[guest student post] Limited Dispersal Leads to High Endemism in Philippine Rafflesia Species

Guest post by Lilcah Angelique Opiña

        Rafflesias are one of the most intriguing flowering plants in the world. They are known for their big, beautiful, and surprisingly putrid flowers that mimic the smell of dead meat to attract pollinators. They are also parasites with no leaves, no chlorophyll, and no roots. Rafflesias only put forth large flowers and inconspicuous fruit. They use vines from the genus Tetrastigma (Vitaceae) as their hosts and completely rely on them for nutrition. These unique flowering plants are found in every major island in the Philippines. Each species sports unique morphological characteristics that differentiate them from one another.  They are also highly endemic, with 12 of the 13 Philippine species located only on a single island.

Distribution map of Philippine Rafflesia species, reproduced with permission from Pelser et al. (2019)

What could contribute to such high endemism? A recent study shows that the high endemism of rafflesias in the Philippines is due to their limited dispersal. This means that the seeds of rafflesias probably were not able to travel long distances among the different islands. But where did they come from? And where did they go? DNA from 12 of the 13 Philippine species was used for biogeographical analyses to reveal the weird dispersal patterns of the rafflesias. Specifically, the study looked for inter-island dispersal events that would show if these plants were crossing to other islands, and they found only a handful of these events. The estimated ancestral range was found to be in Borneo, followed by subsequent colonization of other nearby areas like the Philippine archipelago. Based on the results of the biogeographical analysis, it was proposed that they first arrived on Panay Island. Afterwards, nearby Negros Island was colonized. From Panay Island, they moved to Luzon, and from there they colonized Mindanao, Samar, and Bicol (Pelser et al., 2019).

Now I know what you may be thinking. How does a species with limited dispersal abilities have such a weird immigration pattern? Why was the route from Panay to Luzon to Mindanao? After all, Panay is much closer to Mindanao than Luzon. The answer may lie in the Philippines’ complicated geological history. Did you know that the islands of the Philippines have been constantly moving around? Around 45-50 million years ago, the Philippines looked very different and continued to change to the configuration we see now. At the time, the archipelago may have been connected to Borneo via the Sulu-Cagayan Arc (Hall 2002). This arc could have contained the fragments that would later form Panay Island, right around the time the rafflesias came over. The movement to Luzon would occur later, around 33.5 million years ago. This was followed by Mindanao around 24.8 million years ago when the Zamboanga peninsula was close to Luzon. Meanwhile, Samar was relatively far from Luzon around the time rafflesias arrived there around 20 million years ago. Bicol on the other hand could have been connected to mainland Luzon 5-10 million years ago (Pelser et al., 2019).

                                     Plate tectonics of South East Asia 0-55 Ma (Hall 2002), 

                                                        animation available from SEARG 

Interestingly, most of these island invasions were single, founder events. This means Rafflesia colonized each island only once, and dispersal across islands was very rare. The high endemism also shows that most populations were effectively isolated and had almost no contact with each other. The only species found on more than one island is Rafflesia speciosa. However, the populations of R. speciosa in Panay Island and Negros Island are genetically distinct. This poor genetic connectivity can even be seen if populations are greater than 200 kms from each other on the same island (Pelser et al. 2019). Their absence in other Philippine islands like Palawan, Bohol, and Cebu can also be evidence to support this limited dispersal.

So why do rafflesia species have such poor dispersal abilities? The exact mode of dispersal for these plants are not yet established but animals like pigs, ground squirrels, termites, pangolins and even elephants have been proposed as potential dispersal agents (Hidayati & Walck 2017). Rafflesias produce thousands of tiny seeds housed inside leathery berries. These fruits do not naturally open and presumably need to decay first before the seeds can be released. There is some evidence that ants may be one of their main dispersers. Accounts of field observations describe how decaying fruits were swarmed by ants which seem to be carrying off the seeds (Pelser et al., 2013; Pelser at al. 2018). Rafflesia seeds may have an elaiosome, a nutritious structure that is attractive to ants and a common feature in other ant-dispersed seeds (Pelser et al. 2013). It is possible that ants could carry these seeds towards the roots of their host vines which they can then infect. If this hypothesis is true, it may explain the rarity of over-water dispersals, since ants cannot cover such large distances. Earlier studies also propose that small mammals like ground rats and squirrels could eat these fruits (Bänziger, 2004) and this could possibly account for dispersal over longer distances. However, even if transport is successful, the parasitic nature of rafflesias limits their establishment in a new area, as they still need an appropriate Tetrastigma host to survive.

Unfortunately, these plants are at high risk for extinction. Their inherent rarity is a consequence of their biology: high mortality, imbalance in sex ratios, rare pollination, and parasitic dependence on hosts (Hidayati & Walck, 2017). Individual populations are also very small, with some species like Rafflesia manillana being known from only a single population (Pelser et al. 2017). Different species of rafflesia also need specific Tetrastigma hosts which further narrows their distribution. Also, little is  known about the process of host infection and this information is crucial for any future cultivation attempts.  To top it off, their rainforest habitats are under threat of destruction and fragmentation (Pelser et al. 2019). The combination of these factors will only further reduce their already small populations.

Currently, 12 out of the 13 species of Rafflesia are in the National List of Threatened Philippine plants, with most of them classified as either critically endangered or endangered (DENR Administrative Order 2017-11). These plants are also a model for how parasitism evolved in plants and their biogeography can even shed light on the Philippines’ complex geological history. With the majority of species only being discovered in the past two decades, it is possible that more species could be out there and are potentially endangered. Their rarity, the imminent threat to their habitats, and the mystery still surrounding their biology makes the conservation of these species a priority.

About the author:  Lilcah Opiña is a student currently taking her Masters in Biology at the University of the Philippines Visayas with a special focus on bacterial associates in marine sponges. In her free time, she loves to make biology related art. She frequently posts illustrations of plants and animals on her instagram page (@lilcah.angelique).

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:

Bänziger H. (2004). Studies on hitherto unknown fruits and seeds of some Rafflesiaceae, and a method to manually pollinate their flowers for research and conservation. Linzer Biologische Beiträge 36: 1175–1198

Hidayati, S.N., & Walck, J. (2017). A review of the biology of rafflesia: what do we know and what’s next? Buletin Kebun Raya, 19, 67-78.

Pelser, P.B., Nickrent,  D.L.,  van  Ee,  B.W.,  Barcelona,  J.F. (2019).  A phylogenetic and biogeographic study of Rafflesia (Rafflesiaceae)in the Philippines: Limited dispersal and high island endemism. Molecular  Phylogenetics  and Evolution, 139: 106555.

Pelser, P.B., Nickrent, D.L., Barcelona, J.F. (2018). A conservation genetic study of Rafflesia speciosa (Rafflesiaceae): Patterns of genetic diversity and differentiation within and between islands. Blumea, 63, 93-101.

Pelser, P.B., Nickrent, D.L., Callado, J.R.C., Barcelona, J.F. (2013). Mt. Banahaw reveals: the resurrection and neotypification of the name Rafflesia lagascae (Rafflesiaceae) and clues to the dispersal of Rafflesia seeds. Phytotaxa 131, 35–40.

Pelser, P.B., Nickrent, D.L., Gemmill, C.E.C., Barcelona, J.F. (2017). Genetic diversity and structure in the Philippine Rafflesia lagascae complex (Rafflesiaceae) inform its taxonomic delimitation and conservation. Systematic Botany, 42(3), 543-553

Hall, R. (2002). Cenozoic geological and plate tectonic evolution of SE Asia and the SW Pacific: computer-based reconstructions, model and animations. Journal of Asian Earth Sciences, 20, 353-431.

 

 

 

 

 

[guest student post] Pleistocene Park: Mammoths as Climate Change Engineers

guest post by Kingsley John de los Santos

[Photo by Tristan Colangelo on Unsplash]

    The revival of ancient fauna has long been a topic both in scientific and popular culture. The idea of large beasts has always captured the imagination of the most intelligent species on the planet, arguably - Homo sapiens. Humans influence and dominate almost every ecosystem they inhabit, such that their mere existence has left a lasting mark on the geologic history of the planet. These effects are so persisting and profound that an update to the current geologic epoch (Holocene) has even been proposed - the Anthropocene (Zalasiewicz et al., 2011).

    Although the revival of the dinosaurs has proven to be a long shot, recently extinct large animals - megafauna - have a different case. The resurrection of the non-avian dinosaurs has long been deemed to be nearly impossible even for the best-preserved fossils, simply due to the elapsed time and the fact that DNA only has a 521-year half-life (Allentoft, 2012). For the Pleistocene megafauna, the terms and conditions still apply for the resurrection promo, as they only went extinct 10,000 years ago - a blink of an eye in a geologic sense. The pressing issue is not how, but should it be done? Is it ethical to allocate resources to the resurrection program given the importance of other issues that science can research?

    Interestingly, in a paper published by Macias-Fauria and colleagues last year, this ethical dilemma has been addressed. Not only has the resurrection program been defended, but it has also been justified (Macias-Fauria et al., 2020). For much of the Pleistocene epoch (2.5 million - 11,700 years ago), megafauna such as mammoths roamed the grassland of Siberia and the Americas which have been discovered to have formed strong feedbacks with the carbon-rich permafrost region (Yang et al., 2019). With these findings, the reinstating of mammoth steppe has been raised as one of the unorthodox natural climate solutions (NCS). 

    Floral and pollen fossils suggest that around the 40º N latitude, during the Pleistocene epoch, a type of grassland biome stretched around the Arctic Circle and served as the Earth’s largest terrestrial biome of its time - the mammoth steppe (Zimov et al., 2012). This mammoth steppe formed a wildlife-rich circle like the present-day savannah, with sparse trees, loamy soil, and vast grasslands teeming with large animals. For much of the Pleistocene, this biome was sustained through ecosystem engineering by the large herbivores. The mammoth steppe has been theorized to help cool down the planet through the following propositions:

• Permafrost grasslands have a more reflective surface compared to tundra forests; increasing the radiation released back into space (Zimov et al., 2012).

• The compaction of the snow by the megafauna enables the soil to freeze deeper and longer which increases the layer of underground permafrost every winter (Zimov et al., 2012).

• Snow released during the winter months is deposited on top of the ground instead of evaporating back into the atmosphere (Le Quéré et al., 2018; Sturm et al., 2001).

• The higher density of megafauna increases nutrient cycling. This increases productivity and overwhelms the decomposition in the biome, increasing the carbon (C) stock on the ground (van der Wal, 2006).

• The C in the first meter of the mammoth steppe is higher compared to the current tundra due to the differences in vegetation (Olofsson and Post, 2018).

    The mentioned factors do not seem much until the size of the steppe is realized. The biome interacts with the planet on a global scale. Back in the Pleistocene, the steppe covered 15 million km2 or roughly 10% of the total landmass of the Earth. A simulation model has long suggested that steppe to tundra transition is due to the extinction of large mammals which affected the climate, regionally at least (Zimov et al., 1995).

    This feedback loop between the megafauna and the steppe was disrupted during the late Pleistocene-early Holocene period. The arrival of human species in the region from the African continent has strongly been correlated with the disappearance of the megafauna from the area. This diminished the loop that has helped sustain the biome for the last 2 million years. It is argued that the distribution of the megafauna may only have shrunk with natural climate oscillations but should not have resulted in extinction if the humans never arrived. 

 The timing of extinctions follows the "march of man" (after Martin, 1989); source: Martin P. S. (1989). Prehistoric overkill: A global model. In Quaternary extinctions: A prehistoric revolution (ed. P.S. Martin and R.G. Klein). Tucson, AZ: Univ. Arizona Press. pp. 354–404. ISBN 0-8165-1100-4. 

    One may observe that much of the living megafauna is in Africa, the cradle of the Homo genus. This is where the principle of species interactions can be observed. Newly introduced species that are well adapted to their new environments are often harmful to local species because the natives lack adaptations to deal with the colonizer. This is theorized to what has happened in the Quaternary extinction. African megafauna has already evolved to be aware of the dangers that this specific group of apes poses as compared to the Eurasian, North American, South American, and Australian megafauna which lost 22.9%, 66%, 64%, and 67% of their species richness, respectively. In contrast, the African species only experienced an extinction rate of only around 5% during the same period (Putshkov, 1997). However, it should be noted that these are all merely correlations and there are still objections to the attribution of the extinction. 

    These correlations caused some scientists to argue that the revival of the extinct megafauna and the reintroduction of the remaining arctic/subarctic megafaunal species to the pockets of steppes along the Siberian territory is not only a moral but also an environmental obligation. It is also supported by the fact that no alpine plant species have been lost in the Quaternary extinction which further justifies the favoring of the original steppe-adapted plant species. In the status quo, the project of lessening the effects of climate change through natural engineering by large animals is still in its early stages (Macias-Fauria et al., 2020). 

    A 160 km2 territory in northern Siberia was already fenced off in 2005. This territory, called Pleistocene Park, serves as the experimental area for the reintroduction of bison from western Europe, reindeer herds from the north, Yakutia horses, and other living megafauna. The remaining consideration is whether the mammoths are important in re-establishing and maintaining the mammoth steppe that is going to be established or if the experiment can be successful even with the currently existing species such as bison, oxen, and horses. After all, mammoth’s consumption of the grassland productivity is mediocre (Zimov et al., 2012). 

    Nonetheless, the Pleistocene Park that is being proposed is only a minor step as humans find new ways to reduce the effects of climate change. It is however exciting to see how the study of the biogeography of ancient megafauna has led to a proposal of rebuilding an ancient biome that was once the largest on the planet. 

 

About the author: Kingsley John was born in 1998. He's currently pursuing a Master of Science in Biology degree at the University of the Philippines Visayas. His passions include nerding out to science related media and dog parenting. Trying to practice science can be tough so, generally, Kingsley is still trying to find the right balance among his passions. You can see photos of his doggo on instagram: @kngslyjhn . 

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.

Main Source

    Macias-Fauria, M., Jepson, P., Zimov, N., & Malhi, Y. (2020). Pleistocene Arctic megafaunal ecological engineering as a natural climate solution? Philosophical Transactions of the Royal Society B: Biological Sciences, 375(1794), 20190122. https://doi.org/10.1098/rstb.2019.0122 

Literature Cited

    Allentoft, M. E., Collins, M., Harker, D., Haile, J., Oskam, C. L., Hale, M. L., Campos, P. F., Samaniego, J. A., Gilbert, M. T., Willerslev, E., Zhang, G., Scofield, R. P., Holdaway, R. N., & Bunce, M. (2012). The half-life of DNA in bone: measuring decay kinetics in 158 dated fossils. Proceedings of the Royal Society B: Biological Sciences, 279(1748), 4724–4733. https://doi.org/10.1098/rspb.2012.1745 

    Le Quéré, C., Andrew, R. M., Friedlingstein, P., Sitch, S., Hauck, J., Pongratz, J., ... & Zheng, B. (2018). Global carbon budget 2018. Earth System Science Data, 10(4), 2141-2194.

    Macias-Fauria, M., Jepson, P., Zimov, N., & Malhi, Y. (2020). Pleistocene Arctic megafaunal ecological engineering as a natural climate solution? Philosophical Transactions of the Royal Society B: Biological Sciences, 375(1794), 20190122. https://doi.org/10.1098/rstb.2019.0122 

    Olofsson J, Post E. 2018 Effects of large herbivores on tundra vegetation in a changing climate, and implications for rewilding. Phil. Trans. R. Soc. B 373, 20170437. (doi:10.1098/rstb.2017.0437)

    Putshkov, P. V. (1997). "Were the Mammoths killed by the warming? (Testing of the climatic versions of the Wurm extinctions)". Vestnik Zoologii. Supplement No.4

    Sturm M, Racine C, Tape K. (2001). Climate change – increasing shrub abundance in the Arctic. Nature 411, 546–547. (doi:10.1038/35079180)

    van der Wal R. (2006). Do herbivores cause habitat degradation or vegetation state transition? Evidence from the tundra. Oikos 114, 177–186. (doi:10.1111/ j.2006.0030-1299.14264.x)

    Yang, Y., Tilman, D., Furey, G. et al. (2019). Soil carbon sequestration accelerated by restoration of grassland biodiversity. Nat Commun 10, 718. https://doi.org/10.1038/s41467-019-08636-w

    Zalasiewicz, J., Williams, M., Haywood, A., & Ellis, M. (2011). The Anthropocene: a new epoch of geological time? Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, 369(1938), 835–841. https://doi.org/10.1098/rsta.2010.0339 

    Zimov, S., Chuprynin, V., Oreshko, A., Chapin, F., Reynolds, J., & Chapin, M. (1995). Steppe-Tundra Transition: A Herbivore-Driven Biome Shift at the End of the Pleistocene. The American Naturalist, 146(5), 765-794. Retrieved June 21, 2021, from http://www.jstor.org/stable/2462990

    Zimov S. A., Zimov N. S., Tikhonov A. N., Chapin F. S. (2012). Mammoth steppe: a high-productivity phenomenon. Quat. Sci. Rev. 57, 26–45. (doi:10. 1016/j.quascirev.2012.10.005)

[guest student post] Hitchhike to Invasion: the threat of invasive alien species via ballast waters

guest post by Orlan Celestial

    Ships are known as vectors of non-indigenous species. A ship is like a vehicle that can let you hitchhike when you are stranded in the middle of nowhere,  offering a free ride going to a place where you want to be. But instead of sitting at the back seat of the vehicle, the non-indigenous species take the hull of the ship or the ballast tanks to hitchhike to a new environment where they can invade and dominate.

    Invasive alien species (IAS) are organisms that are not native to an area that have been introduced either intentionally or accidentally. When we think about IAS, the ideas that commonly pop in our minds are large invasive organisms such as cane toads, golden apple snails, Burmese pythons, crown-of-thorns starfish, lionfish, mahogany trees, and other worse known invasive species found in every country. These organisms were introduced then eventually became invasive via different pathways such as the illegal pet trade, plant poaching, intentional introduction as biocontrol, and the underrated way of introduction of some alien species, through ships. Studies have confirmed that ships can transport and disperse non-indigenous species including marine microbes, plants, and animals, particularly biofouling organisms such as mussels and barnacles (Butrón et al., 2011; Sarinas et al., 2014; Nacorda et al., 2018). The problem of biofouling organisms can be easily solved by direct removal and cleaning of the ship hauls. But how about our tiny but potentially deadly problem? Now let’s magnify our discussion and focus on our microscopic dilemma before it becomes macroscopic and uncontrollable.

(Releasing of ballast water. Photo from Ocean Science and Technology)    

    Taking in and discharging ballast waters is a common practice of ships to have proper stability during a voyage. This practice is perceived as a long-standing environmental concern that needs to be effectively addressed as soon as possible. Loaded seawater from the point of origin is transported to a specific destination around the globe. Along with this ballast water are the organisms who hitchhiked and set to invade new areas (Carney et al., 2017). What organisms are commonly transported by ballast waters and why it is considered a threat not just for the environment but as well as for the country’s economy and human health? 

    The species composition and diversity of organisms found in the ballast water of the ships have been determined through numerous studies. The composition includes microscopic plants or phytoplankton, microscopic animals or zooplankton, and bacteria. For instance, the recent study of Cabrini and colleagues (2018) identified the organisms found in ballast waters in the inter-islands and international ships docked in the Adriatic ports. They also determined the viability of these organisms when introduced to a new environment. They found out that the ship ballast waters contained a high abundance of viable organisms. The hitchhikers included 82 zooplankton taxa wherein 6 taxa are non-indigenous, 141 phytoplankton taxa wherein 6 taxa are potentially harmful and toxic (e.g. Alexandrium minutum, a species of dinoflagellates that can cause red tides), Escherichia coli, and suspected enterococci bacteria. They also noted that water salinity, temperature, and light availability can affect the survival of these organisms during the voyage. Their data provide evidence for the viability of the harmful hitchhikers despite changes in the environment, suggesting that these viable organisms could potentially survive, invade, and dominate the new areas after being discharged. Their presence can eventually affect or disrupt the present communities, especially if they can successfully reproduce. In addition, harmful bacteria or viruses that can be carried along can cause spread of diseases to aquaculture or even in humans. 

(Photomicrograph of potentially harmful phytoplankton Pseudo-nitzchia sp. 
Photo from Kudela Biological and Satellite Oceanography Laboratory)

    The questions are: how can we prevent this invasion? Do we have existing actions or programs regarding the management of these ballast waters? Fortunately, there are existing programs in place, however, it seems that these are not effective enough to really prevent or stop the introduction of non-indigenous species. Ships, unlike human drivers, cannot just ignore the thumb-up hitchhiking gesture or the signage that says “anywhere but here” or “to the great beyond”. Ships really do need ballast water to operate and they have certain standards and procedures to follow. The International Convention for the Control and Management of Ship’s Ballast Water and Sediments was established as one of the global responses against the introduction of invasive species via ballast tanks adopted by the International Maritime Organization (IMO). Ballast Water Exchange (BWE) is one of the standards in the management program included in the treaty, where ships must exchange ballast water in deep seas and away from coastal areas and estuaries. Another standard includes the installation of an on-board ballast water treatment system which can determine the maximum allowed discharged volume of viable organisms, including specified indicator microbes harmful to human health. The BWE is presently the most commonly implemented standard, especially in older ships, however, it is expected that all new ships should comply with the latter standard that involves the installation of devices and equipment for biomonitoring and treatment of the ballast tanks (IMO, 2021).

    Nonetheless, results from several studies show that BWE practice cannot really help prevent the spread of harmful hitchhikers. Although there are other proposed ballast water management strategies including mechanical treatments such as filtration and separation, sterilization methods, and chemical treatments (IMO, 2021), we should still keep planning and creating more effective strategies that would prevent the spread of IAS through ballast waters. 

    The Philippines as one of the maritime countries also follows the ballast water management program, however, only a few studies have been conducted to investigate the species present in the international and local ships as well as species released in the Philippine oceanic waters (Sarinas et al., 2014). Hence, it is highly encouraged to conduct studies to address this emerging environmental concern. 

As the world economy continues to grow, seaborne trades also tend to intensify leading to more and intensified environmental concerns. Therefore, the protection and conservation of our environment, particularly our seas and its indigenous communities should be put on our top priority list. We should make plans and establish strategies that can prevent these hitchhikers from invading and dominating our seas, and exterminate these aliens once and for all!

About the author: Orlan “OG” Celestial is an MSc Biology student at the University of the Philippines Visayas. His research interest is mainly about plankton diversity and ecology. He is an outgoing person. He likes hiking and going outdoors with friends and meeting new people along with it. As a biologist, he likes animals more than plants. His ultimate dreams are to become a Veterinary Doctor, a licensed scuba diver, and a NatGeo Explorer. 

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

Butrón, A., Orive, E., Madariaga, I. (2011). Potential risk of harmful algae transport by ballast waters: The case of Bilbao Harbour. Marine Pollution Bulletin, 62(4), 747 757. doi:10.1016/j.marpolbul.2011.01.008 

Cabrini, M., Cerino, F., de Olazabal, A., Di Poi, E., Fabbro, C., Fornasaro, D., David, M. (2018). Potential transfer of aquatic organisms via ballast water with a particular focus on harmful and non-indigenous species: A survey from Adriatic ports. Marine Pollution Bulletin. doi:10.1016/j.marpolbul.2018.02.004 

Carney, K.J., Minton., M.S., Holzer, K.K, Miller, A.W., McCann., L.D., Ruiz, G.M. (2017) Evaluating the combined effects of ballast water management and trade dynamics on transfers of marine organisms by ships. PLoS ONE 12(3): e0172468. doi:10.1371/ journal. pone.0172468

International Maritime Organization (2021, May 20). Ballast Water Management. https://www.imo.org/en/OurWork/Environment/Pages/BWMTechnologies.aspx.

Kudela Biological and Satellite Oceanography Laboratory (2021, June 06). Phytoplankton identification guide. http://oceandatacenter.ucsc.edu/PhytoGallery/index.html 

Nacorda, H.M.E., Austero, N.M., Pagdilao, C.R., Tan, K.S., Azanza, R.V. (2018). Marine Biofouling Communities of Manila South Harbor, Philippines. ASEAN J. Sci. Technol. Dev. 35(1–2): 115–123. doi: 10.29037/ajstd.481

Ocean Science and Technology (2021, May 20). Could your ballast water treatment be dangerous to your health? https://www.oceannews.com/news/science-technology/could-your-ballast-water-treatment-be-dangerous-to-your-health 

Sarinas, B.G.S., Gellada, L.D., Magramo, M.M., Baria, L.O., Tirazona, D.B., Sorio, L.R.D., Tornalejo, J.A. (2014). Plankton diversity in the ballast water of an inter-island passenger-cargo ship calling the  Philippine ports.  Asian Journal of Biodiversity, 5(1): 78-91. doi: 10.7828/ajob.v5i1.482

[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 

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