Invasive Parasites, Habitat Change and Heavy Rainfall Reduce Breeding Success in Darwin's Finches

Habitat Change and Heavy Rainfall Reduce Breeding Success in Darwin's Finches. PLoS ONE 9(9): e107518. doi:10.1371/journal.pone.0107518 Invasive Parasites, Habitat Change and Heavy Rainfall Reduce Breeding Success in Darwin's Finches Arno Cimadom 0 Angel Ulloa 0 Patrick Meidl 0 Markus Zo ttl 0 Elisabet Zo ttl 0 Birgit Fessl 0 Erwin Nemeth 0 Michael Dvorak 0 Francesca Cunninghame 0 Sabine Tebbich 0 Csaba Moskat, Hungarian Academy of Sciences, Hungary 0 1 Department of Behavioural Biology, University of Vienna , Vienna, Austria, 2 Charles Darwin Foundation, Puerto Ayora, Santa Cruz Island, Gala pagos, Ecuador , 3 Institute for Science and Technology , Klosterneuburg , Austria , 4 Department of Zoology, University of Cambridge , Cambridge , United Kingdom , 5 BirdLife Austria, Vienna , Austria Invasive alien parasites and pathogens are a growing threat to biodiversity worldwide, which can contribute to the extinction of endemic species. On the Gala pagos Islands, the invasive parasitic fly Philornis downsi poses a major threat to the endemic avifauna. Here, we investigated the influence of this parasite on the breeding success of two Darwin's finch species, the warbler finch (Certhidea olivacea) and the sympatric small tree finch (Camarhynchus parvulus), on Santa Cruz Island in 2010 and 2012. While the population of the small tree finch appeared to be stable, the warbler finch has experienced a dramatic decline in population size on Santa Cruz Island since 1997. We aimed to identify whether warbler finches are particularly vulnerable during different stages of the breeding cycle. Contrary to our prediction, breeding success was lower in the small tree finch than in the warbler finch. In both species P. downsi had a strong negative impact on breeding success and our data suggest that heavy rain events also lowered the fledging success. On the one hand parents might be less efficient in compensating their chicks' energy loss due to parasitism as they might be less efficient in foraging on days of heavy rain. On the other hand, intense rainfalls might lead to increased humidity and more rapid cooling of the nests. In the case of the warbler finch we found that the control of invasive plant species with herbicides had a significant additive negative impact on the breeding success. It is very likely that the availability of insects (i.e. food abundance)is lower in such controlled areas, as herbicide usage led to the removal of the entire understory. Predation seems to be a minor factor in brood loss. - Funding: The study was funded by the University of Vienna (Focus of Excellence grant), the Galapagos Conservation Trust, and the Ethologische Gesellschaft e.V. During the study Sabine Tebbich was funded by the FWF (project number V95-B17) and Arno Cimadom by a scholarship from the University of Vienna. The publication was supported by the publication fund of the University of Vienna. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Invasive alien pathogens and parasites are a major and growing threat to biodiversity worldwide. Small host populations of endemic species are particularly vulnerable because extinction can occur before the hosts have a chance to evolve effective defences [1,2]. This is especially true if the parasite is a generalist because it can switch to another host if it has driven one close to extinction [3]. The adverse effect of introduced parasites has been documented in a range of avian species (reviewed in [2]). A famous example is the extinction of most of the endemic Hawaiian honeycreepers because of the introduction of avian malaria and its vector [4]. The avifauna of almost all islands of the Pacific Ocean has been dramatically altered by introduced species or other human impact [5]. In this respect the Galapagos archipelago is one of the exceptions, as no bird species has become extinct in modern times. This archipelago hosts the endemic Darwins finches which have provided the inspiration for some of the most important ideas in evolutionary biology. However, the introduction of predators, pathogens, and parasites have led to increasing pressures affecting several Darwins finch species [610]. One of the biggest threats to the Galapagos avifauna is the obligate bird parasite Philornis downsi [11], which was first discovered on the archipelago in 1997 [12]. Adult flies lay their eggs in bird nests where the parasitic larvae then hatch and suck blood from the nestlings [13]. Correlative as well as experimental studies have shown that P. downsi has a negative impact on nestling growth, haemoglobin levels, and fledgling success [1418]. The influence of parasitism on breeding success in Darwins finches is highly variable from year to year, and mortality ranges from 16 to 95% in all finch nests (reviewed in [18,19]). The reasons for this high variation are poorly understood so far but could stem from differences in precipitation between years [20], but also see [21]. The Galapagos archipelago is characterised by a highly seasonal climate with pronounced wet and dry seasons, as well as extraordinary yearly variation in rainfall [22]. Years with intense rainfalls (El Ni no years) and severe drought years reoccur at irregular intervals. However, within the wet season there is also variation in precipitation, which has received little attention so far. Rainfall can reach 50 ml and more on some days, whereas on other days no precipitation is measured. An interaction between rainfall and P. downsi prevalence and intensity has been found in Philornis sp. which affect various bird species in Puerto Rico [23] and Argentina [24]. The highest prevalence and intensity (larvae per nest or chick; [25]) of P. downsi infestation on the Galapagos Islands was found on Santa Cruz Island [26]. On this island, several insectivorous passerines declined between 1997 and 2010 [27]. The greatest decline was observed in the warbler finch (Certhidea olivacea). This insectivorous species is an arboreal finch and is the smallest of the Darwins finches. It is restricted to the highlands, which were previously covered by the endemic humid Scalesia forest. During the last century this forest has to a large extent been transformed into agricultural areas. The warbler finch population has shrunk by 50% in the Scalesia forest and by up to 75% in the agricultural areas [27]. The closely related grey warbler finch (Certhidea fuscua) has already gone extinct on Floreana Island as there are no records of this species since more than sixty years [28]. Other than parasitism, the loss of primary habitat could be a possible reason for the population decline of the warbler finch. By 2009, the Scalesia forest, which holds the highest density of warbler finches [27], was reduced to only 2% of its original area [29]. Additionally, intr (...truncated)