Western Scrub-jays Research Articles

Exploring the bird mind: A review of episodic memory and metacognition studies of western scrub-jays

Exploring the bird mind: A review of episodic memory and metacognition studies of western scrub-jays

HOUSE FINCH ( HAEMORHOUS MEXICANUS)-ASSOCIATED MYCOPLASMA GALLISEPTICUM IDENTIFIED IN LESSER GOLDFINCH ( SPINUS PSALTRIA) AND WESTERN SCRUB JAY ( APHELOCOMA CALIFORNICA) USING STRAIN-SPECIFIC QUANTITATIVE PCR.

: In 1994 Mycoplasma gallisepticum was found to be the etiologic agent of House Finch ( Haemorhous mexicanus) conjunctivitis, a rapidly expanding epidemic caused by a genetically discrete, House Finch-associated strain of M. gallisepticum (HFMG). While most prominent in House Finches, HFMG has been reported in other members of the family Fringillidae, including American Goldfinches ( Spinus tristis), Purple Finches ( Haemorhous purpureus), Pine Grosbeaks ( Pinicola enucleator), and Evening Grosbeaks ( Coccothraustes vespertinus). Herein we report two new potential host species of HFMG strain, the Lesser Goldfinch ( Spinus psaltria), belonging to the Fringillidae family, and the Western (California) Scrub Jay ( Aphelocoma californica), belonging to the Corvidae family. The latter is one of only two reports of HFMG being found outside the Fringillidae family, and of these is the only one reported outside of captivity. Furthermore, non-HFMG M. gallisepticum was identified in an American Crow ( Corvus brachyrhynchos), indicating presence of additional strains in wild birds. Strain typing of M. gallisepticum isolates was done via HFMG-specific quantitative PCR analysis and validated using random amplified polymorphic DNA analysis. Our results suggested an expanded host range of HFMG strain, and further suggested that the host range of HFMG was not limited to members of the family Fringillidae.

Cataracts in corvids: health and welfare implications of lens opacification in a colony of Western scrub-jays (Aphelocoma californica)

Cataracts in corvids: health and welfare implications of lens opacification in a colony of Western scrub-jays (Aphelocoma californica)

Western scrub-jays (Aphelocoma californica) solve multiple-string problems by the spatial relation of string and reward.

String-pulling is a widely used paradigm in animal cognition research to assess what animals understand about the functionality of strings as a means to obtain an out-of-reach reward. This study aimed to systematically investigate what rules Western scrub-jays (Aphelocoma californica) use to solve different patterned string tasks, i.e. tasks in which subjects have to choose between two or more strings of which only one is connected to the reward, or where one is more efficient. Arranging strings in a parallel configuration showed that the jays were generally capable of solving multiple-string tasks and acted in a goal-directed manner. The slanted and crossed configurations revealed a reliance on a “proximity rule”, that is, a tendency to choose the string-end closest to the reward. When confronted with strings of different lengths attached to rewards at different distances the birds chose according to the reward distance, preferring the reward closest to them, and were sensitive to the movement of the reward, but did not consistently prefer the shorter and therefore more efficient string. Generally, the scrub-jays were successful in tasks where the reward was closest to the string-ends they needed to pull or when string length and reward distance correlated, but the birds had problems when the wrong string-end was closest to the reward or when the food items were in close proximity to each other. These results show that scrub-jays had a partial understanding of the physical principles underlying string-pulling but relied on simpler strategies such as the proximity rule to solve the tasks.Electronic supplementary materialThe online version of this article (doi:10.1007/s10071-016-1018-x) contains supplementary material, which is available to authorized users.

House Finch (Haemorhous mexicanus) Conjunctivitis, and Mycoplasma spp. Isolated from North American Wild Birds, 1994-2015.

Sampling wild birds for mycoplasma culture has been key to the study of House Finch (Haemorhous mexicanus) conjunctivitis, yielding isolates of Mycoplasma gallisepticum spanning the temporal and geographic ranges of disease from emergence to endemicity. Faced with the challenges and costs of sample collection over time and from remote locations for submission to our laboratory for mycoplasma culture, protocols evolved to achieve a practical optimum. Herein we report making M. gallisepticum isolates from House Finches almost every year since the disease emerged in 1994, and we now have 227 isolates from 17 states. Our wild bird host range for M. gallisepticum isolates includes Blue Jay ( Cyanocitta cristata ), American Goldfinch (Spinus tristis), Lesser Goldfinch (Spinus psaltria), Purple Finch (Haemorhous purpureus), Evening Grosbeak ( Coccothraustes vespertinus ), and herein first reports for Western Scrub-jay ( Aphelocoma californica ), and American Crow ( Corvus brachyrhynchos ). By collecting and identifying isolates from birds with clinical signs similar to those of House Finch conjunctivitis, we also expanded the known host range of Mycoplasma sturni and obtained isolates from additional wild bird species. Accumulating evidence shows that a diverse range of wild bird species may carry or have been exposed to M. gallisepticum in the US, as in Europe and Asia. Therefore, the emergence of a pathogenic M. gallisepticum strain in House Finches may actually be the exception that has allowed us to identify the broader epidemiologic picture.

Counting on your friends: The role of social environment on quantity discrimination

Quantity discrimination has been established in a range of species. However, most demonstrations of quantity discrimination control for social factors by testing animals individually. I tested whether sociality affects quantity discrimination in the wild by comparing the performances of the highly social Mexican jay (MJ; Aphelocoma wollweberi) and the territorial Western scrub jay (WJ; Aphelocoma californica). The birds were given a choice between two lines of peanuts that differed in initial quantity ranging from 2 vs 8 to 14 vs 16. Their choices were recorded until all peanuts were eaten or cached. Whereas non-social WJ selected the larger quantity across all the trials significantly more than chance, social MJ selected the larger line only when the difference in the number of peanuts between lines was small. In MJ, individual choice when selecting the large or small quantity was influenced by what line the previous bird had chosen when the difference in lines was large, with followers significantly more likely to select the smaller quantity. WJ were not significantly affected by the choices of other individuals. The only factors that influenced WJ choice were ratio and total differences between the two quantities. These results suggests that in certain scenarios, both species can discriminate between different quantities. However, MJ were greatly influenced by social factors, a previously untested factor, while WJ were only influenced by ratio and total difference between the quantities, consistent with findings in other species. Overall, this study demonstrates the important role of sociality in numerical cognitive performance, a previously overlooked factor.

Surveys for Antibodies Against Mosquitoborne Encephalitis Viruses in California Birds, 1996-2013.

From 1996 through 2013, 54,546 individual birds comprising 152 species and 7 orders were banded, bled, and released at four study areas within California, from which 28,388 additional serum samples were collected at one or more recapture encounters. Of these, 142, 99, and 1929 birds from 41 species were positive for neutralizing antibodies against western equine encephalomyelitis virus (WEEV), St. Louis encephalitis virus (SLEV), or West Nile virus (WNV) at initial capture or recapture, respectively. Overall, 83% of the positive serum samples were collected from five species: House Finch, House Sparrow, Mourning Dove, California Quail, and Western Scrub-Jay. Temporal data supported concurrent arbovirus surveillance and documented the disappearance of birds positive for WEEV in 2008 and SLEV in 2003 and the appearance of birds positive for WNV after its invasion in 2003. Results of these serosurveys agreed well with the host selection patterns of the Culex vectors as described from bloodmeal sequencing data and indicated that transmission of WNV seemed most effective within urban areas where avian and mosquito host diversity was limited to relatively few competent species.

Western scrub-jays do not appear to attend to functionality in Aesop's Fable experiments.

Western scrub-jays are known for their highly discriminatory and flexible behaviors in a caching (food storing) context. However, it is unknown whether their cognitive abilities are restricted to a caching context. To explore this question, we tested scrub-jays in a non-caching context using the Aesop’s Fable paradigm, where a partially filled tube of water contains a floating food reward and objects must be inserted to displace the water and bring the food within reach. We tested four birds, but only two learned to drop stones proficiently. Of these, one bird participated in 4/5 experiments and one in 2/5 experiments. Both birds passed one experiment, but without attending to the functional differences of the objects, and failed the other experiments. Scrub-jays were not motivated to participate in these experiments, suggesting that either this paradigm was ecologically irrelevant or perhaps their flexibility is restricted to a caching context.

The effect of within-year variation in acorn crop size on seed harvesting by avian hoarders.

Spatial and temporal variation in resource distribution affect the movement and foraging behavior of many animals. In the case of animal-dispersed trees, numerous studies have addressed masting-the synchronized variation in seed production between years-but the fitness consequences of spatial variation in seed production within a year are unclear. We investigated the effects of variable acorn production in a population of valley oaks (Quercus lobata) on the composition and behavior of the avian-disperser community. We found that western scrub-jays (Aphelocoma californica), high-quality dispersers that store seeds in the ground, were attracted to, and exhibited increased per capita dispersal rates from, trees with large acorn crops. In contrast, acorn woodpeckers (Melanerpes formicivorus), low-quality dispersers that store acorns in trees where they are unlikely to germinate, increased per capita hoarding rates but did not attend trees with large seed crops in higher numbers, suggesting that the two species responded to resources on different spatial scales. Antagonistic interactions within and between species increased with the number of birds attending a tree, resulting in a potential cost for foraging birds, but did not reduce dispersal rates. Using a simulation model, we estimated that trees with large initial crops experienced a greater proportion (77 %) of high-quality seed dispersal events than trees with small crops (62 %). Our findings provide support for a mechanistic link between seed production and foraging behavior of seed dispersers as predicted by the predator dispersal hypothesis for the functional consequences of variable seed production in hoarder-dispersed trees.

Intelligence Over Time: Intelligence in Corvids and Apes

INTELLEGENCE OVER TIME: THE EVOLUTION OF INTELLIGENCE IN CORVIDS AND APES BY KATIE SANKO K itty, a New Caledonian crow, became famous when National Geographic highlighted her ability to solve a puz- zle that bewildered many five-year-old children. 5 In order to obtain a small piece of meat floating in a tube of water, Kitty placed rocks in a seemingly unrelated tube, causing the water to rise and the meat to float to the top. 5 Kitty and her fellow crows possess remarkable cognitive ability, prompting many to wonder what could be behind the evolution of such intelligence. Animal intelligence is tricky to define, despite the efforts of numerous researchers over the years. A quantitative measure of animal intelligence has yet to be agreed upon. It is often assumed that as brain size (both absolute and relative) increases, so does intelligence. However, both of these measures have been ruled out by bascre- search. For example, cetaceans (whales and dolphins) have a larger absolute brain size than humans, 10 yet humans are considered far more intelligent. Similarly, the shrew’s brain contains 10% of its body mass while a human’s contains only 2%. Generally, the definition of intelligence involves the performance of complex behaviors and the use of novel solutions to problems. 10 Humans are not alone in the possession of great intelligence. In fact, advanced cogni- tion has evolved in many taxa. 9 While the intelligence of primates such as chimpan- zees has been widely publicized, it has also been found that birds in the group of corvids (crows, jays, ravens, ect.) have cog- nitive abilities comparable to apes. 4 Exam- ples of higher cognition in both primates and corvids include object permanence (memory for objects that cannot be seen by the organism), 4 the delay of gratification (control of impulsivity), 4 and mental time travel (memory for past events and plan- ning for future events) 4 and tool making. 1,13 Although the brains of these organisms are structuredof these organisms are struc- tured differently, 4 their intellectual abilities are remarkably similar, 4 thus making the evolution of intelligence in these groups particularly fascinating. The evolution of intelligence in crows and apes can be described as convergent evolu- tion. Convergent evolution is the devel- opment of similar traits in organisms that are not closely related. Although mammals and birds share a common ancestor with all vertebrates, approximately 300 million years separate them from their closest relative, indicating that their advanced cognition must have evolved separately. 4 Currently, there are several hypotheses for the factors behind this convergent evolu- tion. These factors mainly fall under the broad categories of dietary and social. Apes rely on a diet of tropical fruit, and one hypothesis behind their advanced cognition is centered on this diet. Many plants only bear ripe fruit at certain times of the year, and these plants were widely dispersed throughout the habitats of early primates11. Because these primates were often required to travel large distances to forage for food, larger brains and more complex cognition allowed for the pri- mates to travel the most energy-efficient routesw. Corvids, however, do not rely on ripe fruit. Instead, many corvids “cache” food, and cognitive evolution would have aided their common ancestor in remem- bering the location of its caches3. Further- more, corvids such as the Western scrub jay know when the food in their cache is going to spoil and become inedible3. Simi- larly, many corvids steal from the caches of other birds and employ complex strategies to prevent their ownyear, and these plants were widely dispersed throughout the habitats of early primates. 11 Because these primates were often required to travel large FALL 2016 | Berkeley Scientific Journal

Sequence capture of ultraconserved elements from bird museum specimens

New DNA sequencing technologies are allowing researchers to explore the genomes of the millions of natural history specimens collected prior to the molecular era. Yet, we know little about how well specific next-generation sequencing (NGS) techniques work with the degraded DNA typically extracted from museum specimens. Here, we use one type of NGS approach, sequence capture of ultraconserved elements (UCEs), to collect data from bird museum specimens as old as 120years. We targeted 5060 UCE loci in 27 western scrub-jays (Aphelocoma californica) representing three evolutionary lineages that could be species, and we collected an average of 3749 UCE loci containing 4460 single nucleotide polymorphisms (SNPs). Despite older specimens producing fewer and shorter loci in general, we collected thousands of markers from even the oldest specimens. More sequencing reads per individual helped to boost the number of UCE loci we recovered from older specimens, but more sequencing was not as successful at increasing the length of loci. We detected contamination in some samples and determined that contamination was more prevalent in older samples that were subject to less sequencing. For the phylogeny generated from concatenated UCE loci, contamination led to incorrect placement of some individuals. In contrast, a species tree constructed from SNPs called within UCE loci correctly placed individuals into three monophyletic groups, perhaps because of the stricter analytical procedures used for SNP calling. This study and other recent studies on the genomics of museum specimens have profound implications for natural history collections, where millions of older specimens should now be considered genomic resources.

Hint-seeking behaviour of western scrub-jays in a metacognition task.

Metacognitive processes during memory retrieval can be tested by examining whether or not animals can assess their knowledge state when they are faced with a memory test. In a typical foraging task, food is hidden in one of the multiple tubes and the subjects are given an opportunity to check the contents of the tubes before choosing the one that they thought contained food. Following the findings from our previous study that western scrub-jays (Aphelocoma californica) can make prospective metacognition judgements, this study tested the scrub-jays' concurrent metacognition judgements. In a series of experiments, uncertainty about the food location was induced in three ways: by making the baiting process visibly unavailable, by inserting a delay between the baiting and food retrieval, and by moving the location of the bait. The jays looked into the tubes more often during the conditions that were consistent with high uncertainty. In addition, their looking behaviour was associated not with the sight of food but with information about the location of the food. These findings suggest that the jays can differentiate the states of knowing and not knowing about certain information and take appropriate action to complement their missing knowledge.

Sex, estradiol, and spatial memory in a food-caching corvid

Estrogens significantly impact spatial memory function in mammalian species. Songbirds express the estrogen synthetic enzyme aromatase at relatively high levels in the hippocampus and there is evidence from zebra finches that estrogens facilitate performance on spatial learning and/or memory tasks. It is unknown, however, whether estrogens influence hippocampal function in songbirds that naturally exhibit memory-intensive behaviors, such as cache recovery observed in many corvid species. To address this question, we examined the impact of estradiol on spatial memory in non-breeding Western scrub-jays, a species that routinely participates in food caching and retrieval in nature and in captivity. We also asked if there were sex differences in performance or responses to estradiol. Utilizing a combination of an aromatase inhibitor, fadrozole, with estradiol implants, we found that while overall cache recovery rates were unaffected by estradiol, several other indices of spatial memory, including searching efficiency and efficiency to retrieve the first item, were impaired in the presence of estradiol. In addition, males and females differed in some performance measures, although these differences appeared to be a consequence of the nature of the task as neither sex consistently out-performed the other. Overall, our data suggest that a sustained estradiol elevation in a food-caching bird impairs some, but not all, aspects of spatial memory on an innate behavioral task, at times in a sex-specific manner.

WEST NILE VIRUS-RELATED TRENDS IN AVIAN MORTALITY IN CALIFORNIA, USA, 2003-12.

West Nile virus (WNV) is an arbovirus transmitted enzootically by Culex mosquitoes among avian hosts. Since 2000, the California Dead Bird Surveillance Program (DBSP) has tracked avian mortality reported by the public on a telephone hotline and website and measured the prevalence of WNV infection in dead birds. We summarize herein WNV prevalence in dead birds tested and variation of WNV transmission over time and space with the use of DBSP data from 2003 to 2012. Prevalence among dead birds was highest in 2004, 2008, and 2012. This pattern was similar to peak WNV infection years for mosquitoes but not to human WNV incidence. Although American Crows (Corvus brachyrhynchos) were most frequently reported and tested, this species ranked third in infection prevalence (44%) after Yellow-billed Magpies (Pica nuttalli; 62%) and Western Scrub-Jays (Aphelocoma californica; 48%). Overall prevalence in American Robin (Turdus migratorius), House Finch (Haemorhous mexicanus), and House Sparrow (Passer domesticus) carcasses ranged from 18% to 22%. Corvid WNV prevalence was highest in South Coast, Bay/Delta, Sacramento, and San Joaquin valleys, and Klamath/North Coast bioregions, overlapping areas of elevated WNV activity in other surveillance measurements. Bioregional analysis revealed the avian species most likely to be reported and found positive in each bioregion. Our results may be useful to WNV surveillance and control efforts and provide insight into bird population trends in California.

Occurrence of western scrub-jays (Aphelocoma californica) near forest edges in fragmented golden-cheeked warbler (Setophaga chrysoparia) habitat

The western scrub-jay (Aphelocoma californica) is a common nest predator and has been documented depredating nests of the federally endangered golden-cheeked warbler (Setophaga chrysoparia), a woodland songbird, in central Texas. We conducted opportunistic and transect surveys for western scrub-jays across two vegetation classes (woodland and shrub-scrub) to investigate the proximity of scrub-jays to golden-cheeked warblers breeding in a fragmented landscape. We used a chi-square test to compare the number of observed and expected scrub-jay detections for each vegetation class. To investigate if scrub-jays are an edge-occupying species, we compared the distance to nearest vegetation edge of actual scrub-jay detections to a null distribution of mean random distances. We found that scrub-jays occur in areas closer to vegetation class boundaries but do not appear to prefer one vegetation type over the other. Our findings suggest that golden-cheeked warblers may have higher nest predation risk in fragmented areas of their breeding range.

Speciation in Western Scrub-Jays, Haldane's rule, and genetic clines in secondary contact.

BackgroundHaldane’s Rule, the tendency for the heterogametic sex to show reduced fertility in hybrid crosses, can obscure the signal of gene flow in mtDNA between species where females are heterogametic. Therefore, it is important when studying speciation and species limits in female-heterogametic species like birds to assess the signature of gene flow in the nuclear genome as well. We studied introgression of microsatellites and mtDNA across a secondary contact zone between coastal and interior lineages of Western Scrub-Jays (Aphelocoma californica) to test for a signature of Haldane’s Rule: a narrower cline of introgression in mtDNA compared to nuclear markers.ResultsOur initial phylogeographic analysis revealed that there is only one major area of contact between coastal and interior lineages and identified five genetic clusters with strong spatial structuring: Pacific Slope, Interior US, Edwards Plateau (Texas), Northern Mexico, and Southern Mexico. Consistent with predictions from Haldane’s Rule, mtDNA showed a narrower cline than nuclear markers across a transect through the hybrid zone. This result is not being driven by female-biased dispersal because neutral diffusion analysis, which included estimates of sex-specific dispersal rates, also showed less diffusion of mtDNA. Lineage-specific plumage traits were associated with nuclear genetic profiles for individuals in the hybrid zone, indicating that these differences are under genetic control.ConclusionsThis study adds to a growing list of studies that support predictions of Haldane’s Rule using cline analysis of multiple loci of differing inheritance modes, although alternate hypotheses like selection on different mtDNA types cannot be ruled out. That Haldane’s Rule appears to be operating in this system suggests a measure of reproductive isolation between the Pacific Slope and interior lineages. Based on a variety of evidence from the phenotype, ecology, and genetics, we recommend elevating three lineages to species level: A. californica (Pacific Slope); A. woodhouseii (Interior US plus Edwards Plateau plus Northern Mexico); A. sumichrasti (Southern Mexico). The distinctive Edwards Plateau population in Texas, which was monophyletic in mtDNA except for one individual, should be studied in greater detail given habitat threat.

Crouching towhee, hidden scrub-jay: California towhees,Melozone crissalis,attack conspecific mobbing partners while assaulting a western scrub-jay,Aphelocoma californica

We describe an encounter of eight territorial California towhees (Melozone crissalis), alternately engaged in mobbing a western scrub-jay (Aphelocoma californica) and vigorous conspecific attack and display. We additionally characterize a previously unreported crouching posture adopted by the towhees while surrounding the scrub-jay and hypothesize that this posture communicates submissiveness to conspecific owners of a territory. We suggest that this behavioral sequence resulted from a conflict between cooperation among pairs and defense of resources among pairs, wherein behaviors consistent with both were exhibited nearly simultaneously.

Dead heterospecifics as cues of risk in the environment: Does size affect response?

Organisms can minimize their exposure to risk of death or injury by assessing their environment and modifying their behavior accordingly. There is evidence that the current or recent presence of a predator introduces cues to the environment that organisms may use in risk assessment. However, we know little about whether terrestrial organisms use the remains of victims of predation as one such cue of elevated predation risk. A previous study showed that western scrub-jays (Aphelocoma californica) respond both to dead conspecifics and to encounters with a predator with alarm calling and aggregation (cacophonous aggregations), suggesting that they use dead conspecifics as indirect evidence of predation risk. Here we examine whether western scrub-jays also use dead heterospecifics as an indicator of risk. We find that jays respond with cacophonous aggregations to dead sympatric and allopatric jay-size heterospecifics but react weakly if at all to smaller heterospecifics. This suggests that size may be an important factor in determining whether a dead heterospecific is a relevant cue of risk. To our knowledge this is the first controlled experiment showing an animal using the visual cue provided by a dead heterospecific as an indicator of risk and communicating this risk to other conspecifics.

No evidence of temporal preferences in caching by Western scrub-jays (Aphelocoma californica)

Humans and other animals often favour immediate gratification over long-term gain. Primates, including humans, appear more willing to wait for rewards than other animals, such as rats or pigeons. Another group displaying impressive patience are the corvids, which possess large brains and show sophisticated cognitive abilities. Here, we assess intertemporal choice in one corvid species, the Western scrub-jay (Aphelocoma californica). These birds cache food for future consumption and respond flexibly to future needs. Cache-theft and cache-degradation are time-dependent processes in scrub-jay ecology that might necessitate sensitivity to delays between caching and retrieval. We adopt a caching paradigm with delays of up to 49h. Across two experiments we find no evidence of a preference for earlier recovery. We highlight the possibility that, although scrub-jays can discriminate between the present and the future, they may not understand how far into the future an event will occur.

Western scrub-jays allocate longer observation time to more valuable information

When humans mentally reconstruct past events and imagine future scenarios, their subjective experience of mentally time travelling is accompanied by the awareness of doing so. Despite recent popularity of studying episodic memory in animals, such phenomenological consciousness has been extremely difficult to demonstrate without agreed behavioural markers of consciousness in non-linguistic subjects. We presented western scrub-jays (Aphelocoma californica) with a task requiring them to allocate observing time between two peepholes to see food being hidden in either of two compartments, one where observing the hiding location was necessary to later relocate the food, and another where food could easily be found without watching. Jays first separately experienced these consequences of possessing information in each compartment and subsequently, once given a choice, made more looks and spent more time looking into the compartment where information was necessary than into the compartment where it was unnecessary. Thus, the jays can collect information to solve a future problem. Moreover, they can differentiate sources of information according to their potential value and modify behaviour to efficiently collect important, usable information. This is the first evidence of metacognition in a species that passes the behavioural criteria for both retrospective and prospective mental time travel.