The lost benefits of cryptic grey colouration in a changing winter landscape

Blog written by Patrik Karell. Read the full paper here.

For most animals, it is of crucial importance that they are not visible to their predators. This is why predation is considered one of the most important selection pressures shaping the wide variety in colouration we find among animals. For animals relying on cryptic colouration, natural selection is expected to favour the colouration or colour pattern that is least conspicuous in the natural environment where the species lives. When the environment also changes the effect of camouflage is altered, which in turn leads to changes in selection pressure on colouration. In Northern Europe winters are getting shorter due to climate change: the probability of a lasting snow cover is getting lower and the duration of the snow covered winters is decreasing. This change from whiter to darker winters is a major challenge for many species living in these regions around the year.

Our study species, the tawny owl, Strix aluco, come in a brown and a grey colour morph. The tawny owl is widespread in the Western Palearctic and individuals of the same species live in very different types of landscapes with relatively large variation in seasonal climates. Therefore, selection may favour certain colour phenotypes depending on the type of landscape (i.e. background) they live in. In Southern Finland, which is at the northernmost limit of the tawny owl’s distribution, we have previously found evidence that there is strong survival selection against the brown morph in winters with lots of snow, whereas this selection is absent in winters with no or very little snow.

In our recent paper in Ecology and Evolution we test the prediction that this snow condition-dependent selection against the brown colour morph is associated with differential camouflage of the colour morphs depending on the snow conditions. We took stuffed grey and brown tawny owls and a camera out into the woods in winter in an area in the outskirts of Helsinki where tawny owls naturally occur (and close to the area where we know survival of the brown morph is decreased in snowy conditions). We placed the owl mounts in trees in natural roosting positions in their natural environments and took photos of them. We took one set of pictures of both the grey and the brown morph when there still was no snow and an identical set of pictures after snowfall. We randomised the pictures and made a number of series of pictures to be used in the experiment.

A brown tawny owl in a boreal winter landscape

The online “spot the owl” game

The experiment was conducted as an online game, where people could visit a website and participate. The participants were shown a series of pictures and their task was to spot the owl in the picture as fast as possible. If they could not detect the owl they were shown the next picture in the series. The online game was successful and attracted more than 5000 participants worldwide in a short time. The results were as we expected: in pictures of snowy conditions the participants were more likely to find the owl and they found them faster if the owl in the picture was a brown morph. The grey morph was therefore more cryptic in a snowy landscape. In snowless conditions this crypsis difference between morphs was much less pronounced.

A grey tawny owl in the same winter landscape

Is a human observer comparable to the enemies in the natural environment?

Since birds are able to sense the ultraviolet spectrum of light it is not evident that a bird, be it a hunting goshawk or a mobbing passerine, would perceive the colour of the two tawny owl morphs in a similar way as the human observers. We therefore used an avian vision model to compare how the tawny owl morphs are perceived by a blue tit as compared to a human. As predicted, the avian vision model showed no difference between a bird’s and a human’s perception of the tawny owl colour morphs. However, this exercise showed that the plumage of the brown morph deviates more from a spruce or pine trunk than the grey plumage. Therefore, a roosting tawny owl in a boreal coniferous forest is likely to be less conspicuous if it has a grey plumage.

Is difference in camouflage related to climate-driven selection on colour in tawny owls?

We were able to show that the brown morph is more conspicuous in snowy conditions, as predicted based on previous findings of strong survival selection against the brown morph in snowy conditions. We therefore suggest that if it takes longer to detect a tawny owl or if it completely remains undetected it will have a higher probability of survival in winter. The tawny owl is nocturnal and roosts during daytime when most other (diurnal) birds are active. If a roosting tawny owl is detected in the forest by a passerine or a corvid, these potential avian prey species will harass the owl and try to chase it away. Fleeing is often the solution for a tawny owl and this requires energy, which desperately needs to be saved in order to survive when winter conditions in general are harsh in Northern Europe. Fleeing also reinforces the likelihood of being detected and killed by predators such as goshawks.

Warmer winters with less snow makes the brown tawny owl less conspicuous. Together with other potential benefits of warmer winters, such as more easily accessible small mammal prey which cannot hide under the snow and overall more favourable thermal conditions, warmer snow-free winters may benefit the brown morph. Indeed, our analyses of ringing data from Finland do show that the brown morph has steadily increased in frequency in Finland in the past 50 years.

Hiding in plain sight: Why would a butterfly have a greenish-blue band?

Blog written by Eunice J. Tan, Bodo D. Wilts and Antónia Monteiro. Read the full article here.

Animals have a bewildering variety of colour patterns, many of which provide protection from potential predators. However, to identify how these colour patterns, or “signals”, serve to protect the animals can be often challenging.  

Research in the last decades have focused on the mechanistic origin of colour in animals (e.g.Srinivasarao (1999)) and on understanding how various signals function to protect animals (e.g. Stevens and Merilaita (2009)). An important strategy, crypsis, prevents the initial detection of the animal. There are two main ways how animals become cryptic: one way is to have colours that allow them to blend in with their background, thus making the animal’s shape difficult to detect or recognise; another way is to have continuous patterns, such as bands, traverse different but adjacent body parts, thus making it difficult to detect or recognise individual body parts.

Butterflies are well-known for their dazzling colour patterns, but the functions of these patterns are still poorly understood. The Banded Swallowtail butterfly, Papilio demolion demolion, is a mostly black butterfly with a greenish-blue band that crosses the wings (Image of butterfly below), but the origin and the function of the greenish-blue band was unknown. These butterflies occur across Southeast Asia to Australia, can be found in forests and forest edges, and are active and fast fliers, feeding on flowers of shrubs and trees.

Habitat photograph of the Banded Swallowtail butterfly, Papilio demolion. Image credit: Sin Khoon Khew.

To better understand how the colour pattern of the Banded Swallowtail protects the butterfly, we examined the butterfly wing scales that make up this pattern closely with a scanning electron microscope. This allowed us to compare the colours of the green-blue band with the surrounding black wing. We found that this blue-green colour is caused by pigments immersed in the scales, resulting in a matt appearance. Potential predators therefore see an identical green-blue colour pattern from any observation angle.

We hypothesized that the greenish-blue band of the Banded Swallowtail protects it from predators through two possible means: i) its shape could help disguise the butterfly outline, and ii) its greenish-blue colour could help blend it with the surrounding green vegetation, thus preventing recognition by predators.

To test our hypotheses, we created four types of paper butterfly model, imitating the Banded Swallowtail butterfly at rest. The first paper model was like that of the natural butterfly (Model A). In order to test the protective function of the green-blue colour, we created a greyscale version (Model B). Next, to test the protective function of the shape of the band, we distorted the band so that the band is discontinuous (Model C). Finally, to test the protective functions of both the band shape and its green-blue colour simultaneously, we created a greyscale version with a distorted band (Model D). We placed these paper models, with mealworms attached as live baits, in the natural habitats of the Banded Swallowtail, in Singapore. To monitor the predation on the paper models, we checked the models daily over three days, to see if the mealworms had been eaten.

Paper models of the Banded Swallowtail. Image credit: Brent Tan

We found that the natural-looking models (Model A) suffered the least predation, while the grey model with distorted band (Model D) suffered the highest predation. Both models that had only the colour or shape of the band changed (Models B and C) suffered similar, moderate predation.

Our results indicate that both the colour and the shape of the band are important to protect the butterfly. We suggest that the shape of the band helps disguise the butterfly outline, and its greenish-blue colour, by matching the surrounding green vegetation, helps further in preventing recognition by predators.

The presence of bands on animals is an intriguing feature. Bands were shown to reduce predation in other invertebrates such as in another species of butterfly, and in spiders (Hoese, Law, Rao, & Herberstein, 2006; Seymoure & Aiello, 2015). In fish, bands are more frequently found on the bodies of fast-moving fish (Barlow, 1972). We speculate that bands are effective in disguising fast-moving species across a range of animal species, including the fast-flying Banded Swallowtail.

We also considered whether the green-blue colour could be a warning colour, i.e., a colour that warns predators about a prey’s unpalatability. The Banded Swallowtail is probably palatable because the Banded Swallowtail larvae feed on the leaves of non-toxic plants. However, not all warning colours signal unpalatability, some of these colours could be used to signal unprofitability. Pinheiro, Freitas, Campos, DeVries, and Penz (2016) showed that warning colouration in butterflies can also function as a signal to indicate difficulty of capture by insectivorous birds. As the Banded Swallowtail is a strong flier, its blue-green band may serve as a warning colour to signal unprofitability to potential predators.

Both the colour and the band of the Banded Swallowtail may help it form a mimicry ring with other similar-looking local species. Animals in a mimicry ring look similar and advertise their common unprofitability to predators. In fact, the Common Bluebottle butterfly, Graphium sarpedon luctatius, may be involved in a mimicry ring with the Banded Swallowtail. We have seen both butterfly species in the same forests, and both species possess green-blue bands across black wings.

While our experiments cannot distinguish whether the natural-looking models were least attacked because of crypsis or warning colouration, future experiments could test this. Following previous studies (e.g. Wüster et al. (2004)), the predation rates of models in a background with vegetation versus in an artificial grey background could help distinguish among these two possibilities.

Coping without oxygen, under water.

Blog written by Dr. Noelle Lucey and photos by Mary Collins. Read the full paper here.

When most people think of coastal hypoxia, polluted areas with lots of people living nearby come to mind – not remote tropical coral reefs. Yet, in a large Caribbean bay where tropical jungles are practically kissing the shallow coral reefs in the warm waters below, severe hypoxia has also made its mark.

Our study found seasonally predictable hypoxic waters at the bottom of Almirante Bay, Panama during the warmer half of the year. The bay during this time is highly stratified, with deoxygenated water at depth (20m) separated from a small top layer where oxygen levels are higher. This has resulted in the mortality of reefs deeper than 3 meters in some areas.

Hypoxic waters shoaled to 3 meters on the reef slope off of Cayo Roldon in 2017; coral below this oxycline has been reduced to rubble and sand.

We found that deoxygenation is most extreme close to the mainland, where highly stratified hypoxic waters shoal onto shallow reef sites. It is clear that corals and associated life die after chronic exposures to low oxygen waters, however it isn’t clear to what extent, or how badly these processes are affecting the marine life on the reef sites above this.

One of the most interesting findings of this study was that the intensity of hypoxia documented at depth appears to be reflected in adjacent shallow water as the magnitude of diurnal change in dissolved oxygen. So the shallow reefs that haven’t experienced the impact of persistent, chronic hypoxia at depth (resulting in severe mortality) are still being impacted by a type of hypoxia. The dissolved oxygen here widely fluctuates throughout the day with oxygen levels almost declining to zero at night, and then soaring in the afternoon to super saturated levels.

We wanted to know how such frequent changes in oxygen affect the organisms living on these reefs. To study this we used the widely distributed tropical polychaete fireworm, Hermodice carunculata, which is associated with coral-dominated areas and reef decline. These worms can be as long as your foot and often openly flaunt their brilliant colors on the reef where they can be found sucking down coral polyps. They are called fireworms because of their potent harpoon-like chaetae that line their sides and can cause a nasty sting if touched.

Hermodice carunculata fireworm flaring its white bristle harpoon–like chaetae and attempting to escape from the prying microscope lens

Right next to each bunch of stinging chaetae there are branching gill structures (branchiae) consisting of many filaments that extract oxygen from the environment. More gill filaments should mean an increased capacity for gas exchange, and more oxygen available for the worm to go along with its daily activities.

Fireworm gills

We manipulated oxygen levels in the lab to reflect the shallow hypoxic environment, where oxygen levels change widely throughout the day, and kept fireworms in these conditions for eight weeks. We wanted to determine if the gills of these fireworms would grow in response to low oxygen, and if they could regenerate faster if they were cut off.

We thought that worms would grow and regenerate larger gills to compensate for the low oxygen. Sure enough, after only 4 weeks, gills of worms in hypoxic conditions regenerated faster than worms kept in consistently oxygenated waters. Interestingly, worms in these oxygenated conditions regenerated smaller gills than they started with in the same time frame.

Smaller gills seen in the well-oxygenated group

These results suggest that the reefs further from the mainland actually may be experiencing more hypoxia than we thought or measured, and that the worms from these reefs may already be prepared to deal with periodic hypoxia.

Along with gill morphology changes, we expected worms to have an increased ability to take up oxygen from the water after being in hypoxic conditions. We predicted that the worms would be metabolically depressed under low oxygen conditions (breathing less), and after re-oxygenation they would breath more to make up for the oxygen deficit occurring during hypoxia stress. Oxygen consumption rates were measured to see how much oxygen worms were actually taking from the environment immediately after hypoxic exposure. Yet after 8 weeks, we found no significant differences in the oxygen consumption rates of worms exposed to periodic hypoxia. In other words, these worms had the ability to bounce back quickly, metabolically speaking, with normal respiration rates despite previously being in water with very little oxygen. Surprisingly, this was not the case with the worms that had been kept in oxygenated conditions for 8 weeks. After this control group was put in hypoxic conditions, they had dramatically depressed respiration rates upon re-oxygenation.

This suggests that by switching metabolic efforts on and off promptly in response to oxygen availability worms with prior hypoxic conditioning may be able to take advantage of oxygen when it is present in the environment—a trait of great functional importance in rapidly changing environments.

The findings here indicate that hypoxic conditions in shallow coral reefs may be underestimated, and also that H carunculata has the physiological ability to maintain and withstand hypoxia without much of a cost. This is important because it could mean that fireworms have an advantage in rapidly changing environments. They are already considered to be detrimental to coral, degrading living coral reefs and spreading coral disease. As hypoxia is becoming more common and globally prevalent, it is imperative to understand the organismal responses to determine the implications of these processes for reef invertebrates and ecosystems.

Hermodice carunculata

This work would not have been possible without the support and funding from the Smithsonian Tropical Research Institute. We also wish to thank the Bocas Research Station team, Plinio Gondola, Lucia Rodríguez, and Travis Scott, as well as the valuable contributions from reviewers.

Migrants vs residents: a difference in birdsong output

Blog post by Dustin Brewer and Adam Fudickar. Read the full paper here. Photo above of a song sparrow by Mark Hainen

Studying the behavior of animals is like eating a cake and trying to figure out what made it taste the way that it does. Our changing world has baked a spectacular diversity of behaviors into the lives of animals which we are only beginning to understand. Hibernating Arctic ground squirrels, bugling elk, and migrating fish, for example, provide curious people much to feast on, as do multitudes of other species.

Given that behaviors must occur at the right time of year for a species to survive and reproduce, changing conditions can result in mismatches between an animal’s behavior and environment. For example, if an Arctic ground squirrel is still hibernating when its preferred food source is most available, then that squirrel may later starve. When such a mismatch happens, an individual, population, or even a species could disappear from the Earth. For this reason, studying animal behavior can inform conservation efforts in addition to allowing us to ‘eat a tasty cake’ for the fun of it.   

Animals often rely on environmental cues to initiate behaviors. For example, a bird that has migrated to Florida for the winter might migrate back to where it breeds in the spring based on daylength, which also affects when it sings. For many bird species, singing is the primary way for males to attract mates and defend territories.

We asked a simple question, which was, ‘how often, and when, do individual birds that don’t migrate sing compared to individuals that do migrate?’ For some bird species, like Song Sparrows, the breeding population at a location can consist of both ‘residents’ (they spend the entire year where they breed) and ‘migrants’ (they spend the winter away from where they breed). Considering that photoperiod, the amount of time each day that an animal is exposed to daylight, varies based on latitude, we thought that there might be a difference in singing behavior between residents and migrants.

To answer this question, we caught Song Sparrows from a breeding population in Indiana just after the breeding season and randomly assigned them to separate rooms in the lab. In one room, we used photoperiod to simulate a migration from Bloomington, IN to Tampa, FL, then an entire winter in Tampa, and finally a migration back to Bloomington. We called these 10 birds ‘migrants.’ In the other room, we used photoperiod to simulate a winter spent in Bloomington until the breeding season. We called these 10 birds ‘residents.’

Visualisation of a song sparrow song, on a spectrogram

Throughout the 4.5 months that this study took place, we counted the number of songs that each bird in each room sang. Because each Song Sparrow has a unique repertoire of 4 to 13 song types, we were able to identify each individual by its songs and so could count the number of times that it sang, even though many of the birds were singing at the same time. We sampled on 20 November and 6 December (‘non-breeding’ stage), on 27 January and 7 February (‘pre-breeding’ stage), and on 21 March and 4 April (‘breeding’ stage). We found that little singing occurred during the non-breeding stage in the resident group, and that none of the migrants sang. In the pre-breeding stage, however, the residents sang significantly more than the migrants (about 60 songs per bird vs 26 songs per bird in one hour). During the breeding stage, we didn’t find a difference between how much the residents and migrants sang (both sang about 50 songs per bird per hour).

Our results informed us about how Song Sparrows might behave in the wild. Namely, it seems, Song Sparrows that migrate may begin singing at a high rate later than those that don’t migrate. Residents sang more than migrants during the pre-breeding stage, which could help residents establish territories where they will later breed. Given that singing and breeding often co-occur, it could be a disadvantage for migrants if they sang less than residents when they reached the breeding grounds. Our results, however, suggest that both migrants and residents sing the same amount during the beginning of the breeding stage. The act of migrating, it seems, doesn’t put Song Sparrows at a disadvantage with respect to song output during the beginning of the breeding stage.

Recording a song sparrow song in the field. Photo by Dustin Brewer

Understanding when and how much Song Sparrow migrants and residents sing in the wild, and how much other migratory bird species do the same, could help to determine how strategies such as migration affect the ability of individuals to compete for mates. Also, studies like ours could help to determine how much variability exists in the timing of breeding within a population. For example, if migrants begin singing (and breeding) a couple weeks later than residents, then that breeding population of birds would possess variability which could help it to withstand environmental changes, such as climate change.

Our study primarily helps to understand the interplay between two awe-inspiring behaviors, bird migration and bird song. Additionally, our study could provide a framework for determining how much variability in timing of singing (and breeding) particular species display, which could inform conservationists about which species have a better chance of withstanding environmental changes. If so, then we could ‘have our cake and conserve, too.’

Does community-based wildlife conservation work?

Blog written by Talia Speaker, Seth Thomas and Christian Kiffner. Read the full article here.

Since the turn of the century, community-based natural resource management models have risen to the forefront of conservation efforts around the globe. And for good reason—they gained popularity for their promise of meeting both livelihood and conservation goals through empowering local communities to sustainably manage their own land and resources. Particularly in ecologically rich, yet economically poor regions (including many regions in sub-Saharan Africa), this conservation approach sounds like a win-win solution for both human communities lacking basic commodities and declining wildlife populations. But how effective are these conservation models in practice?

Research on these questions has raised major concerns about the socio-economic consequences of current community-based conservation models; namely the results of poor governance and unequal benefit-sharing. These concerns are valid and require urgent attention, but another equally important question has been lacking in the literature: Are these community-managed areas meeting their conservation goals? A handful of studies across East Africa over the last decade suggest a tentative ‘yes’ to this question, but few of these areas have long-term wildlife monitoring programs in place that can be used to assess their sustainability.

Elephant and wildebeest use the swamps and grasslands of Tarangire National Park during the dry season.

Our research takes an important step in addressing this gap by investigating how wildlife populations in a community-based Wildlife Management Area in Tanzania compared to a neighboring state-managed national park over an eight-year study period. More specifically, we tracked changes in species richness and population densities of ten mammal species in both locations from 2011 to 2018 using seasonal and time-matched walking and vehicle based transect surveys. By comparing the community-based model to a national park, we tested it against the “gold standard” of species conservation models, which prioritizes conservation and removes most human disturbances.

Zebra and wildebeest herds aggregate along the Tarangire river during the dry season.

Our results are largely promising. We found that both species richness and population densities across species were comparable between the park and community-managed area, suggesting that these areas can support wildlife communities that are similar to those of a national park, despite different management schemes. We also noted significant increases in the populations of at least three species (elephant, wildebeest, and impala) in the Wildlife Management Area throughout the study period, which further supports the conservation effectiveness of the model but raises concerns about potential negative effects (e.g. crop raiding) of growing wildlife populations on local livelihoods.

Zebras drinking from the Tarangire river during the dry season.

While these findings are good news for this specific Wildlife Management Area, our work is far from done. On a local level, persistent conservation efforts and adaptive management will be critical to the continued success of the wildlife management area model. In the bigger picture, this research only sets the precedent for a much-needed widespread effort to monitor and evaluate the long-term conservation value of community-based models across Tanzania.

Zebras standing in the grasslands of Burunge Wildlife Management Area.

For too long it has been assumed that effective management will come as a de facto result of the (partial) ownership and direct economic benefits derived from wildlife. In our study area, this assumption appears to be valid. We advocate for similar, rigorous assessments of the ecological effectiveness of community-based conservation schemes to test their effectiveness and inform adaptive management. Ideally, assessments are done neither from a wildlife-only nor a livelihood-only perspective but from a holistic and interdisciplinary perspective that takes the social and ecological components into account. To capitalize on this model that holds real potential for facilitating the coexistence of people and wildlife, we must invest now in monitoring its effectiveness and sustainability.

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