Avian malaria, haematocrit, and body condition in invasive wetland passerines settled in southwestern Spain

Jaime Muriel, Luz García-Longoria, Sergio Magallanes, Juan Antonio Ortiz, Alfonso Marzal. 2023: Avian malaria, haematocrit, and body condition in invasive wetland passerines settled in southwestern Spain. Avian Research, 14(1): 100081. DOI: 10.1016/j.avrs.2023.100081

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Avian malaria, haematocrit, and body condition in invasive wetland passerines settled in southwestern Spain

a.
Instituto de Investigación en Recursos Cinegéticos (IREC), CSIC-UCLM-JCCM, Ronda de Toledo 12, 13005, Ciudad Real, Spain
b.
Universidad de Extremadura, Facultad de Biología, Departamento de Anatomía, Biología Celular y Zoología, Avenida de Elvas s/n, 06006, Badajoz, Spain
c.
Estación Biológica de Doñana (EBD-CSIC), Departamento de Ecología de los Humedales, Avda. Américo Vespucio 26, 41092, Sevilla, Spain
d.
Hirundo Bird Ringing Group, Badajoz, Spain
e.
Grupo de Investigaciones en Fauna Silvestre. Universidad Nacional de San Martín, Jr. Maynas 1777, 22021, Tarapoto, Peru

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Corresponding author:
E-mail address: amarzal@unex.es (A. Marzal)
¹ These authors contributed equally to this work.
Received Date: 28 Aug 2022
Rev Recd Date: 28 Dec 2022
Accepted Date: 31 Jan 2023
Available Online: 14 Apr 2023
Publish Date: 07 Feb 2023

Graphical Abstract

Abstract

Abstract

Avian malaria and related haemosporidian parasites can negatively impact fitness in many songbirds. Research on the malaria infection and its physiological costs on their avian hosts is heavily skewed toward native passerines, with exotic species underrepresented. However, introduced species may carry on and spread new pathogens to native species, and play a role on parasite transmission cycle in invaded bird communities as pathogen reservoir. Here, we molecularly assess the prevalence and diversity of haemosporidian parasites in three introduced wetland passerines (the Red Avadavat Amandava amandava, the Yellow-crowned Bishop Euplectes afer, and the Common Waxbill Estrilda astrild) captured during the same season in southwestern Spain. We also explored the relation between parasite infection, body condition, haematocrit, and uropygial gland volume. We detected an overall parasite prevalence of 3.55%, where Common Waxbills showed higher prevalence (6.94%) than Red Avadavats (1.51%). None Yellow-crowned Bishops were infected with haemosporidians. Almost 60% of infections were caused by Leucocytozoon, and about 40% by Plasmodium. We identified four unique lineages of Plasmodium and three of Leucocytozoon. Moreover, 91% of the identified host–parasite interactions represented new host records for these haemosporidian parasites. Parasite infection was not related to body condition, haematocrit, and uropygial gland volume of the wetland passerines. Haematocrit values varied seasonally among bird species. Additionally, haematocrit was positively related to body condition in the Yellow-crowned Bishops, but not in the other species. Red Avadavats had higher haematocrit levels than Yellow-crowned Bishops, whereas Common Waxbills showed the lower haematocrit values. The uropygial gland volume was positively correlated with body condition in all bird species. Common Waxbills showed higher uropygial gland volumes related to their body size than birds from other two species. These outcomes highlight the importance of exotic invasive species in the transmission dynamics of haemosporidian parasites.
- Avian malaria,
- Exotic species,
- Introduced birds,
- Leucocytozoon,
- Plasmodium,
- Uropygial gland

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1. Introduction

Avian interspecific brood parasitism, the laying of eggs in the nest of other species to evade subsequent parental care duties, represents an important threat to host breeding success (Davies, 2000). Brood parasites can reduce the reproductive output of the host in several ways. The nestlings of the Common Cuckoo (Cuculus canorus) and other 'evicting' brood parasites cause complete host reproductive failure as their young usually eliminate all host progeny by evicting or directly killing them (Honza et al., 2007; Spottiswoode and Koorevaar, 2012). Parasitic females also destroy nests unsuitable for parasitism to force hosts to renest, thereby increasing the chances of future parasitism (Zahavi, 1979; Soler et al., 2017). In addition to these direct reproductive costs, brood parasitism can lead to other indirect costs for the host. Prolonged care for the parasitic chick and increased number of replacement nests, for example, may reduce host survival and future reproduction (Koleček et al., 2015). Thus, brood parasitism can, in some cases, be even more costly for host individual fitness than nest predation (Rothstein, 1990; Payne, 2005).

Given that the productivity, the rate at which animals produce their offspring, is a key demographic measure of population growth, reduced productivity due to brood parasitism may also have important population level consequences for host species. These effects on host populations vary depending on the parasite species and the host. Generalist brood parasites, like the cowbirds, may dramatically reduce the growth rates of heavily parasitized host populations and lead to their significant declines (Smith et al., 2002; Kosciuch and Sandercock, 2008), whereas host-specific brood parasites, such as cuckoos, are supposed to have only little population level effects on host species as they occur at low densities, i.e., being much less abundant than their hosts (Payne, 1977; May and Robinson, 1985). However, when the parasitism rate by the Common Cuckoo is extraordinarily high for a long time (64%–66%; Moskát and Honza, 2002), such a host population is usually maintained by immigrants from other, less parasitized or unparasitized populations (Barabás et al., 2004; Krüger, 2007). So, the question is how does brood parasitism affect local, more or less isolated populations of hosts with varying intensity of defence against parasitism? However, while most studies of the Common Cuckoo parasitism have to date focused primarily on specific host anti-parasite behaviours and parasite counter-adaptations, i.e., coevolutionary arms-race between parasites and hosts, the extent to which the Common Cuckoo threatens individual host populations is poorly understood.

The objective of this study was to determine the effect of Common Cuckoo parasitism on the annual productivity, i.e., number of fledglings produced per female within a nesting season, of a regularly parasitized host population. To assess this issue, a local population of one of the major cuckoo hosts in Europe, the Great Reed Warbler (Acrocephalus arundinaceus) (Leisler and Schulze-Hagen, 2011), was monitored for 15 years (2008–2022) in south-western Slovakia, and the factors that might play a role in the annual reproductive success of this host population were evaluated. Specifically, I tested for an effect of year, population size (number of breeding females), laying date, the length of the breeding season, clutch size, polygyny rate, nest failure, successful parasitism rates (i.e., when cuckoo chick successfully evicted host eggs or chicks), local spring temperature and spring total precipitation. I predicted lower annual productivity of the study population in years with higher rates of successful parasitism. Since nest predation is one of the most important factors influencing reproductive success in birds (Ricklefs, 1969; Martin, 1993), I also expected reduced annual productivity with increased nest failure rates due to nest predation and other causes such as nest destruction and nest abandonment.

2. Materials and methods

2.1 Study site and study species

The study was carried out in a fishpond system near Štúrovo, southwestern Slovakia (47°51′ N, 18°36′ E, 114–116 m a.s.l.) with a total area of 45 ha. The ponds were surrounded by narrow belts of reed beds (maximum width 2–10 m) and scattered willows used by female cuckoos as vantage points for watching potential hosts and locating their nests. Due to intensive pond management, the littoral vegetation was maintained at the similar extent throughout the study period. The most frequent predators of reed passerine nests in the study area were the Little Bittern (Ixobrychus minutus) and the Marsh Harrier (Circus aeruginosus).

The Great Reed Warbler is a medium size (31 g) open-nesting passerine breeding throughout mainland Europe and the West Palearctic (Cramp, 1992). Birds arrive on their breeding grounds in mid-April – early-May and start laying eggs in May, continuing until late July. In central Europe, the Great Reed Warblers breed usually once per year, two broods in one season are very scarce (Trnka and Samaš, 2024), and on average lay clutches of five eggs. Only the female builds the nest and incubates the clutch, however, both the female and male feed and defend the young (Požgayová et al., 2009; Trnka and Grim, 2013). The Great Reed Warbler has a polygynous mating system, with polygynous males providing significantly less parental care to their offspring than monogamous males (Sejberg et al., 2000; Požgayová et al., 2015). The rates of social polygyny range between 8% and 56% (Catchpole et al., 1985; Hasselquist, 1998; Leisler and Wink, 2000). The nests of the Great Reed Warbler suffer relatively high rates of predation and Common Cuckoo parasitism. Rates of parasitism (the percentage of nests in which cuckoo eggs were laid) in European Great Reed Warbler populations range from 0 to 68 % (Moskát et al., 2008; Trnka et al., 2012). There is also known intraspecific nest predation in this species, where lower-ranking females destroy eggs of higher-ranking females to gain increased paternal investment (Trnka et al., 2010).

In the study area, the Great Reed Warbler is the predominant reed-nesting passerine species. Its population comprised 18–56 breeding females during the study period. For specific breeding parameters of the studied population, see Trnka and Samaš (2024).

2.2 Data collection

The fieldwork was conducted in 2008–2022. All birds in the study population were individually marked with one aluminium ring and a unique combination of two or three coloured plastic rings (adults). Great Reed Warbler nests were searched systematically at 4–5 day intervals between May and late July and then checked at 1–2 day intervals where possible to determine the day of clutch completion, the final clutch size and to detect the presence of a cuckoo egg (see also Trnka et al., 2012). As almost all nests were found during nest building or egg-laying, the onset of laying was assessed directly, and only in some cases it was recalculated according to the date of hatching. The brood size and number of fledglings were recorded when the young were 10–12 days old. The social mating status of each male and female was determined based on their captures at or near the nests or on direct observations of colour-ringed birds defending their nests or feeding their young. The rate of polygyny was calculated as the percentage of males mated with two or more females, i.e., number of polygynous males divided by the total number of males in the population. The length of the breeding period was defined as the time between the first egg laid and the last young fledged or last nest failure (see also Trnka and Samaš, 2024). The annual rates of successful cuckoo parasitism were calculated as the number of nests in which cuckoo chick successfully hatched and evicted host eggs or chicks/total number of nests where cuckoo eggs were laid. Analogically, the nest failure rate was calculated as the proportion of nests that failed due to predation, abandonment, destruction (e.g., by wind), flooding, etc. A nest was considered predated if eggs or nestlings disappeared or only eggshells were found in the nest cup. Because of the uncertainty in determining the causes of egg losses in some clutches (see Discussion for details), cases of partial clutch predation were not included in the analyses. Abandoned nests were nests with incomplete or complete clutches with cold eggs that were seen without attending breeders after two consecutive inspections. In the case of nests destroyed by wind or larger animals (e.g., swans, herons, wild boars), the reeds with the nest as well as neighbouring reeds were bent or broken, and the nest itself was often squeezed, leaving at least some nest contents (eggs or dead young) in or under the nest. Flooded nests were nests covered by surface water after heavy rainfall and increased water level in ponds. Annual productivity was calculated as the mean number of fledglings produced per breeding female throughout the breeding season. The meteorological data were obtained from the national climate station (the city Hurbanovo) located 28 km west of the study site.

2.3 Statistical analysis

All statistical analyses were conducted in R v. 4.3.2 (R Core Team, 2023). We used a general linear model with normal distribution and identity link to test the effects of breeding and environmental variables on annual productivity. Continuous predictors included year, total number of breeding females as a proxy of population size, median of first egg laid in breeding season (1 = 1st May), length of breeding season (in days), average clutch size, annual nest failure rate, annual successful parasitism rate, average temperature (℃) from April to June, and total precipitation (mm) from April to June. We standardized all predictors to have a mean of 0 and a standard deviation of 1 because the covariates were on different scales. This also improved the interpretability of the intercept and model overall, ensuring that the coefficients reflect the standardized effect of each predictor.

We presented the outputs of the full and final models. The final model was the one with the lowest AIC_c and was selected using function dredge in the package MuMIn v. 1.47.5 (Bartoń, 2023). Potential collinearity among the covariates was low, and variance inflation factors were < 2 in all cases (Zuur et al., 2010). We performed model residual diagnostics with R package RVAideMemoire v. 0.9-83-7 (Herve, 2023) and did not detect any violation of model assumptions.

3. Results

A total of 495 breeding pairs (females) of Great Reed Warblers successfully reared 1321 of their own young and 63 young of the Common Cuckoo in the study population over the course of 15 years. Annual productivity of birds ranged from 1.7 to 4.3 (Fig. 1) and was primarily and negatively affected by the successful Common Cuckoo parasitism (Table 1, Fig. 2A). A 21% increase in parasitism rate reduced annual productivity by approximately one host chick. Likewise, annual productivity was negatively affected by nest failure rate, where a 23% increase in nest failure rate resulted in a reduction in annual productivity for one host chick (Table 1, Fig. 2B). A less pronounced but significant effect was also found for the number of breeding females, where a reduction in annual productivity of approximately one chick was associated with an increase in population size of 40 breeding females. Other environmental and breeding parameters had no effect on the annual productivity of Great Reed Warbler females in the study population. Similarly, successfully parasitized nests with a young cuckoo were predated to approximately the same extent as non-parasitized nests with host nestlings regardless of their age (19.1% vs. 21%, respectively, χ² = 0.65, df = 1, p = 0.29).

Figure 1. Annual productivity (number of fledglings per female per year) over the 2008–2022 period. Numbers at the top of the bars indicate population size (total number of breeding females).

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Table 1. Output of full and final general linear models with normal distribution testing effect of breeding and environmental variables on the annual productivity in the Great Reed Warbler. Final model was selected according to the lowest AIC_c.

Model	Parameter	Estimate ± S.E.	t value	P value
Full	Intercept	2.89±0.05	54.35	< 0.001
	Year	−0.04±0.08	−0.55	0.61
	First egg laid	−0.09±0.19	−0.48	0.65
	Number of breeding females	−0.19±0.08	−2.43	0.07
	Clutch size	−0.09±0.18	−0.51	0.64
	Season length	−0.10±0.09	−1.05	0.36
	Polygyny rate	0.00±0.12	0.02	0.99
	Nest failure rate	−0.27±0.06	−4.32	0.01
	Parasitism rate	−0.50±0.08	−6.54	0.003
	Temperature	0.02±0.07	0.33	0.76
	Rainfall	0.04±0.08	0.53	0.62
Final	Intercept	2.89±0.05	59.78	< 0.001
	Number of breeding females	−0.20±0.05	−3.89	0.003
	Nest failure rate	−0.29±0.05	−5.72	< 0.001
	Parasitism rate	−0.55±0.05	−10.57	< 0.001

| Show Table

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Figure 2. Effect of (A) parasitism rate, (B) nest failure rate and (C) total number of breeding females on the annual productivity in the Great Reed Warbler.

DownLoad: Full-Size Img PowerPoint

4. Discussion

Contrary to the general assumption that host-specific brood parasites have only little impact on the productivity of their hosts at the population level because of the small proportion of parasitized nests (Payne, 1977; May and Robinson, 1985), the results of this study showed, for the first time to my knowledge, a significant negative effect of Common Cuckoo parasitism on the annual productivity of a local Great Reed Warbler population. More importantly, successful nest parasitism contributed to a reduction in Great Reed Warbler annual productivity at about the same rate as overall nest failure caused by predation, nest destruction, or nest abandonment. This is not so surprising given that the annual rate of successful parasitism of the Common Cuckoo was as high as 18%–44% in some years in the population studied (this study), and female Great Reed Warblers rarely reared their own chicks after the successful fledging of a Common Cuckoo chick from their first nest in the same season (Trnka and Samaš, 2024).

In addition, lower annual productivity may also be caused by partial or complete predation of host eggs by the Common Cuckoo. According to "mafia" scenario (Zahavi, 1979), these cuckoo predators may probably be females which did not parasitize particular nests (Jelínek et al., 2016). Moreover, Common Cuckoo females usually remove one or two host eggs at laying which they subsequently eat (Davies, 2000) and some or all of host eggs may even be thrown or destroyed by the hosts during the ejection of a cuckoo egg. Such cases of cuckoo predation and host egg losses also contribute to reduced annual host productivity caused directly or indirectly by cuckoo parasitism, thereby strengthening obtained findings. However, without direct observation it is difficult to determine the true reason of the loss of host eggs. In the study population, Great Reed Warblers rejected the parasitic egg in 53.9%–65.7%, most frequently by ejection (42.9%), and less by desertion (22.8%) (Trnka et al., 2012, 2023), and the rate of nest predation on the Great Reed Warbler nests by predators other than the Common Cuckoo averaged about 20% (Trnka and Prokop, 2010). Thus, nest parasitism and nest predation are interconnected and may skew the true impact of nest parasitism on the annual productivity of a host population. Therefore, additional studies focusing specifically on the impact of predation by the Common Cuckoo on the annual productivity of a host population will be very valuable.

However, the fact that brood parasites can limit or regulate population size in hosts has been clearly demonstrated for hosts of the cowbirds (Molothrus spp.) in North America. There have even been implemented cowbird removal programs as an effective management strategy to restore host populations (Clotfelter and Yasukawa, 1999; Kostecke et al., 2005; Ladin et al., 2016).

Nevertheless, despite a relatively high rate of successful parasitism and its negative impact on the annual productivity of the local Great Reed Warbler population, the studied population has been successfully surviving for more than three decades (own data). One reason for this may be the immigration of individuals from another neighbouring populations (see also Barabás et al., 2004). This is partly supported by the relatively high proportion of new unringed individuals in the study population, as evident from the low annual return rate of breeding females, which ranged from only 23%–29.3% (Trnka and Samaš, 2024), and by several recoveries of Great Reed Warbler adults from adjacent breeding sites (unpublished data). These findings suggest that local population dynamics of hosts may be influenced by spatial variation in patch quality where brood parasites may create differences in reproductive success among host populations. According to this model of source-sink dynamics individuals from populations of high-quality habitat, i.e., the source, maintain populations of low-quality habitat, the sink (Yang et al., 2014).

Another possible explanation is that annual productivity of fledglings in the Great Reed Warbler is a subject of density-dependent selection for lower reproductive output at high abundance (Travis et al., 2023), which is also indicated by the results obtained. Such a negative relationship between the increased number of breeding females and annual productivity has been found in several other bird species (Sæther et al., 2021; Monnier-Corbel et al., 2022).

In summary, brood parasitism by the Common Cuckoo significantly reduced the annual productivity of the local Great Reed Warbler population, which was likely maintained by immigrants from other populations and density-dependent selection. Thus, the level of population isolation and the interactions of density-dependent factors such as nest parasitism and nest predation can affect the demography of host populations of the Common Cuckoo. However, further long-term studies assessing the consequences of Common Cuckoo parasitism on host population dynamics are needed to clarify this issue.

Ethics statement

The study was carried out in accordance with Slovak law. Licences and permits for handling and ringing of birds were issued by the Ministry of Environment of the Slovak Republic.

CRediT authorship contribution statement

Alfréd Trnka: Writing – review & editing, Writing – original draft, Validation, Methodology, Investigation, Formal analysis, Data curation, Conceptualization.

Declaration of competing interest

The author declare that he has no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

I thank to all the people who helped me in the field. Peter Samaš did the statistical analyses and read an earlier version of the manuscript. I am also grateful to two anonymous reviewers for valuable comments on the manuscript.

References (114)

References

Abellán, P., Carrete, M., Anadón, J.D., Cardador, L., Tella, J.L., 2016. Non-random patterns and temporal trends (1912-2012) in the transport, introduction and establishment of exotic birds in Spain and Portugal. Divers. Distrib. 22, 263-273. .

Baquero, R.A., Barbosa, A.M., Ayllón, D., Guerra, C., Sánchez, E., Araújo, M.B., et al., 2021. Potential distributions of invasive vertebrates in the Iberian Peninsula under projected changes in climate extreme events. Divers. Distrib. 27, 2262-2276. .

Bates, D., Maechler, M., Bolker, B., Walker, S., Bojesen Christensen, R.H., Singmann, H., et al., 2015. Package "lme4": Linear Mixed-Effects Models using "Eigen" and S4. J. Stat. Software 67, 1-48.

Bensch, S., Pérez-Tris, J., Waldenström, J., Hellgren, O., 2004. Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution 58, 1617-1621. doi: .

Bensch, S., Hellgren, O., Pérez-Tris, J., 2009. MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol. Ecol. Resour. 9, 1353-1358.

Blackburn, T.M., Ewen, J.G., 2017. Parasites as drivers and passengers of human-mediated biological invasions. Ecohealth 14, 61-73. .

Blackburn, T.M., Lockwood, J.L., Cassey, P., 2009. Avian Invasions: The Ecology and Evolution of Exotic Birds. Oxford University Press, Oxford.

Booth, C.E., Elliott, P.F., 2002. Hematological responses to hematozoa in North American and neotropical songbirds. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 133, 451-467.

Campbell, T. W., Ellis, C. K., 2007. Avian & Exotic Animal Hematology and Cytology. Blackwell, Ames, Iowa.

Cardoso, G.C., Reino, L., 2018. Ecologically benign invasions: the invasion and adaptation of Common Waxbills (Estrilda astrild) in Iberia. In: Queiroz, A., Pooley, S. (Eds.), Histories of Bioinvasions in the Mediterranean. Environmental History, vol. 8. Springer, Cham, pp. 149-169. .

Carrete, M., Tella, J.L., 2008. Wild-bird trade and exotic invasions: a new link of conservation concern? Front. Ecol. Environ. 6, 207-211. https://www.jstor.org/stable/20440873.

Chinchio, E., Crotta, M., Romeo, C., Drewe, J.A., Guitian, J., Ferrari, N., 2020. Invasive alien species and disease risk: an open challenge in public and animal health. PLoS Pathog. 16, e1008922. .

Christe, P., Møller, A.P., González, G., de Lope, F., 2002. Intraseasonal variation in immune defence, body mass and hematocrit in adult house martins Delichon urbica. J. Avian Biol. 33, 321-325. .

Cornet, S., Bichet, C., Larcombe, S., Faivre, B., Sorci, G., 2014. Impact of host nutritional status on infection dynamics and parasite virulence in a bird-malaria system. J. Anim. Ecol. 83, 256-265. .

Crowl, T.A., Crist, T.O., Parmenter, R.R., Belovsky, G., Lugo, A.E., 2008. The spread of invasive species and infectious disease as drivers of ecosystem change. Front. Ecol. Environ. 6, 238-246. .

Damas-Moreira, I., Riley, J.L., Carretero, M.A., Harris, D.J., Whiting, M.J., 2020. Getting ahead: exploitative competition by an invasive lizard. Behav. Ecol. Sociobiol. 74, 117. .

Dawson, R.D., Bortolotti, G.R., 2000. Effects of hematozoan parasites on condition and return rates of American Kestrels. Auk 117, 373-380.

Delhaye, J., Glaizot, O., Christe, P., 2018. The effect of dietary antioxidant supplementation in a vertebrate host on the infection dynamics and transmission of avian malaria to the vector. Parasitol. Res. 117, 2043-2052.

Dimitrov, D., Marinov, M.P., Bobeva, A., Ilieva, M., Bedev, K., Atanasov, T., et al., 2019. Haemosporidian parasites and leukocyte profiles of pre-migratory rosy starlings (Pastor roseus) brought into captivity. Anim. Migr. 6, 41-48. .

Emiroğlu, Ö., Atalay, M.A., Ekmekçi, F.G., Aksu, S., Başkurt, S., Keskin, E., et al., 2020. One of the world's worst invasive species, Clarias batrachus (Actinopterygii: Siluriformes: Clariidae), has arrived and established a population in Turkey. Acta Ichthyol. Piscat. 50, 391-400.

Essl, F., Nehring, S., Klingenstein, F., Milasowszky, N., Nowack, C., Rabitsch, W., 2011. Review of risk assessment systems of IAS in Europe and introducing the German-Austrian Black List Information System (GABLIS). J. Nat. Conserv. 19, 339-350.

Fair, J., Whitaker, S., Pearson, B., 2007. Sources of variation in haematocrit in birds. Ibis 149, 535-552. .

Falaschi, M., Melotto, A., Manenti, R., Ficetola, G.F., 2020. Invasive species and amphibian conservation. Herpetologica 76, 216-227. .

Fallis, A.M., Smith, S.M., 1964. Ether extracts from birds and CO₂ as attractants for some ornithophilic simuliids. Can. J. Zool. 42, 723-730. .

Galván, I., Sanz, J.J., 2006. Feather mite abundance increases with uropygial gland size and plumage yellowness in Great Tits Parus major. Ibis 148, 687-697.

García-Longoria, L., Marzal, A., de Lope, F., Garamszegi, L., 2019. Host-parasite interaction explains variation in the prevalence of avian haemosporidians at the community level. PLoS One 14, e0205624.

González, G., Sorci, G., Møller, A.P., Ninni, P., Haussy, C., de Lope, F., 1999. Immunocompetence and condition-dependent sexual advertisement in male house sparrows (Passer domesticus). J. Anim. Ecol. 68, 1225-1234.

Granthon, C., Williams, D.A., 2017. Avian malaria, body condition, and blood parameters in four species of songbirds. Wilson J. Ornithol. 129, 492-508.

Hahn, S., Bauer, S., Dimitrov, D., Emmenegger, T., Ivanova, K., Zehtindjiev, P., et al., 2018. Low intensity blood parasite infections do not reduce the aerobic performance of migratory birds. Proc. R. Soc. B-Biol. Sci. 285, 20172307. .

Hall, T.A., 1999. BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/ NT. Nucleic Acids Symp. Ser. 41, 95-98. .

Health, W., Who, O., 2021. WHO Guidelines for Malaria. World Health Organization, Geneva. .

Hellgren, O., Waldenström, J., Bensch, S., 2004. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J. Parasitol. 90, 797-802. .

Hõrak, P., Jenni-Eiermann, S., Ots, I., Tegelmann, L., 1998. Health and reproduction: the sex-specific clinical profile of great tits (Parus major) in relation to breeding. Can. J. Zool. 76, 2235-2244.

Ilgūnas, M., Bukauskaitė, D., Palinauskas, V., Iezhova, T.A., Dinhopl, N., Nedorost, N., et al., 2016. Mortality and pathology in birds due to Plasmodium (Giovannolaia) homocircumflexum infection, with emphasis on the exoerythrocytic development of avian malaria parasites. Malar. J. 15, 256. .

Ishtiaq, F., Barve, S., 2018. Do avian blood parasites influence hypoxia physiology in a high elevation environment? BMC Ecol. 18, 15. .

Ishtiaq, F., Gering, E., Rappole, J.H., Rahmani, A.R., Jhala, Y.V., Dove, C.J., et al., 2007. Prevalence and diversity of avian hematozoan parasites in Asia: a regional survey. J. Wildl. Dis. 43, 382-398. .

James, J., Mrugała, A., Oidtmann, B., Petrusek, A., Cable, J., 2017. Apparent interspecific transmission of Aphanomyces astaci from invasive signal to virile crayfish in a sympatric wild population. J. Invertebr. Pathol. 145, 68-71.

Jarić, I., Cvijanović, G., 2012. The tens rule in invasion biology: measure of a true impact or our lack of knowledge and understanding? Environ. Manage. 50, 979-981.

Jeschke, J.M., 2014. General hypotheses in invasion ecology. Divers. Distrib. 29, 1229-1234. .

Jovani, R., Tella, J.L., 2006. Parasite prevalence and sample size: misconceptions and solutions. Trends Parasitol. 22, 214-218. .

Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., et al., 2012. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647-1649. .

Kettunen, M., Genovesi, P., Gollasch, S., Pagad, S., Starfinger, U., ten Brink, P., et al., 2008. Technical Support to EU Strategy on Invasive Species (IAS) – Assessment of the Impacts of IAS in Europe and the EU (Final Module Report for the European Commission). Institute for European Environmental Policy (IEEP), Brussels. .

Krams, I., Cirule, D., Krama, T., Hukkanen, M., Rytkönen, S., Grell, M., et al., 2010. Effects of forest management on haematological parameters, blood parasites, and reproductive success of the Siberian tit (Poecile cinctus) in northern Finland. Ann. Zool. Fennici 47, 335-346. .

Krams, I., Suraka, V., Rantala, M.J., Sepp, T., Mierauskas, P., Vrublevska, J., et al., 2013. Acute infection of avian malaria impairs concentration of haemoglobin and survival in juvenile altricial birds. J. Zool. 291, 34-41.

Lima, M.R., Simpson, L., Fecchio, A., Kyaw, C.M., 2010. Low prevalence of haemosporidian parasites in the introduced house sparrow (Passer domesticus) in Brazil. Acta Parasitol. 55, 297-303. .

Lipa, J.J., 2013. The Impacts of Invasive Alien Species in Europe. European Environmental Agency Technical, Copenhagen. Report No. 16/2012.

Lopes, R.J., Correia, J., Batalha, H., Cardoso, G.C., 2018. Haemosporidian parasites missed the boat during the introduction of common waxbills (Estrilda astrild) in Iberia. Parasitology 145, 1493-1498. .

Lowe, S., Browne, M., Boudjelas, S., de Poorter, M., 2000. 100 of the World's Worst Invasive Alien Species: A Selection from the Global Invasive Species Database. The Invasive Species Specialist Group (ISSG) - a Specialist Group of the Species Survival Commission. SSC of the World Conservation Union (IUCN), New Zealand.

Lutz, H.L., Hochachka, W.M., Engel, J.I., Bell, J.A., Tkach, V.V., Bates, J.M., et al., 2015. Parasite prevalence corresponds to host life history in a diverse assemblage of Afrotropical birds and haemosporidian parasites. PLoS One 10, e0128851.

MacLeod, C.J., Paterson, A.M., Tompkins, D.M., Duncan, R.P., 2010. Parasites lost - do invaders miss the boat or drown on arrival? Ecol. Lett. 13, 516-527. .

Magallanes, S., Møller, A.P., García-Longoria, L., de Lope, F., Marzal, A., 2016. Volume and antimicrobial activity of secretions of the uropygial gland are correlated with malaria infection in house sparrows. Parasites Vectors 9, 232. .

Magallanes, S., Møller, A.P., Luján-Vega, C., Fong, E., Vecco, D., Flores-Saavedra, W., et al., 2021. Exploring the adjustment to parasite pressure hypothesis: differences in uropygial gland volume and haemosporidian infection in palearctic and neotropical birds. Curr. Zool. 67, 147-156. .

Magory Cohen, T., Hauber, M.E., Akriotis, T., Crochet, P., Karris, G., Kirschel, A.N.G., et al., 2022. Accelerated avian invasion into the Mediterranean region endangers biodiversity and mandates international collaboration. J. Appl. Ecol. 59, 1440-1455. .

Maguire, I., Jelić, M., Klobučar, G., Delpy, M., Delaunay, C., Grandjean, F., 2016. Prevalence of the pathogen Aphanomyces astaci in freshwater crayfish populations in Croatia. Dis. Aquat. Organ. 118, 45-53. .

Martínez-de La Puente, J., Merino, S., Tomás, G., Moreno, J., Morales, J., Lobato, E., et al., 2010. The blood parasite Haemoproteus reduces survival in a wild bird: a medication experiment. Biol. Lett. 6, 663-665. .

Marzal, A., García-Longoria, L., 2020. The role of malaria parasites in invasion biology. In: Santiago-Alarcon, D., Marzal, A. (Eds.), Avian Malaria and Related Parasites in the Tropics. Springer, Cham, pp. 487-512. .

Marzal, A., Ricklefs, R.E., Valkiūnas, G., Albayrak, T., Arriero, E., Bonneaud, C., et al., 2011. Diversity, loss, and gain of malaria parasites in a globally invasive bird. PLoS ONE 6, e21905.

Marzal, A., Balbontín, J., Reviriego, M., García-Longoria, L., Relinque, C., Hermosell, I.G., et al., 2016. A longitudinal study of age-related changes in Haemoproteus infection in a passerine bird. Oikos 125, 1092-1099. doi: .

Marzal, A., Møller, A.P., Espinoza, K., Morales, S., Luján-Vega, C., Cardenas-Callirgos, J.M., et al., 2018. Variation in malaria infection and immune defence in invasive and endemic house sparrows. Anim. Conserv. 21, 505-514.

Marzal, A., Ferraguti, M., Muriel, J., Magallanes, S., Ortiz, J.A., García-Longoria, L., et al., 2022. Circulation of zoonotic flaviviruses in wild passerine birds in western Spain. Vet. Microbiol. 268, 109399.

Matias, R., 2002. Aves Exoticas Que Nidificam Em Portugal Continental, first ed. ICN, Lisbon.

Matias, R., Catry, P., Costa, H., Elias, G., Jara, J., Moore, C.C., et al., 2007. Systematic list of the birds of Mainland Portugal. An. Ornitol. 5, 74-132.

Mazza, G., Tricarico, E., Genovesi, P., Gherardi, F., 2014. Biological invaders are threats to human health: an overview. Ethol. Ecol. Evol. 26, 112-129. .

McClure, K.M., Fleischer, R.C., Kilpatrick, A.M., 2020. The role of native and introduced birds in transmission of avian malaria in Hawaii. Ecology 101, e03038. .

Molina, B., Nebreda, A., Muñoz, A.R., Seoane, J., Real, R., Bustamante, J., et al., 2022. III Atlas de aves en época de reproducción en España. SEO/BirdLife. .

Møller, A.P., Arriero, E., Lobato, E., Merino, S., 2009. A meta-analysis of parasite virulence in nestling birds. Biol. Rev. 84, 567-588. .

Moreno-Rueda, G., 2015. Body-mass-dependent trade-off between immune response and uropygial gland size in house sparrows Passer domesticus. J. Avian Biol. 46, 40-45. .

Moreno-Rueda, G., 2017. Preen oil and bird fitness: a critical review of the evidence. Biol. Rev. 92, 2131-2143. doi: .

Morinha, F., Carrete, M., Tella, J.L., Blanco, G., 2020. High prevalence of novel beak and feather disease virus in sympatric invasive parakeets introduced to Spain from Asia and South America. Diversity 12, 192. .

Muriel, J., 2020. Ecophysiological assessment of blood haemosporidian infections in birds. Ecosistemas 29, 1979. .

Muriel, J., Marzal, A., Magallanes, S., García-Longoria, L., Suarez-Rubio, M., Bates, P.J.J., et al., 2021. Prevalence and diversity of avian haemosporidians may vary with anthropogenic disturbance in tropical habitats in Myanmar. Diversity 13, 111. .

Navarro, C., Marzal, A., de Lope, F., Møller, A.P., 2003. Dynamics of an immune response in house sparrows Passer domesticus in relation to time of day, body condition and blood parasite infection. Oikos 101, 291-298. doi: .

Neto, J.M., Mellinger, S., Halupka, L., Marzal, A., Zehtindjiev, P., Westerdahl, H., 2020. Seasonal dynamics of haemosporidian (Apicomplexa, Haemosporida) parasites in house sparrows Passer domesticus at four European sites: comparison between lineages and the importance of screening methods. Int. J. Parasitol. 50, 523-532. .

Norte, A.C., Ramos, J.A., Sampaio, H.L., Sousa, J.P., Sheldon, B.C., 2010. Physiological condition and breeding performance of the Great Tit. Condor 112, 79-86. .

Nylund, V., Westman, K., 2000. The prevalence of crayfish plague (Aphanomyces astaci) in two signal crayfish (Pacifastacus leniusculus) populations in Finland. J. Crustacean Biol. 20, 777-785. .

Palinauskas, V., Valkiūnas, G., Bolshakov, C.V., Bensch, S., 2011. Plasmodium relictum (lineage SGS1) and Plasmodium ashfordi (lineage GRW2): the effects of the co-infection on experimentally infected passerine birds. Exp. Parasitol. 127, 527-533. .

Pap, P.L., Vágási, C.I., Osváth, G., Mureşan, C., Barta, Z., 2010. Seasonality in the uropygial gland size and feather mite abundance in house sparrows Passer domesticus: natural covariation and an experiment. J. Avian Biol. 41, 653-661. .

Pap, P.L., Vágási, C.I., Bǎrbos, L.A., Marton, A., 2013. Chronic coccidian infestation compromises flight feather quality in house sparrows Passer domesticus. Biol. J. Linn. Soc. 108, 414-428. .

Peel, M.C., Finlayson, B.L., Mcmahon, T.A., 2007. Updated world map of the Köppen-Geiger climate classification. Hydrol. Earth Syst. Sci. Discuss. 4, 439-473. .

R Core Team, 2019. R: a language and environment for statistical computing. R Foundation Stat. .

Ricklefs, R.E., Swanson, B.L., Fallon, S.M., Martínez-Abrain, A., Scheuerlein, A., Gray, J., et al., 2005. Community relationships of avian malaria parasites in southern Missouri. Ecol. Monogr. 75, 543-559.

van Riper III, C., van Riper, S.G., Goff, M.L., Laird, M., 1986. The epizootiology and ecological significance of malaria in Hawaiian landbirds. Ecol. Monogr. 56, 327-344. .

de Roode, J.C., Helinski, M.E.H., Anwar, M.A., Read, A.F., 2005a. Dynamics of multiple infection and within-host competition in genetically diverse malaria infections. Am. Nat. 166, 531-542.

de Roode, J.C., Pansini, R., Cheesman, S.J., Helinski, M.E.H., Huijben, S., Wargo, A.R., et al., 2005b. Virulence and competitive ability in genetically diverse malaria infections. P. Natl. Acad. Sci. USA 102, 7624-7628.

Roy, H.E., Rabitsch, W., Scalera, R., Stewart, A., Gallardo, B., Genovesi, P., et al., 2018. Developing a framework of minimum standards for the risk assessment of alien species. J. Appl. Ecol. 55, 526-538. .

Russell, C.B., Hunter, F.F., 2005. Attraction of Culex pipiens/restuans (Diptera: Culicidae) mosquitoes to bird uropygial gland odors at two elevations in the Niagara Region of Ontario. J. Med. Entomol. 42, 301-305. .

Sánchez-Guzmán, J.M., Villegas, A., Corbacho, C., Morán, R., Marzal, A., Real, R., 2004. Response of the haematocrit to body condition changes in Northern Bald Ibis Geronticus eremita. Comp. Biochem. Phys. A 139, 41-47.

Sandland, G.J., Minchella, D.J., 2004. Life-history plasticity in hosts (Lymnaea elodes) exposed to differing resources and parasitism. Can. J. Zool. 82, 1672-1677. .

Santiago-Alarcon, D., Marzal, A., 2020. Research on avian haemosporidian parasites in the tropics before the year 2000. In: Santiago-Alarcon, D., Marzal, A. (Eds.), Avian Malaria and Related Parasites in the Tropics. Springer, Cham, pp. 1-44. .

Santiago-Alarcon, D., Mettler, R., Segelbacher, G., Schaefer, H.M., 2013. Haemosporidian parasitism in the blackcap Sylvia atricapilla in relation to spring arrival and body condition. J. Avian Biol. 44, 521-530. doi: .

Santiago-Alarcon, D., MacGregor-Fors, I., Kühnert, K., Segelbacher, G., Schaefer, H.M., 2016. Avian haemosporidian parasites in an urban forest and their relationship to bird size and abundance. Urban Ecosyst. 19, 331-346.

Scheuerlein, A., Ricklefs, R.E., 2004. Prevalence of blood parasites in European passeriform birds. Proc. R. Soc. B Biol. Sci. 271, 1363-1370. .

Schoener, E.R., Tompkins, D.M., Parker, K.A., Howe, L., Castro, I., 2020. Presence and diversity of mixed avian Plasmodium spp. infections in introduced birds whose distribution overlapped with threatened New Zealand endemic birds. New Zeal. Vet. J. 68, 101-106. .

Schulte-Hostedde, A.I., Zinner, B., Millar, J.S., Hickling, G.J., 2005. Restitution of mass - size residuals: validating body condition indices. Ecology 86, 155-163.

Schultz, A., Underhill, L.G., Earlé, R.A., Underhill, G., 2010. Infection prevalence and absence of positive correlation between avian haemosporidian parasites, mass and body condition in the Cape Weaver Ploceus capensis. Ostrich 81, 69-76. .

Scrimshaw, N.S., Taylor, C.E., Gordon, J.E., 1959. Interactions of nutrition and infection. Am. J. Med. Sci. 237, 367-403. .

Silva, T., Reino, L.M., Borralho, R., 2002. A model for range expansion of an introduced species: the common waxbill Estrilda astrild in Portugal. Divers. Distrib. 8, 319-326. .

Sodhi, N.S., 2010. Birds. In: Simberloff, D., Rejmanek, M. (Eds.), Encyclopedia of Biological Invasions. University of California Press, Berkeley, pp. 70-74.

Souviron-Priego, L., Muñoz, A.R., Olivero, J., Vargas, J.M., Fa, J.E., 2018. The legal international wildlife trade favours invasive species establishment: the monk and ring-necked parakeets in Spain. Ardeola 65, 233-246. .

Srebaliene, G., Olenin, S., Minchin, D., Narscius, A., 2019. A comparison of impact and risk assessment methods based on the IMO Guidelines and EU invasive alien species risk assessment frameworks. PeerJ 7, e6965.

Sullivan, M.J.P., Franco, A.M.A., 2018. Changes in habitat associations during range expansion: disentangling the effects of climate and residence time. Biol. Invasions 20, 1147-1159. .

Sullivan, M.J.P., Davies, R.G., Mossman, H.L., Franco, A.M.A., 2015. An anthropogenic habitat facilitates the establishment of non-native birds by providing underexploited resources. PLoS ONE 10, e0135833. .

Torchin, M.E., Lafferty, K.D., Dobson, A.P., McKenzie, V.J., Kuris, A.M., 2003. Introduced species and their missing parasites. Nature 421, 628-630. .

Tsiamis, K., Gervasini, E., D'Amico, F., Deriu, I., Katsanevakis, S., Crocetta, F., et al., 2016. The EASIN Editorial Board: quality assurance, exchange and sharing of alien species information in Europe. Manag. Biol. Invas. 7, 321-328. .

UNEP, 2020. Preventing the Next Pandemic: Zoonotic diseases and how to break the chain of transmission. United Nations Environment Programme and International Livestock Research Institute, Nairobi.

Valkiūnas, G., 2004. Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton. .

Valkiūnas, G., Atkinson, C.T., 2020. Introduction to life cycles, taxonomy, distribution, and basic research techniques. In: Santiago-Alarcon, D., Marzal, A. (Eds.), Avian Malaria and Related Parasites in the Tropics. Springer Nature, Cham, pp. 45-80. .

Valkiūnas, G., Iezhova, T.A., 2018. Keys to the avian malaria parasites. Malar. J. 17, 212. .

Valkiūnas, G., Zickus, T., Shapoval, A.P., Iezhova, T.A., 2006. Effect of Haemoproteus belopolskyi (Haemosporida: Haemoproteidae) on body mass of the Blackcap Sylvia atricapilla. J. Parasitol. 92, 1123-1125. .

Venables, W.N., Ripley, B.D., 2002. Modern applied statistics with S-PLUS. 4th ed. Springer, New York.

Ventim, R., Mendes, L., Ramos, J.A., Cardoso, H., Pérez-Tris, J., 2012. Local haemoparasites in introduced wetland passerines. J. Ornithol. 153, 1253-1259. .

White, N.J., 2018. Anaemia and malaria. Malar. J. 17, 371.

Williamson, M., Fitter, A., 1996. The varying success of invaders. Ecology 77, 1661-1666. .

Wu, M., Xiao, Y., Yang, F., Zhou, L., Zheng, W., Liu, J., 2014. Seasonal variation in body mass and energy budget in Chinese Bulbuls (Pycnonotus sinensis). Avian Res. 5, 4. .

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Avian malaria, haematocrit, and body condition in invasive wetland passerines settled in southwestern Spain