Mainland versus Island Adaptation: Paleobiogeography of Sunda Shelf Primates Revisited

3.1.1 Bergmann’s rule

Southeast Asia with wide span of latitude ranging from 6°N to 14°S is split by the equator line, demanding at least two comprehensive separations that require thermoregulation connection from the equator to southern and northern latitudes. Mammals of mainland Southeast Asia have been subjected to describe body size variation following thermoregulation effect, widely termed as Bergmann’s rule [6]. Concluding that Bergmann’s rule may occur within a species, it predicts that population in warmer climates (commonly referred to lower latitudes) have smaller mean body size than conspecifics in colder climates (generally marked with higher latitude) [6]. Published accounts applying this ecogeographical rule on non-human primates has been intensively investigated in the widely distributed species in Southeast Asia: M. fascicularis [4, 5, 10] and M. nemestrina [3]. The Bergmann’s rule was positively performed on northern pig-tailed macaques (M. leonina) [3, 6] and crab-eating macaques (M. fascicularis) [4, 5, 10] in the mainland, demonstrated by the increasing body size toward higher latitude.

Interestingly, anti-Bergmann’s rule appears north side of Kra Isthmus (the narrowest area differing Indochinese mainland and Malay Peninsula at 12.2°N) [4, 5]. Explanatory cause for this inversed Bergmann’s rule has not been uncovered. In response to this matter, M. fascicularis population from the northeastern localities that is bound by the geographic barrier of north–south oriented high topographic range of Tenasserim Hills most likely underwent different and unique ecomorphological adaptations to the rest of the western low land area of Indochinese mainland population. Due to the limitation number on available samples, to date, there is no further study testing this ecogeographical rule in this species or in other non-human primate taxa.

Although serious attempts to test Bergmann’s rule on insular non-human primates have increased, the result of the statistical analysis on the cranial size of southern pig-tailed macaque (M. nemestrina) surprisingly demonstrates anti-Bergmann’s rule [3]. However, insular M. fascicularis tested in western Southeast Asian archipelago [4, 5, 10] and large-sized islands of Sunda Shelf still shows constant Bergmann’s rule [27]. Taken together from observed results correlating non-human primate body size to thermoregulation mechanism in Southeast Asian archipelago, they frequently came as debatable subjects [6] because (i) most islands are situated in short range of latitudinal position referring to low temperature variation; (ii) the equator line that passes over or nearby most of the islands, both northward and southward, directs to similar typical tropical habitat; and (iii) each island is addressed to various unique insular geographical properties (e.g., island area, max. Depth separating to mainland, and island-island distance), which likely gives the stronger island effect than the latitude effect to the population. This aspect needs a more complicated operation when we apply Bergmann’s rule in islands than in mainland.

3.1.2 Foster’s rule

In the context of conservative classification on island area, primate insularity has been investigated into categorization of area size, e.g., small and large island, which was directly calculated by metric size of island [31]. This ecogeographical rule implemented exclusively on island, commonly known as Foster’s rule, proposes that population of large-bodied mammals on island tend to have a smaller mean body size than mainland population (dwarfism), while small-bodied mammals become larger (gigantism) [6]. One suggested that, in the scope of insularity on Southeast Asian mammals, the small island criterion is defined by the island size <12.000 km² [34] (Table 3). Without providing the specific primate species group, one suggested that primates follow island rule [19]. However, a study tested in body length of Macaca fascicularis found that island area and body length shows no significant relationship [10].

The most spectacular evidences of dwarfism on extinct Homininae taxa are Homo floresiensis aged 60,000–100,000 years ago in oceanic island of Flores, Indonesia [11, 24], and Homo luzonensis (judging from the small molar) aged 66.700 ± 1000 years ago discovered in Callao Cave, Luzon Island, Philippines [25]. The consideration of island rule causing diminutive character on Homo luzonensis remains enigmatic, since Luzon Island is a large island (Table 3). However, the coexisted fossil macaque, M. f. philippinensis, which still occurs in modern western, eastern, and northern islands of the Philippines, suggests that it occupied the island since 160,000 years ago [5]. It permits the long duration of isolation that impacted not necessarily on body size reduction, but the possibility of endemism. Furthermore, insular dwarfisms that were reported on M. fascicularis in Bintan Island and Singapore are possibly caused by ecological effects, such as food limitation and high population density [6], not geographical effect such as island size.

Among gibbons, diminutive body size has been presented by Hylobates klossii, an endemic species of four Mentawai islands (Siberut, Sipora, North Pagai, and South Pagai). There are few gibbons occupying small-sized island in continental Sunda Shelf (only found in Paku Island, collection of Lee Kong Chian Natural History Museum), because the small island usually tends to do not support the development of dense rain forest habitat with high canopy cover where gibbon is dependable to live [34].

Researchers have long endeavored to uncover the Foster’s rule in Southeast Asian archipelago [4, 5, 10], but most outcomes show no statistically significant results [11]. On exclusively M. fascicularis inhabiting shallow-water fringing islands over Sunda Shelf, small-sized island was found to contribute more to the variation of subspecies [4, 5] (Table 3). The implementation only using island size or the distance between island and mainland as a proxy is unlikely relevant to the test of Foster’s rule in Southeast Asian archipelago, neither. Deep bathymetric barrier possessed by oceanic islands (Table 3) convincingly appears as the main factor of island rule, followed by the unique island ecological condition in the duration of island isolation.

3.1.3 Vicariance biogeography

Mainland Southeast Asia contains the high variation of non-human primate species. Recent molecular biological studies revealed critical systematics of non-human primates (i.e., Macaca [28, 29] and Hylobates [30]), showing the high intra- and interspecific variation. Topographic diversity in mainland Asia is likely correlated to the speciation process of animals [11, 35], and islands are not exception for this correlation. Historical change of paleobiogeography in large-sized islands (Sumatra, Java, and Borneo) over Sunda Shelf can be explained by Pleistocene volcanic activities caused by the geologic subduction between Sunda and Australian Plates.

In Java, a chain of 38 mountains forming east–west spine with various slopes, illustrated by jagged highlands by alternating peaks and valleys, leads to classes of topographic diversity [35]. This phenomenon led the geographically separated populations to undergo allopatric speciation. According to the modern Javanese mammal fauna, the low topographic diversity in East Java resulted in less variation in endemic mammals than in the West and Central Java. This topographic profile is supported by the presence of two endemic non-human primate species/subspecies strictly occupying western Java forests; Hylobates moloch and Trachypithecus auratus auratus. This endemism also shows the high correlation with the number of natural parks in West and Central Java [32], which probably corresponds to the high soil fertility rates gained from the high-contained mineral of the eruption sediments.

Conversely, a higher endemic mammal species diversity was more visible in East Java during the Middle Pleistocene, in the stage of Stegodon-Homo erectus [32]. Two Hominoidae taxa, Gigantopithecus sp. [39] and Homo erectus, co-existed in the eastern part of the island during the Middle Pleistocene (Table 4). It is also followed by the known primate fossils, including Trachypithecus auratus, Presbytis comata, M. nemestrina, M. fascicularis, Hylobates sp., and later Pongo pygmaeus in the Late Pleistocene [33, 44]. All cercopithecid species are comparable to extant species inhabiting Java Island, while Hominoidae taxa are all extinct. Gigantopithecus sp., Homo erectus, Pongo pygmaeus, and M. nemestrina, which have disappeared in recent Java Island, are assumed to indicate the incapability to adapt toward paleoclimatic changes resulting in habitat loss or ecological replacement from rain forest to open woodland and possible human intervention such as hunting. Although this result is likely related to excavation bias where most of the archeological localities are located in East Java [32, 37], the possible intraspecific variation is reported in Homo erectus, which is commonly discovered in eastern Java localities, specifically as craniodental specimens [25].

With the numerous Homo erectus findings in Java Islands, it leads to the high morphological diversity [25] exclusively on cranial morphology. A comprehensive study on comparison of Homo erectus cranial morphology between island and mainland population has been investigated showing the peculiar distinction on mainland vs. island population. Zhoukoudian Homo erectus represents mainland population (Table 4), and the common ancestor of Javan Homo erectus demonstrates a less morphological variability to the Early Pleistocene Java Homo erectus (that mostly unearthed in Sangiran Dome), while Late-Middle Pleistocene Javan Homo erectus are reported to share similarities in cranial shape [25]. It is suggestive that the lower habitat vicariance in mainland during Middle Pleistocene and Java Island during Middle-Late Pleistocene indicates less genetic isolation. Taking this into account, geographic barriers such as volcanic mountains, added with the isolation of Java, might enforce high intraspecific variation during Early-Middle Pleistocene, supported by the extensive paleoclimatic change. Out of Sunda Shelf, the obvious record of this mechanism appears in Wallacea non-human primates inhabiting Sulawesi. High bathymetric boundaries to Sunda Shelf and the islands surrounding, and diversed topographic barrier of Sulawesi contributes to six endemic macaque species; Macaca nigra, Macaca tonkeana, Macaca maura, Macaca nigrescens, Macaca ochreata, and Macaca hecki that some of the species were found in the archeological cave Leang Burung 2 that occupied with the early human occupation on the island in Late Pleistocene.

3.2.1 Duration

Time by duration and particular period falls to the temporal scope of inhabitation of certain population on island is pronounced to impact body size evolution [12]. Higher duration of island isolation increases the chance for ecological release to influence functional characters (e.g., diet, locomotion, and bauplan) among species. The report on paleoinsular mammals has claimed that body size shift on island mammal species occurred when residence time reached more than 10,000 years [12]. While the evidences are prominently strong on terrestrial herbivores, including terrestrial primates (e.g., Homo floresiensis, 60,000–100,000 years ago [26]), it also evidently impacts the arboreal non-human primate species or subspecies (e.g., Macaca fascicularis and endemic primate species on Simeulue, Lasia, Nicobar, Mentawai Islands).

Typically expressed by the estimated dispersal chronology in Southeast Asian Archipelago, duration of island isolation shows the function of maximum sea depth separating island from mainland or neighboring large island, mainly in small-sized island. Some oceanic islands in the region (Simeulue, Lasia, Siberut, Sipora, North Pagai, South Pagai) remarked with bathymetric barrier more than 120 m (Figure 1) display clear effect of isolation than the shallow-water fringing island over Sunda Shelf. The shallow depth of Sunda Shelf sea floor (0–40 m) allows the emergence of exposed dry land that permits colonization, reversed colonization, or recolonization of the island which most commonly occur during the sea level drop during the Last Glacial Maximum (LGM), which reduces the optimum genetic isolation.

On the level of subspecies, the long duration of island isolation appears to indicate the development of new intraspecific features in Macaca fascicularis inhabiting oceanic islands. Estimated from the last connection with the progenitor mainland species ca. 160 ka (gained from recent bathymetric barrier), some oceanic islands mostly located in western archipelago are interpreted to develop unique M. fascicularis subspecies, such as M. f. umbrosa in Nicobar Islands, M. f. fusca in Simeulue Island, M. f. lasiae in Lasia Island, M. f. tua in Maratua Island, and M. f. philippinensis in western, northern, and eastern islands of the Philippines. The subspecies variation also took place later in continental islands, with shorter island isolation duration started ca. <18 ka such as M. f. karimoendjawae in Karimun Jawa Island, M. f. atriceps in Khram Yai Island, and M. f. condorensis in Con Son Island, marking weak differentiation based on superficial characters [5].

3.2.2 Changes through time

According to the previous paleontological works on mammal evolution of Southeast Asia, there is no fossil evidence of primates before ca. 0.9 Ma in Java Island. The first colonization of primates to Java is estimated to occur at the end of Early Pleistocene, when Sunda Shelf fully emerged and then periodically entered Java via Siva-Malayan corridor route during Middle Pleistocene [33]. Along with the balanced mammal association, including Homo erectus, this period seemingly shows the suitable ecological condition for arboreal high-adapted non-human primates (Macaca, Trachypithecus, and Presbytis) to adapt to mainly open woodlands in relatively dry climate condition [33]. The long duration allowing the dry landmass that connected recent mainland and island during this period possibly permits the occupation access for a hominine species (elaborated as Homo cf. floresiensis [42]) to inhabit the oceanic island of Flores.

To date, there is no chronological and geographical comparative study demonstrating body size of non-human primates between fossils and recent on Java Island. It rather revealed the similarities on morphological characters in accordance with the attempt in determining species. So, it was difficult to answer whether Middle Pleistocene non-human primates of Java are the continuously highly adapted species until recent or the extinct species that disappeared in the Middle Pleistocene like other mammals (including Homo erectus).

Late Pleistocene displays the rise of tropical rain forest non-human primates (Hylobates and Pongo) to develop in Sunda Shelf where the Chinese origin fauna enter to exhibit similar association to recent fauna [33]. Primate species/subspecies that became native to some oceanic islands (e.g., M. siberu, M. pagensis, H. klossii, P. potenziani, P. pagensis, and Simias concolor in Mentawai islands, M. f. condorensis in Nicobar Islands, M. f. fusca in Simeulue Island, M. f. lasiae in Lasia Island, and M. f. tua in Maratua Island). Considering the limitation of swimming ability (max. Swimming distance limit 100 m in M. fascicularis [5]) and large island-mainland distance, dispersal route to the oceanic island is most likely through corridor route over dry landmass, furthermore by passive dispersal, such as natural rafting [5]. The dispersal scenario passing deep sea barrier to reach oceanic islands of Lesser Sunda presumably occurred by human transport during <4.5 ka [5], because swimming is not possible due to the strong sea current in Lombok Strait. This data is supported by the presence of M. fascicularis remains in archeological cave aged ca. 7 ka in Timor Island [5, 27].

3.3.1 Fauna association

With limited connection to the diverse mainland fauna, isolated island promotes the poor taxonomic diversity and the imbalanced rate between herbivores and carnivores. Small island has been claimed to reduce the sympatric speciation than large island [31]. This condition drove a disharmonic inter- and intraspecific variation [12]. For instance, in severe ecological condition when food resources are limited in long duration, the large-bodied species tends to expand their territory where small-bodied species fails to compete and being enforced to undergo stronger dietary adaptation. This response to ecological condition led to a radiation into different size classes and morphotypes, which arrives to appear in the form such as anatomical modification (e.g., dental pattern, size, and shape of limb bone) causing genetic radiation [12].

In most case, this disharmonic taxonomic diversity condition dropped the survivability. The heavily impoverished condition leads to some species to extinction, for example, in all Late Pliocene-Early Pleistocene (Sinomastodon-Megalochelys stage) species in Java and large- to intermediate-bodied fauna in Flores Island in Late Pleistocene. It is followed by imbalanced condition where the normal ratio between carnivores and herbivores is high. Predator avoidance is suggested to cause the limb bone modification. A species that is not threatened by the carnivores might not often walk and run leading to the less development of limb bones.

3.3.2 Vegetation

The vegetation type of an area derives from mean temperature caused from latitudinal position, geographical topography, seasonality by monsoon, and geological sediments. During Quaternary, the fluctuating temperature prominently contributes to habitat changes. The ecological shift from tropical rainforest to more open environment in Early-Mid Holocene resulted in biodiversity loss in non-human primates; for example, it is shown by the disappearance of Presbytis comata (Javan langur) in eastern Java that was previously found in Braholo Cave, East Java (Late Pleistocene to Mid Holocene) [45], and the extinction of Pongo in Java that was formerly discovered in Punung rockshelter, East Java (Late Pleistocene) [46, 47, 48]. This open environment niches created the mosaic ecological niche in eastern Java [45, 49] that enforced the early Homo sapiens inhabiting Java to hunt the remaining arboreal fauna including non-human primates as food resources. Archeological evidence depicting Homo sapiens that consumed monkeys (Macaca, Presbytis, and Trachypithecus) are also discovered in Song Terus cave in the period from 9000 to 5000 years ago [50] and Niah Cave, Borneo [51]. Further ethnographic account resembling this phenomenon is found as butchery marks and burnt bone fragments on cercopithecids assemblage in Punan Vuhang, Sarawak, Borneo [52].