Rebecca Croston

Individual variation in spatial memory performance in wild mountain chickadees from different elevations

For food-caching animals inhabiting environments with strong seasonal variation, harsh winter conditions may limit access to naturally available food and favour the evolution of enhanced spatial memory. Spatial memory enables animals to remember the locations of food caches for overwinter survival, therefore animals in harsher conditions may benefit more from more accurate spatial memory than conspecifics living under relatively mild conditions. Despite numerous laboratory studies lending indirect support to the hypothesis that a harsh environment favours the evolution of spatial memory, there is no direct evidence showing fitness consequences of variation in spatial memory. As a step towards evaluating this hypothesis in natural populations, we established spatial arrays of programmable bird feeders equipped with radio frequency identification technology (RFID) to test for individual variation in spatial memory in food-caching mountain chickadees, Poecile gambeli , at two elevations differing in winter climate severity. Individuals could only access food at a single rewarding feeder within an array of eight, and each individual had to learn the location of their unique rewarding feeder. Birds at higher elevations visited the arrays significantly more frequently than birds at lower elevations, suggesting more intense food caching. They also performed better at locating their rewarding feeder than birds from lower elevations. Individuals showing better performance participated in more overall trials, suggesting a link between food-caching propensity and memory performance, but higher overall levels of activity within each array yielded less accurate memory performance. Finally, rotating the arrays showed that birds relied specifically on spatial memory in order to locate their rewarding feeder. To our knowledge, this is the first explicit test of spatial memory performance in food-caching birds under natural conditions. Our results corroborate earlier laboratory-based work showing large individual variation in spatial memory performance and lay the groundwork for future investigation into the fitness consequences of individual variation and the evolution of spatial memory.

Using 3D printed eggs to examine the egg-rejection behaviour of wild birds

The coevolutionary relationships between brood parasites and their hosts are often studied by examining the egg rejection behaviour of host species using artificial eggs. However, the traditional methods for producing artificial eggs out of plasticine, plastic, wood, or plaster-of-Paris are laborious, imprecise, and prone to human error. As an alternative, 3D printing may reduce human error, enable more precise manipulation of egg size and shape, and provide a more accurate and replicable protocol for generating artificial stimuli than traditional methods. However, the usefulness of 3D printing technology for egg rejection research remains to be tested. Here, we applied 3D printing technology to the extensively studied egg rejection behaviour of American robins, Turdus migratorius. Eggs of the robin’s brood parasites, brown-headed cowbirds, Molothrus ater, vary greatly in size and shape, but it is unknown whether host egg rejection decisions differ across this gradient of natural variation. We printed artificial eggs that encompass the natural range of shapes and sizes of cowbird eggs, painted them to resemble either robin or cowbird egg colour, and used them to artificially parasitize nests of breeding wild robins. In line with previous studies, we show that robins accept mimetically coloured and reject non-mimetically coloured artificial eggs. Although we found no evidence that subtle differences in parasitic egg size or shape affect robins’ rejection decisions, 3D printing will provide an opportunity for more extensive experimentation on the potential biological or evolutionary significance of size and shape variation of foreign eggs in rejection decisions. We provide a detailed protocol for generating 3D printed eggs using either personal 3D printers or commercial printing services, and highlight additional potential future applications for this technology in the study of egg rejection.

The role of egg–nest contrast in the rejection of brood parasitic eggs

ABSTRACT Hosts of avian brood parasites can avoid the reproductive costs of raising genetically unrelated offspring by rejecting parasitic eggs. The perceptual cues and controls mediating parasitic egg discrimination and ejection are well studied: hosts are thought to use differences in egg color, brightness, maculation, size and shape to discriminate between their own and foreign eggs. Most theories of brood parasitism implicitly assume that the primary criteria to which hosts attend when discriminating eggs are differences between the eggs themselves. However, this assumption is confounded by the degree to which chromatic and achromatic characteristics of the nest lining co-vary with egg coloration, so that egg–nest contrast per se might be the recognition cue driving parasitic egg detection. Here, we systematically tested whether and how egg–nest contrast itself contributes to foreign egg discrimination. In an artificial parasitism experiment, we independently manipulated egg color and nest lining color of the egg-ejector American robin (Turdus migratorius), a host of the obligate brood parasitic brown-headed cowbird (Molothrus ater). We hypothesized that the degree of contrast between foreign eggs and the nest background would affect host egg rejection behavior. We predicted that experimentally decreasing egg–nest chromatic and achromatic contrast (i.e. rendering parasitic eggs more cryptic against the nest lining) would decrease rejection rates, while increasing egg–nest contrast would increase rejection rates. In contrast to our predictions, egg–nest contrast was not a significant predictor of egg ejection patterns. Instead, egg color significantly predicted responses to parasitism. We conclude that egg–egg differences are the primary drivers of egg rejection in this system. Future studies should test for the effects of egg–nest contrast per se in predicting parasitic egg recognition in other host–parasite systems, including those hosts building enclosed nests and those parasites laying cryptic eggs, as an alternative to hypothesized effects of egg–egg contrast. Summary: We tested whether and how egg–nest visual contrast contributes to parasitic egg discrimination in American robins. We found no effect of egg–nest contrast on egg rejection rates, and conclude that egg–egg contrasts are the primary drivers of egg rejection in this system.

High repeatability of egg rejection in response to experimental brood parasitism in the American robin (Turdus migratorius)

Repeatability is a measure of the amount of variation in a phenotype that is attributable to differences between individuals. This concept is important for any study of behaviour, as all traits of evolutionary interest must be repeatable in order to respond to selection. We investigated the repeatability of behavioural responses to experimental brood parasitism in American robins, a robust (100%) rejecter of parasitic brown-headed cowbird eggs. Because tests of repeatability require variation between individuals, we parasitized the same robin nests twice successively with model eggs dyed with colours known to elicit rejection at intermediate rates (58–70%). We calculated the repeatability of responses to parasitism, and used a generalized linear mixed model to also test for potentially confounding effects of ordinal date, presentation order, and clutch size. We found that repeatability in response to brood parasitism in this host species is high, and the best model predicting responses to sequential artificial parasitism includes only nest identity. This result is consistent with a critical assumption about egg rejection in this cowbird host as an evolved adaptation in response to brood parasitism.

Predictably harsh environment is associated with reduced cognitive flexibility in wild food-caching mountain chickadees

Cognition is one of the mechanisms underlying behavioural flexibility, but flexibility of cognition itself may vary as a result of trade-offs between the ability to learn new information and the ability to retain old memories. How and when cognitive flexibility is constrained by this trade-off remains poorly understood. We investigated cognitive flexibility in wild food-caching mountain chickadees, Poecile gambeli, at different elevations experiencing different levels of environmental harshness during the nonbreeding season, using a spatial learning and memory reversal paradigm. There were no significant differences in sampling strategies between elevations, but high-elevation chickadees performed worse than low-elevation chickadees on the reversal task, indicating lower cognitive flexibility. Compared to the initial learning task, low-elevation chickadees improved their performance during the reversal task, while high-elevation chickadees performed worse. High-elevation birds inspected previously rewarding locations more frequently than other locations, suggesting that reduced cognitive flexibility is associated with proactive interference. Considering that high-elevation chickadees cache more food and are likely more dependent on these caches than their conspecifics from low elevation, and that chickadees from both elevations use similar sampling strategies, our findings suggest that stronger memories of more caches might interfere with acquisition and retention of new memories. Overall, our results suggest that predictably harsh environments might favour stronger memories at the expense of decreased cognitive flexibility, which is likely driven by increased proactive interference.

Repeated Brood Parasitism by Brown-Headed Cowbirds (Molothrus ater) at Nesting Sites of Eastern Phoebes (Sayornis phoebe) across Non-consecutive Years

Abstract The temporal and spatial patterns of avian brood parasitism can critically influence host fitness, the coevolution of parasitic strategies and host resistance, and their reciprocal effects on population dynamics. This study examined spatial patterns of Brown-headed Cowbird (Molothrus ater) parasitism on Eastern Phoebe (Sayornis phoebe) hosts in 2009–2011 near Ithaca, NY, USA, and compared them with published data from 1999–2002 at the same nest sites, encompassing a period long enough for a turn-over of most of the breeding adult host and parasite populations. Relative to non-parasitized nests, host nests, that were more likely to be parasitized annually in 2009–2011, had also been parasitized more often during years 1999–2002. These findings are consistent with the hypothesis that Brown-headed Cowbirds, even across generations, show a consistent preference for particular Eastern Phoebe nest sites, although it remains unclear what the relative roles of the biological traits of the hosts occupying those sites versus the ecological and physical characteristics of the actual nest sites may be in yielding these patterns. Nonetheless, the results imply that knowing the site-specific historys of parasitism of reusable nests and breeding sites can be used to predict variation in the risk and future impact of cowbirds on this host species.

Experimental Shifts in Intraclutch Egg Color Variation Do Not Affect Egg Rejection in a Host of a Non-Egg-Mimetic Avian Brood Parasite

Avian brood parasites lay their eggs in the nests of other birds, and impose the costs associated with rearing parasitic young onto these hosts. Many hosts of brood parasites defend against parasitism by removing foreign eggs from the nest. In systems where parasitic eggs mimic host eggs in coloration and patterning, extensive intraclutch variation in egg appearances may impair the host’s ability to recognize and reject parasitic eggs, but experimental investigation of this effect has produced conflicting results. The cognitive mechanism by which hosts recognize parasitic eggs may vary across brood parasite hosts, and this may explain variation in experimental outcome across studies investigating egg rejection in hosts of egg-mimicking brood parasites. In contrast, for hosts of non-egg-mimetic parasites, intraclutch egg color variation is not predicted to co-vary with foreign egg rejection, irrespective of cognitive mechanism. Here we tested for effects of intraclutch egg color variation in a host of nonmimetic brood parasite by manipulating egg color in American robins (Turdus migratorius), hosts of brown-headed cowbirds (Molothrus ater). We recorded robins’ behavioral responses to simulated cowbird parasitism in nests where color variation was artificially enhanced or reduced. We also quantified egg color variation within and between unmanipulated robin clutches as perceived by robins themselves using spectrophotometric measures and avian visual modeling. In unmanipulated nests, egg color varied more between than within robin clutches. As predicted, however, manipulation of color variation did not affect rejection rates. Overall, our results best support the scenario wherein egg rejection is the outcome of selective pressure by a nonmimetic brood parasite, because robins are efficient rejecters of foreign eggs, irrespective of the color variation within their own clutch.

Mountain chickadees return to their post-natal dispersal settlements following long-term captivity

There is little work investigating the relationship between environmental changes and associated hippocampal effects on animal homing. We took advantage of previous studies in which wild, non-migratory mountain chickadees spent six months in captivity prior to being released. Over the following three years, 45.8% of the birds were resighted, and in all cases birds were identified less than 300 m from their initial capture locations at their respective elevation, despite previous studies documenting ca 30% captivity-related reduction of the hippocampus. Reproductive success of birds that spent six months in captivity did not differ from control birds that did not experience captivity. Our findings suggest that chickadees are highly site faithful and can return to their original capture location after spending time in captivity. Our results also have important implications for animal welfare practices as birds held in captivity bred successfully and may not need to be sacrificed following captivity.