Modelling habitat suitability in Jordan for the cutaneous leishmaniasis vector (Phlebotomus papatasi) using multicriteria decision analysis.

Cutaneous leishmaniasis (CL) is a zoonotic vector-borne neglected tropical disease transmitted by female Phlebotomine sand flies. It is distributed globally but a large proportion of cases (70-75%) are found in just ten countries. CL is endemic in Jordan yet there is a lack of robust entomological data and true reporting status is unknown. This study aimed to map habitat suitability of the main CL vector, Phlebotomus papatasi, in Jordan as a proxy for CL risk distribution to (i) identify areas potentially at risk of CL and (ii) estimate the human population at risk of CL. A literature review identified potential environmental determinants for P. papatasi occurrence including temperature, humidity, precipitation, vegetation, wind speed, presence of human households and presence of the fat sand rat. Each predictor variable was (a) mapped; (b) standardized to a common size, resolution and scale using fuzzy membership functions; (c) assigned a weight using the analytical hierarchy process (AHP); and (d) included within a multicriteria decision analysis (MCDA) model to produce monthly maps illustrating the predicted habitat suitability (between 0 and 1) for P. papatasi in Jordan. Suitability increased over the summer months and was generally highest in the north-western regions of the country and along the Jordan Valley, areas which largely coincided with highly populated parts of the country, including areas where Syrian refugee camps are located. Habitat suitability in Jordan for the main CL vector-P. papatasi-was heterogeneous over both space and time. Suitable areas for P. papatasi coincided with highly populated areas of Jordan which suggests that the targeted implementation of control and surveillance strategies in defined areas such as those with very high CL vector suitability (>0.9 suitability) would focus only on 3.42% of the country's total geographic area, whilst still including a substantial proportion of the population at risk: estimates range from 72% (European Commission's Global Human Settlement population grid) to 89% (Gridded Population of the World) depending on the human population density data used. Therefore, high impact public health interventions could be achieved within a reduced spatial target, thus maximizing the efficient use of resources.

Indirect effects of parasitism: costs of infection to other individuals can be greater than direct costs borne by the host.

Parasitic infection has a direct physiological cost to hosts but may also alter how hosts interact with other individuals in their environment. Such indirect effects may alter both host fitness and the fitness of other individuals in the host's social network, yet the relative impact of direct and indirect effects of infection are rarely quantified. During reproduction, a host's social environment includes family members who may be in conflict over resource allocation. In such situations, infection may alter how resources are allocated, thereby redistributing the costs of parasitism between individuals. Here, we experimentally reduce parasite burdens of parent and/or nestling European shags (Phalacrocorax aristotelis) infected with Contracaecum nematodes in a factorial design, then simultaneously measure the impact of an individual's infection on all family members. We found no direct effect of infection on parent or offspring traits but indirect effects were detected in all group members, with both immediate effects (mass change and survival) and longer-term effects (timing of parents' subsequent breeding). Our results show that parasite infection can have a major impact on individuals other than the host, suggesting that the effect of parasites on population processes may be greater than previously thought.

Parasitism in early life: environmental conditions shape within-brood variation in responses to infection.

Parasites play key ecological and evolutionary roles through the costs they impose on their host. In wild populations, the effect of parasitism is likely to vary considerably with environmental conditions, which may affect the availability of resources to hosts for defense. However, the interaction between parasitism and prevailing conditions is rarely quantified. In addition to environmental variation acting on hosts, individuals are likely to vary in their response to parasitism, and the combined effect of both may increase heterogeneity in host responses. Offspring hierarchies, established by parents in response to uncertain rearing conditions, may be an important source of variation between individuals. Here, we use experimental antiparasite treatment across 5 years of variable conditions to test how annual population productivity (a proxy for environmental conditions) and parasitism interact to affect growth and survival of different brood members in juvenile European shags (Phalacrocorax aristotelis). In control broods, last-hatched chicks had more plastic growth rates, growing faster in more productive years. Older siblings grew at a similar rate in all years. Treatment removed the effect of environment on last-hatched chicks, such that all siblings in treated broods grew at a similar rate across environmental conditions. There were no differences in nematode burden between years or siblings, suggesting that variation in responses arose from intrinsic differences between chicks. Whole-brood growth rate was not affected by treatment, indicating that within-brood differences were driven by a change in resource allocation between siblings rather than a change in overall parental provisioning. We show that gastrointestinal parasites can be a key component of offspring's developmental environment. Our results also demonstrate the value of considering prevailing conditions for our understanding of parasite effects on host life-history traits. Establishing how environmental conditions shape responses to parasitism is important as environmental variability is predicted to increase.

Impacts of parasites in early life: contrasting effects on juvenile growth for different family members.

Parasitism experienced early in ontogeny can have a major impact on host growth, development and future fitness, but whether siblings are affected equally by parasitism is poorly understood. In birds, hatching asynchrony induced by hormonal or behavioural mechanisms largely under parental control might predispose young to respond to infection in different ways. Here we show that parasites can have different consequences for offspring depending on their position in the family hierarchy. We experimentally treated European Shag (Phalacrocorax aristoteli) nestlings with the broad-spectrum anti-parasite drug ivermectin and compared their growth rates with nestlings from control broods. Average growth rates measured over the period of linear growth (10 days to 30 days of age) and survival did not differ for nestlings from treated and control broods. However, when considering individuals within broods, parasite treatment reversed the patterns of growth for individual family members: last-hatched nestlings grew significantly slower than their siblings in control nests but grew faster in treated nests. This was at the expense of their earlier-hatched brood-mates, who showed an overall growth rate reduction relative to last-hatched nestlings in treated nests. These results highlight the importance of exploring individual variation in the costs of infection and suggest that parasites could be a key factor modulating within-family dynamics, sibling competition and developmental trajectories from an early age.