Red listing isn’t all black and white: embracing the grey areas of a penguin conservation assessment

Blog written by Christina Hagen and Andrew de Blocq. Read the full paper here.

The International Union for the Conservation of Nature’s (IUCN) Red List of Threatened Species is a useful conservation tool for prioritising conservation and tracking the status of species. During a Red List assessment, a species’ extinction risk is given as one of nine categories ranging from Extinct to Least Concern. There are five criteria used to classify extinction risk which look at changes in population size or geographic range, quantitative analysis showing probability of extinction and the special cases of small populations. By far the mostly commonly used criterion examines the rate of decrease in the population over 10 years or three generations (whichever is longer).

While the criteria are quite clear-cut, the interpretation and analytical methods can differ between assessors and species. Some species are incredibly difficult to count (e.g. if they live in difficult-to-access areas or are cryptic) and this can lead to incomplete, inaccurate, or irregular population estimates. While there are different methods for filling missing data points, most consider the “true” population to follow a deterministic (without randomness) trend which is not realistic in terms of what we know about the real world.

JARA (Just Another Red List Assessment) is a new decision-support tool for assessments using the rate of population change criterion. JARA is notreally just another assessment tool, but rather one that takes uncertainty into account. Essentially, this algorithm considers the uncertainty in population estimates and plots the probability distribution of the population decline against the ICUN Red List categories. This means that a species can be classified as Endangered with 70% confidence, for instance, but with the likelihood that the assessment may have been too harsh (and should be Vulnerable) or too soft (and should be Critically Endangered). If for example, there was a 25% chance that the assessment should have been Critically Endangered, then more urgent action is needed, which may not be recognised without incorporating the uncertainty. Another useful way to use JARA is to plot these trends over time. This shows whether a species’ status is declining steadily or at an accelerating rate, stabilizing, or increasing either slowly or quickly. One can also use the JARA method on different sub-populations to see if the extinction risk differs spatially.

Penguins should normally make burrows in guano, but guano harvesting until the 1960s removed this insulating layer, forcing birds to nest on the surface, putting chicks at risk from predation and the elements. Photo: Andrew de Blocq

In our paper, we use JARA to analyse the decline in African Penguin numbers over the last 40 years. The African Penguin breeds only in South Africa and Namibia, with 32 colonies across the two countries. The colonies are clustered into three regions each separated by about 600 km: Namibia, South Africa’s Western Cape, and the Eastern Cape. Our results support the classification of this species as Endangered, with a high probability (97%). However, using the JARA framework also allowed us to deconstruct the trends over space and time, showing that the African Penguin has not decreased equally across its range nor over time. This is important as understanding the causes of the variation allows conservationists to prioritise different management strategies in each subpopulation.

The Namibian population has declined more slowly than the other regions, enough to allow it to be regionally classified as Vulnerable. However, this masks the fact that the population had decreased by over 70% prior to the start of our dataset in 1986. This is due to the collapse of the Namibian sardine stocks in the 1970s, and the species is at critically low levels compared to when fish stocks were healthy. The Namibian population also experienced an outbreak of avian influenza in 2018 which was much more lethal than a similar outbreak in the Western Cape colonies, so this again shows the importance of considering spatial differences in subpopulations when assessing risk.

The decreases in the South African population have been much more rapid over recent years. The decrease in penguin numbers has coincided with a decrease in sardine and anchovy biomass and the eastward displacement of spawning sardine and anchovy, which when combined with fishing pressure has decreased the availability of prey for penguins to the north of Cape Town. This region is changing the most rapidly, with decreases of 10% per year for the last 20 years. The Eastern Cape population, after decreases in the 2000s and late 2010s, has been relatively stable and now hosts the largest proportion of the global population.

African Penguins at the iconic Boulders Beach colony, a major tourist attraction but historically one of the smaller colonies that has remained relatively stable. Photo: Christina Hagen

The African Penguin is at serious risk as a species. However, it is also clear from our study that these declines are different for the three regional populations and that we cannot implement a one-size-fits-all conservation approach. Ongoing population monitoring is needed in Namibia to keep track of this vulnerable population. The Western Cape was traditionally seen as the stronghold for African Penguins, but with changing environmental conditions and the lack of food, the Eastern Cape has overtaken it as the new population stronghold. This mirrors the southwards and eastward shift shown by other marine species and raises the concern that the bulk of the penguin population is now on the edge of the species’ range. This should influence the priority of conservation action, especially with the colonies in Algoa Bay now facing novel threats from increased ship traffic and marine pollution related to ship-to-ship bunkering and the development of the local harbour.

The IUCN Red List is used extensively to inform scientific and conservation work, policies, and funding resource allocation. This means that assessment methods need to be as robust and transparent as possible, which includes an acknowledgement of the uncertainty that is inherent in each assessment and the breakdown of risk in space and time. The JARA method incorporates observation error (i.e. errors made during data collection or processing) and the variation that is part of any biological process.

Amid the current biodiversity crisis with many competing conservation priorities, we cannot afford for threatened species to be misclassified due to imperfect count data. We also need to make sure that conservation actions are appropriate and will address the correct threats at the correct sites and scales. JARA is a decision-support tool that can be applied to many taxa and can shed light on some of the inevitable uncertainty surrounding population trends.

Bat CATastrophe: the cause of many wing tears in UK bats

Blog written by Robyn Grant & Kirsty Shaw. Read the full paper here. Featured image of a common pipistrelle bat copyright Hugh Clark (bats.org.uk)

More than a quarter of all mammal species in the United Kingdom (UK) are bats, they also make up around 20% of all mammal species worldwide. Bats play important roles in many ecosystems, being pest controllers, pollinators and seed dispersers. Urbanisation is one of the most dramatic forms of land-use change and many bats, such as the Common pipistrelle (P. pipistrellus), exploit urban environments for roosting, water, and foraging under artificial lights. However, this also exposes them to urban risks, including collisions with man-made structures and predation from species that are concentrated in urban areas, such as cats.

In the UK, thousands of bats are found and rehabilitated by specialist bat carers every year, many of them for wing tear injuries. Indeed, when we surveyed bat carers around the UK, more than 2000 bats with wing tear injuries were reported to be taken to rescue centres annually. This is not a problem that is specific to the UK, wing tears are commonly found in bat populations worldwide. Tears are considered significant and severe injuries. Despite bat wings having resilient fibre structures and a good blood supply to encourage healing, rehabilitation in captivity can take a long time, which can significantly affect a bat’s health and welfare.

The causes of wing tears are not always clear, but may include collisions, fungal infections and predator attacks. We spoke to many bat carers around the UK, and they believed that the main cause of wing tears were cat attacks; however, positively identifying a cat attack can be difficult. In some cases cats can present a bat to their owners, or the tears “appear” to be made by claws. Previous studies have identified that 20-68% of bats admitted to rescue centres may be as a result of cat attacks; however, there is not yet an objective method to corroborate this.

We applied an objective, forensic DNA analysis method to identify the presence of cat DNA on bat wing tears. We asked bat carers to swab bats with wing tears and send us the swabs. We also asked them to take a photograph of the tear, and tell us what they think caused it. Overall, we collected 72 samples from bat carers, including 40 Common pipistrelles, 18 Soprano pipistrelles, 4 Whiskered bats, 4 brown long-eared bats, 2 Natterer’s bats and one Serotine, as well as 3 swabs from unknown species.

Bat wing swab sampling kit provided to bat rehabilitators

Our results showed that 48 out of 72 (67%) samples had cat DNA present. The presence of cat DNA appeared relatively equally across different bat genders, ages, and species, indicating that all bats may be targeted equally. While our method is a very sensitive technique for the detection of cat DNA, this value of two-thirds could still be an underestimation, due to bats not always being brought to carers, low amounts of DNA being transferred from the cat to the bat during the attack and variability in swabbing and storage techniques.

Bat carers tended to receive bats from a small working area within a 20 mile radius. The same bat carers sent us many samples, especially in Kent and East Dorset, so we also looked at using forensic DNA profiling to identify individual cats within these areas. We did not identify any of the same individuals. Other studies have suggested that there are likely to be “super predator cats” that repeatedly target bat roosts, so identifying any individuals that repeatedly predate on bats within a small area will be a useful thing to do in the future.

An example DNA profile which can be matched to an individual cat

Photographs of the tears showed that when cat DNA was present, these tears were often large, running from the internal membrane to the trailing edge, and tended to appear in the more proximal wing sections, close to the body. When bat carers supplied the suspected cause of the tear, they successfully identified a cat attack in all but one sample (in 93% of all cases). This confirms that bat carers are able to make strong, positive identifications of cat attacks.

An example of a bat wing tear close to the body, and an illustration of the most commonly affected areas of the bat wing

Free-roaming domestic cats cause a huge number of bird and mammal fatalities and, with the number of cats increasing annually, the effect of cat predation on wildlife is only likely to rise. Unfortunately, this means that the number of injured bats from cat attacks is also likely to increase in the future. As well as causing wing tears, cat attacks can also lead to bacterial diseases in bats. Cats may even receive a viral infection from the bats, such as Nipah virus and European bat lyssaviruses, which can lead to cat mortality. We would suggest that night-time curfews for cats, as well as anti-predator collars, will have beneficial impacts on the local bats as well as other nearby wildlife.

This is the first time that cat attacks on bats have been objectively identified using forensic DNA analysis techniques. Our results suggest that cat predation on bats, at least in the UK, is likely to be much higher than previously estimated. A better understanding of cat and bat interactions has implications for both cat and bat populations, as well as their health and welfare.

The Mystery of the Glacier Bear

Written by Tania Lewis and Neil Barten. Read the full paper here. Featured picture: Glacier Bear in Glacier Bay Alaska, by T. Hausler

There are few animals as elusive and mysterious as the glacier bear in Southeast Alaska and northwestern British Columbia, a region characterized by deep marine fjords left by the Pleistocene ice advances, steep rugged mountains from ongoing tectonism, and large glaciers and ice fields maintained by persistent cold precipitation. Glacier bears, also known as blue bears, are uncommon color variants of black bears (Ursus americanus) whose pelage ranges from white to grey to black with silver tipped guard hairs. The Alaskan Native Tlingit name for these bears was “siknoon” which translates into “a bear that disappears” in reference to their elusiveness and ability to blend in with snowfields (Lewis et al. 2020). These unique creatures are the subject of stories and books, and rare sightings are a once in a lifetime experience for a few lucky people. Glacier bears are also targeted and opportunistically harvested by sport hunters in some areas. Previously there was very little scientific knowledge regarding their range, the frequency, or the genetic basis of their unusual pelage color. This lack of knowledge has made it difficult to manage and predict the future survival of glacier bears.

A black bear mother with two glacier cubs in Glacier Bay, Alaska by C. Edwards

Neil Barten worked as a biologist for Alaska Department of Fish and Game (ADF&G) in Juneau in early 2000s, managing bear-human conflicts during a time when glacier bears were quite common in Alaska’s capital city. Bear problems in Juneau were increasing due to improperly stored trash and other attractants, and a few glacier bears were guilty of perpetuating this problem. Several glacier bears were hit by cars and up to six “nuisance” glacier bears were translocated, including a black mother bear with two glacier cubs and one black cub. Despite their prevalence in the capital city, Neil knew that glacier bears were uncommon in most areas, with only a couple harvested by hunters each year primarily near Yakutat over 100 miles to the northwest. Neil began collecting tissues from glacier bears captured or harvested to take advantage of recently developed genetic methods. As a management biologist, he recognized that genetics may be the key to answering basic questions about this little understood animal.

A glacier bear interacts with a police officer in Juneau, Alaska

Meanwhile Tania Lewis was hired to conduct bear research and management in Glacier Bay National Park and Preserve (GBNP&P), which lies halfway between Juneau and Yakutat. When Tania started digging into park archives to write the park’s first Bear Management Plan, she found a map of glacier bear sightings and harvest locations compiled by Linda Wiggins, wife of Canadian bear safety expert Steve Hererro. Linda had conducted visits to the region to attempt to determine the range of this rare color phase (Lewis et al. 2020). In 2009, at the Third International Human-Bear Conflicts Workshop in Canmore BC, Tania, Neil, Linda and others met for dinner to discuss glacier bears and the need for a collaborative research study to learn more about these mysterious creatures.

Glacier bear hide sealed and sampled by ADF&G

The team began collecting more genetic material of black bears across the range of the glacier bear color morph. GBNP&P and ADF&G staff collected DNA noninvasively from hair as well as tissue samples from harvested bears, noting the color of the pelage. Researchers used the DNA to examine genetic structure between populations of black bears within the geographic extent of glacier bears and explored how this structure related to pelage color and landscape features of a recently glaciated and highly fragmented landscape.

Glacier bear cub in Glacier Bay, Alaska, by E. Weiss

Ten populations of black bears were found in the study area divided largely by geographic features such as glaciers and marine fjords. Glacier bears were assigned to four of the ten populations found on opposite sides of two long fjords (Glacier Bay and Lynn Canal) with a curious absence in the non-glaciated peninsula between. Lack of genetic relatedness and geographic continuity between black bear populations containing glacier bears suggest a possible unsampled population and/or an association between glacier bears and large icefields, which would suggest a selective advantage for glacier bears in glacial environments. Such an association would increase the conservation risk of the color morph as glaciers recede suggesting further investigation is needed to determine the adaptive and evolutionary significance of the glacier bear color morph. Determining the genetic basis of the glacier bear color morph will also be necessary to determine the frequency of the gene(s) across black bear populations containing the rare phenotype. These results shed light on the distribution and population structure of the color morph across the region and may help focus conservation efforts to maximize and preserve genetic diversity of black bears as glaciation of the region decreases with climate change.

Lewis, T. M., Stanek, A. E. & Young, K. B. 2020. Bears in Glacier Bay National Park and Preserve: Sightings, human interactions, and research 2010–2017. Natural Resource Report NPS/GLBA/NRR—2020/2134. National Park Service, Fort Collins, Colorado.

Evolution of rat crania in an urban environment

Blog written by Emily Puckett & Liz Carlen. Read the full paper here.

Observations of numerous animal populations have documented morphometric changes in response to urbanization.  Examples abound including: urban populations of anole lizards have longer limbs and more toe lamellae that aid in moving on artificial substrates, urban fish have more streamlined body shapes for swimming in faster flowing streams, and urban damselflies have greater flight endurance.  Additionally, there are numerous examples of changes in skull shape in response to urbanization.  There’s an intuitiveness to these results; artificial lighting means eyes could be smaller and still see at night, complex landscapes could increase brain size/cognition as animals explore novel environments, and altered food resources could shift dentition or beak shapes.  And yet there is a counter argument that urban environments are highly stable in resources, temperature, and landscape, lacking the disturbance of natural environments.  For example, urban environments have stable sources of anthropogenic food waste year-round.

One hypothesis is that populations living in environments that transition from rural to urban show increases in braincase and brain size over time due to plasticity, that then decreases following acclimatization (blue line in figure).  Yet, a second pattern could emerge where the rate of shape change slows precipitously following exposure to the new environment, and thus shape is either maintained through time or changes more slowly (purple lines in figure). Thus, for any population, has urbanization affected cranial shape to increase survival; and if so, how?

We were part of a team investigating the evolution of urban brown rats (Rattus norvegicus) in Manhattan, NY, USA.  We trapped, euthanized and prepared 44 rats as museum specimens.  Fortunately, a series of brown rats were also collected between 1891-1895 allowing us to compare cranial and mandible shape over time using geometric morphometrics.  We hypothesized that due to increasing selection pressures from urbanization, the braincase would increase (in response to exploration of novel environments), the nose would shorten (in response to a warmer urban environment), and the tooth row would shorten (in response to higher quality and softer anthropogenic food).

We observed morphometric differences in both the crania and mandibles between the two sampling times (1890s and 2010s).  Crania of the contemporary samples (2010s) differed from the historic samples (1890s) with a slightly shallower hindbrain case, longer nose, and shorter tooth row.  Our hypothesis about an increasing brain size over time was not supported by our data, although we did observe variation in the hindbrain case related to allometry.  Our hypothesis regarding nose length was in the opposite direction to that we predicted.  We thought that heat island effects would select for larger nasal cavities able to better dissipate heat.  Our hypothesis of a shorter molar tooth row was supported.  This is consistent with rural-urban gradient studies that have shown that as rodents encounter either higher quality and/or softer diets, tooth row length decreases.

We also used the EvolQG package in R to test if the observed shape changes were consistent with directional selection, or the null model of genetic drift.  Our analysis suggested directional selection for shape change of the crania, and drift on the mandible.  Beyond a dietary shift towards softer and more processed foods, our data do not suggest specific aspects of urbanization that may explain the change in shape over time.  We recognize that urbanization creates multiple novel selection pressures, which likely acted jointly on this population of rats.

The prescient question now is, what’s next?  Specifically, will one or more aspects of skull shape shift towards the 1890s shape suggesting a plastic change?  Or will the morphometric changes be retained in the population (or continue on a directional trend)?  And if the latter, how long has this population maintained the current variation for shape?  Due to the presence of only two time points in our temporal sample, we were unable to distinguish between the trajectories for brown rats in Manhattan.

We want to end by acknowledging the collaborators we never knew, the AMNH scientists who collected and prepared the 1890s series of brown rats.  We would not have a study without their work.  Our paper highlights how museum collections benefit from collecting local species. No one knows what questions scientists will want to ask or be able to answer in the future, and by documenting the wildlife that is currently occurring in cities around the world we will be better able to understand how urbanization influences the evolution of species.

Rock hyraxes in the city; the bi-directional effects of cultural norms on urban wildlife

Blog written by Noam Ben-Moshe and Takuya Iwamura . Read the full paper here.

At first sight, it looked like a junkyard in the middle of the neighbourhood, but as we approached, we noticed it was actually a kindergarten. In the Hassidic neighbourhood of Neve Ya’akov of north Jerusalem, several mobile structures stood surrounded by messy piles of children’s chairs, broken swings, and construction waste. The makeshift playground was covered with small, round feces and the acrid smell of urine was strong.

As we entered the compound, the doors burst open and the children came running out, eager to enjoy every second of their break time. There were no proper toys to play with, but everyone seemed to be aiming for a familiar attraction. They began to throw stones at the waste piles. Suddenly, as though responding to the children’s demands upon them, a large group of rock hyraxes appeared from the crevices.

Some of the children started chasing them in circles until the animals fled under one of the trailers while other hyraxes climbed the walls of the structures and began jumping from roof to roof to the sound of the children’s wailing. Another group of hyraxes gathered in the corner of the yard and ate flakes of an Israeli snack called Bamba that a number of children threw at them. The manager of the place approached us to ask if we were from the municipality and if we had come to pick up the animals that he said had “taken over” the garden. Whilst we were talking, we noticed that the manager, on an exposed area of his arm, had a large, muggy lesion. We were familiar with this type of skin infection. It looked like Leishmaniasis, a zoonotic skin disease transferred to humans by a sandfly sting. Rock hyraxes, as found only in recent years, are reservoir hosts of the pathogen causing the disease.

Artificial rock mounds, a by-product of the common building practices in Jerusalem, encircle the new neighbourhoods and create great shelters for wild rock hyraxes next to rich foraging grounds in the city parks.

We were visiting this community as part of our field study work, to understand the drivers that brought these wild animals from their native habitats in secluded canyons in the Judean desert to establish colonies in a core urban area up on the mountains. We also tried to understand why the animals had proliferated in one particular neighbourhood but not in another. Following the hyraxes’ expansion route, we based our research on habitat surveys and hyrax observations in the peripheral areas outside Jerusalem as well as inside the city.

The natural distribution of the rock hyraxes, as their names suggest, is associated with rock piles where they find shelter from predators and adverse weather conditions. While urban sprawl usually causes the extinction or relocation of local wildlife species, observation records show that hyraxes moved towards the city as it expanded.

Urban building practices and heavy machinery, used for the excavation and laying of new roadways, have pushed discarded piles of the rocks down the mountains and into valleys below. This debris have built up over time, and have become urban simulations of the hyrax habitats enveloping the new neighborhoods. We found that these artificial rock piles are great shelters for the hyraxes and they come with the added benefits of providing access to human waste and rich foraging grounds in the adjacent city parks. This combination of shelter and food security has created a fertile environment, which is promoting extremely dense population of hyraxes, while new unoccupied shelters become scarce.

Our findings suggest that these processes have caused a “spill-over” into the urban areas where these new urban invaders are demonstrating highly adaptive skills while taking advantage of the human cultural norms.

Hyraxes demonstrate little fear of humans in the urban parks of north Jerusalem.

Remarkably, we found that in the poorer and more religious areas of the urban environment, there were plenty of sites offering shelter and food in the middle of the urban area. The reason being was that in the poor areas, there seemed to be lack of municipal care, which you would find in more affluent areas. Moreover, in the poor areas there was a lack of awareness around environmental waste management by the local residents, which was demonstrated by the disposal and accumulation of dry waste in open grounds, as well as illegal building with mobile structures that are elevated from the ground; both make complex shelters that are an urban alternative to natural rock piles. To compliment this, a religious prohibition of dumping valuable food means that food items are left in open spaces. Consequently, the rock hyraxes are more common in the poor religious areas, and were not found in high-maintained areas.

In regard to the kindergarten manager we met earlier, and consistent with our research, we found that the largest outbreak of leishmaniasis in the city was next to the highest concentrations of hyrax colonies.

The story of the rock hyrax in Jerusalem could have been a great example for reconciliation ecology, a win-win situation in which a wildlife species flourishes amidst humans, while humans can enjoy observing these playful diurnal animals by their houses. Unfortunately, it is not so, as the animals dispersal is related to a spread of a disease in highly populated areas.

However, since the process is human-driven, we have the means to control it, instead of it controlling us. If we are smarter and adopt a more informed rural-urban strategy, we can manage the spread of the hyraxes in human settlements.

From our studies, observations and investigations, we feel that the following measures should be considered;

  • Enforcement of regulations on building practices, to prevent the common practice of pushing over rock debris from construction sites outside the city and improper placement of mobile structures in the urban areas.
  • Municipal investment in the maintenance of open grounds and a robust waste removal service.
  • Raise awareness and educate human communities about sanitation and how traditions, although well intentioned, may be having a negative effect on their health and well-being.

In these strange times when most of the world’s urban population is under the risk of another zoonotic disease, the last measure may be of the highest priority. 

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