[guest student post] Sky Islands Drive Philippine Megadiversity

 guest post by Kaola Alezandra Pamonag

     Beyond our famous dreamy white beaches and pristine landscapes, the Philippines is also a biodiversity hotbed, home to a multitude of unique, cute, and cuddly critters found nowhere else on the planet. A recent study showed that the ancestor of the endemic forest rat (at this point, I think some of you are now disagreeing that these rodents are cute and cuddly), Bullimus, found its way to our shores and radiated into three recognized species (B. gamay in Leyte, B. bagobos in Mindanao & B. luzonicus in Luzon) and eight new possible species from Luzon populations, currently undergoing speciation (Kyriazis et al., 2017).

        The diversification of Bullimus rodents in Luzon is strongly driven by “sky islands”. Although this may sound like a cosmic phenomenon or a place where some deity lives, like the Earth’s great matriarch, Gaia, ‘sky islands’ are simply defined as isolated mountain ranges (Kyriazis et al., 2017). Luzon’s dynamic geologic history from its origin 26-30 million years ago has shaped its rugged topographic features, from its rolling hills, narrow valleys to its massive ranges and isolated high mountains. Luzon is geologically active to this day, with volcanic eruptions constantly altering habitats and environmental regimes. Environmental conditions such as rainfall, temperature and vegetation vary within Luzon’s many isolated mountains. This has created habitat and climate heterogeneity along the elevational gradient, which have been the primary drivers of speciation (Heaney et al., 2016b). Sky islands create multiple habitats within habitats. They hamper dispersal between mountains, resulting in incipient isolation and ultimately fostering diversification within islands (Collver, 2016; Heaney et al., 2016a; Kyriazis et al., 2017).

(Bullimus luzonicus. Photo edited from: https://thewebsiteofeverything.com/img/Luzon_forest_rat.jpg)

Bullimus belongs to the ‘new endemic’ group of forest rats that reached the Philippines fairly recently -- and by that, I mean about 1-3 million years ago! The colonization occurred during the late Pliocene or Pleistocene, an epoch marked by extreme glacial cycles and sea level fluctuations but that is best known as the “Great Ice Age”. These rodents initially landed in southern Philippines, but how they did it and from exactly where remains largely unknown (Heaney et al., 2016b; Kyriazis et al., 2017). They could have swum across the harsh ocean, with their tiny feet, walked on those historical land bridges or most likely rode a log or a patch of vegetation and rafted to Mindanao (Heaney et al., 2016b; Ali & Vences, 2019). Genetic data suggest that these ground-living rodents are close relatives of Sundamys from the Sunda Shelf in Southeast Asia (Schenk et al., 2013).

Bullimus luzonicus is a large omnivorous rat, reaching about 520g with a tail shorter than its head and body. They have big eyes and ears with dark brown fur on the upper part and a silvery brown underside but may appear grayish brown or golden brown in some populations (Heaney et al., 2016b). B. luzonicus has a wide habitat range, probably the widest among Luzon’s small mammals, from sea level to 2740m elevation, but they are surprisingly more common in lowland areas (>300m). Their habitat includes highly disturbed forests with dense grasses, secondary growth forests and mossy forests (Heaney et al., 2016b; Kyriazis et al., 2017).

Bullimus starkly contrasts with the ‘old endemic’ rats that came earlier, approximately 7-15 million years ago, when the Central Cordillera of Luzon was just forming. Members of this older group are the two most diverse lineages of Luzon endemics: the arboreal and herbivorous cloud rats that live in cloud forests and the earthworm mice, named so because of their predominantly earthworm diet. The old endemics flourish in areas towering above sea level (>1500 m) and they make up 84% of Luzon’s endemic diversity of non-flying small mammals (Heaney et al., 2016a; Heaney et al., 2016b; Kyriazis et al., 2017). Their remarkable diversity and abundance in forests high in the mountains suggest that they may have, in some way prevented the elevation tolerant Bullimus from successfully invading habitats in higher altitudes (Heaney et al., 2016b). Intriguingly, lowland habitats like river valleys also prevent dispersal to adjacent mountains, isolating them in mountaintops that eventually promote diversification (Kyriazis et al., 2017).

The traditional method of utilizing morphological features in species delineation, combined with modern molecular techniques, provided more precise and comprehensive knowledge on Bullimus’ diversification pattern. DNA analysis identified Luzon populations of Bullimus luzonicus as several distinct species but only the southern Luzon population was morphologically diagnosable. The greater distinction in southern Luzon is a consequence of longer isolation, while speciation of B. luzonicus populations in the rest of Luzon is considered incomplete. Hence, there is a pattern of increasing differentiation from southern to northern Luzon, confirming that the jump-off point of their island-hopping journey was in Mindanao and recently expanded, northwards to Luzon. With the dearth of habitable lowland areas, B. luzonicus is expected to differentiate further and in time fully represent incipient intra-island diversification (Kyriazis et al., 2017).

In contrast to B. luzonicus, B. bagobos populations found in different sky islands in Mindanao did not show any pattern of intra-island diversification. This was attributed to: (1) the difference in topographic/habitat complexity and historical lowland connections of Luzon and Mindanao, (2) varying species ecologies between B. bagobos and B. luzonicus, and/or (3) inadequate geographical sampling in Mindanao (Kyriazis et al., 2017). Could diversification dynamics really differ between Luzon and Mindanao, despite having roughly the same area (ca. 98,000 km²) and topography? And will more comprehensive sampling in Mindanao reveal congruence? These questions remain as the untold stories of the enigmatic Bullimus diversification (Heaney, et al., 2016a). Nonetheless, the study makes a convincing argument that sky islands generate different ecological niches, which support Luzon’s burgeoning endemic diversity. Now harboring 52 endemic species of non-flying small mammals, Luzon’s endemic species richness is the highest record yet in the world (Collver, 2016; Heaney, et al., 2016a).

The diversification of forest rats in the sky islands of Luzon is indeed an exceptional spectacle of endemic evolution. Its discovery proves that studies on small mammals in the Philippines have come a long way, yet a great amount of information still needs to be learned. It also gives a powerful message to intensify field surveys and to continue research efforts on Philippine biodiversity. The Philippines is endowed with over 7,000 islands teeming with native biodiversity that awaits to be uncovered. All we need is a shared passion for nature, a curious mind, and probably strong legs to explore our megadiverse islands --- in the sky and across the seas.

   -guest post by Kaola Alezandra Pamonag

About the author: Kaola is currently pursuing a Master's degree in Biology at the University of the Philippines Visayas and is primarily interested on the biology of sardines. She loves outdoor activities but due to quarantine restrictions, she now spends her spare time watching TV series or  fan girling over her favorite boyband.

Blog owner's note: As a culminating activity to my MS Biology class in Biogeography, I asked my students to write a blog post on a topic in biogeography. We welcome constructive comments on this student piece.

References:

Ali, J. R., & Vences, M. (2019). Mammals and long‐distance over‐water colonization: The case for rafting dispersal; the case against phantom causeways. Journal of Biogeography. doi:10.1111/jbi.13659

Collver, J. (2016, July 15). Cloud Rats of Sky Island: The Philippine Island with the highest number of unique mammals. BBC Science Focus Magazine. https://www.sciencefocus.com/nature/cloud-rats-of-sky-island-the-philippine-island-with-the-highest-number-of-unique-mammals/

Heaney, L. R., Balete, D. S., Duya, M. R. M., Duya, M. V., Jansa, S. A., Steppan, S. J., & Rickart, E. A. (2016a). Doubling diversity: a cautionary tale of previously unsuspected mammalian diversity on a tropical oceanic island. Frontiers of Biogeography, 8(2). doi:10.21425/f58229667 

Heaney, L. R., Balete, D. S., & Rickart, E. A. (2016b). The mammals of Luzon Island: Biogeography and natural history of a Philippine fauna. Johns Hopkins University Press.

Kyriazis, C. C., Bates, J. M., & Heaney, L. R. (2017). Dynamics of genetic and morphological diversification in an incipient intra-island radiation of Philippine rodents (Muridae: Bullimus). Journal of Biogeography, 44(11), 2585–2594. doi:10.1111/jbi.13063

Schenk, J. J., Rowe, K. C., & Steppan, S. J. (2013). Ecological Opportunity and Incumbency in the Diversification of Repeated Continental Colonizations by Muroid Rodents. Systematic Biology, 62(6), 837–864. doi:10.1093/sysbio/syt050 

https://thewebsiteofeverything.com/img/Luzon_forest_rat.jpg