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Research Highlights from the Martin Lab

PNAS cover Derek Zaraza

Economic Development intensifies Competition for Cities

Cities are poor quality habitats for most species, and yet if we drive downtown in any city, we will see a few species that thrive. In a study of almost 300 species of birds across 260 large cities worldwide, we found evidence that direct competition - where birds fight over resources - determines which city-loving species persist in cities, and which do not. Specifically, the subordinate species - the species that lose most fights for resources - were missing or rare in cities when closely-related dominant species were already there. But when the subordinate species occurred in regions without their dominant nemesis, subordinates thrived in cities. Remarkably, these competitive effects among urban-adapted species depended on the level of economic development of the country. In economically developing countries, dominant and subordinate species lived side-by-side in cities, but in economically-developed counties, subordinates were rare or absent from cities whenever the dominant species was present. How economic development alters the consequences of  competitive interactions remains a mystery, but possible explanations include differences in the distribution of resources, where resources in cities in developing countries may be more accessible to subordinate species, allowing them to persist. Another possible explanation is that death rates of dominant species may be higher in developing cities, opening the door for subordinates to enter. This work was a collaboration with Fran Bonier (Queen's University) and was possible thanks to the participation of over 600 birders and ornithologists from around the world who generously shared their expertise on the breeding birds of cities.
(Proceedings of the National Academy of Sciences, USA, 2018; cover photo by Derek Zaraza)

Links: pdf 

Crimson-mantled Woodpecker

Color Pattern Evolution Among Coexisting Birds

Birds come in many colors and patterns, even when species are closely related. When these closely related species overlap their geographic ranges, we might expect that they would have similar colour patterns if colour patterns are an important adaptation to their shared environment. Alternatively, closely related species that live together might evolve to be very different in their colour patterns, if different colour patterns are important to reduce the chances of hybridization, or other costly interactions. In this study, we tested among these alternative ideas across a diversity of birds worldwide. We found a surprising pattern: closely related species with intermediate levels of geographic range overlap showed more divergent color patterns relative to both species that did not overlap their ranges at all, and species that completely overlapped their ranges. Geographic range overlap typically increases over time, suggesting a dynamic pattern of colour pattern divergence, followed by convergence, as closely related species increase the overlap of their geographic ranges. This work was done in collaboration with Bob Montgomerie and Steve Lougheed, also here at Queen's.
(American Naturalist, 2015)

Links: pdf 

Andean Emerald, western Ecuador

When David Beats Goliath

Larger animals usually win aggressive contests for food, shelter and other resources, and this ecological "rule" influences where smaller, subordinate species live in nature. And yet, occasionally, smaller species can break the rule, overcome the disadvantage of small size, and prevail over larger species in aggressive contests. We investigated when and why smaller species occasionally prevail using a dataset of over 23,000 interactions involving three different groups of birds that commonly fight over food: vultures feeding on carrion, hummingbirds feeding on nectar, and woodcreepers and antbirds feeding on prey flushed by army ants. While larger species usually dominated, we found that smaller species were more likely to win when they competed with more distantly related species. The reason? Some smaller species evolve traits (like weapons or behaviours) that can help them overcome the disadvantage of small size, and some larger species evolve adaptations (like long-distance migration) that compromise their abilities to compete aggressively. These results suggest that the "larger animal wins" rule that usually governs species interactions, and often influences where smaller species can live, is more likely to break down as species diverge over evolutionary time. This work was done in collaboration with
Cameron Ghalambor (Colorado State University).
(PLOS ONE, 2014)

Links: pdf   featured in Inside Science

Purple Sandpiper, Wolfe Island, Ontario

Dominant and Subordinate Bird Species Differ in Diverse Ecological Traits

Closely related species often interact aggressively, with one species behaviorally dominant to the other. If asymmetric interactions among closely related species are an important selective pressure, then we may expect the position of a species within a social hierarchy to vary with diverse ecological traits. Indeed, subordinate species of North American birds arrive on their breeding grounds and initiate breeding later, have lower annual survival rates, lay relatively heavier eggs, and migrate further than closely related dominant species (in the same genus), controlling for the effects of both evolutionary relatedness (phylogeny) and body size. These consistent differences between dominant and subordinate species could result from direct interactions between species (e.g., dominant species exclude subordinate species from preferred habitats), or from correlations among traits that are associated with behavioural dominance (e.g., correlations with metabolic rate or testosterone). This work was Cameron Freshwater's honours thesis project in our lab (Cam is now a graduate student at the University of Victoria) and was done in collaboration with Cameron Ghalambor at Colorado State University.
(Ecology, 2014)

Links: pdf 

Swamp Sparrow, Lake Opinicon, Ontario

Virtuous Sparrows of the Highlands

Many animals, from humans to birds, are promiscuous—they mate outside of their social pair—but levels of promiscuity vary markedly across species and populations. Why species and populations vary in their levels of promiscuity is poorly understood, but a clue comes from broad geographic trends. Our recent work explores these trends across sparrows, documenting not only high promiscuity at higher latitudes (a pattern previously documented for birds) but also lower promiscuity at higher elevations, a pattern that had not previously been demonstrated across species. High latitudes and elevations share at least one thing in common: breeding seasons are highly synchronous, and synchronicity is thought to facilitate promiscuity through increased opportunity. But evidence suggests that high elevations may also require something quite different that trumps opportunity, specifically help from dads in caring for young. With the need for good fathers at high elevations comes virtue: females can attract paternal help by providing confidence of paternity. Alternative hypotheses to explain the elevational and latitudinal patterns have not yet been rejected, but these geographic patterns suggest that when fathers are important for raising young, virtue becomes the norm. This work was done in collaboration with 
Fran Bonier (Queen’s University), Cas Eikenaar (Institute of Avian Research, Germany), and Ignacio Moore (Virginia Tech).
(American Naturalist, 2014)

Links: pdf  featured in Science

two colour morphs of nestling Yellow Warblers

Colour Variation in Nestling Yellow Warblers

Nestling Yellow Warblers come in two colours: yellow and white. For years, scientists had thought the two colours corresponded to sex, with yellow males and white females. We tested this idea using spectrometry measures of colour and genetic sexing of nestlings and found no support — male and female nestlings could be white or yellow. So what, if anything, do the distinct colours of nestlings signify? Our most promising idea is that they correspond two distinct adult colour morphs that have been described in Yellow Warblers — a dull morph that is associated with attentive dads that feed their kids at high rates, and a bright morph associated with poor dads who are more attractive to neighbouring females with a wandering eye. This work was led by graduate student Vanya Rohwer, who also took the photograph on the left. (Condor, 2012)

Links: pdf

records of Yellow-nosed Albatross in North America

Yellow-nosed Albatross strays to Kingston, Ontario

The Yellow-nosed Albatross in Kingston represented the first record of an albatross in Ontario and on the Great Lakes. The adult female was over 8,000 km away from her normal distribution in the southern hemisphere. We documented this record, and reviewed all cases of Yellow-nosed Albatross in North America. Yellow-nosed Albatross have been documented in North America on 47 occasions, exclusively along the Atlantic Coast from the Gulf of Mexico to the Gulf of St. Lawrence. Unlike most vagrant seabirds, vagrant Yellow-nosed Albatross in North America often approach land and appear to be searching out potential nest sites. Birds are often seen from shore and have been documented flying back and forth along shorelines, roosting on beaches, and lingering around other seabird colonies. Most records of Yellow-nosed Albatross represent the Atlantic race; however, two Texas records represent the Indian Ocean race ("Indian" Yellow-nosed Albatross) that breeds in the Indian and Pacific oceans. Records of Yellow-nosed Albatross in North America have increased since the late 1990's, which may reflect more bird watchers along the Atlantic Coast, or an increase in vagrancy associated with changes in fish stocks and climate. (Ontario Birds, 2011)

Links: pdf

Rufous-collared Sparrow, Papallacta, Ecuador

Preference for Local Songs in a Tropical Sparrow

How many species of birds live in the tropics? This straightforward question is more difficult to answer than you might think. The answer depends on when geographically isolated (allopatric) populations evolve reproductive isolation, and thus become distinct species. In collaboration with researchers at Virginia Tech University, we found evidence that Andean bird populations may be diverging over very short distances with respect to traits important in the formation of new species. Collaborator Julie Danner presented female and male Rufous-collared Sparrows with songs of males from populations located between 25 and 4,000 km away. Remarkably, females showed little interest in songs of males from only 25 km away, while males showed only modest declines in their aggressive responses to songs from increasing distances. Given that females use male song to select mates, the lack of response of females to male song from only 25 km away suggests that these populations are on their way to becoming new and distinct species. This work was led by Julie Danner - Julie was a PhD student in Ignacio Moore's lab at Virginia Tech. (American Naturalist, 2011)

Links: pdf  New York Times article

Viridian Metaltail, recently fledged, Papallacta, Ecuador

Breeding Biology of High Andean Birds in Ecuador

We still know little about the biology of most tropical birds. We collaborated with biologists in Ecuador and the United States to provide details of the breeding biology of 76 species of birds that breed in the high Andes of Ecuador above 2,700 m, including 13 species of hummingbirds. The work was based on over 300 observations of breeding, and included the first descriptions of the nests of two species of birds (Plain-capped Ground-Tyrant and Chestnut-winged Cinclodes). This work was led by Harold Greeney at the Yanayacu Biological Station in Cosanga, Ecuador. (Bulletin of the British Ornithologists' Club, 2011)

Links: pdf

Black-throated Green Warbler, Lake Opinicon, Ontario

Rapid Evolution of Colour Patterns in High Latitude Birds

Rates of evolution in birds are believed to vary with latitude, but not in the way that you might expect. We provide evidence that the rates of evolution of distinct colour patterns of birds are accelerated at higher latitudes compared to the tropics, opposite the global patterns of species richness where the tropics are most diverse. The cause of this rapid evolution at higher latitudes? Rapid shifting of ranges through glacial cycles that allow closely-related species that were once isolated to overlap each other's ranges. Once closely-related species coexist with each other, they either (i) hybridize, reducing the number of weakly-differentiated birds at higher latitudes, or (ii) persist together with a strong potential for interaction with each other, accelerating each other's rates of evolution. These simple consequences of rapid range shifting at high latitudes can create some of the striking colour patterns we see in high latitude birds, such as the Chestnut-sided Warbler and White-headed Woodpecker. (Evolution, 2010)

Links: pdf

spatial asynchrony in the seasonality of solar radiation

The Asynchrony of Tropical Seasons and the Formation of New Species

Rates of species formation are generally believed to be highest in the tropics, but the reasons for high tropical speciation rates are not clear. We presented evidence for a new hypothesis that could potentially explain higher rates of species formation in the tropics. The idea centers on the spatial asynchrony of seasons, and adaptations in the timing of breeding, growth, dormancy, and other life history events in organisms. At high latitudes, seasonal variation in life history events are synchronous across broad regions, coinciding with the spring, summer, fall and winter and driven by variation in temperature. In the tropics, temperature varies little through the year, and seasons are more frequently defined by changes in precipitation that vary geographically depending on mountain ranges and patterns of airflow. In the tropics, seasons are more often spatially asynchronous  the seasons differ in their timing between locations  and this asynchrony can isolate populations from each other, promoting the formation of new species. This "Asynchrony of Seasons Hypothesis" has not yet been tested, but some evidence to support its role in isolating populations comes from birds in the Ecuadorian Andes. (Ideas in Ecology and Evolution, 2009)

Links: pdf

Tree Swallow, photo by P-G Bentz

Stress Hormones and Conservation

Stress hormone levels are often used in conservation as an indicator of populations in trouble. High levels of stress hormones (corticosteroids) are believed to occur in individuals and populations experiencing challenging conditions, including those caused by detrimental human activities (e.g., habitat degradation, pollution). We reviewed the evidence for this perceived link between high stress hormone levels and individual/ population success across all vertebrates and found that this assumption is not always true. In fact, stress hormones play many roles in the bodies of vertebrates, sometimes occurring at high levels in the healthiest individuals and populations. We expect our results to change the way conservation biologists interpret stress hormone levels in the future. This work was led by Dr. Frances Bonier. Photo by P-G Bentz. (Trends in Ecology and Evolution, 2009)  

Links: pdf

Ontario Birds, April 2009, painting by Barry Kent MacKay

Population Densities of Golden-winged Warblers

Global populations of Golden-winged Warblers are in decline. The decline has sparked a great deal of research on this species by Raleigh Robertson at the Queen's University Biological Station (QUBS) over the past 10 years. This past year, we collaborated with Raleigh and Rachel Vallender (Cornell University) to provide the first ever estimated densities of Golden-winged Warblers, Blue-winged Warblers, and their hybrids on the three main tracts of land at QUBS. We estimated populations in the area at about 200 breeding pairs, and banded and mapped 30 male Golden-winged Warblers, one male Blue-winged Warbler, and 3 male hybrids (all "Brewster's") on our intensive study plots. We will revisit these same plots in 5-10 years to measure changes in population sizes and proportion of hybrids. This work was led by two Queen's undergraduate students, Laura King and Virginia Emery(Ontario Birds, 2009) 

Links: pdf

Brown-bellied Swallow, Papallacta, Ecuador

Blood Parasites in Andean Birds

Blood parasites, like the disease malaria, are found in many species of birds, but we know very little about their prevalence in the tropics. We examined blood from a number of species of birds occurring in the Ecuadorian Andes, documenting some of the first blood parasite infections for a number of species. We also found blood parasites in young nestlings. Infections take time to develop, and these results suggest that some blood parasites may be transferred from mother to offspring through the egg itself! We will conduct further work to confirm if this is indeed a mode of disease transmission. This work was led by Queen's undergraduate student Hannah Munro. (Ornitologia Neotropical, 2009) 

Links: pdf

Glossy Flowerpiercer at sap well, Papallacta, Ecuador

Sap-well Use and Maintenance in a Tanager

We described the first record of sap-well use and maintenance in a tanager, based on observations of a Glossy Flowerpiercer on the east slope of the Andes in Ecuador. Sap-well use is well known in the sapsuckers and in some other woodpeckers, but is otherwise rare in birds. Only four non-woodpeckers have been observed to maintain sap-wells: a strange New Zealand parrot (the Kaka), a species of Hawaiian Honeycreeper (the Akiapolaau), Indian Ocean white-eyes (Zosterops), and now, the Glossy Flowerpiercer. Flowerpiercers usually steal nectar from flowers by piercing the base of the flower using their hooked upper mandible to hold the flower, their sharp lower mandible to pierce it, and their paint-brush-like tongues to lick the nectar. Like many flowerpiercers, Glossy Flowerpiercers steal nectar and eat fruit, but are unique in using their specialized bill and tongue for sap. (Wilson Journal of Ornithology, 2009)  

Links: pdf

nestling Yellow Warbler, Chaffey's Lock, Ontario

Begging Kids and Stress Hormone Levels

Stress hormones (corticosteroids) are secreted in response to environmental challenges or stressful conditions. When a bird or other vertebrate encounters a severe storm, drought, predation attempt, or disease, they secrete stress hormones that promote a diversity of responses in the organism. In our work on Tree Swallows (led by Dr. Frances Bonier), we showed that stress hormones are also secreted in response to the peak demands of nestlings in the nest. Thus, hungry nestlings elicit the same kind of physiological response as bad weather or other challenge facing the swallows, prompting them to reallocate their resources towards provisioning their brood. (General and Comparative Physiology, 2009)  

Links: pdf 

Tawny Antpitta, Papallacta Pass, Ecuador

The Breeding Biology of Antpittas

We summarize the breeding biology for two genera of Neotropical antpittas – understory birds that are notoriously shy and secretive. One species is so secretive that it went undescribed by scientists until 1999, despite occurring at a birding lodge with a history of ornithological work! Nests for over half of the 39 species are still unknown. This work was led by Harold Greeney at the Yanayacu Biological Station in Cosanga, Ecuador. (Journal of Field Ornithology, 2008)  

Links: pdf

Nestling Agile Tit-Tyrant, Papallacta, Ecuador

New Nests of Tropical Andean Birds

We described the first nests known to science for two Andean species: the Agile Tit-Tyrant (Uromyias agilis), a small, uncommon flycatcher with a fondness for bamboo, and the Spectacled Whitestart (Myioborus melanocephalus), a stunning wood warbler that flashes its white outer tail feathers to scare insects from leaves in montane forests. (Ornitologia Neotropical, 2008)  

Links: Uromyias pdf
Myioborus pdf

White-crowned Sparrow, Chaffey's Lock, Ontario

Mother Birds Manipulate the Sex of Their Offspring

Mother birds can manipulate the sex of their offspring using changes in corticosterone – a hormone secreted in response to stressful conditions. Higher corticosterone levels lead to more daughters, which are a safer investment because all females breed each year. In contrast, poor quality males often remain unpaired and may not breed – quite a gamble when environmental conditions are stressful. This work was led by Dr. Frances Bonier. (Behavioral Ecology, 2007)  

Links: pdf

Sparkling Violetear near Quito, Ecuador

Coping with Life in the City

Urbanization dramatically changes the composition and diversity of animal and plant communities. The characteristics distinguishing species that persist in urban environments, however, are poorly understood. In this study, we found that  species of bird able to cope with urban environments have broader environmental tolerances compared with closely-related species. This pattern is consistent across Europe, Asia, Africa, Australia, and North and South Americas. Our results suggest that broad environmental tolerance may predispose some birds to thrive in urban habitats. This work was led by Dr. Frances Bonier. (Biology Letters, 2007)  

Links: pdf
Sciencentral News Feature (video)

swallowtail butterflies, Mindo, Ecuador

Narrow Thermal Tolerance of Tropical Insects

The impact of climate change on terrestrial organisms is often predicted to be greatest in regions that are warming the fastest - typically regions occurring at higher latitudes. Yet the impact of rising temperatures also depends on the sensitivity of organisms to temperature change. In this study, we review evidence that tropical insects and "cold-blooded" vertebrates (such as lizards and turtles) show very little tolerance to warming temperatures. The narrow thermal tolerances of these tropical organisms may amplify the impacts of climate warming on tropical species, potentially placing the majority of the earth's biodiversity at risk. This work was led by Curtis Deutsch and Josh Tewksbury. (Proceedings of the National Academy of Sciences USA, 2008)

Links: pdf
BBC World News article

Mourning Dove, Chaffey's Lock, Ontario

Subspecies Diversification in Birds

Patterns of evolution are believed to vary with latitude, but our understanding of this variation remains limited. In this work, we found that subspecies of birds occur more frequently at lower latitudes within the distributions of species in almost all regions on earth. Subspecies represent the early stages of species formation, and thus these results suggest that more species are currently being formed at tropical latitudes within species. (Evolution, 2008)  

Links: pdf

The Natural History Museum, London

Mechanistic Causes of Latitudinal Variation in Diversity

Biodiversity increases dramatically from the poles to the equator. From a mechanistic perspective, abiotic factors produce the gradient in diversity by creating latitudinal variation in rates of formation of new taxa, extinction, immigration and/or emigration, the latter two processes resulting from range expansion, contraction and shifting. In this study, we tested the contributions of all four possible mechanisms underlying a present day latitudinal gradient in the diversity of orders of marine invertebrates with good fossil histories. In these orders, high tropical biodiversity was caused by higher rates of formation of new taxa in the tropics, followed by the expansion of these new taxa into other tropical regions. Extinction rates were highest in the tropics, and thus extinction reduced tropical diversity relative to higher latitudes. (Journal of Evolutionary Biology, 2007) (photo: The Natural History Museum, London)

Links: pdf

north slope of Alaska, near Toolik Lake

Costs, Constraints, and Trade-offs in Young Arctic Birds 

Many young arctic birds are confronted by a challenging task: they must change their feathers (moult) and accumulate fat stores for the autumn migration before climatic conditions deteriorate. We used field studies from northern Alaska coupled with controlled aviary experiments to show significant costs to moulting body feathers. These costs of moulting feathers result in an allocational tradeoff between moult and fat accumulation, caused by a fundamental limitation of food for juvenile arctic sparrows. (Ecology, 2007)  

Links: pdf

White-crowned Sparrow, San Francisco, California

Sex-specific Costs of Life in the City

The vast majority of species are excluded from human-dominated landscapes, but some species persist and appear to thrive. Stress hormones (corticosteroids) may play a significant role in enabling an animal to cope with urban breeding habitat because they help mediate physiological and behavioral responses to urban challenges. In our study, male but not female sparrows had higher levels of corticosteroids in urban compared with rural habitats. In contrast, female but not male sparrows living in urban environments had low reproductive success when they had high levels of stress hormones. The results illustrate sex-specific differences in corticosteroid secretion and associated costs between urban and rural habitats. This work was led by Dr. Frances Bonier. (photo: F. Bonier) (Behavioral Ecology, 2007)  

Links: pdf

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