Main studies on the role of avian malaria parasites in the global spread of their bird hosts.
Abstract
Emerging infectious diseases (EIDs) impose a burden on economies and public health. Because EIDs on wildlife are mainly affected by environmental and ecological factors, the study of EIDs in wildlife provides valuable insights to improve our understanding on their causes and their impact on global health. Malaria is an EID that has increased its prevalence in the last few decades at an alarming rate. Avian malaria parasites are abundant, widespread and diverse, which turn these parasites into an excellent model for the study of EIDs. In the face of new health and environmental challenges in the twenty- irst century, studies on avian malaria will provide new approaches for this old disease. The identfiication of essential genes for the malaria invasion, the study of modification of host behaviour by malaria parasites in order to promote the parasite transmission, and the knowledge of factors contributing to the emergence of infectious diseases in wildlife are essential for understanding parasite epidemiology, local patterns of virulence and evolution of host resistance. In this chapter, we will review the results of some recent investigations on these topics that will be useful for predicting and preventing EIDs in wildlife, livestock and humans.
Keywords
- avian malaria
- emerging infectious diseases
- Haemoproteus
- haemosporidians
- Plasmodium
1. Introduction
Malaria is one of the world’s deadliest diseases, with 214 million cases and an estimated 1 million malaria deaths every year. Although the first human recording of malaria was in China in 2700 B.C., most probably this disease is older than humans. Fossil evidence shows that modern malaria was transmitted by mosquitoes at least 20 million years ago, and the recent analysis of the pre-historic origin of malaria has suggested that earlier forms of the disease, carried by biting midges, are at least 100 million years old and probably much older [1]. Hence, malaria not only infects humans. In fact, systematic parasitologists have erected more than 500 described species belonging to 15 genera within the order Haemosporidia (phylum Apicomplexa) that infect reptiles, birds and mammals, and use at least seven families of dipteran vectors for transmission [2, 3]. These parasites are widely distributed in every terrestrial habitat on all the warm continents. Within these parasites, avian malaria is the largest group of haemosporidians by the number of species. They are widespread, abundant and diverse, and are easily sampled without disrupting the host populations. Although the term ‘malaria parasites’ has been a controversial issue among parasitologists, ecologists and evolutionary researchers [4, 5], authors usually include genera
Investigations on avian malaria have contributed significantly to the knowledge on biology and ecology of malaria parasites of other vertebrates, including human malaria [6]. Since the discovery of the mosquito transmission of malaria in birds by Sir Ronald Ross, studies on malaria parasites of birds have saved millions of human lives. For example, essential advances in medical parasitology such as the development of anti-malarial compounds (e.g. plasmochin, primaquine and atebrin), the study of the life cycle and cultivation in vitro were initially developed using bird haemosporidian models.
Also, during the 2000s, research on bird malaria was at the very peak because scientists recognised the benefits of using studies on avian malaria to answer ecological, behavioural and evolutionary questions. Nowadays, far to be outdated, investigations on avian malaria will be essential to face new health and environmental challenges in the twenty-first century. In this chapter, we will review the newest contributions on bird studies helping in the fight against malaria.
2. Emerging infectious diseases and wildlife studies
In the last century, advances in vaccines and antibiotics, as well as other improvements in food intake and sanitation, contributed to the fast development in demography and economic growth in many parts of the world [7]. These advances brought the erroneous idea of a possible world without the burden of pathogens, followed by a flawed policy of reducing investment in the research of infectious diseases [8]. Pathogenic microorganisms rapidly evolve using multiple genetic evolutionary mechanisms, thus steadily adapting to new environments and escaping host’s defences. As a consequence, more than 300 events of emerging and re-emerging infectious diseases (EIDs) have killed millions of people since the 1940s and represent one of the major threats to human, livestock and wildlife in the twenty-first century [9]. These diseases are caused by pathogens from animals that now infect humans (HIV-1), or pathogens that have been probably presented in humans for centuries, but continue to appear in new locations (Lyme disease) or have evolved resistance to drugs (malaria resistance to chloroquine, mefloquine and artemisinin), or that reappear after apparent control or elimination (tuberculosis). Ironically, the health improvements and economic developments of the last century also contributed to the increase of these pathogenic diseases, as ‘hidden costs’ of this wellness. The economic and demographic growth led to millions of people live in crowded urban areas, thereby facilitating the spread of infections [10]. Also, the deforestation for logging and farming in tropical rainforests to meet the demands of growing population have provoked changes in the ecology and epidemiology of vector-borne diseases (e.g. malaria, leishmania and Chagas disease), thus favouring the spread of the disease [11].
Studies on wildlife may provide essential information in the fight against EIDs for several reasons. On the one hand, wildlife is an essential component in the epidemiology of many EIDs. In this sense, more than 60% of these diseases in humans are caused by pathogens spread from animals, and 71.8% of these zoonotic diseases events are provoked by pathogens with a wildlife origin [9]. On the other hand, socio-cultural and economic drivers (e.g. population density, economic growth), as well as ecological and environmental conditions (wildlife species richness, rainfall), may be major determinants of surge and spread of diseases in humans. In opposition to human studies on EIDs, wildlife studies are free of socio-economics and cultural confounding variables, thus providing reliable conclusions on the ecological drivers of the epidemiology.
2.1. Avian malaria and deforestation
Infections with vector-borne pathogens have become one of the main EIDs in the last years. Arthropods such as mosquitoes, ticks and bugs are responsible for transmission of viruses (dengue, chikungunya, Zika), bacteria (Lyme disease) and protozoans (malaria, Chagas). Anthropogenic deforestation and land use change have been proposed to cause the spread of vectors and the re-emergence of malaria in South America [12]. In this sense, it has been shown that the biting rate of
In recent years, several studies have analysed the effects of habitat fragmentation and deforestation on the prevalence of bird haemosporidian parasites in different continents. Bonneaud et al. [16] examined the prevalence of infection of bird malaria in both pristine and disturbed forests from Cameroon, showing a higher prevalence of
In Hawaiian Islands, malaria is thought to be responsible of the population decline and even extinctions of many native bird species [19]. In addition, deforestation could also have contributed to the population decimation by altering the patterns of malaria transmission [20, 21]. In this sense, it has been suggested that deforestation of the Alaka‘i Wilderness Preserve on Kaua‘i Island could have changed the pattern of seasonal transmission of avian malaria to a pattern of continuous transmission through all the year [20], which could enormously increase the prevalence and pathogenic effects of avian malaria.
Moreover, Laurance et al. [22] investigated the effects of habitat fragmentation and ecological parameters on the prevalence of malaria parasites (genera
In Brazil, Belo et al. [23] examined the presence and genetic diversity of haemosporidian parasites in 676 wild birds from three different environmental regions (intact cerrado, disturbed cerrado and transition area Amazonian rainforest-cerrado) with the aim to determine whether different habitats are associated with differences in the prevalence and diversity of malaria infection. Surprisingly, they found that neither the prevalence nor the diversity of infection of
2.2. Avian malaria parasites as emerging infectious diseases: the role in biological invasions
Alien, also called non-indigenous, exotic or non-native species, are defined as those species that colonise an area beyond their natural range, where they reproduce and establish a population. In addition to urbanisation, demographic growth and land-use change, the introduction of domestic and wildlife alien species can also provoke emerging diseases with tremendous costs in terms of loss of biodiversity, mortality and economic expenses [25]. In this sense, several studies have shown zoonosis linked to birds spreading diseases to humans. For example, it is thought that the West Nile virus, a bird pathogen but also causing mortality to humans, was introduced to New York by migratory or invasive bird species [26]. Also, the bird flu virus (H5N1), which has been registered, was transported by invasive bird species [27]. But despite these negative impacts of invasive species and the efforts from scientists to understand biological invasions, the mechanisms that allow one species to become invasive are still poorly understood.
Since the eighteenth century, more than 1400 human attempts to introduce 400 bird species have been recorded worldwide [28]. But not all of these introduced birds have resulted in established populations of invasive birds in the new regions. In fact, only 10% of introduced species are able to colonise new environments and become successful invaders [29]. In consequence, some life history traits and ecological attributes could allow some alien species to maintain high survival and reproductive success in new locations and to become successful invaders [28]. It has been proposed that parasites may play this role facilitating the successful colonisation of their bird hosts [30]. Hence, parasitic infections (or sometimes, their absence) may facilitate or limit invasions impacting native species via both direct and indirect effects. Three hypotheses (novel weapon hypothesis, enemy release hypothesis and biotic resistance hypothesis) have been proposed to explain the role of parasites in invasions in bird- parasite systems (Table 1). On the one hand, exotic bird species can act as a ‘Trojan horse’ because they can bring alien parasites and pathogens inside them, which could favour the dissemination in the new areas of their avian host species. In the history, pathogens have played a role bringing diseases in humans that become epidemic in susceptible native populations [39]. As example, in European conquest in the Americas smallpox spread rapidly killing an estimated 95% of the indigenous population far in advance of the European themselves [39]. Following this idea, the novel weapon hypotheses (NWH) states that invasive species gain advantages over native species by bringing their own parasites to the new environments against which the introduced species but not the natives have evolved defences [40, 41]. These co-introduced parasites may switch to native bird hosts and spread in the new communities, hence becoming themselves invasive parasites provoking serious damages to indigenous bird species. But the role of parasites in invasions may extend well beyond such direct effects, and hence some indirect effects may also be expected. In this sense, the enemy release hypothesis (ERH) states that non-native bird species could become invaders because they have lost their co-evolved malaria parasites during the process of colonisation, and thus they may increase their competitive ability and displace native species in the new areas. Conversely, the biotic resistance hypothesis states that native parasites in the indigenous species may reduce the fitness of the potential bird invader and prevent its spread and establishment. Next, we will focus on the role of avian malaria parasites co-introduced with their bird hosts.
Avian malaria parasites are among the most pathogenic species of poultry and wildlife birds, being responsible for economic losses, mass mortality, population declines and even extinctions of many bird species worldwide after its introduction outside its native range [42]. For all these reasons, the International Union for Conservation of Nature (IUCN) classifies avian malaria to be among the 100 of the world’s worst invasive alien species [43]. The spread of exotic avian malaria in Hawaiian Islands is the best documented example of the effects of invasive malaria on native bird communities. Since the discovery of Hawaiian Archipelago by the Captain Cook in 1774, more than a half of over 100 endemic bird taxa in Hawaii have been driven to extinction by a combination of habitat loss, introduced species and diseases [19, 44]. In 1826, the primary vector for avian malaria
|
|
|
---|---|---|
Hawaii | van Ripper et al. [21] | |
Hawaii | Atkinson et al. (2005) [46] | |
Hawaii | Lapointe (2005) [47] | |
Hawaii | Atkinson and Samuel (2010) [48] | |
New Zealand | Doré (1920) [49] | |
New Zealand | Tompkins and Gleeson [31] | |
New Zealand | Barraclough et al. [32] | |
New Zealand | Howe et al. [33] | |
New Zealand | Ewen et al. (2012) [50] | |
New Zealand | Schoener et al. (2014) [51] | |
Galapagos Islands | Levin et al. [34] | |
Galapagos Islands | Santiago-Alarcón et al. [35] | |
Galapagos Islands | Levin et al. [36] | |
Perú | Marzal et al. (2015) [52] | |
|
||
Southern Asia | Beadell et al. (2006) [53] | Mixed results with NWH |
Seychelles Islands | Hutchings (2009) [54] | |
Brazil | Lima et al. (2010) [55] | |
6 continents (58 locations) | Marzal et al. [37] | |
|
||
Lesser Antilles | Ricklefs et al. (2010) [56] |
Similar to Hawaii, recent investigations have detected avian malaria
Malaria parasites were historically considered to be absent in Galápagos Islands, because studies based on microscopic and molecular screening of parasites failed to detect malaria parasites in Galápagos birds [49, 50], most probably due to the absence of competent vectors. However, in the last decade, several studies have showed malaria-infected birds in several islands in the archipelago, thus suggesting recent arrival of avian malaria parasites. In this sense, the only known competent vector for
Marzal et al. [56] have recently showed the first report of this invasive pathogen in the mainland Americas. They analysed more than 100 blood samples from native bird species from South America, showing the presence of
Would it be possible to eliminate emerging infectious diseases? We do not think so. Indeed, it seems unlikely that most emerging infectious diseases will be eradicated in a close future [57]. In the fight against emerging infectious diseases, we have to follow the advice of the Red Queen to Lewis Carroll’s Alice in Wonderland: ‘…it takes all the running you can do, to keep in the same place. If you want to get somewhere else, you must run at least twice as fast as that!’ Therefore, this is a continuous process, where we have to keep on researching to avoid being out of step in the fight against malaria and other emerging infectious diseases. Studies on avian malaria research may play an essential role in these investigations to determine the key factors (e.g. deforestation and land-use change, biological invasions) contributing to the emergence of these diseases.
3. Identification of malaria genes
Approximately, 40% of the world population lives in areas where malaria is transmitted. In some areas, as sub-Saharan Africa, malaria may cause a rate of mortality in 5-year-old children around 90% [58]. An important tool in the fight against malaria parasites is the identification and sequencing of malaria genes that could give essential information about this harmful disease. Hence, in 1996, an international effort was launched to sequence the
Moreover, these chromosomes possess a high number of genes related to immune evasion and host-parasite interactions and fewer enzymes and transporters. In the short term, however, it has been suggested that the genome sequence alone provides little information about malaria parasites. As Gardner et al. [59] claim ‘much remains to be done’. These results might need to be accompanied by new methods of control, including new drugs and vaccines, improved diagnostics and effective vector control techniques. In this section, we will deal with some malaria genes that are essential for identification of malaria transmission areas and to develop strategies to avoid spread of the disease.
Also, we will show some recent studies on the identification of malaria genes that are crucial in the parasite life cycle, and could be used as a target for future vaccines or anti-malaria drugs.
3.1. Identification of merozoite surface protein gene 1 (MSP1) and malaria transmission areas
Malaria parasites have an important effect in populations where it is present affecting the survival of the community and la
In 2013, Hellgren et al. [67] identified this gene in
By barcoding the msp1 gene in SGS1 and GRW4, a recent study has determined whether haemosporidian transmission in house martins occurs at European sites by sampling juvenile birds house martins (a migratory species with a high fidelity to its area of hatching and nesting) [30].
Moreover, they analysed the msp1 alleles in both adult and juvenile house martins in order to identify their potential areas of transmission. Surprisingly, their results showed that some juvenile and adult house martins were infected by Pr2 allele of
3.2. New target to avoid completion of malaria life cycle: the chitinase gene (CHT1)
Malaria parasites (including human malaria) show a complex life cycle that requires mechanisms adapted to enable the parasite invasion into the different tissues from the vertebrate host to the arthropod vector. Apparently, arthropods develop a protective peritrophic membrane (PM) against pathogens around their midgut after each blood meal. This PM blocks the penetration of blood parasites and avoids the spreading of the parasite to other organs. In turn, malaria parasites have developed a mechanism to overcome the PM barrier. Once the malaria parasite has complete its sexual stage in the mosquito stomach, the ookinete has the ability to cross the PM by secreting a chitinase that has catalytic and substrate-binding sites breaking down this layer. After crossing the PM, ookinetes finally transform into oocytes, which after maturing releases the sporozoites that move to the salivary glands where they are ready for infecting a new host [69]. Therefore, the role of the chitinase gene is essential in the life cycle of malaria parasites.
The chitinase gene has been study for years due to the variability of structures that it shows. In mammals, some
4. Malaria parasites and escape behaviour
Behavioural traits are an important factor in the life cycle of all live organisms. Behaviour may determine whether an individual ends up as a survivor or as a prey [74] or it can even acts as a defence against some parasites. For example, some organisms modified their behaviour by plastically changing their life history in order to evade parasite or to minimise the impact of infection [75]. A good example of behaviour as a defence mechanism to avoid is displayed in
Anti-predator behaviour is a specific kind of behaviour that is consistent in the presence of a predator across time and contexts [78] and imposes an important selection pressure on preys [79]. Thus, when a predator stalks a prey, the first mean of avoidance of predation is escaping from the predator. However, when the prey is already captured by the predator, the behaviour displayed by the prey can be much more specific: the escape behaviour. Among others, escape behaviour includes several behavioural traits such as (i) the intensity with which a captured individual wriggles to escape, (ii) biting or attacking the predator,(iii) whether it loses feathers, limbs, or a tail and thereby manages to escape, (iv) fear screaming and (v) akin behaviour to feigning death [80]. These variables are closely related to the probabilities that one individual has to escape; thus, the more intense this escape behaviour in one individual is, the more probabilities would have this individual to escape from the predator. For example, a prey individual may emit a loud fear scream that can either warn co-specifics or to attract secondary predators, thus facilitating the escape [81]. Additionally, in 2011, Møller et al. [82] showed that birds with high levels of predation wriggled more when captured by a human, hence increasing their probabilities to escape from the predator, showing that intense escape behaviour is related with high levels of predation.
In addition to predation, parasite represents another major cause of mortality in birds. Some studies demonstrated that the presence of parasites and predators may provoke stress to animals and reduce the immune function in one individual suggesting a relationship between malaria parasites and predation [83]. Later, Møller and Nielsen [81] showed that individuals infected with blood parasites showed lower intense of escape behaviour. Both studies reveal an underlying mechanism that links predation to prevalence of blood parasites. Recently, this underlying mechanism has been analysing. In this sense, Garcia-Longoria et al. [84] tested whether species with higher prevalence of
Regarding to this latter hypothesis, the behavioural manipulation hypothesis posits that manipulation of host behaviour by parasites may confer fitness benefits to the parasite, usually increasing transmission success to the parasite [85]. There are some studies supporting this hypothesis. One of the most well-known examples is the manipulation displayed by
5. Conclusions
Malaria parasites and other emerging infectious diseases are one of the major challenges for global health in the twenty-first century. Despite the efforts made by scientist and health care providers, malaria parasites are becoming drug-resistant, as well as they are boosting their mortality rate in some regions and increasing their areas of transmission. These risings can be provoked by some anthropogenic alterations as deforestation or biological invasions, thus provoking changes in the ecology and epidemiology of vector-borne diseases and outbreaks in human, livestock and wildlife emerging infectious diseases. Moreover, in human malaria studies, it is very difficult to assess if the changes in parasite prevalence are due to socio-ecological factors or to the effects of environmental alterations. These facts emphasise the importance of the study of malaria parasites in wild animals, free from social and economic factors, to fight against this pathogen. Here, we have also focused our attention in the identification of new avian malaria genes that could help in the detection of malaria transmission areas around the world. In addition, the identification of malaria genes with high genetic variability will supply essential information in the evolution of both human and avian malaria pathogens and would provide scientists with new tools for the development of anti-malaria drugs. Our current knowledge about malaria and EIDs is still limited. Further investigation and exploration are needed in order to gain a better understanding of the malaria distribution and the global economic and health impact of malaria. Moreover, it is important to increase awareness of the consequences of introducing non-native species in different habitats and to increase the control in biosecurity borders for avoiding the introduction of alien pathogens such as malaria parasites. Finally, we should be fully aware that there is no ending in the fight against EIDs, where ‘it will take all the running (
Acknowledgments
This study was funded by research projects of the Spanish Ministry of Economy and Competitiveness (CGL2015-64650P) and Junta de Extremadura (GRU15117). Sergio Magallanes was supported by a PhD grant from Ministry of Economy and Competition of Spain.
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