Modelling the spatial distribution of aquatic insects (Order Hemiptera) potentially involved in the transmission of Mycobacterium ulcerans in Africa

Background Biting aquatic insects belonging to the order Hemiptera have been suggested as potential vectors of Mycobacterium ulcerans in endemic areas for Buruli ulcer (BU). If this is the case, these insects would be expected to co-exist with M. ulcerans in the same geographical areas. Here, we studied the geographical distribution of six aquatic Hemiptera families that are thought to be vectors of M. ulcerans and explored their potential geographical overlapping with communities reporting BU cases in endemic countries. Methods We have developed ensemble ecological models of predicted distribution for six families of the Hemiptera (Naucoridae, Belostomatidae, Notonectidae, Nepidae, Corixidae and Gerridae) applying a robust modelling framework over a collection of recorded presences and a suite of environmental and topographical factors. Ecological niche factor analysis (ENFA) was first used to identify factors that best described the ecological niches for each hemipteran family. Finally, we explored the potential geographical co-occurrence of these insects and BU in two endemic countries, Cameroon and Ghana. Results Species of the families Naucoridae and Belostomatidae, according to our models, are widely distributed across Africa, although absent from drier and hotter areas. The other two families of biting Hemiptera, the Notonectidae and Nepidae, would have a more restricted distribution, being more predominant in western and southern Africa. All these four families of biting water bugs are widely distributed across coastal areas of West Africa. They would thrive in areas where annual mean temperature varies between 15–22 °C, with moderate annual precipitation (i.e. 350–1000 mm/annual) and near to water courses. Species of all hemipteran families show preference for human-made environments such as agricultural landscapes and urbanized areas. Finally, our analysis suggests that M. ulcerans and species of these aquatic insects might coexist in the same ecological niches, although there would be variation in species diversity between BU endemic areas. Conclusions Our findings predict the geographical co-existence of some species of aquatic hemipteran families and BU. Considering the existing biological evidence that points to some of these aquatic insects as potential phoretic vectors of M. ulcerans, its presence in BU endemic areas should be considered a risk factor. The ecological models here presented may be helpful to inform future environmental based models intended to delineate the potential geographical distribution of BU in the African region. Electronic supplementary material The online version of this article (10.1186/s13071-018-3066-3) contains supplementary material, which is available to authorized users.

Text S2. Description of ecological niche for the Hemiptera insects of the Fam. Belostomatidae across Africa. According to our model, this Hemiptera family shows a ubiquitous geographical distribution across Africa. It is widely distributed in western Africa, where appears to occupy not only coastal areas but also inland areas. Drier areas limiting with the Sahara desert from Cameroon, Nigeria, Central African Republic (CAR) and the nearly whole Namibia seems to be unsuitable environments for species of this family. Also according to the ensemble model, it would be present in all middle Africa.
As we observed in Naucoridae family, its distribution appears to be strongly mediated by temperature, showing preference for mean temperatures between 16°C and 23°C degrees and close to streams. Belostomatidae species seems to prefer human-transformed landscapes ("other" land cover category comprises urban and bare areas) followed by crops, what it can favour the contact with population. Figure S9. Environmental suitability for Fam. Notonectidae across Africa and prediction uncertainty (95% confidence interval). Insect image from Wikimedia Commons  Figure S11. Partial dependence plots of the relative contribution of covariates to the boosted regression tree (BRT) model for Fam. Notonectidae, averaged over 80 ensembles. Blue lines represent the mean partial dependence over all 80 BRT ensembles and grey envelopes the standard deviation from the mean. The y-axis is the transformed logit response and x-axis is the full range of covariates values. Figure S12. Partial dependence plots of the relative contribution of covariates to the random forest (RF) model for Fam. Notonectidae, averaged over 80 ensembles. Blue lines represent the mean partial dependence over all 80 RF ensembles and grey envelopes the standard deviation from the mean. The y-axis is the transformed logit response and x-axis is the full range of covariates values.

Notonectidae
Text S3. Description of ecological niche for the Hemiptera insects of the Fam. Notonectidae across Africa.
Notonectidae species seems to have a more restricted distribution in Africa, being more predominant in western and southern Africa but narrowly distributed in middle Africa. In eastern Africa (Ethiopia, Kenya, Tanzania and Madagascar), it seems to be present at high altitude areas, whereas it would be distributing along coastal areas of western and southern Africa (i.e. Angola).
The marginal effect plots show this Hemiptera family to be more resistant to higher LST, even though environment suitability sharply declines from 35°C. Surprisingly, optimal environmental mean temperature for these water bugs varies between 10°C and 20°C degrees, what likely is making its distribution more restricted comparing to Naucoridae and Notonectidae species. Environmental suitability for this family is also driven by moderate annual precipitation (350 -1,000 mm/annual) and they seem to inhabit all type of land covers with major preference for human-made landscapes (i.e. urban settings and agricultural lands). Figure S13. Environmental suitability for Fam. Nepidae across Africa and prediction uncertainty (95% confidence interval). Insect image from Wikimedia Commons Figure S14. Predicted occurrence for Fam. Nepidae across Africa and uncertainty. Optimal threshold was fitted to get better trade-off between sensitivity, specificity and proportion correctly classified (PCC). Insect image from Wikimedia Commons Figure S15. Partial dependence plots of the relative contribution of covariates to the boosted regression tree (BRT) model for Fam. Nepidae, averaged over 80 ensembles. Blue lines represent the mean partial dependence over all 80 BRT ensembles and grey envelopes the standard deviation from the mean. The y-axis is the transformed logit response and x-axis is the full range of covariates values. Figure S16. Partial dependence plots of the relative contribution of covariates to the random forest (RF) model for Fam. Nepidae, averaged over 80 ensembles. Blue lines represent the mean partial dependence over all 80 RF ensembles and grey envelopes the standard deviation from the mean. The y-axis is the transformed logit response and x-axis is the full range of covariates values.

Text S4. Description of ecological niche for the Hemiptera insects of the Fam. Nepidae across Africa.
Nepidae species distribution is restricted to coastal areas of western and eastern Africa, northern Africa and eastern areas of South Africa. Our model depicts a more restricted distribution in middle Africa throughout a double belt, which encircle the upper basin of Congo River. This Hemiptera family would be absent in arid and semi-arid zones. It is also predicted to be absent in the eastern coast of Madagascar.
According to partial effect plots for environmental covariates, their distribution seems to be strongly driven by precipitation, being more tolerant to wide range of mean temperature and tolerate high LST (suitability declines abruptly from 33°C degrees). They also show affinity for agricultural lands over other type of land covers.  Figure S20. Partial dependence plots of the relative contribution of covariates to the random forest (RF) model for Fam. Corixidae, averaged over 80 ensembles. Blue lines represent the mean partial dependence over all 80 RF ensembles and grey envelopes the standard deviation from the mean. The y-axis is the transformed logit response and x-axis is the full range of covariates values.

Corixidae
Text S5. Description of ecological niche for the Hemiptera insects of the Fam. Corixidae across Africa.
Our ecological model for Fam. Corixidae shows a wide distribution of this Hemiptera family across Africa, even in desert areas at some extent. Nevertheless, it is mostly predicted in wide areas of western and northern Africa, and eastern coast of South Africa. In eastern Africa, this aquatic Hemiptera will also find suitable environments to thrive in both coastal areas and inland. It seems to be nearly absent or scarce in vast areas of middle Africa (i.e. Cameroon, Equatorial Guinea and Democratic Republic of the Congo (DRC). Only coastal areas of Angola, Gabon and Congo offers suitable conditions for this Hemiptera family to prosper across south-west of Africa.
Corixidae species will more likely present in human transformed landscapes, agriculture landscapes according to random forest based models, and forest. The probability of occurrence declines with the distance to rivers and sharply from environment temperatures above 17°C degrees. It appears that species of this Hemiptera family do not tolerate well extreme temperatures, thriving in areas with moderate temperature throughout the year: around 10°C and 20°C at the coldest and warmest months respectively.