Bird diversity on shelf islands does not benefit from recent land-bridge connections.

Above: Brown-throated Sunbird Anthreptes malacensis, a species very commonly found on islands in Sundaland.

When studying biogeography, I make a constant effort to tell myself that what I am witnessing today is just a mere snapshot in time. I’m still in my 20s, while the planet is quite a number of times older than me. Seemingly strange observations hence make much more sense once I consider various historical influences of Earth’s climatic variations and land movements. When I first started this project, I fully expected the data to tell such a story: that species distribution and composition of birds on islands in Sundaland are primarily determined by historical factors too.

Cover image article: (Free to read online for a year.)
Sin, Y. C. K., Kristensen, N. P., Gwee, C. Y., Chisholm, R. A., & Rheindt, F. E. (2022). Bird diversity on shelf islands does not benefit from recent land-bridge connections. Journal of Biogeography, 49, 189-200. https://doi.org/10.1111/jbi.14293 

Satellite images of Sundaic Southeast Asia show that the region comprises many islands today – roughly 17,000 of varying shapes and sizes. Had such technology (and us) existed half a million years ago, we would have witnessed a completely different landscape: no islands scattered across the region, and the whole of Sundaland completely exposed as land instead. It was only ~400,000 years ago that consistent subsidence of the entire shelf led to its partial drowning, and since then, sea level fluctuations have been constantly changing the land configuration. During interglacials, high sea level causes land to be broken up into islands, while during glacial periods, the sea level is ~120 metres lower than it is today and Sundaland gets “reunited” by land-bridges. While we live in a period of interglacial, the last glacial maximum occurred only as recently as ~20,000 years ago. Furthermore, during the Holocene sea level peak ~7,000 years ago, the sea level was 3-5 metres higher than it is today. This rise causing low-lying islands to be completely submerged before they re-emerged again when the sea level returned to its current form. The configuration of Sundaland we see is truly ephemeral: a majority of the islands are shelf islands that get connected to the mainland by land-bridges during glacial periods, while a small subset are deep-sea islands that have no historic connection to the mainland.

As a consequence of the Sundaland’s complex geologic chronicles, we would expect biodiversity patterns on its islands to be heavily influenced by the past: an island that enjoyed more land-bridge connection to the mainland and used to be bigger throughout evolutionary history should harbour more species. This phenomenon where species richness in an area exceeds the expected value given its size is called supersaturation and is observed in lizard diversity on land-bridge islands in Baja California and birds on some satellite islands of New Guinea. In addition to supersaturation, recently submerged islands that just had terrestrial biodiversity obliterated should be expected to have species composition differing from similar-sized islands that did not drown.

Map of Sundaland delineated by the Sunda shelf in light blue. Study islands (n=94) are highlighted, with deep-sea islands in yellow and shelf islands in red. Many small islands are not visible at this scale and circle sizes indicate the number of study islands within a 50 km radius. The number of endemic species-level bird taxa, if any, is indicated adjacent to islands following the same colour scheme (only one shelf island—Kangean, in the extreme southeast of the shelf— has an endemic species-level taxon). In the case of the Mentawai islands (dotted yellow ellipse), three taxa are endemic to the whole island group which forms one connected paleo-island.

We investigated these hypotheses by analysing the effects of various past and present geographical variables on diversity patterns of birds on islands distributed across Sundaland. We found evidence that bird endemicity was mainly restricted to deep-sea islands. The lack of any historical land-bridge precluded gene flow between the bird populations and gave rise to endemic species. This initial result provided a strong clue that historical processes shaped diversity. However, contrary to our expectation, neither the duration of mainland connection in the past 20,000 years nor the average change in island area in recent geologic history was shown to influence the number of species breeding on the shelf-islands. Instead, the classic Island Biogeography parameters of island area and distance from mainland predominantly explained species richness. Our unexpected results suggest that once a landmass is disconnected from the mainland due to rising sea levels – effectively becoming an island – extinction kicks in rapidly, leaving no room for “excess” species as the island shrinks. We also found that in addition to island area and distance from mainland, the proportion of landmass surrounding an island played an important role in maintaining species richness. For example, a solitary island that is 50 kilometres from the mainland would have lower species richness than a similar sized island, also 50 kilometres away, but clustered together with a group of other islands. In Sundaland, avian species richness of an island equilibrates quickly based on extinction-immigration processes, which are in turn influenced by the island’s present-day geographical parameters.

We additionally discovered that species composition on similar-sized islands did not differ across recently submerged and unsubmerged islands. On recently submerged islands, the bird population present today could only have arisen from entirely new colonisers since the island was wiped clean when it drowned. These birds, by their capability of occupying brand-new islands, can be said to have high dispersal and colonising ability. On the contrary, islands that were never submerged should technically be able to host both colonisers and surviving populations from before the islands shrank. Yet our results showed that the two island classes had species composition unaffected by their history of submergence. This observation implies that only a subset of species is capable of persisting on the tiniest islands in Sundaland: the strongly dispersive birds. Our result makes sense when we think about the biology of these animals – their population density is generally low, hence, once an island shrinks below a certain size, an isolated island population is unable to sustain itself. Resultantly, small islands become home only to the most dispersive species as these birds are able to fly around and find partners in nearby islands. Having said that, a majority of these species were intriguingly not island specialists – they were also birds that do well on the mainland too, but all on edge habitats; forest dependent species are the first to disappear once an island shrinks.

Examples of non-island specialists that are commonly found on small Sundaic islands: top left – Collared Kingfisher Todiramphus chloris; top right – Olive-winged Bulbul Pycnonotus plumosus; bottom left – Ashy Tailorbird Orthotomus ruficeps; bottom right – Pink-necked Green Pigeon Treron vernans. Example of an island specialist that is found across islands in Sundaland: middle – Pied Imperial Pigeon Ducula bicolor.

Birds are known for their flight ability, and it might be a counterintuitive idea that endemicity and species composition is shaped due to their reluctance to fly to other islands. However, flying across water is actually a behaviour that many tropical birds generally avoid due to the high risks involved, and this is why only the most adventurous of species do well on tiny islands.

Our work shows that species richness of birds on shelf islands in Sundaland is predominantly determined by present-day geographical parameters. It turns out that, at least for birds, Sundaic islands themselves are also only witnessing a snapshot in time.

Written by:
Yong Chee Keita Sin
Research Assistant, Avian Evolution Lab, National University of Singapore

Additional information:
Instagram @okamoto_keita_sin

Acknowledgements:
I am greatly indebted to the co-authors of our manuscript Nadiah (Twitter @NadiahKrist; nadiah.org) , Chyi Yin, Ryan (ryanchisholm.com) and Frank (Twitter @avianevo; avianevonus.com) for the support and mentorship offered throughout the work. I would also like to thank everyone who helped out in the fieldwork and analyses of our manuscript and Geraldine Lee for comments on this blog post.

Canopy physiognomy governs the distribution of peninsular Indian flying lizards in regions of climatic suitability.

Above: Silhouette of an Indian Flying Lizard in its arboreal habitat.

I have always been intrigued by organismal distributions. Why do certain species occur in certain regions? Why do they stop, sometimes abruptly, at certain latitudes where there aren’t any physical barriers to dispersal? So, when I decided to work on peninsular Indian Flying dragons (Draco dussumieri) for my PhD, it was quite natural to ask why Dracos do not cross the Goa gap (15.8° N) in the Western Ghats mountains of peninsular India.

The Western Ghats is a great laboratory to study various aspects of organismal biology. Life here comprises of organisms with remarkably distinct evolutionary histories that have colonized these mountains at different periods in geological time. The distribution of a species in the Western Ghats is largely a factor of when its ancestor first colonized these mountains and its ecological ability to disperse and adapt to a constantly changing environment.

Cover image article: (Free to read online for two years.)
Chaitanya, R, & Meiri, S. (2021). Can’t see the wood for the trees? Canopy physiognomy influences the distribution of peninsular Indian flying lizards. Journal of Biogeography, 49, 1– 13. https://doi.org/10.1111/jbi.14298 

This mountain range is characterized by three prominent biogeographic breaks, the Shencottah pass, the Palghat gap and the Goa gap. While the former two are physical barriers – deep valleys that cut across the mountains horizontally, the Goa gap is not a physical barrier but an invisible boundary that certain organisms have failed to span. Naturally, biogeographers have long been flummoxed by the absence of certain organisms north of this ‘hypothetical’ barrier. What exactly is going on north of the Goa gap that has prevented otherwise vagile organisms such as Flying dragons from crossing over?

Studies in the past have suggested that the Goa gap may be a boundary that demarcates two different climatic regimes in the Western Ghats, the northern region being warmer and drier. While this is true, certain organisms that are dependent on high rainfall such as the Roux’s lizard (Monilesaurus rouxii) have successfully crossed the gap and colonized regions north of it, but not certain others like Draco that could easily persist in dry forests. So, why have the wet-adapted, arboreal Roux’s lizards been able to colonize the drier regions north of the Goa gap when the more climatically pliant Dracos have not?

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To solve this riddle, Shai and I compared the ecological niches of the Roux’s lizard and Draco to try and decode the environmental variables that govern their distributions. We expected a complex concoction of reasons for Draco absence, but to our surprise we received a very simple answer: tree heights! Draco could not traverse the Goa gap because trees north of this barrier were not tall enough to support them. Simple statistical analyses of canopy physiognomy in regions of Draco presence (south of the gap) versus absence (north of the gap) revealed great disparity in canopy height and coverage. Further, niche models built based only on climatic variables revealed vast expanses of suitable habitats for Draco north of the Goa gap. This indicated that in regions of climatic suitability, the height of canopies influences the presence of these exclusively arboreal lizards.

During fieldwork, my colleagues and I have noticed that Draco occupy the upper reaches of trees closer to the canopy and only descend about midway through the tree trunk during courtship or to forage for ants. The females come down to the ground only once, when they have to lay eggs. The males never do! Roux’s lizards on the other hand, are often found mid-trunk, often even lower near the base of the tree. They are regularly seen sleeping on low shrubs too. So, despite requiring more rainfall for their persistence, Roux’s lizards have been able to disperse across the Goa gap chiefly because they are not dependent on tall canopies.

Our study belabours the point that in the absence of topographic barriers to dispersal, the environmental regime an organism occupies governs its spatial boundaries. It proposes a new, canopy physiognomy based biogeographic hypothesis for the Western Ghats region that can be tested against other model organisms.

Curiously, King Cobras, Slender Lorises and Hump nosed pit-vipers reach the Goa gap from the south but do not pass over. So, what stops these animals from spanning the Goa gap?

The Peninsular Indian Flying lizard, Draco dussumieri, takes flight. Location: Agumbe, India.
Photographed by Vinod Venugopal.

Written by:
R. Chaitanya; School of Zoology, Tel Aviv University, Tel Aviv, Israel

Spatial patterns of species and haplotypes suggest long-term continuity of steppes in eastern Central Europe.

Above: A species-rich meadow steppe near Cristuru Secuiesc (Hungarian: Székelykeresztúr), Harghita County, Transylvania, Romania. Photographed on 29 May 2017 by Wolfgang Willner..

The steppe grasslands of eastern Central Europe have attracted botanists and vegetation scientists for more than two centuries. Not only are they exceptionally species rich, but they also show a great regional diversity. I have been working on these steppe grasslands for many years, and I’m still amazed by the geographical variability of their species composition. However, this variability seems at odds with the often heard opinion that the Central European steppes are, for the most part, human-made habitats created by extensive land-use after clearing the original forests. If that was true, where did all the species come from? And why are the steppes not uniform across large areas, like other anthropogenic vegetation types? Recent paleobotanical studies provide evidence for at least local persistence of steppe-like vegetation in eastern Central Europe throughout the Holocene. Perhaps, the steppe communities of this region are not so anthropic after all?

Cover image article: (Free to read online for two years.)
Willner, W., Moser, D., Plenk, K., Aćić, S., Demina, O. N., Höhn, M., Kuzemko, A., Roleček, J., Vassilev, K., Vynokurov, D., & Kropf, M. (2021). Long-term continuity of steppe grasslands in eastern Central Europe: Evidence from species distribution patterns and chloroplast haplotypes. Journal of Biogeography, 48, 3104–3117. https://doi.org/10.1111/jbi.14269 

We know that large parts of Europe were covered by steppes during the last glacial period. Unfortunately, paleobotanical studies don’t tell us anything about the species composition of the glacial steppes. In any case, the last glacial maximum was not the main problem for the steppe grasslands in eastern Central Europe. The main problem was the mid-Holocene forest optimum. Forests are the natural enemies of steppes, and the period just before the arrival of neolithic farmers offered optimal climatic conditions for forest growth all over Central Europe. However, as mentioned above, steppes might have been able to survive the ‘mid-Holocene bottleneck’ in some refugia. That’s where our current study steps in.

In a previous paper, I showed that the number of European beech forest specialists is inversely correlated with the distance from the glacial refugia of beech. The best explanation for this finding is that many species do not fill their potential geographical range due to a migration lag, that is, they are still expanding from their glacial refugia. I wondered if the same method could be used to shed light on the history of Central European steppe grasslands. However, there were several problems with this idea: First, the mid-Holocene bottleneck might have erased signals of earlier migrations. Second, there was no agreement on the position of potential refugia for European steppe species. One region that had frequently been suggested as a refugial area for the more thermophilous steppe species is the Black Sea coast, in particular the Dobruja region. Other potential refugia mentioned in the literature were the Vojvodina region in Serbia, Transylvania in Romania, western Podolia in Ukraine, and the lower mountain ranges in Hungary. Finally, one of our own studies suggested the northwestern Pannonian region, including the eastern margin of the Alps, as a potential refugium. All these areas are characterised by a high topographic heterogeneity and mostly calcareous substrates, providing potentially suitable habitats for steppe species throughout the whole glacial-interglacial cycle.

The third problem was the ecological heterogeneity of steppe grasslands. The term “steppe” denotes a variety of grassland types, which are quite distinct in their habitat, physiognomy and floristic composition. In our study area, three main types can be distinguished: meadow steppes (which are dominated by broad-leaved grasses and mesophilous herbs, often occurring in a mosaic with forest patches), grass steppes (representing the typical steppe grasslands) and rocky steppes (relatively open grasslands on shallow rocky soils, often with a high portion of dwarf shrubs). As each steppe type might have responded differently to past climatic oscillations, we studied them separately. We tested all combinations of potential refugia and found that, in addition to the current climate and topographic heterogeneity, geographical distance to the Hungarian Central Range is the most important factor in explaining the number of habitat specialists in a region, followed by the northwestern margin of the Pannonian Basin, western Podolia and Transylvania.

To get deeper insights into the history of steppe species, we sampled 3–4 habitat specialists of each steppe type and investigated their intraspecific genetic diversity, using chloroplast DNA. Several species showed a strong geographical differentiation, suggesting migration waves from multiple refugia with only limited subsequent genetic intermixture. The degree of genetic differentiation is clearly inconsistent with the scenario of a late-Holocene immigration of steppe species from areas outside the Pannonian Basin. Most species must have been present in the region since at least the early Holocene, probably much longer, highlighting the importance of the lower mountain ranges surrounding the Pannonian Basin as long-term refugia for European steppe species.

On the basis of these findings, we can confidently say that the steppes of eastern Central Europe are not man-made habitats, although millennia of extensive land-use (mainly grazing) have certainly increased their geographical range. However, land-use has drastically changed since the 19th century. Many steppe grasslands have been converted into arable land or otherwise destroyed. With the large herbivores of the early Holocene extinct, the remaining steppes are dependent on human management. Our study will provide conservationists with additional arguments why these species-rich and unique ecosystems should be preserved.

Written by:
Wolfgang Willner, PhD, Department of Botany and Biodiversity Research, University of Vienna, Austria

Additional information:
https://cvl.univie.ac.at/people/Wolfgang-Willner/

Different species do similar things in anthropic environments.

Above: Two examples of small mammals with very distinct biologies. The Brazilian gracile opossum Gracilinanus microtarsus (left) is a generalist that forages in the ground and inhabits a broad range of habitat types — from primary to secondary forests and forest edges. Such generalists usually profit from human habitat modifications. On the other side, the ihering’s hocicudo Brucepattersonius iheringi (right) is more specialized and spends the majority of its life digging and foraging in forest undergrounds. Pictures taken by Leonardo Crestani in the Aparados da Serra National Park, Rio Grande do Sul, Brazil.

Small mammals are practically everywhere. In fact, they are so successful that they can be found in almost all kinds of habitats. A popular saying states that “if you kick a stone, a mouse appears”. The truth might be not as extreme, but we are often not aware of how many of these often shy and elusive species are actually living around us. Sometimes we can get a glimpse at their abundance and diversity, when we see large numbers of them scurrying around after crop harvests or logging in forests. If they thrive so abundantly in frequently disturbed habitats, should we actually expect differences in species richness and ecological functions between human-modified and undisturbed, natural habitats?

Editors’ choice article: (Free to read online for two years.)
Luza, A. L., Graham, C. H., Hartz, S. M., & Karger, D. N. (2021). Functional redundancy of non-volant small mammals increases in human-modified habitats. Journal of Biogeography, 48, 2967– 2980. https://doi.org/10.1111/jbi.14264 

Ecological theory and empirical data already provide evidence that small mammals are quick in recolonizing habitats after disturbances took place, cancelling out the local extinctions that happened. But simply replacing a locally extinct population with that of another species is just one side of a coin. It might keep the number of species constant, but it will not tell us much about the structural changes within these small mammal communities. A functionally unique species might simply be replaced by a generalist that does not add anything ecologically new to an ecosystem, or replaces a function that has been lost (Figure 1). To understand the structural dynamics of small mammal communities in modified habitats (Figure 2), we therefore need metrics that are sensitive to changes in species composition and ecological functions, like functional diversity, which measures the range of functional traits found into local communities.

Bearing the apparent success of small mammals in human-modified habitats in mind, I went to the literature. I searched for global, geographically replicated data on small mammal communities to understand if the ‘success’ of small mammals in human modified habitats generally translates into more or fewer ecological functions. These data already gave a good overview on the status quo of small mammal diversity in a wide variety of habitats. However, a major hurdle needed to be overcome to draw global, and general conclusions from these data. The diversity of small mammals is geographically very heterogeneous, with for example many more species in the tropics than in the subtropics. These global patterns in species richness are the effect of millions of years of biogeographic and evolutionary processes that created a geographically very distinct biodiversity of small mammals. While a success story for small mammals, it became apparent that these biogeographical differences actually pose a scientific problem in better understanding species richness and functional changes in human-modified habitats at a specific location. How could we be sure that functional diversity at one location is lower than at another, if one of them has a smaller species pool, i.e. less species around that can colonize a habitat due to different biogeographical histories? Equipped with this question I went over to the Swiss Federal Research Institute to work with Dirk Karger and Catherine Graham, to include a framework that explicitly considers the size and structure of the species pool while measuring small mammal community responses to human influence.

Human modified (top) and natural grasslands (bottom) in the municipality of Palmas, Paraná, southern Brazil. Cattle raising has been a predominant economic activity in the region for at least three centuries. Currently, these grasslands have been afforested with exotic pine or converted into crop fields, resulting in dramatic alterations in the landscape and in the economy of the region. Elusive to the human eye, these natural habitats are filled with a large number of small mammal species with a set of unique traits that provide many important ecosystem functions. Pictures taken by A.L. Luza.

The framework we used basically involved creating a spatially explicit potential species pool for all locations globally. Now we were able to see the ‘potential’ species richness and ‘potential’ functional diversity of a locality, and could compare it to the richness and functional diversity we actually observed. The first thing we saw was that most human-modified habitats are actually quite close to what they are able to achieve in terms of species numbers. While this sounded like good news in the beginning, a second pattern quickly emerged. A higher species richness in human-modified habitats comes with an increase in functional redundancy, as those species which profit from human-modification do not add new functional traits into modified habitats. This means that practically, the species profiting from human habitat modifications all do the same when it comes to their functional role in an ecosystem.

So what exactly should we take from these results? Mainly that human modifications are changing the functional roles of small mammal communities by making generalists the winners, and severely penalizing functionally distinct species. Humans are homogenizing the functions in ecosystems, which could lead to severe changes in ecosystem services and nature’s contribution to people.

Written by:
André Luza; Institution: Universidade Federal do Rio Grande do Sul

Additional information:
https://luzaandre.weebly.com/

Acknowledgements:
I would like to thank Dirk N. Karger for helping me write this blog, as well as Catherine H. Graham, and Sandra Maria Hartz for many fruitful discussions on these topics during the course of my PhD.