisons are made against the strategy Parasitised Mammals from the main text. For low vector frequency (fv=0.1) all the reported strategies behave worse than Hemoculture (Highest 3) and were therefore not discussed in the main text.

https://doi.org/10.7554/eLife.32814.023
Appendix 8—figure 1
The best and the worst performing strategies presented in the main text for the Canastra ecosystem are here presented relatively to the null model with equal abundances.

In this null model we consider an ecomultiplex network where all animal groups have equal abundance, that is, occur with equal frequency. The error margins in the plot are the same size of the dots and are based on 500 iterations. Even providing equal abundances to different species does not remove the gap in global infection time that was observed in the main text.

https://doi.org/10.7554/eLife.32814.025
Appendix 8—figure 2
The best network-based and the worst performing strategies presented in the main text for the Canastra ecosystem are here presented relatively to the null model with equal abundances.

In this null model we consider an ecomultiplex network where all animal groups have equal abundance, that is, occur with equal frequency. The error margins in the plot are the same size of the dots and are based on 500 iterations. Even providing equal abundances to different species does not remove the gap in global infection time that was observed in the main text.

https://doi.org/10.7554/eLife.32814.026

Tables

Table 1
Immunisation types, names and targets of the strategies we tested (Appendix 1).
https://doi.org/10.7554/eLife.32814.007
Immunisation typeStrategy nameStrategy targets
Ecomultiplex Topological FeaturesInsectivoresSpecies feeding on the vector in a food-web
Parasitised DidelphidaeDidelphidae contaminated by the vector on a vectorial layer
Parasitised MammalsAll species contaminated by the vector on a vectorial layer
Taxonomic/morphological featuresAll CricetidaeAll Cricetidae
All DidelphidaeAll Didelphidae
Large MammalsAll species with a body mass > 1 kg
Epidemiological FeaturesHemoculture NThe N species with the highest likelihood of being found infected with the parasite in field work (see Appendix 1).
Serology NThe N species with the highest likelihood of having been infected with the parasite during their life time (see Appendix 1).
Appendix 1—table 1
Taxonomic and ecological data of different animal species in Canastra area (1- (Reis et al., 2006), 2- (Myers et al., 2008), 3- (Herrera et al., 2011), 4- (Bonvicino et al., 2008), 5- (Schofield, 1994)).

(Rocha et al., 2013) report prevalence measurements for some genera, indicating the species that were collected during the study. Because those species are ecologically similar we calculated the average body size of the genus considering species that were collected. aM. americana, M. domestica and M. sorex. b A. sp., A. lindberghi, A. cursor. cO. sp, O. nigripes, O. rupestris. dC. sp, C. tener.

https://doi.org/10.7554/eLife.32814.012
IDSpeciesCommon nameFamilyDiet typeBiomass [gr]References   
CHRChrysocyon brachyurusManed wolfCanidaeomnivorous25000[1, 2]
LEOLeopardus pardalisOcelotFelidaecarnivorous9740[1, 2, 3]
CERCerdocyon thousCrab-eating foxCanidaeomnivorous6600[1, 2, 3]
LYCLycalopex vetulusHoary foxCanidaeomnivorous3350[1, 2]
CONConepatus semistriatusStriped˙hog-nosed skunkMustelidaeomnivorous2567[1, 2]
DIDDidelphis albiventrisWhite-eared opossumDidelphidaeomnivorous1625[1, 2]
LUTLutreolina crassicaudataThick-tailed opossumDidelphidaeomnivorous600[1, 2]
CAPCaluromys philanderBare-tailed˙woolly opossumDidelphidaeomnivorous255[1, 2]
NECNectomys squamipesSouth American water ratCricetidaeomnivorous270[1, 2]
MONMonodelphis spp aShort-tailed opossumDidelphidaeomnivorous72.8[1, 2, 3]
MARMarmosops incanusGray slander opossumDidelphidaeomnivorous80[1, 2]
OXYOxymycterus delatorSpy hocicudoCricetidaeomnivorous78.3[4]
CESCerradomys subflavusRice ratCricetidaeomnivorous73[4]
NECNecromys lasiurusHairy-tailed bolo mouseCricetidaeomnivorous52[1, 2, 4]
AKMAkodon montensisMontane grass mouseCricetidaeomnivorous40.5[1, 2, 4]
AKOAkodon spp bGrass mouseCricetidaeomnivorous33.25[1, 4]
GRAGracilinanus agilisAgile gracile opossumDidelphidaeomnivorous27.25[1, 2, 3]
OLIOligoryzomys spp cPygmy rice ratsCricetidaeomnivorous21.23[1, 4]
CALCalomys spp dVesper mouseCricetidaeherbivorous18.65[1, 4]
TRITriatominaeKissing bugReduviidaeblood0.2[5]
Appendix 1—table 2
Taxonomic and ecological data of different animal species in Pantanal area (1- (Reis et al., 2006), 2- (Myers et al., 2008), 3- (Herrera et al., 2011), 4- (Bonvicino et al., 2008), 5- (Schofield, 1994)).
https://doi.org/10.7554/eLife.32814.013
IDSpeciesCommon nameFamilyDiet typeBiomass [gr]References   
LEOLeopardus pardalisOcelotFelidaecarnivorous9740[1, 2, 3]
CETCerdocyon thousCrab-eating foxCanidaeomnivorous6600[1, 2, 3]
NANNasua nasuaSouth American coatiProcyonidaeomnivorous5140[1, 2, 3]
SUSSus scrofaWild boarSuidaeomnivorous105750[1, 2, 3]
PETPecari tajacuCollared peccaryTayassuidaeomnivorous24000[1, 2, 3]
HYHHydrochaeris hydrochaerisCapybaraCaviidaeherbivorous46200[1, 2, 3]
TAPTayassu pecariWhite-lipped peccaryTayassuidaeomnivorous30200[1, 2, 3]
EUSEuphractus sexcinctusSix-banded armadilloChlamyphoridaeomnivorous4450[1, 2, 3]
PHFPhilander frenatusSoutheastern four-eyed opossumDidelphidaeomnivorous306.2[1, 2, 3]
THPThrichomys pachyurusParaguayan punarEchimyidaeherbivorous291.25[1, 3, 4]
CLLClyomys laticepsBroad-headed spiny ratCricetidaeherbivorous187.33[1, 3, 4]
HOBHolochilus brasiliensisWeb-footed marsh ratCricetidaeherbivorous196[1, 3, 4]
CESCerradomys scottiLindbergh’s rice ratCricetidaeomnivorous92.34[3, 4]
MODMonodelphis domesticaGray short-tailed opossumDidelphidaeomnivorous111.2[1, 2, 3]
OEMOecomys mamoraeMamore arboreal rice ratCricetidaeherbivorous83.75[1, 3, 4]
THMThylamys macrurusLong-tailed fat-tailed opossumDidelphidaeomnivorous46.6[1, 2, 3]
CACCalomys callosusLarge vesper mouseCricetidaeherbivorous37.45[1, 3]
GRAGracilinanus agilisAgile gracile opposumDidelphidaeomnivorous27.25[1, 2, 3]
TRITriatominaeKissing bugReduviidaeblood0.2[5]
Appendix 6—table 1
Scheme on which species are immunised as animal groups in the ecomultiplex network in the different immunisation strategies presented in the main text.

The average frequency, serology and hematology of the animal groups immunised in each strategy are presented as well. Error margins indicate standard deviations.

https://doi.org/10.7554/eLife.32814.021
CANASTRAImmune and Susceptible Species in the Immunisation Strategies ↓
Species ↓All CricetidaeAll DidelphidaeLarge MammalsParasitised MammalsParasitised DidelphidaeInsectivoresHemoculture 3
Chrysocyon brachyurus
Leopardus pardalis
Cerdocyon thous
Lycalopex vetulus
Conepatus semistriatus
Didelphis albiventris
Lutreolina crassicaudata
Caluromys philander
Nectomys squamipes
Monodelphis spp
Marmosops incanus
Oxymycterus delator
Cerradomys subflavus
Necromys lasiurus
Akodon montensis
Akodon spp
Gracilinanus agilis
Oligoryzomys spp
Calomysspp
Mean Frequency (fv = 0.1)640 ± 50480 ± 70200 ± 20560 ± 80520 ± 50510 ± 50400 ± 100
Mean Frequency (fv = 0.25)540 ± 40400 ± 60170 ± 20470 ± 70430 ± 40430 ± 40400 ± 100
Mean Serology0.02 ± 0.020.2 ± 0.10.3 ± 0.20.3 ± 0.20.3 ± 0.30.12 ± 0.070.7 ± 0.3
Mean Hemoculture0.07 ± 0.040.1 ± 0.10.2 ± 0.20.3 ± 0.10.3 ± 0.20.07 ± 0.040.6 ± 0.2
PANTANALImmune and Susceptible Species in the Immunisation Strategies ↓
Species ↓All CricetidaeAll DidelphidaeLarge MammalsParasitised MammalsParasitised DidelphidaeInsectivoresHemoculture 3
Leopardus pardalis
Cerdocyon thous
Nasua nasua
Sus scrofa
Pecari tajacu
Hydrochaeris hydrochaeris
Tayas supecari
Euphractus sexcinctus
Philander frenatus
Thrichomys pachyurus
Clyomys laticeps
Holochilus brasiliensis
Cerradomys scotti
Monodelphis domestica
Oecomys mamorae
Thylamys macrurus
Calomys callosus
Gracilinanus agilis
Mean Frequency (fv = 0.1)730 ± 60800 ± 100210 ± 20540 ± 90700 ± 100530 ± 80600 ± 200
Mean Frequency (fv = 0.1)610 ± 50650 ± 80170 ± 20450 ± 80630 ± 100440 ± 60500 ± 200
Mean Serology0.24 ± 0.020.5 ± 0.10.3 ± 0.10.37 ± 0.090.5 ± 0.10.35 ± 0.060.50 ± 0.09
Mean Hemoculture0.02 ± 0.010.18 ± 0.060.04 ± 0.030.12 ± 0.30.23 ± 0.030.07 ± 0.020.25 ± 0.02

Data availability

All data generated or analysed during this study are included in the manuscript and appendices.

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