Timing of infestation influences virulence and parasite success in a dynamic multi-host-parasite interaction between the invasive parasite, Philornis downsi, and Darwin's finches.

Recently commenced host-parasite interactions provide an excellent opportunity to study co-evolutionary processes. Multi-host systems are especially informative because variation in virulence between hosts and temporal changes provides insight into evolutionary dynamics. However, empirical data under natural conditions are scarce. In the present study, we investigated the interaction between Darwin's finches and the invasive fly Philornis downsi whose larvae feed on the blood of nestlings. Recently, however, the fly has changed its behavior and now also attacks incubating females. Two sympatric hosts are affected differently by the parasite and parasite load has changed over time. Our study observed a reversal of trends described two decades ago: while, currently, small tree finches (Camarhynchus parvulus) experience significantly higher parasite load than warbler finches (Certhidea olivacea), this was the opposite two decades ago. Currently, fledging success is higher in warbler finches compared to small tree finches. Our data indicate that not only intensity but also timing of infestation influences hosts' reproductive success and parasite fitness. During incubation, prevalence was higher in warbler finches, but once chicks had hatched, prevalence was 100% in both species and parasite load was higher in small tree finches. Furthermore, our results suggest faster development and higher reproductive success of P. downsi in small tree finch nests. A change in host preference driven by larvae competition could have led to the reversal in parasite load.

Identification and Optimization of Microbial Attractants for Philornis downsi, an Invasive Fly Parasitic on Galapagos Birds.

We investigated the role of olfactory cues from actively fermenting yeast (Saccharomyces cerevisiae) in attraction of adult Philornis downsi and identified two synergistically attractive yeast volatiles. Larvae of this invasive fly parasitize the hatchlings of passerines and threaten the Galapagos avifauna. Gas chromatography coupled with electroantennographic detection (GC-EAD), coupled gas chromatography-mass spectrometry (GC-MS), and field trapping experiments were used to identify volatile compounds from a yeast-sugar solution. EAD responses were consistently elicited by 14 yeast volatiles. In a series of field trapping experiments, a mixture of the 14 EAD-active compounds was similarly attractive to P. downsi when compared to the yeast-sugar solution, and we found that acetic acid and ethanol were essential for attraction. A mixture of 0.03 % acetic acid and 3 % ethanol was as attractive as the 14-component blend, but was not as attractive as the yeast-sugar solution. Philornis downsi showed positive and negative dose-responses to acetic acid in the ranges of 0.01 ~ 0.3 % and 0.3 ~ 9 %, respectively. Further optimization showed that the mixture of 1 % acetic acid and 3 % ethanol was as attractive as the yeast-sugar solution. Both mixtures of acetic acid and ethanol were more selective than the yeast-sugar solution in terms of non-target moths and Polistes versicolor wasps captured. These results indicate that acetic acid and ethanol produced by yeasts are crucial for P. downsi attraction to fermented materials on which they feed as adults and can be used to manage this invasive fly in Galapagos.

Persistence associated with extractive foraging explains variation in innovation in Darwin's finches.

The capacity to create new behaviors is influenced by environmental factors such as foraging ecology, which can lead to phylogenetic variation in innovativeness. Alternatively, these differences may arise due to the selection of the underlying mechanisms, collaterally affecting innovativeness. To understand the evolutionary pathways that might enhance innovativeness, we examined the role of diet breadth and degree of extractive foraging, as well as a range of intervening cognitive and behavioral mechanisms (neophilia, neophobia, flexibility, motivation, and persistence). Darwin's finches are very suitable to this purpose: the clade is composed of closely related species that vary in their feeding habits and capacity to develop food innovations. Using a multi-access box, we conducted an interspecies comparison on innovative problem-solving between two diet specialists, extractive foragers (woodpecker and cactus finch), and two diet generalists, non-extractive foragers (small and medium ground finch). We predicted that if extractive foraging was associated with high innovativeness, variation would be best explained by species differences in persistence and motivation, whereas if diet generalism was the main driver, then variation would be due to differences in flexibility and responses to novelty. We found a faster capacity to innovate and a higher persistence for extractive foragers, suggesting that persistence might be adaptive to extractive foraging and only secondarily to innovation. Our findings also show that diet generalism and some variables linking it to innovation were unrelated to innovativeness and call for the development of joint experimental approaches that capture the diversity of factors giving rise to novel behaviors.

Habitat restoration to conserve the Little Vermilion Flycatcher on Santa Cruz Island, Galapagos.

The endemic Little Vermilion Flycatcher (LVF), Pyrocephalus nanus, has suffered a drastic decline on Santa Cruz Island, where it was common 30 years ago. Currently, less than 40 individuals remain in the last remnants of natural humid forest in the Galapagos National Park on this island. This small population has low reproductive success, which is contributing to its decline in Santa Cruz. Previous studies have identified Avian Vampire Fly, Philornis downsi, parasitism, changes in food sources, and habitat alteration as threats to this species. In Santa Cruz, invasive plants may strongly affect the reproductive success of the LVF because they limit accessibility to prey near the ground, the preferred foraging niche of these birds. Since 2019, we restored the vegetation in seven plots of one hectare each by removing invasive blackberry plants and other introduced plant species. In all nests that reached late incubation, we also reduced the number of Avian Vampire Fly larvae. In this study, we compared foraging and perch height, pair formation, incubation time and reproductive success between managed and unmanaged areas. As predicted, we found significantly lower foraging height and perch height in 2021 in managed areas compared to unmanaged areas. In 2020, daily failure rate (DFR) of nests in the egg stage did not differ between management types; however, in 2021, DFR in the egg stage was significantly lower in managed areas than in unmanaged areas. The DFR during the nestling stage was similar between managed and unmanaged areas in 2020, but in 2021, only nests in managed areas reached the nestling stage. Females brooded significantly more during the incubation phase in managed areas. Additionally, we found significantly higher reproductive success in managed areas compared to unmanaged areas in 2021, but not in 2020. Habitat restoration is a long-term process and these findings suggest that habitat management positively affects this small population in the long term.

Parental food provisioning and nestling growth under Philornis downsi parasitism in the Galapagos Green Warbler-Finch, classified as 'vulnerable' by the IUCN.

In the Galapagos Islands, many endemic landbird populations are declining due to habitat degradation, food availability, introduced species and other factors. Given nestlings typically lack efficient defense mechanisms against parasites, hematophagous ectoparasites such as the larvae of the introduced Avian Vampire Fly, Philornis downsi, can impose high brood mortality and cause threatening population declines in Darwin finches and other landbirds. Here, we assess whether the food compensation hypothesis (i.e., the parents' potential to compensate for deleterious parasite effects via increased food provisioning) applies to the Green Warbler-Finch. We differentiated nests with low or high infestation levels by P. downsi and quantified food provisioning rates of male and female parents, time females spent brooding nestlings, and nestling growth. Male provisioning rates, total provisioning rates and female brooding time did not significantly vary in relation to infestation levels, nor by the number of nestlings. Opposed to the predictions of the food compensation hypothesis, females showed significantly reduced provisioning rates at high infestation levels. Nestling body mass was significantly lower and there was a reduction of skeletal growth, although not significantly, in highly infested nests. The females' response to high infestation may be due to parasites directly attacking and weakening brooding females, or else that females actively reduce current reproductive effort in favor of future reproduction. This life-history trade-off may be typical for Darwin finches and many tropical birds with long lifespans and therefore high residual reproductive value. Conservation strategies may not build on the potential for parental food compensation by this species.

Ratcheting up tool innovation in Goffin's cockatoos (Cacatua goffiniana): The effect of contextually diverse prior experience.

The ability to gain information from one situation, acquire new skills and/or perfect existing ones, and subsequently apply them to a new situation is a key element in behavioural flexibility and a hallmark of innovation. A flexible agent is expected to store these skills and apply them to contexts different from that in which learning occurred. Goffin's cockatoos (Cacatua goffiniana) are highly innovative parrots renowned for their problem-solving and tool-using skills and are thus excellent candidates to study this phenomenon. We hypothesized that birds allowed to use a tool in a larger variety of contingencies would acquire a broader expertise in handling it, facilitating its transfer to new tasks. In our study, we compared the performance of two groups of captive Goffin's cockatoos (N = 13): A test group received more diverse learning and motor experiences on multiple applications of a hook-type tool, while a control group received intensive, total trial-matched, experience with a single application of the same tool. Then, both groups were tested on two novel tasks to determine whether experience with the tool in multiple contexts would facilitate performance during transfer. While both groups transferred to both novel tasks, group differences in performance were apparent, particularly in the second transfer task, where test birds achieved a higher success rate and reached criteria within fewer trials than control birds. These results provide support for the prediction that experiencing a diverse range of contingencies with a tool appears to allow birds to acquire generalizable knowledge and transferrable skills to tackle an untrained problem more efficiently. In contrast, intensive experience with the tool in a single context might have made control birds less flexible and more fixated on previously learned tool-dependent instances.

Flexible tool set transport in Goffin's cockatoos.

The use of tool sets constitutes one of the most elaborate examples of animal technology, and reports of it in nature are limited to chimpanzees and Goffin's cockatoos. Although tool set use in Goffin's was only recently discovered, we know that chimpanzees flexibly transport tool sets, depending on their need. Flexible tool set transport can be considered full evidence for identification of a genuine tool set, as the selection of the second tool is not just a response to the outcomes of the use of the first tool but implies recognizing the need for both tools before using any of them (thus, categorizing both tools together as a tool set). In three controlled experiments, we tested captive Goffin's in tasks inspired by the termite fishing of Goualougo Triangle's chimpanzees. Thereby, we show that some Goffin's can innovate the use and flexibly use and transport a new tool set for immediate future use; therefore, their sequential tool use is more than the sum of its parts. VIDEO ABSTRACT.

Plant invasion causes alterations in Darwin's finch feeding patterns in Galápagos cloud forests.

Invasive species pose a major threat to forest biodiversity, particularly on islands such as the Galapágos. Here, invasive plants are threatening the remnants of the unique cloud forest and its iconic Darwin's finches. We posit that food web disturbances caused by invasive Rubus niveus (blackberry), have contributed to the rapid decline of the insectivourous green warbler finch (Certhidae olivacea). We compared the birds' dietary changes in long-term management, short-term management and unmanaged areas. We measured C:N ratios, and δ15N­nitrogen and δ13C­carbon values in both consumer tissues (bird-blood) and food sources (arthropods), as indicators of resource use change, and collected mass abundance, and arthropod diversity data. We characterised the birds' diets using isotope mixing models. The results revealed that finches in (blackberry-invaded) unmanaged areas foraged more on abundant, yet lower quality, arthropods present in the invaded understory. This suggests that blackberry encroachment leads to a decrease in food source quality with physiological consequences for green warbler finch chicks. Results also implied that blackberry control has a short-term impact on food source quantity, which led to a decrease in chick recruitment that we observed in our previous studies; despite this, in the long-term, these managed systems show signs of recovery within three years of restoration.

Innovative composite tool use by Goffin's cockatoos (Cacatua goffiniana).

Composite tool use (using more than one tool simultaneously to achieve an end) has played a significant role in the development of human technology. Typically, it depends on a number of specific and often complex spatial relations and there are thus very few reported cases in non-human animals (e.g., specific nut-cracking techniques in chimpanzees and capuchin monkeys). The innovative strategies underlying the innovation and spread of tool manufacture and associative tool use (using > 1 tools) across tool using animals is an important milestone towards a better understanding of the evolution of human technology. We tested Goffin's cockatoos on a composite tool problem, the 'Golf Club Task', that requires the use of two objects in combination (one used to control the free movement of a second) to get a reward. We demonstrate that these parrots can innovate composite tool use by actively controlling the position of the end effector and movement of both objects involved in a goal directed manner. The consistent use of different techniques by different subjects highlights the innovative nature of the individual solutions. To test whether the solution could be socially transmitted, we conducted a second study, which provided only tentative evidence for emulative learning. To our knowledge, this indicates that the cognitive preconditions for composite tool use have also evolved outside the primate lineage.

Parental care in the Small Tree Finch Camarhynchus parvulus in relation to parasitism and environmental factors.

The parental food compensation hypothesis suggests that parents may compensate for the negative effects of parasites on chicks by increased food provisioning. However, this ability differs widely among host species and may also depend on ecological factors such as adverse weather conditions and habitat quality. Although weed management can improve habitat quality, management measures can bring about a temporary decrease in food availability and thus may reduce parents' ability to provide their nestlings with enough energy. In our study we investigated the interaction of parasitism and weed management, and the influence of climate on feeding rates in a Darwin's tree finch species, which is negatively impacted by two invasive species. The larvae of the invasive parasitic fly Philornis downsi ingest the blood and body tissues of tree finch nestlings, and the invasive Blackberry Rubus niveus affects one of the main habitats of Darwin's tree finches. We compared parental food provisioning of the Small Tree Finch Camarhynchus parvulus in parasitized and parasite-free nests in three different areas, which differed in invasive weed management (no management, short-term and long-term management). In a parasite reduction experiment, we investigated whether the Small Tree Finch increases food provisioning rates to nestlings when parasitized and whether this ability depends on weed management conditions and precipitation. Our results provide no evidence that Small Tree Finches can compensate with additional food provisioning when parasitized with P. downsi. However, we found an increase in male effort in the short-term management area, which might indicate that males compensate for lower food quality with increased provisioning effort. Furthermore, parental food provisioning was lower during rainfall, which provides an explanation for the negative influence of rain on breeding success found in earlier studies. Like other Darwin's finches, the Small Tree Finch seems to lack the ability to compensate for the negative effects of P. downsi parasitism, which is one explanation for why this invasive parasite has such a devastating effect on this host species.

Can Habits Impede Creativity by Inducing Fixation?

In a competitive and ever-changing world, the ability to generate outstanding ideas is crucial. However, this process can be impeded by factors such as fixation on ideas that emerged through prior experience. The aim of the present study was to shed light on the fixating effect of habits on creativity. To this end, healthy young adults were asked to generate alternative uses for items that differed in their frequency of use in the Alternative Uses Task (a standardized test for divergent thinking). We predicted that frequent past use of an item would lead to the formation of stimulus-response associations between the item and its most frequent use(s) and thereby hinder idea generation. Indeed, individuals were less flexible (but more fluent) in generating ideas for frequently used items than for unknown items. Additionally, we found that subjective automaticity of idea generation was negatively related with flexibility. Finally, we investigated whether individual differences in general habit tendency influence creativity, by relating performance on the Slips-of-Action task (an outcome devaluation paradigm extensively used in habit research) to performance on the Alternative Uses Task, the Candle Problem (a classic convergent thinking task) and two puzzles (non-conventional problem-solving tasks). While we did not find a significant relationship between habit tendency and the Alternative Uses Task or the Candle Problem scores, the tendency to rely on habits predicted probability to succeed and latency to solve one of the puzzles: less habit-prone participants were more likely to solve it and to do so faster. In conclusion, our study provides evidence for the notion that habits can negatively impact creativity and opens promising future avenues of research in this field.

Under adverse conditions, older small tree finch males (Camarhynchus parvulus) produce more offspring than younger males.

Females of many bird species prefer mating with older males, presumably because they provide superior parental care and possibly superior genes. A previous study found that female small tree finches (Camarhynchus parvulus) preferred pairing with old males and had a higher breeding success when paired with old males because their nests were more concealed, higher up in the canopy and therefore less likely to be depredated. However, causes for brood loss have changed over the last decade: predation of small tree finch nests has decreased, whereas brood losses due to parasitism by the invasive parasitic fly Philornis downsi have increased. In the present study, we investigated (a) how the change in predation and parasitism by P. downsi influenced the breeding success of small tree finches, (b) whether there were still differences in breeding success between young and old males, (c) whether P. downsi infestation had a differential effect on nests of young and old males and (d) whether young and old males differed in foraging success. During 2012-2016, we found an overall low influence of predation and a high influence of P. downsi, but neither differed between nests of young and old males. Nests of old males had more fledglings than those of young males. However, the difference in breeding success disappeared when P. downsi numbers were experimentally reduced by injecting an insecticide into nests. This indicates that older males were able to compensate for the detrimental effects of parasitism.

Investigating physical cognition in rooks, Corvus frugilegus.

Although animals (particularly tool-users) are capable of solving physical tasks in the laboratory , the degree to which they understand them in terms of their underlying physical forces is a matter of contention. Here, using a new paradigm, the two-trap tube task, we report the performance of non-tool-using rooks. In contrast to the low success rates of previous studies using trap-tube problems , seven out of eight rooks solved the initial task, and did so rapidly. Instead of the usual, conceptually flawed control, we used a series of novel transfer tasks to test for understanding. All seven transferred their solution across a change in stimuli. However, six out of seven were unable to transfer to two further tasks, which did not share any one visual constant. One female was able to solve these further transfer tasks. Her result is suggestive evidence that rooks are capable of sophisticated physical cognition, if not through an understanding of unobservable forces , perhaps through rule abstraction. Our results highlight the need to investigate cognitive mechanisms other than causal understanding in studying animal physical cognition.

Population dynamics of an invasive bird parasite, Philornis downsi (Diptera: Muscidae), in the Galapagos Islands.

The invasive parasitic fly, Philornis downsi (Muscidae), is one of the greatest threats to the avifauna of the Galapagos Islands. The larvae of this fly feed on the blood and tissues of developing nestlings of at least 18 endemic and native birds. The aim of the current study was to investigate biotic and abiotic factors that may influence the population dynamics of this invasive parasite. To study the influence of vegetation zone and related climatic factors on fly numbers, a bi-weekly monitoring program using papaya-baited traps was carried out at a dry, lowland site and at a humid, highland site on Santa Cruz Island between 2012-2014. Female flies, a large proportion of which were inseminated and gravid, were collected throughout the year at both sites, indicating females were active during and between the bird breeding seasons. This is the first evidence that female flies are able to persist even when hosts are scarce. On the other hand, catch rates of male flies declined between bird breeding seasons. Overall, catch rates of P. downsi were higher in the drier, lowland habitat, which may be a consequence of host or resource availability. Time was a stronger predictor of adult fly numbers than climate, further suggesting that P. downsi does not appear to be limited by its environment, but rather by host availability. Seasonal catch rates suggested that populations in both habitats were continuous and multivoltine. Numbers of adult female flies appeared to be regulated chiefly by simple direct density dependence, and may be governed by availability of bird nests with nestlings. Nevertheless, confounding factors such as the existence of reservoir hosts that perpetuate fly populations and changes in behavior of P. downsi may increase the vulnerability of bird hosts that are already IUCN red-listed or in decline.

The impact of invasive plant management on the foraging ecology of the Warbler Finch (Certhidea olivacea) and the Small Tree Finch (Camarhynchus parvulus) on Galápagos.

In recent decades, arboreal Darwin's Finches have suffered from a dramatic population decline, which has been attributed to parasitism by the invasive botfly Philornis downsi. However, changes to their primary habitat caused by invasive plant species may have additionally contributed to the observed population decline. The humid cloud forest on Santa Cruz Island is a stronghold of arboreal Darwin's Finches but has been invaded by blackberry (Rubus niveus). In some areas, manual control and herbicide application are used to combat this invasion, both causing a temporary removal of the entire understory. We hypothesized that the removal of the understory reduces the availability of arthropods, which are a main food source during chick rearing. We compared the foraging behaviour of Warbler Finches (Certhidea olivacea) and Small Tree Finches (Camarhynchus parvulus) at three study sites that varied in the degree of R. niveus invasion and the length of time since the last herbicide application. We used prey attack rate and foraging success as an index for food availability and predicted a lower attack rate and foraging success in areas that had recently been sprayed with herbicides. We found that both the invasion and the management of R. niveus influenced microhabitat use, foraging substrate and prey choice in both species. Contrary to our hypothesis, we did not find a lower attack rate or foraging success in the area with recent herbicide application. This may be explained by the finding that both species mainly foraged in the canopy but also used dead plant structures of the understory of the recently controlled area that resulted from the invasive plant management.

From mechanisms to function: an integrated framework of animal innovation.

Animal innovations range from the discovery of novel food types to the invention of completely novel behaviours. Innovations can give access to new opportunities, and thus enable innovating agents to invade and create novel niches. This in turn can pave the way for morphological adaptation and adaptive radiation. The mechanisms that make innovations possible are probably as diverse as the innovations themselves. So too are their evolutionary consequences. Perhaps because of this diversity, we lack a unifying framework that links mechanism to function. We propose a framework for animal innovation that describes the interactions between mechanism, fitness benefit and evolutionary significance, and which suggests an expanded range of experimental approaches. In doing so, we split innovation into factors (components and phases) that can be manipulated systematically, and which can be investigated both experimentally and with correlational studies. We apply this framework to a selection of cases, showing how it helps us ask more precise questions and design more revealing experiments.

Darwin's finches treat their feathers with a natural repellent.

Darwin's finches are highly innovative. Recently we recorded for the first time a behavioural innovation in Darwin's finches outside the foraging context: individuals of four species rubbed leaves of the endemic tree Psidium galapageium on their feathers. We hypothesised that this behaviour serves to repel ectoparasites and tested the repellency of P. galapageium leaf extracts against parasites that negatively affect the fitness of Darwin's finches, namely mosquitoes and the invasive hematophagous fly Philornis downsi. Mosquitoes transmit pathogens which have recently been introduced by humans and the larvae of the fly suck blood from nestlings and incubating females. Our experimental evidence demonstrates that P. galapageium leaf extracts repel both mosquitoes and adult P. downsi and also inhibit the growth of P. downsi larvae. It is therefore possible that finches use this plant to repel ectopoarasites.

Coping with uncertainty: woodpecker finches (Cactospiza pallida) from an unpredictable habitat are more flexible than birds from a stable habitat.

Behavioural flexibility is thought to be a major factor in evolution. It may facilitate the discovery and exploitation of new resources, which in turn may expose populations to novel selective forces and facilitate adaptive radiation. Darwin's finches are a textbook example of adaptive radiation. They are fast learners and show a range of unusual foraging techniques, probably as a result of their flexibility. In this study we aimed to test whether variability of the environment is correlated with flexibility. We compared woodpecker finches from a dry area (hereafter, Arid Zone), where food availability is variable, with individuals from a cloud forest (hereafter, Scalesia zone) where food abundance is stable. As parameters for flexibility, we measured neophilia and neophobia, which are two aspects of reaction to novelty, reversal learning and problem-solving. We found no differences in performance on a problem-solving task but, in line with our prediction, individuals from the Arid Zone were significantly faster reversal learners and more neophilic than their conspecifics from the Scalesia zone. The latter result supports the notion that environmental variability drives flexibility. In contrast to our prediction, Arid Zone birds were even more neophobic than birds from the Scalesia Zone. The latter result could be the consequence of differences in predation pressure between the two vegetation zones.