A thin skin is key to a successful invasion for cane toads

Blog written by Georgia Kosmala, Gregory Brown, Richard Shine & Keith Christian. Read the full paper here. You might also enjoy the ‘sequel’ published here. Photo of cane toad by Richard Shine.

Cane toads are one of the most infamous amphibian invaders in the world, having been translocated from their native range in South America to many countries including Australia. The toads have been an ecological catastrophe for some Australian wildlife, but have provided an amazing study system for researchers. The species’ global invasion success has been extensively studied by multidisciplinary groups in a number of countries. That’s because the toads have exhibited an ability to change very rapidly to adapt to the new challenges they have encountered. The mechanisms involved in their success involve multiple aspects of biology – physiology, biochemistry, behaviour, ecology – and those elements combine and interact in subtle ways as to allow the survival of cane toads in locations that are very different from each other, and in some cases very different from the conditions under which the species evolved.

Physiological aspects are crucial, because the response to environmental stress triggers rapid adaptive physiological responses. In amphibians, the hydric balance response is especially critical because of the highly permeable skin, which plays a role not only in the movement of water, but also in the gas exchange (a large part of gas exchange in amphibians happens through cutaneous respiration). When an amphibian is placed in a novel environment, where local conditions of moisture and temperature are very different from the ones in its original environment, it must adapt to these new conditions to ensure survival. From an individual’s point, it’ll need an immediate response to each new challenge – and in a broader ecological sense, those responses need to be heritable to new generations so that they persist, enabling survival of the species in the novel location.

Many studies have assessed the skin permeability of amphibians in their natural habitats, in controlled experimental conditions and comparing different species. Those studies have established interspecific patterns of physiological response to environmental stress. Our new study takes this a step further, by comparing populations of the species in countries with very different environmental characteristics. We can ask how an invader rapidly changes its physiology to successfully invade such habitats.

In its original environment, where temperatures are comfortably warm and moisture is constant, there’s little need for a cane toad to be able to resist water loss: the risk of reaching fatal levels of dehydration is low. However, because of such low skin resistance to water loss, a toad in its native range must be able to regain water very quickly. For the populations that we studied in Hawai’i, one of the first locations where the species has been introduced outside of Central and South America, there’s much more variability in temperature and rainfall. We found that skin resistance to water loss was already greater than in the native range, although rehydration capacity was low. Interestingly, the cane toads in Hawai’i are highly associated with anthropogenically disturbed areas like golf courses, where mechanical irrigation and urban shelter is readily available.

The most significant change that we recorded occurred in animals from the Australian introduction. Skin resistance to water flow has increased greatly, as the animals are now exposed to a much harsher climate – temperatures reach much higher values, and seasonal drought is now a challenge they must face. The Australian animals are not as quick at rehydrating, perhaps because water bodies are less abundant, meaning it becomes more important to keep in the water you have, as you won’t be able to gain more water any time soon. Toad physiology is very variable within Australia, and further studies will be needed to clarify the delicate balance between environmental conditions, physiological adaptation, and behavioural modulation needed to colonize such a diverse range of habitats.

Mitochondrial Diversity Offers Insight on Invasive European Starling Populations Worldwide

Blog written by Julia Zichello and Louise Bodt. Read the full manuscript here.

The European starling is one of the most wide-spread and successful invasive avian species in the world. Their native range extends across Europe and into Western Asia. Since the mid-1800’s, there have been multiple deliberate introductions of European starlings outside of their native range. Today, there are populations of starlings on every continent except Antarctica. Starlings are aggressive birds which travel sometimes in massive undulating flocks called murmurations. These birds are ubiquitous, industrious and downright hated. They destroy agricultural crops, spread diseases to livestock, fly into aircrafts and outcompete native birds. And yet, their outsized ability to establish and expand in novel environments, cannot — from an ecological or evolutionary perspective — be ignored.

Although there has been research investigating some of these invasive populations, our new dataset from North American starlings, combined with existing datasets from Australia, South Africa and the UK, allows us to compare mitochondrial diversity of starling populations across multiple continental distributions.

The story of the European starling in North America starts in 1890. Approximately 100 birds were brought to New York City’s Central Park between 1890 and 1891 by Eugene Schieffelin. This was part of an initiative by the American Acclimatization Society to bring all birds mentioned in Shakespeare to the US. The starling is mentioned only once in Shakespeare’s Henry IV. And over the last 130 years the starling population in North America has exceeded 200 million, over one-third of the global population. Several other introductions of starlings occurred in Australia and New Zealand in the mid-1800’s, in South Africa in the late 1800’s and in Venezuela and Argentina in the mid- to late-1900’s. These populations persist today and some continue to expand. These misguided introductions were undoubtedly ecologically destructive, and yet because of the scale, persistence, and repeatability they demonstrate, there is certainly a great deal to learn from these unfortunate experiments.

Starling specimens (Denis Finnin)

            Here, we have presented the most geographically widespread analysis of starling population genetics to date. Our sampling from the United States (tissue samples provided from the USDA) combined with the existing datasets from Australia and South Africa and the native range allow us to compare genetic diversity and population dynamics among continents. We found that the US population shows signs that it is currently expanding, but does not show signs of any population structure. The lack of population structure could be due to the flexible patterns of seasonal migration that are exhibited in the North American population.

            Additionally, the three invasive populations share only one mitochondrial haplotype with each other (see Venn diagram). This is consistent with three independent sub-samples of the mitochondrial diversity of the original native range. We also found that the mitochondrial diversity of the invasive populations in Australia, South Africa and the US are lower than that of the native range, as expected due to founder effects. However, this contributes to a broader understanding of how low genetic diversity is sometimes not an obstacle for evolutionary success (as has often been thought). Instead, perhaps behavioral and ecological plasticity are more primary factors in a species’ successful establishment in a new environment.

Invasive species offer a window into evolutionary processes over short timescales. The starling shows what can happen when a species is introduced to contrasting environments and independent populations are established from different founders. Because European starling invasions span multiple continents, comparisons of these populations can inform how subtle differences in founder populations and expansion rates affect present day patterns of diversity. The climatic variation across the different invasive regions here also provides another powerful variable to explore. Furthermore, studying a species with such a wide distribution across heterogenous environments (both ecologically and politically) has implications for conservation and invasive species management.

            Birdwatchers leave them off their lists, ornithologists and farmers scoff at them and they present intricate and costly ecological challenges wherever they go. But they are — for better or worse— here, there and almost everywhere. Our paper represents intriguing insights into what the multiple European starling invasions across the world reveal about evolution and adaptive changes, and we will be engaging in future research on this unique, troublesome and complex avian system. Because, what is it about European starlings that made them such successful invaders again and again and again? That, is the question. 

Is Smart Sexy? Testing female preferences for problem-solving males in zebra finches

Blog written by Clara Howell. Read the full paper here.

A huge and diverse taxonomic group of birds, from temperate crows to tropical birds-of-paradise, learn their songs by imitating adults of their species that they hear when young. Understanding the complicated genetic and cultural evolution of song is interesting not just in its own right, but also as a window into the mechanisms by which communication systems arise and persist. A large part of understanding how this occurs is learning what kind of information is exchanged via song, and how that information benefits both senders and receivers in order to make it a communication system worth investing in. We have known for many years, for instance, that male song can tell a female a lot about a male’s species, location, and willingness to mate. But with playback experiments, we are just beginning to understand the incredible nuance of song. Females of many species respond differently to songs that vary in geographic origin, age, and developmental conditions of the singer. These sorts of experiments indicate that a female is not only able to use song to find a mate of the right species, but also one from the same area, of the ideal age, and who had a healthy development.

The inspiration for our present study came from a larger body of research investigating the ways in which song—because it is learned during a sensitive period of development and vulnerable to disruption—can signal past developmental stress and allow females to choose healthier mates. In addition to song from developmentally robust males, female songbirds of many species are also known to prefer longer and more complex song, or in species in which males sing multiple song types, a larger repertoire. A 2008 study by Boogert and colleagues found a positive correlation between learning ability in zebra finch males and the complexity of their song, which neatly connected two related theories of bird song—that song serves as a signal of healthy brain development, and that females have sensory preferences that lead to the evolution of more complex song. If song complexity and brain function are connected in males, it could explain why female preference for less monotonous song have persisted—because only males with well-functioning brains can learn and produce complex song, and those well-functioning brains also help take care of more offspring.

As elegant as the theory was, it quickly fell apart. Not only were many “preferred” features of song found to have null or even inverse correlations with the time it took males to learn cognitive tasks, the entire concept of a general cognitive ability in birds also had mounting evidence against it. But we were still interested in the connection between brain function and song, despite the complicated and conflicting evidence for it. Maybe it is too broad to say that song complexity = general cognitive ability, but is it possible that song still contains information about some cognitive abilities? And is it possible that if that information is there, it is encoded in a way that does not map perfectly onto the ways that we as researchers often define song complexity, as numbers of motifs and unique notes?

We decided to test not whether song attractiveness was correlated with general cognitive abilities, but whether song attractiveness was correlated with performance on a specific task we thought most likely to affect parental care: the ability to gather food from a new source. And instead of measuring song complexity by looking at spectrograms and visually categorizing complexity, we decided to present the songs to a set of females to see whether they could determine a difference between high performers and low performers when given only their song.

We used zebra finches as our test subjects because this species had been used in many of the original studies looking at this topic. First we tested male learning ability in their “novel foraging” task—how quickly they would be able to learn to flip an object covering a food reward. We tested a large cohort of males and found two distinctive groups on either end of the spectrum—those who breezed through the task in the minimum number of trials, and those who were unable to learn even after weeks of prompting. Six males were selected from each group and their song recorded, which was then made into pairs of “quick-solver” and “non-solver” songs to present to females. It was critical that the females not know the males—we didn’t want them using song to identify a male that they knew already knew to be particularly attractive or unattractive. We instead used fifteen naïve females who had never been housed with the males in question, and thus could assess the males using only their song.

Examples of solver song (top) vs non-solver song (bottom)

We then tested females on multiple pairs of quick-solver vs. non-solver song. We did this by installing two perches in each female’s home cage that could trigger playback of a song when hopped on, and thus measure a female’s preference through number of hops. To ensure that females understood the perches and were triggering favored songs, we first compared female responses to the songs of zebra finches versus rufous-collared sparrow, knowing that they would prefer song from their own species. When females demonstrated proficiency with the perches, we moved on to quick-solver vs. non-solver. Remarkably—because there was no discernable difference between song types to us—we found that over thousands of hops, females were preferring quick-solver over non-solver songs about 60% of the time. To put this in context, they preferred zebra finch vs. sparrow song 70% of the time. We analyzed our data using three statistical approaches: (1) with a non-parametric Wilcoxon sign-rank test, which essentially determined whether there were more deviations from the null preference than you would expect, (2) with a mixed effects linear model, which also determined whether female preference deviated from the null and whether factors such as order of presentation, specific female, or specific stimulus song had any effect on the findings, and (3) with a hierarchical Bayesian model, which modeled a population-wide preference given individual female preferences for quick-solver songs. In each model, we found a significant (or in the case of the Bayesian model, non-overlapping credible intervals) result: females preferred the quick-solver song in every pair of stimulus songs.

This is an exciting finding because the females knew absolutely nothing about the males, yet were still more interested in the song of a male who had quickly performed a cognitive task over one who was never able to figure it out. There have recently been a few studies showing that females prefer “smarter” males when observing them figure out tasks, and our results added a new dimension: females were preferring the males who solved the task, and they were able to make that distinction based on song alone. Song, in other words, can contain information about problem-solving ability in addition to everything else we already know it encodes. It’s a remarkable communication system, from the males who are able to so accurately advertise various aspects of their brain and behavior, to the females who are so accurately able to decode it. And while there is still a lot more to understand about problem-solving ability and song, this finding indicated to us that while there might not be a straightforward connection between song complexity, female preference, and male brain function, this is still a rich area for further study and a valuable insight into how communication systems arise and persist.  

Skull shape in an endangered marsupial: would northern quolls rather ship out than shape up?

Blog written by Pietro Viacava & Vera Weisbecker. Read the full paper here. Featured image: scientific illustration by Nellie Pease.

When a species is threatened by habitat loss and environmental change, it is important to understand how to best preserve its populations. This cannot be done without a solid understanding of how diverse populations are. For example, if each population is unique, it is best to manage separate conservation units. Conversely, if they are all similar, then individuals from one population can boost the numbers of other, smaller populations without losing much of the species diversity. These conservation management decisions are mostly based on the genetic diversity of populations. However, the genetic patterns used for current conservation aims do not necessarily capture the variation in form (“morphology”). Because genetic and form diversity are not necessarily the same thing, adaptations that might be essential for the survival of a morphologically distinct population might be ignored.

In Australia, marsupials (“pouched” mammals, most famously the kangaroos and koalas) are of particular conservation concern, leading the world in mammal extinctions. Members of this fascinating group give birth at very early developmental stages. Their neonates – called “pouch young” – need to climb towards the pouch and attach to the teat of their mother with strongly developed forelimbs and snouts. To survive their suckling phase, the oral apparatus needs to maintain a certain shape. It has long been suspected that this requirement might also reduce the ability of marsupials to adapt to changing environments, even in the presence of substantial genetic diversity.

We tested this suspicion using a threatened and particularly wide-ranging species of marsupial, the northern quoll. These marsupial carnivores are opportunistic foragers the size of a guinea pig. They are also the largest semelparous animal, where nearly all males die off in their first year after an intense breeding season. Until European invasion and possibly even well before, their distribution ranged across 5000 kilometres of the Northern Australian coast: from the western arid environments of the Pilbara to the humidity of the eastern tropical rainforests. Nowadays, its fragmented distribution consists of four genetically distinct mainland populations and several islands. A perfect scenario to test if these populations show matching morphological differences!

We scanned specimens from museum collections and specimens collected by the Wilson Lab from the field in Groote Eylandt.

We travelled to six museum collections in Australia and North America using a 3D surface scanner to digitally acquire the shape of 101 skulls. We covered these 3D skulls with a dense set of 900 reference points. This allowed us to test for size and shape variation among and within the four mainland populations and one island population, and additionally assess if we could discern morphological adaptations to local climatic conditions.

This portable 3D surface scanner travelled with us to the museum collections.

Unexpectedly, we found that there is little population structure in their skull shape variation and no strong evidence of discrete “morphotypes” according to either population or climate. However, we did observe that size is the strongest contributor to shape variation: smaller individuals tend to present proportionally larger braincases and narrower, less pronounced cheekbones, while larger individuals tended to have proportionally smaller braincases and wider cheekbones that are more pronounced. This results in some small variation between populations because, on average, Northern Territory and Queensland animals are bigger; Kimberley, Groote and Pilbara are smaller. However, because there were no other strong determinants of shape, similarly sized individuals even from distant populations mostly share the same shape.

Shape variation due to size variation (allometry). Spheres represent the reference points (landmarks). Vectors in black show the magnitude and direction of variation from small to big specimens. Most of the allometric shape variation concentrates on the braincase and the zygomatic arches. For example, bigger skulls display proportionally smaller braincases.

We were surprised by the lack of shape differentiation across the extensive distribution of northern quolls, particularly because other species of vertebrates with similar breaks in their distributions tend to show genetic and morphological differences. For example, other marsupials such as wallabies and kangaroos, but also other vertebrates such as lizards, amphibians and birds, reveal distinctions of lineages at the corresponding northern quoll population breaks. Thus, we asked: is there something that is holding the northern quolls back?

It is very possible that northern quoll skulls are just the perfect match for multiple situations and prey types. This “one-shape-fits-all” situation would mean that, depending on the size, the corresponding shape is well adapted to match a range of environmental scenarios and related prey items. Thus, short and rapid modifications of their environment may not require them to “shape up”.

On the other hand, the combination of a substantial effect of size and lack of strong environmental influences might also mean that northern quolls are simply not very adaptable beyond a very narrow, growth-related line of shape variation. One would expect this if a developmental constraint, arising from the need for a strongly developed oral apparatus at birth, prevented the northern quolls from adapting their shape.

There are some intriguing lessons for the diversity and conservation of northern quolls in our study. Firstly, based on our morphological results on the skull, similarly sized individuals from any population share the same shape; therefore, no adaptive variation would be lost in eventual population translocations. Secondly, distinguishing between a comfortable “one shape fits all” scenario and a scenario where northern quolls are incapable of adapting, is crucial for future research. If marsupial carnivores are locked into a particular shape, then they will need far more help to survive environmental change than we might expect. Alternatively, if the “one-shape-fits-all” holds true, we may rest more relaxed in knowing that their adaptive capabilities will equip them for a changing climate. We look forward to unravelling these questions in future work within other species of marsupial carnivores, and deciphering how fast are other species “shaping up”.

Space use by giant anteaters in a protected area within human‐modified landscape

Blog written by Alessandra Bertassoni. Read the full article here.

Shaggy, toothless, great snout and slow… These are common adjectives applied to the Giant Anteater – the largest anteater species in the Neotropic. This is a species that attracts curiosity, as well as having gaps in our knowledge of its ecology. Despite its large distribution (from Honduras to southern South America), it can be locally rare or very threatened in some areas (e.g. Central America and at the south of its distribution).

Numerous risks threaten the persistence of populations, such as wildfires, poaching, conflicts with dogs, road-kills, fragmentation, and habitat loss – these last two are the major threat to populations. To try to preserve natural habitats, countries have adopted the creation and maintenance of protected areas. On one hand, this is a good conservation strategy in times of huge changes to global systems – mostly driven by intensive human activities. On the other hand, some protected areas and their communities are immersed and isolated in human-modified landscapes. Large mammals require extended space, and the borders of the protected area are often bypassed.

This is the background of our study – “Space use by giant anteaters (Myrmecophaga tridactyla) in a protected area within the human‐modified landscape”. Our work took place in the Santa Bárbara Ecological Station (SBES), a protected Cerrado biome remnant (27 km²) surrounded by human-modified landscape in the State of São Paulo, Southeastern Brazil (Figure 1).

Figure 1: Santa Barbara Ecological Station (SBES, black polygon) and its surroundings in Southeastern Brazil. The green polygon is a Pinus sp. Plantation, the red traces are roads and Aguas de Santa Barbara municipality is represented as a light orange diamond.

This area is considered to have high biological importance due to its typical Cerrado vegetation. However, it is surrounded by pasture, sugarcane, exotic timber plantations (green dash line, Figure 1), and urban zones. It is also divided by a road network (red dash line, Figure 1). There is a resident population of giant anteaters within the SBES. We hypothesized that they would be highly dependent on the natural features of the protected Cerrado remnant because of their extreme specializations and habitat requirements. We also predicted that their home ranges will be primarily located within the SBES and the resources inside will be more used than the surroundings. Finally, we predicted that home ranges will overlap by more than 50% due to the small size of the protected area. This was a pioneer study of giant anteaters in a highly human-modified area.

To pursue these ideas it was necessary to track giant anteaters in the SBES and surrounding area. This species needs to be captured actively, as methods such as cage traps or baits are ineffective. Therefore, the team has to be in the field to search, find and catch giant anteaters.

In 2015, we spent three months in the SBES and its surrounding area. We covered approx. 12,000 km (three field campaigns) and we succeeded in capturing eight giant anteaters; four females (F) and four males (M). We fitted them with GPS-harnesses (see Figure 2).

Figure 2. A tracked giant anteater with GPS harness in the Santa Barbara Ecological Station, Southeastern Brazil.

For a few months (10 – 147 days, 91 on average), we were able to record 13,170 locations of the tracked individuals (Figure 3). This enabled us to record a great deal of interesting ecological data. Five giant anteaters (2 F and 3 M) remained almost exclusively inside the SBES and the other three (F1, M2, and M4) had more than 20% of their locations recorded outside of it. This gives us some indication that the SBES area and its requirements are not enough alone to accommodate this population. Residing outside of the protected area could be the best choice for individuals that require more space or are searching for specific resources which are too many exploited or limited within the SBES.

Another clue was the increasing trend in the home-range area of the two males (M2 and M4) to leave the SBES. From a conservation genetic perspective, individuals that leave a population to reach another can be considered propagules that contribute to the genetic pool. But, in a human-modified landscape, leaving protected areas is too risky, especially in a place that has more than one road.

In the two years that we spent in the study area, we found giant anteaters, deer and other animals killed by collisions with traffic. We predicted a great deal of overlap between individuals due to the SBES size, and we reported that dyads of opposite sex presented larger area-overlap than same-sex dyads, using two space-sharing indexes. However, this is not breaking news. Much more elucidative data came from the analysis of combined trajectories. This revealed proximity events in five dyads of opposite sexes and a male-dyad.

Figure 3. Giant anteaters locations inside the SBES and surroundings, Southeastern Brazil. M = male and F = female.

.What does this mean? Proximity events could indicate higher levels of coexistence than previously reported for this species, or that the study site is too small, meaning the anteaters interact more often. In addition, proximity analysis highlights that low home-range overlap cannot be strongly interpreted as a lack of individual interaction. Proximity events could indicate reproductive behaviour.

However, we still do not know if there is reproductive seasonality for the species, and this needs further study to advance our knowledge of this species’ natural history. Despite giant anteaters being most well-studied anteater species, we still lack the basic knowledge to to ask the right questions. We need to apply much more effort to studies on human-modified areas, to reach the minimal information needed to understand population trends and to move conservation forward.

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