Avian malaria transmission dynamics in New Zealand: investigating host and vector relationships along an elevational gradient

Abstract

Avian malaria (Plasmodium spp.) may be of concern to the New Zealand avifauna, considered to be the most extinction-prone in the world. Although avian malaria has impacted both captive populations and wild individuals in New Zealand, whether or not it is a cause of concern for native bird populations in the wild is unknown. This research provides insight into the general ecology and epidemiology of avian malaria, highlighting patterns of infection risk as well as offering recommendations to improve detection via molecular techniques. Factors potentially influencing transmission dynamics in New Zealand were explored, such as elevation, vector abundance, and native or non-native status.

A survey was conducted in Nelson Lakes National Park (NLNP) to assess the prevalence of avian malaria infection across a broad elevational range (650 – 1400 m), at a site experiencing native bird declines in which malaria has been suggested as playing a role. Results from blood samples collected and analysed over three seasons (n = 436) support the potential for an inverse relationship between force of infection and elevation. This research was the first investigation of avian malaria presence across an elevational gradient in New Zealand. Results also show an overall higher prevalence of malaria in non-native (14.1%) versus native birds (1.7%) living in a shared space, suggesting the possibility of a differential impact on host species that show dissimilar reservoir competence. These findings provide evidence that native New Zealand avifauna may impacted by avian malaria at a population scale, and a differential impact on host species is occurring due to specific Plasmodium lineages. If this is indeed occurring, it would carry with it a whole new complexity to the conservation of native wildlife in New Zealand.

Mosquitoes were also sampled to help characterise the surrounding vector community at the field site at NLNP. Sampling results of the native Culex pervigilans (n = 81) were also used to create a model to estimate and make preliminary predictions of mosquito abundance based on actual and projected temperatures. The model shows that temperature influences on mosquito population dynamics in New Zealand likely drives annual, seasonal and elevational differences in mean densities and maximums. The model was used to estimate mosquito abundance at the time and place of known bird mortality events, allowing for speculation into the possible role of vector-borne diseases at each of these independent events. In some cases patterns are observed that support the hypothesis that a mosquito-borne disease played a role in the mortality events, but not in other cases.

Molecular diagnostic techniques, such as PCR, have played an important role in the advancement and understanding of avian malaria ecology. However problems arise when parasites in the blood cannot be amplified, resulting in false negatives. In an attempt to improve the accuracy of diagnostics by PCR, I evaluated the performance of a commercial DNA extraction kit by modifying the protocol with four elution volume alternatives. The results suggest that the best template is the DNA extract obtained from the second eluate of a first 50 µL elution step. In one case, the only band visible was from this second eluate, and thus may not have been identified as positive for Plasmodium spp. if a different elution protocol had been followed. A low ratio of parasite to host DNA is a major concern in detecting chronic infections in which birds typically carry low levels of parasitemia. Results from this study show that the modification of the elution step of a silica-membrane-based extraction protocol can be an effective approach to decreasing the occurrence of false negatives.

A comparative analysis, using a data set compiled from the literature, was also performed to identify large-scale predictors of malaria parasite prevalence in avian populations based on geographic and host characteristics from the Australasia-Pacific region. Results indicate that a negative correlation exists between avian malaria prevalence and elevation, latitude, and length of incubation. Results also show that a positive correlation exists between avian malaria prevalence and body size. Differences in patterns of infection were also seen across locations, with an interesting inverse trend seen for prevalence in non-native and native hosts between New Zealand and Hawaii, leading to questions related to resistance to infection in different regions.

Overall, this thesis presents evidence that avian malaria is potentially involved in native bird population declines in New Zealand, with non-native birds acting as reservoirs. Further information into native bird susceptibility to infection are needed to definitively confirm these findings, which could be obtained through experimental infection studies. Supporting evidence for such disease impacts will enable appropriate management to be developed and put in place, while a lack of evidence will enable resources to remain focused on the other issues facing New Zealand’s native species.