Tragic Destiny: Present and Future Diversity of Scavenging Birds

Home , Aegypius, Cape vulture, Gypaetinae, Gyps

DEPARTMENT OF BIOLOGICAL AND ENVIRONMENTAL SCIENCES

TRAGIC DESTINY: PRESENT AND FUTURE DIVERSITY OF SCAVENGING BIRDS

Tala Mohimani

Degree project for Master of Science (30 hec) with a major in Biology BIO705, Biodiversity and systematics Second cycle Semester/year: Spring/Autumn 2020 Supervisor: Søren Faurby, Department of Biological and Environmental Sciences Examiner: Bengt Oxelman, Department of Biological and Environmental Sciences Co-Supervisor: Robert Cooke

Egyptian Vulture (Neophron percnopterus), Photo by: Stefan Hirsch

Contents Abstracts: ...... 2 Abstract (in English) ...... 2 Abstrakt (in Swedish) ...... 2 Introduction: ...... 3 General role of scavenging birds ...... 3 Scavenger types ...... 3 Extraordinary food source: Carcasses and Carrions ...... 4 Scavenging birds and humans ...... 5 Aim ...... 6 Material and Methods ...... 6 Input data for birds ...... 6 Calculating “Effective scavenging richness value” ...... 7 Other predictors ...... 7 Results ...... 9 Discussion ...... 14 Conclusion ...... 15 Acknowledgements ...... 15 References: ...... 16 Tragic destiny for scavenging birds ...... 20

1 Abstracts: Abstract (in English) Scavenging birds have a large role in controlling and regulating services by evacuating and consuming carcasses of dead animals. Their populations have been through many dangers. Large mammal extinction is one of the biggest threats for different scavenging species. Predictors such as human footprint, temperature, precipitation, elevation, and large mammals’ extinction rate can cause steep decline in scavengers’ diversification and scavenging rate all around the world. “Effective scavenging richness value” is the metric to report the level of scavenging each one of the birds does. Also, large mammals are going down the lane of extinction very quickly. I calculated the current and future distribution for both large mammals and necrophagous bird species. The current situation of birds shows that in Africa and the Indian subcontinent there are higher value for effective scavenging richness. Both scavenging birds and large mammals’ extinction rate have been calculated before. Here I used those predictions to create range maps to see if in the future some large mammals go to extinction, what will happen to scavenging birds. Creating range maps and conducting multiple regression analyses supported the hypothesis; by the extinction of some species of large mammals, the surviving scavenging birds will be threatened by starvation. So, if 20 large mammals are lost, and less than one bird goes extinct in one environment, then all birds face potential extinction threat from starvation above any additional threats.

Abstrakt (in Swedish) Asätande fåglar har en stor roll när det gäller att kontrollera och reglera tjänster genom att evakuera och äta kadaver av döda djur. Deras populationer har genomgått många faror. Utrotning av stora däggdjur är ett av de största hoten för olika asätande arter. Förutsägelser som mänskligt fotavtryck, nederbörd, höjd över havet och stora däggdjurs utrotningsgrad kan orsaka skarp nedgång i asätares mångfald och rensningsgrad över hela världen. " Effective scavenging richness value (ESRV)" är mätvärdet för att rapportera nivån på asätande för var och en av fåglarna. Dessutom går stora däggdjur mycket snabbt ut i utrotningskurva. Jag beräknade den nuvarande och framtida fördelningen för både stora däggdjur och asätande fågelarter. Den nuvarande situationen för fåglar visar att det finns högre värden för ESRV i Afrika och den i Indiska subkontinenten. Både asätande fåglars och stora däggdjurs utrotningsgrad har beräknats tidigare. Här använde jag dessa förutsägelser för att skapa räckviddskartor för att se om några stora däggdjur går till utrotning i framtiden och vad som kommer att hända med asätande fåglar? Genom att skapa intervallkartor och genomföra flera regressionsanalyser stöddes hypotesen; genom utrotning av vissa arter av stora däggdjur kommer de överlevande asätande fåglarna att hotas av svält. Om 20 stora däggdjur går förlorade och mindre än en fågel utrotas i en miljö, så utgör svält ytterligare ett hot, tillsammans med de övriga hoten.

Introduction: Bird species, through time, have had many threats to their existence, including major extinctions. The aim of the project is to predict the patterns of extinction of scavenging birds and hopefully inform ongoing conservation efforts to avoid this fate. This research will analyze the relationship of future scavenger populations and the potential factors, such as the distribution and declining of populations in large mammals, human footprint, etc., that influence their survival. General role of scavenging birds Scavenging birds have a large role in controlling and regulating services by evacuating and consuming carcasses of dead animals. Athwart the common belief, vertebrate scavengers do the highest level of scavenging and microorganism and invertebrates are in the second place1. This consumption can reduce and control human disease. scavengers die for many reasons, such as old age, disease, natural disasters (e.g., storms), accidents, and malnutrition. The current “human footprint” has an enormous role in this matter as well. In the absence of scavenging, the number of non-predatory deaths can increase and after that, their carcasses will amass 2.Carcasses serve as a great source of nutrients and energy, and many bird species have shown the adaptation to utilize this source. Some species are specialized specifically in scavenging like vultures (such as: old world vultures Gypinae and Gypaetinae and new world vultures Cathartidae), but other families like Corvidae (Crow family) also do lots of scavenging 3. Scavenger types Two types of scavenging occur in nature: Obligate scavengers, which get vast majority of their food from scavenging carrion and carcasses 4; and facultative scavengers, which gain most of their needed nourishment through ways other than scavenging, such as predation. 5. Obligate scavengers developed some specific adaptations to be able to use carcasses as food sources. Primarily, they must have adequate mobility. 6, 7. Proper navigation lets obligate scavengers expand their search range, so they opt for the more abundant food source availability in wider ranges than possibly going without a meal by staying closer to their home area1,6. Secondly, a good vision or a good sense of smell is necessary to detect and identify target carcasses from immense distances 1. A good example is the Turkey Vulture (Cathartes aura), which can follow the scent of carrion and detect them from great distance 8. Lastly, obligate scavengers have important physiological adaptations as well. For instance, they have extremely acidic stomachs (pH=1) which helps to reduce the risk of microbial infections and disease 9.

Figure1: Black Vulture (Coragyps atratus), Photo by: Mary Ballard-Johansson

Figure 2: Turkey vulture (Cathartes aura) eating a young Rockhopper (Eudyptes) Photo by: Jan-Michael Breider

Figure 3: A Juvenile Common Raven (Corvus Corax). An example of facultative scavenger. Photo by:David Turgeon On the other hand, we have facultative scavengers. This category is more diverse and it includes many species that scavenge when they find the opportunity, but they don’t specifically rely on scavenging to survive and reproduce10. Extraordinary food source: Carcasses and Carrions Carrion is different from live prey in several ways. Typically, in many areas, live preys are more abundant and easier to find, because carrion is normally subsumed short after an animal dies 1. Therefore, although carrion could be harder to find (however, it is easy to spot because of the strong odor7), it is easier to obtain than live prey, because it does not hide, flee, or defend itself 11. Despite the fact that carrion is infrequent compared to live prey, an important matter is: in a given environment how many animals die in a way to be consumable for scavengers’ 1.

Predators do not leave enough food for scavengers and they consume most of the carrion. Hence, scavengers must find and depend on carrions from animals that die in other ways rather than predation 10. In different environments many animals die for other reasons such as: disease, malnutrition, accidents and human activities, and trapping by humans, and by that become good resource for scavengers. However, this matter varies depends on the environment and habitat of different animals and birds 1. Scavenging birds and humans Since the late Pliocene, humans and scavengers have been connected 12. Scavenging birds provide important regulation and control services for humans4. Numbers of obligate scavengers have dropped during past decades all around the world, mostly because of anthropogenic factors. Scavengers are the most endangered avian functional group 13 and most of the obligate avian scavengers are presently threatened with extinction14. Eating leftovers and carcasses of different types of animals (wild or domestic) has been the most persistent and important ecosystem services provided by scavengers to humankind 4. Scavengers consume carcasses before they start to rot which can reduce the spread of virulent and contagious diseases 5.Avian scavengers could have economic benefits for humanity as well. For example, in India, some traditional industries make fertilizers by using the bones of cattle that scavengers have already cleaned. Without the vultures, bones would be less hygienic, have lower quality, and would be harder to collect (because they would be covered and coated with rotten tissues15. Reduction of biodiversity is just a beginning for the wildlife downturn that menaces the ecosystem. The current decrease in species abundance is impactful: through extinction and the spread of disease. For scavenging birds, this matter is very important because most of those species are specifically developed to consume the carcasses of large animals. Hence, they have an important role in recycling nutrients and inhibiting the deployment of disease13. These birds play a crucial role in maintaining healthy ecosystems by recycling nutrients and removing the potential sources of infectious disease 16. The global biodiversity of different species is vastly affected by human activities. In areas with a high number of people, a small number of scavengers survived, and this matter suggests that human activities supersede other events in forming the scavenger communities17. Killing the birds directly through poaching and using body parts 18 for folk medicines and rituals 19, as well as collisions with man-made structures, such as power lines 20 and wind turbines 21, are responsible for many bird deaths. Scavenging birds such as vultures have experienced the most critical decrease in the population of their species through different years. Humans have caused a great deal of the destruction by, for example, using pesticide-laced carcasses in predator deterrence, and using various chemicals in veterinary medicine 22 such as Diclofenac in livestock to diminish inflammation caused by traumas and infectious diseases 23. In less than 10 years, the population of vultures in the Indian subcontinent, decreased because Diclofenac was poisoning the carcasses of livestock which caused some serious renal malfunctions in vultures and resulted in their death 24. At least three species were affected and were thereby listed as critically endangered by IUCN 25. Taking in the small spheres or fragments from lead bullets causes another serious threat to scavenging birds 26. Fragments of lead bullets become imbedded in muscles and soft tissues of different carcasses. Scavengers can ingest the lead projectiles and their fragments from killed game that is not found, or from the remains after field dressing. Since 1991, using lead-based ammunition is banned for waterfowl in the USA, but are still legal for other gamebirds. Hence, today we have lead poisoning as one of the dominant causes for death of scavenging birds (e.g.

California Condor)27. The lead poisoning problem is also documented for other obligate scavenger, the Turkey vulture, as well as facultative species such as great horned owls (Bubo virginianus), golden eagles (Aquila chrysaetos), bald eagles (Haliaeetus leucocephalus), and common ravens (Corvus corax). 28, 29, 30. Lead poisoning has also been an issue for some other scavenging birds such as the Egyptian vulture(Neophron percnopterus)31 and the bearded vulture(Gypaetus barbatus)32. Absence of scavenging birds, which are obligate scavengers, could favor facultative scavengers. Because they then have more carrion and carcasses to feed on. But this puts other species’ health in danger and at risk. (especially humans’ health). In the India subcontinent sample, populations of dogs and rats infected with rabies and bubonic plague have elevated. 33, 15. Hence, scavenging birds’ populations are the key to pest control in so many regions 4. Aim My objective is to determine the future extinction rate of scavenging birds based on extinction rate of large mammals, which are the prey of these birds, I want to determine how many birds species are going to be affected by food loss. In addition, what is the relationship between the diversity of scavenging birds and other potential predictors, such as temperature seasonality, annual temperature, elevation, annual precipitation, and precipitation seasonality. Material and Methods Input data for birds At the beginning I gathered and identified the relevant input data and as part of this, I explored all bird species to could be classified as scavengers. Moreover, I identified current diversity patterns in scavenging bird species. Two crucial and significant factors to categorize and classify birds for the right threshold are their body mass and their diet and food sources. Based on these factors, species that weighed more than 500 grams and with more than 10 percent of scavenging were included in the analysis. Analysis conducted on the EltonTraits dataset resulted in 77 species of scavenging birds that qualified for the current study. Secondly, it is imperative to ecological, environmental and biological sciences that one investigates and establishes current diversity of scavenger birds in the context of relevant environmental factors (climate and elevation in our case) so that an estimate of how this diversity will change over time can be projected. This topic is especially relevant in the modern world, where climate change and ecological destruction are prominent, and the changing climate in the world today is responsible for the extinction of many different species.

The spatial data of birds was downloaded from IUCN34 website in the form of polygon shapefiles. Shapefiles are sets of spatially precise polygons or shapes that exhibit geographical locations. I rasterized the shapefiles to simplify the distributions into discrete and distinct units, to calculate diversity maps of scavenging birds, and to estimate the distribution of different species. The shapefile of each species contains information about coordination, projections and mapping attributes, such as presence of the birds in each environment, origin (endemic or migratory), and seasonality (yearly distribution). For the matter of this research, I only used extant birds with year-round and breeding season areal distribution. I turned the polygon shapefiles into raster files to transfer values associated with spatial data to raster cells. This is done to see the distribution of birds on a worldwide map by projecting it in CEA (Cylindrical equal-area projection), Behrmann projection. This projection is proper for this analysis because

6 equal-area maps in all areas are proportional to one another. Behrmann projection is equal area projection for all latitudes but the shapes are only accurately represented at 30°N and 30°S.

To project the globe in a map form, I converted geographical degrees to meters. Each degree of the globe represents 100 km. I calculated the range of the scavenging birds which shows where they are distributed. (Figure 4)

Figure 4: Two examples of raster range maps. On the left side it is cinereous vulture (Aegypius monachus) raster and on the right side, it is Turkey vulture (Cathartes aura) raster file

Calculating “Effective scavenging richness value”

Each one of these bird species has a percentage that indicates how much of their diet is based on scavenging. I multiplied all species rasters by the fraction of scavenging they have, and as a result, it is the “Effective scavenging richness value” (ESRV) for each species. From this we can say if a bird is 100% a scavenger, then its scavenging richness value is 1.

I then summed all the raster files for the different species into one large raster file by layering all rasters of all species in form of a map to have a better worldwide overview on the distribution of scavenging birds and their scavenging richness value. The resulting map is discussed later.

Other predictors

After making scavenging birds richness map, the relationship between potential predictors and scavenging birds’ richness and diversity. Subsequently, I downloaded other predictors from different websites:

• Human foot print records: TIF files from Socioeconomic Data and Applications Center35 which is aggregated human pressure on the environment in 2009, in ~1 km resolution and eight variables such as population density, built-up environments, pasture lands, crop lands, electric power infrastructure, roads, railways, and navigable waterways controls it. 36 • Elevation: Global climate and weather data37. These spatial data are the mean of the values and aggregated to 30 arc-second spatial resolution. For each cell grid of elevation rasters, the intervals were enumerated to sea level38. • Large mammals data: The Phylogenetic Atlas of Mammal Macroecology (PHYLACINE)39 and large mammals are the main focal point of this research. • Climate data: Climatologies at high resolution for the earth’s land surface areas (CHELSA)40.

I matched the map resolution and projection of all these predictors to my scavenging richness map, so that the variables could be compared. The values chosen included: annual temperature, temperature seasonality, annual precipitation and precipitation seasonality, as these factors are the elements of the environments of birds. Shifting in temperature and different precipitation patterns yielding from climate change would induce availability of carcasses and can induce strikes on scavenging communities all around the globe41,42 . So, accordingly, I have chosen the mentioned predictors. Such factors have been used in modelling studies to show that large birds, such as the Andean condor (Vultur gryphus), choose sites to sleep and nest that are stable with little rainfall43.

I contemplated and envisaged the fluctuation in large mammals’ population in the future as the main impetus for future scavenging richness and diversity. Thus, as I did for scavenging birds, I classified the right threshold for large mammalian prey as well. I subsetted downloaded data and excluded large mammals weighing less than 9999 grams and extinct species. Extinct species include historically extinct (EX), extinct in the wild(EW), and extinct prehistorically which means that the species went extinct in the late Pleistocene or in the Holocene before 1500 CE(EP) 39

After the data is organized and prepared, I did the statistical analyses to see how the predictors could affect the ESRV. At first, I analyzed the relationship between the scavenging value and each different predictor through linear regression. Multiple linear regression is a simple method to analyze and describe the relationship between one dependent variable and several independent variables. The formula of multiple linear regression is: yi=β0+β1xi1+β2xi2+...+βpxip+ϵ as in:

yi=dependent variable xi=independent variables

β0=y-intercept

βp=slope coefficients for each independent variable

ϵ= residuals

For this research, the dependent variable is ESRV, and the independent variables are: Annual temperature, temperature seasonality, annual precipitation, precipitation seasonality, large mammals’ distribution, elevation, and human footprint, Y- intercept is value of Y when x=0. By generalizing it to this study, it means the value of ESRV when all predictors are 0. Slope coefficient is the value of x.

In linear models we can have a phenomenon called multicollinearity which means independent variables can be closely correlated. This can cause redundancy. A good regression model is one

8 in which each independent variable correlates profoundly with the dependent variable but correlates only minimally with other independent variables. To check up on this matter, after executing previous steps, I also ran VIF (variance inflation factor) to see how correlated my predictors are. VIF for all predictors is below the accepted value of 5, which means they are not highly correlated. Hence, all predictors can be included in the analysis.

Afterwards, I obtained the extinction rates for all bird species and mammals from two papers44,45 that calculated the future probability of their extinctions. The extinction rate was derived by using current IUCN status and applying Markov chain Monte Carlo algorithm in iucn_sim software that simulates the future. I used the extinction rate to calculate survival rate by subtracting the extinction rate from 1 and multiplying it to the heat maps of scavenging birds and large mammals to visualize the result. I coordinated the lists with the list of species in my data set. I multiplied the current birds’ and mammals’ diversity rasters by the probability of their extinction to conclude the probability of survival. Then, by summing up all rasters, I derived a heat map of the future of birds and mammals’ diversity and distribution.

The richness of species of predators is robustly connected to prey richness. On the other hand, for species climate factors are stronger than predator richness46.This indicates that large mammals, as preys, are good proxies for total animal availability. Hence, at the end, I subtracted current birds’ diversity of future birds’ diversity to see how many birds’ species will be eliminated. I repeated the same step for large mammals’ species as well to have result of extinct large mammals in future. Then, I multiplied the map of the extinction of the mammals by the effective size of it to estimate how many bird species will lose food in future and starve. And for the last step, I subtracted Bird extinction from birds’ starvation to see how many bird species will go through extinction for other reasons than starvation.

All analysis was conducted and took place in R Studio and R version 4.0.247.

Results

The heat map resulted from layering the rasters of all 77 species. Most diversification of species occurs in Central and South America, majority part of Africa, and Indian subcontinent. South America is almost completely inhabited by scavenging birds, but it is more yellow color indicating they have lower ESRV. However, in Africa and some parts of Indian subcontinent we can see more green cell rasters and this means these areas have higher total ESRV.

Figure 5: This map shows distribution of scavenging birds over different continents during present time and shows the level of their effective scavenging richness. Green areas show the high level of scavenging, and as it becomes more yellow/pink, it means the level of scavenging richness is decreasing. The unit of the map represent the sum between the number of species present and their dietary scavenging proportion. As it is shown in figure 5 the greener the area is, the higher total ESRV exists. Like in east Africa and Indian subcontinent metric of effective scavenging richness is higher than the rest of the map. As it goes more towards yellow/pink color, the level of total ESRV declines. As it is visible, scavenging birds are more distributed and have higher diversity on South America with lower level of total ESRV.

Figure 6: This is the heat map of effective scavenging richness and distribution of surviving individuals within next 100 year. This was the result of multiplying present heat map by the survival rate of the birds in future. In the legend it is shown that around 1 species is eliminated.

Figure 7: This is the heat map of the current number of mammal species in each area. The number of species is between 0 and 40. This shows how large mammals, >10 kg, are distributed all around the globe during present day.The green indicates highest diversity of large mammals.

Figure 8: This heat map is derived by multiplying the current diversity map of large mammals by the extinction rates, yielding future surviving specie

Table 1: Multiple linear regression estimates for potential predictors. All P-values are artificially low and are calculated assuming independence between sample sites.

Coefficients: Estimate VIF (Intercept) -4.632E-15(0.006) ---- Human Footprint -0.5094(0.008) 1.68 Large Mammals 0.3071(0.008) 1.80 Elevation 0.04999(0.007) 1.60 Temperature Seasonality -0.4258(0.014) 5.52 Annual Temperature -0.07351(0.013) 4.94 Annual Precipitation -0.08782(0.008) 2.02 Precipitation Seasonality 0.1031(0.007) 1.60

Table 1 shows the estimates of multiple linear regressions between the ESRV and other predictors. At first I made a simple linear regression between each predictor and ESRV. After running multiple linear regression, the variables for human footprint, annual temperature, temperature seasonality, and annual precipitation have negative slopes. This means effective scavenging richness is higher when the value of the independent variable decreased. However, for large mammals, elevation, and precipitation seasonality, the slope is positive. This means it has positive effect on effective scavenging richness. Strongest predictor is human footprint and after that, temperature seasonality is also stronge.

Now that we see large mammals have positive effect on the diversity of scavenging birds, what will happen if we simulate the future 100 years extinction, what will happen to scavenging birds?

Table 2: Future estimates for scavenging birds, this table shows the extinction and survival of the birds based on IUCN red list, absence of mammals in the future, and other reasons. CurrentBirdsDiversity is the heat map of scavenging birds’ diversity and distribution during present time. FutureBirdsDiversity is the map of scavenging richness and distribution of surviving individuals within next 100 year. Same premise is for CurrentMammalsDiversity and FutureMammalsDiversity. LargeMammalsEstimate is the estimate of large mammals that was resulted in the multiple linear regression calculations.

The following maps explain what will happen to birds due to the extinction of mammals (Figure 9,10 and 11).

Figure 9: Bird extinction which I concluded by subtracting the present diversity of scavenging birds all around the globe, from the future predicted diversity of scavenging birds within next 100 years. In each cell of the raster, how many birds´ species is expected to go extinct based on IUCN red list status. Up to 1.2 species is predicted to go extinct in the greener areas and as it turns to yellow-pink it fluctuates down to zero number of species.

Figure 10: Mammal’s extinction, which was resulted with the same method as birds’ extinction. In each cell of the raster, the number of large mammals’ species are expected to go extinct based on IUCN red list. Up to almost 7 species are predicted to go extinct in green areas and as it turns to yellow/pink, it shows lesser number of species extinction. (this map is only for terrestrial mammals and aquatic marine mammals e.g., whales, were not included in the calculation.)

Figure 11: Starvation which is the result of multiplying figure 7 by the estimate of large mammals’ that we have calculated in the general linear regression, which is showing reduction in the birds’ diversity due to changes in food availability. So, any cell in this heat map that shows higher value than the cells in figure 6, that is an extinction potential for scavenging birds due to starvation problem. So, now the question is: are there areas of the world where the food loss due to loss in mammals is bigger than the loss of birds? Figure 9 addresses this question:

Figure 12: Bird’s starvation which is the result of subtraction between figure 9 and figure 11. This map shows how many birds will go extinct for reasons other than starvation. This is an additional predicted potential extinction in birds due to the reduction in food. There are areas in world that where relatively larger number of scavenging birds than appears to be food

13 for. So, some places may end up with more scavenging birds than large mammals and that means less food for the birds. (the legend shows the values of differences and this is why the numbers are minus)

Discussion Soaring ability is a common characteristic for many scavenging birds (like Buzzards, Condors etc.). These birds have higher scavenging richness. Hence, more elevated areas can have higher ESRV. As is shown in Table 1, temperature seasonality is the second strong driver for ESRV. Places with less temperature seasonality has higher level of ESRV. Temperature seasonality addresses the differences between the annual minimum and maximum temperature. Lower temperature seasonality is mostly around Ecuador and also close to the water and coastal areas. Water regulates temperature in all seasons and that makes places close to waters suitable for habitation. In the maps it is shown that ESRV is higher around coastal areas because food availability is higher around those areas as well. Figure 11 was calculated by multiplying mammal’s extinction raster by the effective size. This shows us the starvation heat map. Effective size is the non-scaled number of large mammals estimate (slope) in the multiple regressions (non-scaled number of the slope is 0.04699(. For each extra large mammals’ there are average of ~0.05 extra scavenging birds in each cells of the rasters. This means if a cell loses 20 large mammals’ species, but less than a 1 bird, it is a potential threat for starvation. For the birds’ starvation we removed any positive and 0 values. This is because if there is food for scavenging birds, they may still go extinct for other reasons. Basically, the point is in different areas around the world, that will be relatively larger number of scavengers existing than the large mammals. This means less food for scavenging birds. Figure 9 shows loss of scavenging birds based on IUCN and in based on the legend we can see for each cell it is predicted to lose up to 1.2 species in future. In Figure 12 we can see in some places in Africa and South America, starvation has a risk of up to 0.12 This map shows 10% additional extinction rate added because of starvation. Absence of scavenging birds, which are obligate scavengers, could favor facultative scavengers. Because they then have more carrion and carcasses to feed on. But this puts other species’ health in danger and at risk. (especially humans’ health). In the India subcontinent sample, populations of dogs and rats infected with rabies and bubonic plague have elevated. 33, 15. Hence, scavenging birds’ populations are the key to pest control in so many regions 4. In more general overview, scavenging birds, more specifically obligate scavengers, are inseparably and inevitably connected to the abundance and availability of carcasses. Hence, any change in carrion resources affects balance and dynamics of scavenging colonies. The point is, climate directly affects the availability of carcasses and food sources for scavengers. 48, 49, 50. As it was mentioned earlier, temperature and precipitation are important factors for scavenging birds’ diversity. Climate change has a direct effect on precipitation51 and temperature52. Thus, Climate changes can lead to discrepancy and imbalance between animals and plant populations all around the world, resulting in different birds’ communities decline 53. Nevertheless, there is not enough information about the climate change effects on carcasses and carrion. Diversified temperature precipitation system can affect carcasses availability,

14 consequently affects scavenging colonies across the world 41. For example, many diseases can be caused by climate changes in different geographical areas54. These changes in disease create irregular deaths among animal populations, thus creating “feast or famine” situations. Fluctuations in carcasses availability decrease the variation of food sources among scavengers 55. Climate change can also create competitions between vertebrate scavengers and microbes. Because with every ten-degree increase, microbial decomposition doubles up 50 and that causes 20 to 40% decrease in carcasses availability for vertebrates 56. Thereupon, preponderance of obligate scavengers is seriously threatened and critically endangered 14. Some species can be verisimilar to fluctuation of seasonality of annual rainfall, which affect the availability of food and nesting sites required for successful reproduction 57. Conclusion This study shows that large mammals’ extinction is not the main driver of scavenging birds’ extinction. But starvation due to loss of large mammals is a big additional threat for scavenging birds. Another matter is, facultative scavengers have better chance of survival in future. Their propensity to eat other food sources and other methods to obtain food helps them to have a better chance of surviving. On the other hand, obligate scavengers which are more dependent on carcasses, are more vulnerable to the loss of food and they are more threatened. Scavengers are necessary to maintain a clean and stable ecosystem. So, it is vital to have a proper plan to save them all. By protecting large mammals, we are even protecting scavengers.

Acknowledgements Firstly, I want to give a big thanks to Søren Faurby and Robert Cook for their patience and helps in R and statistics and bearing with my ignorance. I also want to thank Mary Ballard- Johansson to be there for me and helping me to write my thesis in way that is understandable. And of course, I want to thank my parents to be the reason I am here and doing my masters. And another big thank to Ali Mohseni for helping me and giving me hope when I was too down to do anything.

References:

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Appendix 1: Popular science summary Tragic destiny for scavenging birds: Scavenging birds have massive roles in cleaning and regulating services. It is a common belief that microorganisms do more and better job at cleaning for environment. But the truth is, vertebrate scavengers do the highest level of scavenging and cleaning1. These services are important for reducing diseases. Through time, the number of scavenging birds is declining for so many reasons such as human footprint, lead poisoning, killing them directly for poaching and rituals, as well as getting stuck in man-made structures such as power lines and wind turbines. There are two type of scavengers: obligate scavengers (like vultures) that are more specialized scavengers that get the vast majority of their food source from scavenging, and facultative scavengers (like crows and ravens), which gain most of their needed nourishment through ways other than scavenging. Scavengers need specific characteristics for surviving. For example, Turkey vultures have a good sense of smell to detect carcasses. They also need good sense of mobility6 and physiological adaptations such as very strong acid in their stomach to reduce the microbial infections risk. Predators do not leave enough food for scavengers. Hence, scavenging birds need to rely on carcasses that died for other reasons than predation. But this could also put them in danger. For example, in Indian subcontinent, many birds died because of consumption of poisoned carcasses with Diclofenac. Beside these matters, fluctuations in precipitation and temperature all around the world are causing problems for these birds as well. But climatic factors are putting most animals in danger. Large mammals are not exceptional. The point is, large mammals are very good strong food source for scavenging birds and decline in their diversity could put birds into an additional jeopardy. I calculated the future extinction rate of birds and mammals based on IUCN red list, it has been settled that there are some areas that the number of extinct large mammals, will be more than the numbers of scavenging birds. This means in some places (like Africa) scavenging birds will going to be in big threat of starvation beside other reasons as well. Large mammals’ extinction is not the main reason for scavenging birds’ extinction. Starvation due to loss of large mammals is a big additional threat for scavenging birds. But in this game, obligate scavengers are in more danger. Facultative scavengers have better chance of survival in future. They can easily rely on other methods to find proper food sources and this helps them to have a better chance of surviving. On the other hand, obligate scavengers which are more dependent on carcasses, are more vulnerable to the loss of food and they are more threatened. Scavengers are necessary to maintain a clean and stable ecosystem. So, it is vital to have a proper plan to save them all. This shows that the chain of environment is unbreakable and it is vital to have a proper plan to save them all. If we have a good conservation plan to prevent large mammals’ extinction, there is a high chance to save scavenging birds on this way as well.