**2. Mainland vs. island: impacts and consequences**

#### **2.1 Body size**

Among mammal taxa, the record of body size shift has not been found spectacular in all primate species [19]. Before the Quaternary, the primate fossil records adapted to island rule are found in Madagascar and Caribbean islands. Strepsirrhine primates found in Madagascar (e.g., *Archaeoindris fontoynontii* and *Megaladapis edwardsi*) are known to have become gigantic [20], while an extinct dwarf lemur, *Cheirogaleus* spp., is known to occupy Nosy Hara Island, a small islet off the northwest coast of Madagascar [21]. The specific examples of island gigantism are also found in platyrrhine monkeys, such as *Paralouatta mariane* from Cuba [22] and *Xenothrix mcgregori* from Jamaica [23].

Hominine taxa represented by the *Homo floresiensis* [24] and *Homo luzonensis* (judging from the small-sized molar [25]) have become the object of comparison to their predicted common ancestor, *Homo erectus*, who inhabited a large-sized island (Java) and Asian continent (Zhoukoudian, China) [24–26]. Until recent, there is no evidence of gigantism found on Southeast Asian insular primates. Looking upon their localities, it shows that the island rule on primates likely occurs in a warmer area within the latitudinal span approaching equator. Throughout several reports [6] island rule on insular primates causing body size change is more evident in oceanic islands due to the deep bathymetric barrier from the mainland regardless of their short island-mainland distance (e.g., Madagascar Island and Mentawai Island) [12].

Gained with the fact that three primate genera (*Macaca*, *Presbytis*, and *Hylobates*) stand as the most widely distributed taxa over Sunda Shelf islands, an attempt is conducted to compare the body size profile between living populations in mainland and island, addressing that an island, regardless of their various sizes, bathymetric barrier, and distance to mainland, is assumed to generate body size changes or body shape variation. Three-dimensional measurements were employed on 20 landmark points on lateral crania (**Figure 1**, **Table 1**, **Table 2**) of five species that strictly inhabit mainland and island (*Hylobates lar*, *Hylobates agilis*, *Macaca fascicularis*,

**65**

**Figure 1.**

**Table 1.**

dimensional size (**Figure 2**).

*Sample size measured in this study.*

*Mainland versus Island Adaptation: Paleobiogeography of Sunda Shelf Primates Revisited*

*Macaca nemestrina*, *Presbytis femoralis*). The landmark points were obtained using 3D digitizer (MicroScribe MX; Immersion Corp., San Jose, CA) and translated into centroid size that stands as alternative check to compensate spatial size over two-

*Map showing two different generalized bathymetric levels from 40 and 120 m throughout Sunda shelf. Closed* 

**Sex group** *Hylobates Macaca Presbytis*

**M** 31 9 60 20 38 **F** 22 12 39 8 43 *All specimens are housed in Lee Kong Chian Natural History Museum and museum Zoologicum Bogoriense Indonesia.*

*H. lar H. agilis M. fascicularis M. nemestrina P. femoralis*

*dash lines present the group of islands with relatively equal range of sea depth.*

The box and whisker plot diagrams (**Figure 3**) exhibit two distinction profiles between Hylobatidae and Cercopithecidae. Island populations of *H. lar* and *H. agilis* show smaller craniolateral size to the mainland population. Noting that most island Hylobatidae population inhabits large-sized islands (Sumatra, Borneo, and Java); their comparatively smaller craniolateral size is seemingly hard to be explained by island rule, knowing that they occupy large-sized islands with shallow bathymetric barrier to the mainland. The presence of much higher-canopy rain forest in mainland may contribute to large-sized body proportion of *Hylobates* in mainland. The reversed results profiled in Cercopithecidae (*M. fascicularis*, *M. nemestrina*, and *P. femoralis*) (**Figure 3**). Given that Southeast Asian islands

*DOI: http://dx.doi.org/10.5772/intechopen.90051*

*Mainland versus Island Adaptation: Paleobiogeography of Sunda Shelf Primates Revisited DOI: http://dx.doi.org/10.5772/intechopen.90051*

#### **Figure 1.**

*Pleistocene Archaeology - Migration, Technology, and Adaptation*

biodiversity changes [11].

appearance in Quaternary until recent.

*Xenothrix mcgregori* from Jamaica [23].

**2.1 Body size**

**2. Mainland vs. island: impacts and consequences**

Lying over a wide range of latitude and various sizes of islands, the Southeast Asian region is frequently subjected for the studies of primate insularity that involved spatial factors (e.g., island size, latitude, and island-mainland distance) [3–5, 10] and temporal factors (e.g., isolation duration and geological chronology) [5]. Insularity on primates is an interesting phenomenon that invites many reports, linking to their ecomorphological complex (body size and body shape) [6] and

In many ecological aspects, mainland environment differs from island environment. In addition, large-sized island provides different ecological scenarios from small-sized island. Certain duration of isolation on a relatively small island may lead to limited resources, fewer predators, and reduced interspecific competition [12]. Although it is not impacted universally, the combinative geographical effects on island size and island isolation can promote gigantism in smaller insular mammal species and dwarfism in larger mammal species. It is widely known as island rule (=Foster's rule) [6, 13–18]. With the wide span of latitudinal range, primates inhabiting the Sunda Shelf region are also assumed to follow Bergmann's rule, by testing the effect of latitudinal position to body size [3–5]. This study aims to elicit the validity of ecogeographical rules affected body size and biodiversity changes of primates around Sunda Shelf throughout the geological chronology, since their

Among mammal taxa, the record of body size shift has not been found spectacular in all primate species [19]. Before the Quaternary, the primate fossil records adapted to island rule are found in Madagascar and Caribbean islands. Strepsirrhine primates found in Madagascar (e.g., *Archaeoindris fontoynontii* and *Megaladapis edwardsi*) are known to have become gigantic [20], while an extinct dwarf lemur, *Cheirogaleus* spp., is known to occupy Nosy Hara Island, a small islet off the northwest coast of Madagascar [21]. The specific examples of island gigantism are also found in platyrrhine monkeys, such as *Paralouatta mariane* from Cuba [22] and

Hominine taxa represented by the *Homo floresiensis* [24] and *Homo luzonensis* (judging from the small-sized molar [25]) have become the object of comparison to their predicted common ancestor, *Homo erectus*, who inhabited a large-sized island (Java) and Asian continent (Zhoukoudian, China) [24–26]. Until recent, there is no evidence of gigantism found on Southeast Asian insular primates. Looking upon their localities, it shows that the island rule on primates likely occurs in a warmer area within the latitudinal span approaching equator. Throughout several reports [6] island rule on insular primates causing body size change is more evident in oceanic islands due to the deep bathymetric barrier from the mainland regardless of their short island-mainland distance (e.g., Madagascar Island and Mentawai Island) [12]. Gained with the fact that three primate genera (*Macaca*, *Presbytis*, and *Hylobates*) stand as the most widely distributed taxa over Sunda Shelf islands, an attempt is conducted to compare the body size profile between living populations in mainland and island, addressing that an island, regardless of their various sizes, bathymetric barrier, and distance to mainland, is assumed to generate body size changes or body shape variation. Three-dimensional measurements were employed on 20 landmark points on lateral crania (**Figure 1**, **Table 1**, **Table 2**) of five species that strictly inhabit mainland and island (*Hylobates lar*, *Hylobates agilis*, *Macaca fascicularis*,

**64**

*Map showing two different generalized bathymetric levels from 40 and 120 m throughout Sunda shelf. Closed dash lines present the group of islands with relatively equal range of sea depth.*


*All specimens are housed in Lee Kong Chian Natural History Museum and museum Zoologicum Bogoriense Indonesia.*

#### **Table 1.**

*Sample size measured in this study.*

*Macaca nemestrina*, *Presbytis femoralis*). The landmark points were obtained using 3D digitizer (MicroScribe MX; Immersion Corp., San Jose, CA) and translated into centroid size that stands as alternative check to compensate spatial size over twodimensional size (**Figure 2**).

The box and whisker plot diagrams (**Figure 3**) exhibit two distinction profiles between Hylobatidae and Cercopithecidae. Island populations of *H. lar* and *H. agilis* show smaller craniolateral size to the mainland population. Noting that most island Hylobatidae population inhabits large-sized islands (Sumatra, Borneo, and Java); their comparatively smaller craniolateral size is seemingly hard to be explained by island rule, knowing that they occupy large-sized islands with shallow bathymetric barrier to the mainland. The presence of much higher-canopy rain forest in mainland may contribute to large-sized body proportion of *Hylobates* in mainland. The reversed results profiled in Cercopithecidae (*M. fascicularis*, *M. nemestrina*, and *P. femoralis*) (**Figure 3**). Given that Southeast Asian islands

### *Pleistocene Archaeology - Migration, Technology, and Adaptation*


#### **Table 2.**

*Abbreviation and definition used in this study [27].*

#### **Figure 2.**

*Frontal (left) and lateral (right) views of the generalized* M. fascicularis *skull, showing 20 landmark positions used in the analysis. Number and position of landmark points are applied with the same procedure in all species measured.*

**67**

*Mainland versus Island Adaptation: Paleobiogeography of Sunda Shelf Primates Revisited*

are geographically characterized with various sizes, latitudinal and longitudinal positions, maximum sea depth, and island-mainland distance, this condition arises to a consequence on more diverse insular adaptation that contributes to numerous

*Box and whisker diagram showing the variation of craniolateral centroid size (CS) among five non-human* 

For the last 30 years, benefited by the advanced methodology of molecular biology, the expansion of studies on primates of Southeast Asia have resulted in the increased number of taxonomic diversification [28–30], which was previously mostly explained by the superficial character (e.g., pelage color, tail length, and behavior) on the living taxa [2, 5]. Mainland and large islands have been claimed to correspond to the higher taxonomic diversity than islands [31]. With the wide span of area, mainland and large islands have a great advantage to develop more topographic diversity, formed as geographic barriers (e.g., peak, valley, river), linking to

Principal component analyses (PCA) on the craniolateral shape of the five species share similarities in the wider shape variance of all three insular species (**Figure 4**). The mixed category between large-sized island and small-sized island in this study (**Table 3**) may strongly correspond to the higher craniolateral morphology, by considering (i) each isolated small island with unique geographicalecological condition and different degrees of isolation may contribute to the shape modification, furthermore to endemism [12]; (ii) large islands may lead to various shape modifications, generated by various topographic-diversity-derived habitat variations [32]. Reflecting the wide variance morphology on three insular genera of this study, insularity does not gain merely on taxonomic diversity; furthermore strong individual differentiation within population or intraspecific variation could

The isolation process on an island may lead to enforce the possibility of extinction in certain species [30]. For example, in Java Island, with area span

*nemestrina*) occurred during Middle-Late Pleistocene, but finally disappeared [33] (**Table 4**). Harsh ecological condition (e.g., low carnivore-herbivore ratio and habitat change) on island will contribute to the adaptability of particular species. *M. nemestrina*, which is more terrestrial species than the survived species, *M. fascicularis* [27] (**Table 4**), is assumed to be less adaptive to avoid terrestrial and predators. *Pongo*, which is recently absent in Java Island and

, three primate species (*Homo erectus*, *Pongo pygmaeus*, and *M.* 

*DOI: http://dx.doi.org/10.5772/intechopen.90051*

variations in body size.

**Figure 3.**

also possibly generated.

138,000 km<sup>2</sup>

**2.2 Biodiversity changes and extinction**

*primate species in mainland and island group.*

high possibility to allopatric speciation [32].

*Mainland versus Island Adaptation: Paleobiogeography of Sunda Shelf Primates Revisited DOI: http://dx.doi.org/10.5772/intechopen.90051*

**Figure 3.**

*Pleistocene Archaeology - Migration, Technology, and Adaptation*

between central and lateral incisors PMS The point where premaxillary suture crosses alveolar margin

DM3 Distal M3: posterior midpoint onto alveolar margin of M3 PMA Most posterior point of maxillary alveolus on the maxilla palatine NSP Nasospinale: inferiormost midline point of piriform aperture WPA Point corresponding lo largest width of piriform aperture

RHI Rhinion: most anterior midline point on nasals

bone or aperture NAS Nasion: midline point on fronto-nasal suture

supraorbital ridges

*Abbreviation and definition used in this study [27].*

on sagittal/nuchal crest or not OPS Opisthion: posterior most point of foramen magnum

NPM Meeting point of nasal and premaxilla on margin of piriform aperture

PMN Premaxillary maximum superior PMS where premaxillo-maxillary suture meets nasal

INI Inion: most posterior point of cranium, when viewed in the Frankfurt horizontal, be it

LOC Most anterior point on the occipital condyle along the margin of the foramen magnum AOC Occipital condyle along the margin of the foramen magnum between POC and AOC

*Frontal (left) and lateral (right) views of the generalized* M. fascicularis *skull, showing 20 landmark positions used in the analysis. Number and position of landmark points are applied with the same procedure in all* 

GLA Glabella: most forward projecting midline point of frontals at the level of the

BRG Bregma: junction of coronal and sagittal sutures, on sagittal crest if necessary

PRS Prosthion: anteroinferior point on projection of premaxilla between central incisors PRS2 Prosthion2: anteroinferiormost point on premaxilla, equivalent to prosthion but

MP3 Mesial P3: most mesial point on P3 alveolus, projected labially onto alveolar margin MM1 Mesial M1: contact points between P4 and M1, projected labially onto alveolar margin MM3 Mesial M3: contact point between M2 and M3, projected labially onto alveolar margin

**Abbreviation Definition**

**66**

**Figure 2.**

*species measured.*

**Table 2.**

*Box and whisker diagram showing the variation of craniolateral centroid size (CS) among five non-human primate species in mainland and island group.*

are geographically characterized with various sizes, latitudinal and longitudinal positions, maximum sea depth, and island-mainland distance, this condition arises to a consequence on more diverse insular adaptation that contributes to numerous variations in body size.

#### **2.2 Biodiversity changes and extinction**

For the last 30 years, benefited by the advanced methodology of molecular biology, the expansion of studies on primates of Southeast Asia have resulted in the increased number of taxonomic diversification [28–30], which was previously mostly explained by the superficial character (e.g., pelage color, tail length, and behavior) on the living taxa [2, 5]. Mainland and large islands have been claimed to correspond to the higher taxonomic diversity than islands [31]. With the wide span of area, mainland and large islands have a great advantage to develop more topographic diversity, formed as geographic barriers (e.g., peak, valley, river), linking to high possibility to allopatric speciation [32].

Principal component analyses (PCA) on the craniolateral shape of the five species share similarities in the wider shape variance of all three insular species (**Figure 4**). The mixed category between large-sized island and small-sized island in this study (**Table 3**) may strongly correspond to the higher craniolateral morphology, by considering (i) each isolated small island with unique geographicalecological condition and different degrees of isolation may contribute to the shape modification, furthermore to endemism [12]; (ii) large islands may lead to various shape modifications, generated by various topographic-diversity-derived habitat variations [32]. Reflecting the wide variance morphology on three insular genera of this study, insularity does not gain merely on taxonomic diversity; furthermore strong individual differentiation within population or intraspecific variation could also possibly generated.

The isolation process on an island may lead to enforce the possibility of extinction in certain species [30]. For example, in Java Island, with area span 138,000 km<sup>2</sup> , three primate species (*Homo erectus*, *Pongo pygmaeus*, and *M. nemestrina*) occurred during Middle-Late Pleistocene, but finally disappeared [33] (**Table 4**). Harsh ecological condition (e.g., low carnivore-herbivore ratio and habitat change) on island will contribute to the adaptability of particular species. *M. nemestrina*, which is more terrestrial species than the survived species, *M. fascicularis* [27] (**Table 4**), is assumed to be less adaptive to avoid terrestrial and predators. *Pongo*, which is recently absent in Java Island and

**Figure 4.**

*Plots of principal component PC1–PC2 displaying the variance between mainland and island population among five species observed.*


**69**

Holocene.

**Table 3.**

*Mainland versus Island Adaptation: Paleobiogeography of Sunda Shelf Primates Revisited*

Borneo (north)

(northeast)

Islands

(southwest)

(southeast)

(central)

(northwest)

(north)

(northeast)

Islands

Islands

Islands

Islands

Islands

*Presbytis rubicunda* [2] Borneo (east) 8°N–2°S 743,330 Large 4095

*Nasalis larvatus* [2] Borneo 8°N–2°S 743,330 Large 4095

*M. f. umbrosa* [5] Little Nicobar 7.32°N 140 Small 435 *M. f. tua* [5] Maratua 2.25°N 22,8 Small 94.18 *M. f. philippinensis* [5] Palawan 9.70°N 14,650 Large 2086 *M. f. philippinensis* [5] Luzon 16.9°N 110,000 Large 2922 *M. f. lasiae* [5] Lasia 2.17°N 15,12 Small 69 *M. f. fusca* [5] Simeulue 2.65°N 2310 Small 567

**size (km2 )**

Java 8°–10°N 128,300 Large 3676

8°N–2°S 743,330 Large 4095

8°N–2°S 743,330 Large 4095

1.2°–3°S 268–4030 Small 384

0.3°N–5.3°S 174,600 Large 3478

0.3°N–5.3°S 174,600 Large 3478

0.3°N–5.3°S 174,600 Large 3478

0.3°N–5.3°S 174,600 Large 3478

0.3°N–5.3°S 174,600 Large 3478

0.3°N–5.3°S 174,600 Large 3478

1.2°–3°S 268–4030 Small 384

1.2–3S 268–4030 Small 384

1.2–3°S 268–4030 Small 384

1.2–3°S 268–4030 Small 384

1.2–3°S 268–4030 Small 384

*) [34].*

**Island size category [33]**

**max. elevation (m)**

**Genera Species/subspecies Island Latitude Island** 

*Presbytis hosei* [2] Borneo

*Macaca ochreata* [2] Sulawesi

*Macaca tonkeana* [2] Sulawesi

*Macaca hecki* [2] Sulawesi

*Macaca nigrescens* [2] Sulawesi

*Macaca nigra* [2] Sulawesi

*Macaca siberu* [2] Mentawai

*Macaca pagensis* [2] Mentawai

*Presbytis potenziani* [2] Mentawai

*Simias concolor* [2] Mentawai

*The category of island refers to the indicator of small island category (<12,000 km2*

Colobinae *Presbytis pagensis* [2] Mentawai

mainland, became extinct probably due to the deterioration of the habitat from tropical forest to more open environment [33] during Late Pleistocene to

*List of modern non-human primate species/subspecies native to islands with the latitudinal position.*

*DOI: http://dx.doi.org/10.5772/intechopen.90051*

*Presbytis chrysomelas* [2]

*Trachypithecus auratus* [2]

Hylobatidae *Hylobates klossii* [2] Mentawai

Cercopithecinae *Macaca maura* [2] Sulawesi

**OCEANIC ISLAND**


## *Mainland versus Island Adaptation: Paleobiogeography of Sunda Shelf Primates Revisited DOI: http://dx.doi.org/10.5772/intechopen.90051*

#### **Table 3.**

*Pleistocene Archaeology - Migration, Technology, and Adaptation*

*Plots of principal component PC1–PC2 displaying the variance between mainland and island population* 

Ponginae *Pongo pygmaeus* [2] Borneo 8°N–2°S 743,330 Large 4095

Hylobatidae *Hylobates moloch* Java (west) 8°–10°N 128,300 Large 3676

Cercopithecinae *M. f. atriceps* [5] Khram Yai 12.70°N 20,28 Small 219

Colobinae *Presbytis natunae* [2] Natuna Besar 4°N 1720 Small 187

(north)

*M. f. condorensis* [5] Con Son 8.71°N 51,52 Small 560.8 *M. f. mandibularis* [5] Riau Islands 2.50°–3.13°N 106 Small 959 *M. f. baweana* [5] Bawean 5.80°S 196,27 Small 655

*Presbytis frontata* [2] Borneo 8°N–2°S 743,330 Large 4095

Karimun Jawa 5.85°S 71,2 Small 506

(north)

Sumatra (north)

(south)

(north)

**size (km2 )**

2°–4°N 473,481 Large 3805

2°–4°N 473,481 Large 3805

8°N–2°S 743,330 Large 4095

8°N–2°S 743,330 Large 4095

2°–4°N 473,481 Large 3805

**Island size category [33]**

**max. elevation (m)**

**Genera Species/subspecies Island Latitude Island** 

*Pongo abelii* [2] Sumatra

*H. albibarbis* [2] Borneo

*H. muelleri* [2] Borneo

*Presbytis thomasi* [2] Sumatra

*Pongo tapanuliensis* [34]

*M. f. karimoendjawae* [5]

**68**

**Figure 4.**

*among five species observed.*

**CONTINENTAL ISLAND**

*List of modern non-human primate species/subspecies native to islands with the latitudinal position.*

mainland, became extinct probably due to the deterioration of the habitat from tropical forest to more open environment [33] during Late Pleistocene to Holocene.
