Gorilla beringei Matschie, 1903

Canington, Stephanie L, 2018, Gorilla beringei (Primates: Hominidae), Mammalian Species 50 (967), pp. 119-133 : 119-125

Gorilla beringei Matschie, 1903

Eastern Gorilla

Gorilla beringeri Matschie, 1903:257 . Incorrect original spelling of Gorilla beringei Matschie, 1903 ; type locality “Nördlich vom Kivu-See und südlich vom Albert-Edward-See auf dem Vulkan Kirunga y Sabinyo.”

Gorilla beringei: Matschie, 1903:259 . First use of current name

Volcanoes National Park, Virunga Mountains, Rwanda. Photograph used with permission of Alexandra Kralick. Plant identification by Laurence Dorr.

Gorilla beringei mikenensis Lӧnnberg, 1917:7 . Type locality “Bamboo-forest on the volcano Mikeno, Virunga Mountains.”

Gorilla gorilla rex-pygmaeorum Schwarz, 1927:333 . Type locality “Luofu, à l’ouest du lac Albert-Edouard [Eastern Congo].”

CONTEXT AND CONTENT. Context as for genus. Gorilla beringei graueri is intermediate in morphology and feeding behavior between G. gorilla and G. b. beringei ( Tuttle 1986; Uchida 1998). Morphological and genetic differences between the Bwindi and Virunga populations of G. b. beringei are proposed to reflect the ecological and functional (i.e., masticatory) differences between the 2 ( Sarmiento et al. 1996; Elgart 2010). Such distinctions prompted consideration for the taxonomic reassignment, though it is not fully supported ( Stanford 2001), of the Bwindi population from the Virunga population within G. b. beringei ( Sarmiento et al. 1996) . More recently, Groves (2001) recognized 2 subspecies in G. beringei :

G. b. beringei Matschie, 1903:257 . See above; beringeri Matschie , manyema Rothschild, and mikenensis Lӧnnberg are synonyms.

G. b. graueri Matschie, 1914:324 . See above, rex -pygmaeorum Schwarz is a synonym.

NOMENCLATURAL NOTES. The taxonomic status of Gorilla is rooted in historical controversy ( Savage 1847; Owen 1848; Geoffroy 1852; Yerkes and Yerkes 1929) as more recently discussed by Groves (2003). Too often, individual size, sex, age, and differences in geographic distributions were taken as evidence for a new species ( Dixson 1981). G. beringei ( Matschie 1903) was named for Captain Robert von Beringe, the German army officer who shot the first 2 specimens (only one of which was preserved) in 1902. Common names include: Bwindi gorilla, the eastern gorilla, eastern highland and lowland gorilla, Grauer’s gorilla, mountain gorilla, and Virunga gorilla.

DIAGNOSIS

Gorillas are the largest of the great apes. Gorilla beringei can be distinguished from Gorilla gorilla (G. g. gorilla and G. g. deihli, the western lowland and Cross River gorilla, respectively), the only other species in the genus, by a combination of morphological features. Body mass means (kg; n) of males and females are similar for both species: G. g. gorilla males (170.4; 10) and females (71.5; 3), G. b. beringei males (162.5; 5) and females (97.5; 1), and G. b. graueri males (175.2; 4) and females (71; 2—Smith and Jungers 1997). G. beringei typically has a greater mean (mm) ± SE palate length (G. b. beringei males = 120.9 ± 2.43 [n = 16] and females = 95.8 ± 2.03 [n = 9]; G. b. graueri males = 119.8 ± 1.48 [n = 20] and females = 97.8 ± 3.39 [n = 5]) and mean basicranial length (G. b. beringei males = 135.9 ± 2.54 [n = 14] and females= 115.7 ± 1.03 [n = 9]; G. b. graueri males= 135.9 ± 1.35 [n = 19] and females = 113.2 ± 0.88 [n = 15]) than G. gorilla : mean palate length (males = 103 ± 1.73 [n = 32] and females = 83.8 ± 1.04 [n = 25]) and mean basicranial length (males = 130.5 ± 1.56 [n = 29] and females = 113.2 ± 0.92 [n = 23—Taylor and Groves 2003]). Mean midfacial breadth is wider (> 120 mm) in adult males of G. g. gorilla (125.7 mm; n = 20) and G. b. graueri (122.8 mm; n = 16) than in G. b. beringei (115.8 mm; n = 13— Uchida 1996). Mandibular depth is uniformly deep in G. b. beringei , though distally shallow in G. b. graueri and G. g. gorilla ( Uchida 1996) . G. beringei has greater mean scapular length (178.2 mm; n = 12) and mean breadth (253.7 mm; n = 12) than G. gorilla (length = 173.6 mm; n = 74; breadth = 249.6 mm; n = 74) adult males ( Taylor 1997b). Metatarsals and metacarpals are shorter in G. beringei ( Inouye 1994) and the hallux is more stable and plantigrade ( Tocheri et al. 2011) than in G. gorilla . Mean trochlear breadth of the talus is greater in adult males of G. beringei (G. b. beringei = 33.8 mm [n = 4]; G. b. graueri = 34 mm [n = 5]) than in G. gorilla (31.8 mm [n = 21— Uchida 1996]).

GENERAL CHARACTERS

Gorilla beringei is a large, sexually dimorphic primate ( Figs. 1 and 2 ). Like all great apes, G. beringei lacks a tail, possesses forward-facing eyes with stereoscopic vision, a dry nose with downward-facing nostrils, a continuous upper lip, opposable 1st digits for grasping, and nails rather than claws ( Fleagle 2013; Gebo 2014). Its pelage varies in length, color, and coverage with age, sex, and altitudinal distribution. G. b. beringei is covered with long, shaggy jet-black or blue-black hair which obscures the face, whereas in G. b. graueri , the hair is generally shorter, though similar in color (Groves and Stott 1979; Dixson 1981). Adolescent males, called “blackbacks,” will eventually develop a silvery gray “saddle” along the back at full maturity, the source of the term “silverback” male ( Schaller 1963). The skin is bare on the face, hands, and soles of its feet.

Mean external measurements (mm; range if available, n) of G. b. beringei (measurements reported for males and females combined, unless indicated otherwise) were: standing height, 1,700 (1,610 –1,710, 5); girth, 1,490 (1,380 –1,630, 8); arm span, 2,310 (2,000 –2,760, 8); hind foot length, 305 (286–320, 10); forelimb length, males 788.3 (7) and females 646.6 (8); hindlimb length, males 676.7 (7) and females 557.2 (8—Jungers and Susman 1984; Williamson and Butynski 2013). Mean postcranial measurements (mm; range, n) for G. b. beringei males and females, respectively, from the Virunga population were: humerus length, 419.0 (398.5–445, 16) and 356.9 (336–382, 14); radius length, 348.7 (310–364, 15) and 296.5 (282–314, 14); femur length, 371.5 (332–390, 15) and 314.0 (293–340, 13); and tibia length, 294.7 (264–309, 15) and 252.0 (232–275, 13— Sarmiento et al. 1996). Mean (mm; range, n) postcranial measurements for G. b. beringei males and females, respectively, from the Bwindi population were: humerus length, 427.0 (382– 472, 2) and 339.5 (327–352, 2); radius length, 353.8 (322.5–385; 2) and 279.0 (275–283; 2); femur length, 363.8 (340.5–387; 2) and 278.5 (270–287; 2); and tibia length, 305.5 (274–337; 2) and 237.0 (235–239; 2— Sarmiento et al. 1996). Mean ± SE scapular measurements (mm), respectively, for adult male (n = 12) and female (n = 6) G. b. beringei (populations unspecified) were: scapular length, 178.2 ± 3.03 and 133.1 ± 2.61; scapular breadth, 253.7 ± 5.63 and 190.9 ± 4.37; and scapular spine length, 229.8 ± 5.37 and 176.8 ± 4.49 ( Taylor 1997b).

Mean cranial measurements (mm; range, n) of G. b. beringei adult males only or males and females were: greatest length of skull, males 311 (287–342, 22) and females 247 (236–260, 15); greatest width of skull, males 183 (170–197, 23) and females 148 (140–160, 16); and ear length, males 58 (50–65, 6—Jungers and Susman 1984; Williamson and Butynski 2013). Mean cranial measurements (mm; range, n or mean ± SE, n) for adult G. b. beringei from the Virunga population were: cranial length, males 200.2 ± 3.30 (13); biorbital breadth, the distance between 2 orbits, males 138.7 ± 1.11 (13); bigonial breadth, the straight distance between 2 gonia, males 144.6 ± 2.44 (13); palate length, males 133.7 (126.1–143.1, 16) and females 103.6 (87.8–119, 17); bicanine breadth, distance to the outside of both canines, males 80.6 ± 0.94 (13); length of maxillary toothrow, males 73.5 ± 1.25 (13); premolar-molar toothrow length, males 73.8 (68.1–78.1, 16) and females 69.3 (62–76.2, 15); maximum diameter of upper incisor toothrow, males 44.6 (41.6–48.8, 16) and females 40.6 (28.3–43.3, 17); and molar area (mm 2), males 859 (734–1,053, 16) and females 709 (604– 853, 9— Casimir 1975; Sarmiento et al. 1996). Mean ± SE (mm 2; range, n) surface area of cheekteeth in adult males was 1,269 ± 23.99 (943.7–1,487, 29) and females 1,088 ± 12.60 (956.4–1,198, 23—Sarmiento and Oates 2000). Among the Virunga population, the percentage of multiple mental foramina occurrence was 100 (n = 6–9, exact sample count number not specified— Elgart 2010). Within the Bwindi population of G. b. beringei , mean measurements (mm; range, n) for males and females, respectively, were: palate length, 123.1 (115.6– 131, 5) and 99.9 (92.5–111.4, 4); premolar-molar toothrow length, 70.9 (69.4–72.8, 5) and 65 (61.1–67.1, 4); incisor width, 45 (43.9–45.9, 5) and 40.2 (35.3–44.4, 4); molar area (mm 2), 868 (808–923, 4) and 682 (627–719, 3— Sarmiento et al. 1996). Mean ± SE surface area (mm 2; range) of cheekteeth in adult males was 1,211 ± 56.39 (1,034 –1,387; n = 5) and females was 971 ± 41.44 (920.5–1,022; n = 3—Sarmiento and Oates 2000). Among the Bwindi population, the percentage occurrence of multiple mental foramina was 57.1 (n = 5— Elgart 2010).

Mean external measurements (mm; ranges reported when available, n) of G. b. graueri adult males, or males and females, were: standing height, males 1,820 (1,690 –1,960, 6); girth, males 1,540 (1,420 –1,600, 4); arm span, males 2,510 (2,340 –2,700, 3); hind foot length, males 297 (287–312, 4); forelimb length, males 790.4 (3) and females 652.9–671.8 (2); and hindlimb length, males 683 (3) and females 562–584.2 (2—Williamson and Butynski 2013).

Mean cranial measurements (mm; range, n) of G. b. graueri adult males, or males and females, were: greatest length of skull, males 302 (276–334, 43) and females 243 (219–258, 31); greatest width of skull, males 182 (167–200, 40) and females 149 (135–164, 29), and ear length, males 52 (50–54, 4—Williamson and Butynski 2013). Interpopulation values of mean cranial measurements ± SD values (mm) for 2 distinct groups of G. b. graueri included adult males from the Kahuzi-Biega National Park (n = 6–8), and Utu group males (n = 12), from the lowlands east of the Lualaba river, respectively: cranial length, 188 ± 7.4 and 186.5 ± 6.3; biorbital breadth, 134.2 ± 4.9 and 137.7 ± 6.9; bigonial breadth, 129.5 ± 9.3 and 128.4 ± 8.1; bicanine breadth, 80.1 ± 3.4 and 77.5 ± 2.4; and length of maxillary toothrow, 74.6 ± 3.9 and 71.3 ± 4.0 ( Casimir 1975).

DISTRIBUTION

Gorilla beringei is an equatorial African ape ( Fig. 3 ) endemic to northwestern Rwanda and southwestern Uganda as G. b. beringei and to eastern Democratic Republic of the Congo as G. b. beringei and G. b. graueri , respectively (26°30′E to 29°45′E and 0°20′N to 3°50′S —Rothschild and Rühli 2005). Areas include: Bwindi Impenetrable National Park (including the Sarambwe Reserve), Itombwe forest, Kahuzi-Biega National Park, Maiko National Park, Mgahinga Gorilla National Park, Mount Tshiaberimu, Shingisha Mabeshi gorilla reserve, Virunga National Park, and Volcanoes National Park. Coordinates specific to research sites in these areas are published ( Goldsmith 2003; Sarmiento 2003).

Gorilla b. beringei (mountain gorilla) is represented by just 2 populations: the Virunga population in the Virunga Mountains along the borders of Rwanda, Uganda, and the Democratic Republic of the Congo, residing at elevations between 2,000 and 3,600 m and the Bwindi population north of the Virunga Mountains within the Bwindi Impenetrable National Park of southwestern Uganda, residing at a lower elevation range between 1,160 and 2,607 m. The populations, separated by approximately 30 km, are both in close proximity to humans ( Roy et al. 2014b). The Virunga population of G. b. beringei is restricted to an area of 450 km 2 (M. Robbins et al. 2011) and the Bwindi population in Bwindi Impenetrable National Park to an area of 330 km 2 ( Grueter et al. 2013a).

By contrast, G. b. graueri (Grauer’s gorilla) occurs exclusively in the Democratic Republic of the Congo between elevations of 600 and 2,500 m ( Rothman et al. 2014). Lowland populations reside in the lower sector of Kahuzi-Biega National Park and Maiko National Park, while highland G. b. graueri make up the Tshiaberimu, Kahuzi, and Itombwe populations ( Tocheri et al. 2016). Within the Kahuzi-Biega National Park, the highland sector is approximately 600 km 2, with an elevation range of 1,800 –3,308 m, and the lowland sector is approximately 5,400 km 2, with an elevation range of 600–1,800 m ( Yamagiwa et al. 2012). Populations of G. b. graueri are fragmented and do not occupy their entire range (Williamson and Butynski 2013). Due to a major decline in population numbers (ca. 77% in 1 generation), the total range size has been reassessed for all areas inhabited by this subspecies to be around 19,700 km 2 ( Plumptre et al. 2016a).

FOSSIL RECORD

The ape fossil record is notoriously sparse, compared with that of early hominins ( Fleagle 2013). A potential basal member of the gorilla clade is the Late Miocene ape, Chororapithecus abyssinicus ( Suwa et al. 2007) , described from fossilized teeth discovered in the southern margin of the Afar Rift of Ethiopia and dated to about 8 million years ago ( Katoh et al. 2016). Its evolutionary relationship with living gorillas remains in question (Schroer and Wood 2013). A 2nd fossil taxon exhibiting gorilla-like characteristics is the Kenyan Nakalipithecus nakayamai ( Kunimatsu et al. 2007) , described from a right mandibular fragment enclosing M1–M3. Additional fossils, including apelike teeth from the late Middle to Late Miocene of Kenya, are questionable in terms of their relationship to modern gorillas (Pickford and Senut 2005). More recently, a study on the paleoenvironmental conditions has identified the rapid expansion of Holocene lowland forests in central Africa and their subsequent connection to expanding highland forests as the time the G. b. beringei subspecies split ( Tocheri et al. 2016). This change in paleolandscape supports the founder-effect hypothesis for G. b. beringei and G. b. graueri ( Tocheri et al. 2016) .

FORM AND FUNCTION

Form. —Except where noted, the following descriptions are based on specimens representing both subspecies of Gorilla beringei . Further, because skeletal specimens of Bwindi mountain gorillas are rare, all descriptions of G. b. beringei are based on the Virunga population except where noted. Dental formula is i 2/2, c 1/1, p 2/2, m 3/3, total 32. Occlusal surfaces of molars have the Y-5 fission pattern characteristic to Hominidae . The 4 cusps on upper molars and 5 on lower molars are separated by deep lingual marginal ridges ( Swindler 1976; Groves 1986). A 6th and sometimes a 7th cusp are seen in lower molars ( Swindler 2002). Canines are robust, elongated mediodistally ( Groves 1986; Schwartz and Dean 2001), and differ between the sexes in maxillary crown height ( Booth 1971), being much larger in males. G. b. beringei has greater dimorphism in canine and lower molar size, whereas G. b. graueri has greater dimorphism in upper molars and a higher frequency occurrence of supernumerary teeth ( Uchida 1998; Ackerman and Bishop 2010). In general, G. b. graueri has relatively larger teeth, with relatively longer molar crests and shorter cusps, than those of G. b. beringei ( Pilbrow 2003) .

The skulls are strongly prognathous and sexually dimorphic ( Fig.4 ), with prominent sagittal and nuchal crests on adult males. The zygomatic bone is curved and the glabella is thickened (Napier and Napier 1985; Groves 1986). Orbits are overhung by supraorbital tori (Ankel-Simons 2000). In G. b. beringei , skulls are generally larger, jaw angles are flared, ascending rami are higher, mandibles are longer, and the mandibular symphysis is wider and shorter compared to that of G. b. graueri ( Vogel 1961; Groves and Stott 1979; Elgart 2010). Within G. b. beringei , ecological and biomechanical factors may explain morphological variations at the subspecific level, with the Virunga population having a shorter face and longer mandible than those from the Bwindi population ( Elgart 2010).

The brain of Gorilla is narrow, ovate, and sexually dimorphic ( Elliot 1913; Tuttle 1986). Mean brain mass (g) ± SE of G. b. beringei adult males from the Virunga population is 498 ± 12.90 (n = 6) and 460 ± 9.73 (n = 13) in females; neonatal brain weight of one 10-day-old male was 208 g ( McFarlin et al. 2013). The hippocampus and volume of cerebellar structures are smaller in G. beringei than in G. gorilla ( Barks et al. 2015) .

In Gorilla , the sternum is broad and made of 6–8 separate elements ( Schultz 1950). The ribcage is funnel-shaped with 13 pairs of ribs. The most basic vertebral formula is 7 C, 13 T, 2–4 L, 5–7 S, and 2–5 Ca (which are fused into a coccyx), 29–36 total (Schultz and Straus 1945 [describing Gorilla ]; Russo and Williams 2014), with notable variability ( Williams et al. 2016). Caudal displacement of diaphragmatic vertebrae occurs at a higher degree in G. beringei than in any other hominoid, which may aid in improving the sagittal stability of the vertebral column ( Williams 2012). In G. beringei , the ilium is broad and very long, with a mean length of 263 mm (n = 4) in males and 226 mm (n = 2) in females ( Schultz 1930). The ischiopubic index (pubis length as a percentage of ischium length) and the relative breadth of the pelvic inlet (percent relationship between greatest breadth of pelvic inlet and overall breadth) are higher in females than in males (Sigmon and Farslow 1986).

There are 18 muscles of the forearm (reported in G. gorilla —Diogo et al. 2012), yet to be confirmed in G. beringei . Forelimbs, in adults, are relatively longer than hindlimbs ( Ruff et al. 2013). The humeri of G. b. beringei are shorter than those of G. b. graueri ( Taylor 1997a) . Humeral heads have a relatively large articular surface ( Ruff et al. 2013) and, like all great apes, exhibit medial torsion, that is, the twisting of the head relative to its shaft ( Gebo 2014). Radii are strongly bowed outward ( Taylor 1997a). The femur has a moderately straight shaft and a distal epiphysis that is elongated mediolaterally (Sigmon and Farslow 1986).

The relatively short and broad hand ( Sarmiento 1994) has 20 muscles (reported in G. gorilla —Diogo et al. 2012) and is made of 8 carpal bones, 5 metacarpals, and 3 phalanges for digits 2–5, with the pollux having only 2. Metacarpals and phalanges are robust and the proximal phalanges have mediolaterally broad shafts. The base of the 3rd metacarpal has a strongly formed styloid process and the os central is fused to the scaphoid ( Sarmiento 1994). The relatively short and broad foot ( Sarmiento 1994) has 7 tarsus bones, the largest being the calcaneus, 5 metatarsals, and 3 phalanges for digits 2–5, with the hallux having only 2. The 1st metatarsal is relatively long and all metatarsal heads are mediolaterally narrow and superiorly projected. The calcanean process of the cuboid bone is reduced or absent ( Sarmiento 1994).

Most descriptions of the soft tissue anatomy of Gorilla are for G. gorilla ( Raven 1950; Diogo and Wood 2012). The male gorilla has a relatively small baculum, short penis ( Raven 1950), and relatively small testes ( Vigilant et al. 2015), which weighed 8.8 g in 1 G. b. beringei (Hosokawa and Kamiya 1961) . The seminal vesicles are elongated and flat (Hosokawa and Kamiya 1961) and the prostate is subdivided ( Groves 1986). Female gorillas possess 2 pectoral mammae, 1 small pair of labia, and a small vagina ( Graham 1981). The ovaries are elongated and flattened and the placenta is discoidal and hemochorial ( Groves 1986).

The bright pink skin of a neonate ( Stewart 1977) changes from a pinkish-gray to black during the 1st year (Williamson and Butynski 2013). The chest is wide and short, housing the broad and dome-shaped diaphragm ( Raven 1950), which is positioned at the level of the last thoracic vertebra ( Gebo 2014). The trilobed right lung and the bilobed left lung of G. b. beringei weighed 1,800 g and 1,500 g in an adult male and 830 g and 760 g in a female, respectively (Hosokawa and Kamiya 1961). An extension of the larynx forms air pouches, allowing for the characteristic deep chest-beating sounds ( Dixson 1981). The trachea of a G. beringei is 3 cm in diameter and the bronchi are 2.3–3.4 cm in diameter (Hosokawa and Kamiya 1961).

The large intestine in Gorilla is divided into the cecum, colon, and rectum. The appendix arises from the posteromedial aspect of the cecum, its base with 3 fused teniae coli ( Scott 1980) . The vermiform appendix of an adult male G. b. beringei was 16 cm long and 1.2–1.4 cm in diameter and the pear-shaped bladder was 10 cm long, 8 cm wide, and 1.5 cm in thickness (Hosokawa and Kamiya 1961). The simple stomach, nonfermenting and adapted to a highly folivorous diet (Williamson and Butynski 2013), is 720 g and 700 g in an adult male and female G. b. beringei , respectively, and the pancreas and spleen form a pronounced shelf inferior to the stomach (Hosokawa and Kamiya 1961).

Function. — Gorilla beringei is a knuckle-walking quadruped possessing 62 lower limb muscles (reported in Gorilla gorilla — Ferrero et al. 2012; Ibáñez-Gimeno et al. 2014). During locomotion, the body is supported on the dorsal aspect of the 2nd and 3rd phalanges of the 2nd–5th front digits, where the callused skin is noticeably thickened (Ankel-Simmons 1983). G. b. beringei infants from the Virunga population do not travel quadrupedally until they are 3.5 months of age, with frequency gradually increasing over time. By 10 months, they change from a predominantly palmigrade to a knuckle-walking form of quadrupedal locomotion and become proficient knuckle-walkers by 17–21 months ( Doran 1997). G. beringei rarely exhibits bipedal locomotory behaviors (Tuttle and Watts 1985), though bipedalism occurs more frequently in juveniles (particularly between 4 and 6months) than adults ( Doran 1997). Arboreality is variable between populations of G. beringei . Although adults of G. b. beringei are the most terrestrial of nonhuman great apes, infants and younger juveniles more closely resemble the higher degrees of arboreality observed in adult G. gorilla ( Doran 1997; Ruff et al. 2013). Individuals of the Bwindi population are more arboreal than those of the Virunga population ( Sarmiento et al. 1996), although none are brachiators ( Schaller 1965).

Both species of Gorilla have type-B blood ( Socha et al. 1995). Adults of the high-elevation Virunga population of G. b. beringei have a mean ± SE (range) body temperature (°C) of 37.8 ± 0.53 (35.4–39.6; n = 7) and an average ± SE (range) O 2 saturation (%) of 86.7 ± 0.69 (86–88; n = 3— Sleeman et al. 2000). Within this population of G. b. beringei , urine, which ranges in color from pale yellow to dark yellow and brown in Gorilla , has a pH mean ± SE (range) of 8.45 ± 0.06 (7–9; n = 43—Sleeman and Mudakikwa 1998).

ONTOGENY AND REPRODUCTION

Ontogeny. —Differences between great apes in timing and degree of ossification at birth are difficult to determine, though attempts were made in Gorilla gorilla ( Randall 1944; Hill and Spatz 1970; Rosen 1972). This includes timing of deciduous dental eruption ( Swindler 2002).

In Gorilla beringei , 7 significant stages in dental eruption are described by Taylor (2003): (1) incompletely erupted deciduous teeth, (2) full deciduous eruption, (3) stage 2 plus M1 partially– fully erupted, (4) M2 partially–fully erupted, (5) C, M3 erupting, (6) C, M3 fully erupted, and (7) full permanent dentition with moderate wear. By the time of eruption of the 1st permanent molar in G. b. beringei , the mandibular symphysis is thicker, the temporomandibular joint is more elevated, and the mandibular ramus is higher than in G. b. graueri . At full dental eruption, G. b. beringei is significantly larger in overall craniomandibular size than G. b. graueri (Taylor 2003) . In G. b. beringei , root formation of M1 occurs from 7.1 to 8.2 years and of M2 at about 8.4 years, with closure of M3 root apices at about 14.9 years in 1 individual ( Kralick et al. 2017).

Infants of G. beringei have relatively stronger forelimbs than hindlimbs until approximately 2 years of age, when limb strength proportions switch. This switch corresponds with the terrestrial locomotor behavior of older juvenile G. b. beringei ( Ruff et al. 2013) . Epiphyseal fusion of long bones begins before complete dental eruption ( Gordon et al. 2013; Ruff et al. 2013).

Females seemingly have early growth spurts because they attain a larger skeletal size than males by the stage of full eruption of the adult dentition ( Taylor 1997a). Male secondary sexual characteristics include massive supraorbital ridges, prominent sagittal and nuchal crests, elongated palates and mandibles, and distinctively large canines ( Schaller 1963; Tuttle 1986). In G. b. beringei , sex differences are evident by 8.5–10 years of age, with 98% of maximum body length achieved at 11.7 years in females and 13.1 years in males ( Galbany et al. 2017).

Age classes (in years) assigned to Virunga G. b. beringei are: infant = 0–3.5; juvenile = 3.5–6; subadult = 6–8; adult female> 8; blackback male = 8–12; silverback male> 12 (Williamson and Gerald-Steklis 2001). Age classes (in years) assigned to G. b. graueri are: infant = 0–4; juvenile = 4–7; subadult = 7–10; adult female> 10; blackback male = 10–13; silverback male> 13 (Yamagiwa and Kahekwa 2001).

Reproduction. —No breeding season is recognized in Gorilla b. beringei ( Watts 1998; Habumremyi et al. 2016), though the May–July birth peak reported for G. b. graueri corresponds to an increase in availability of ripe fruit (Yamagiwa etal. 2012). Conception events in G. b. beringei are independent of mean monthly rainfall ( Watts 1991b, 1998). Reproductive differences between Virunga and Bwindi populations may correlate with seasonality in food availability, because food availability may slow or speed life history (M. Robbins et al. 2009). Gestation length is about 255 days (Czekala and Sicotte 2000) and pregnancy failures for G. b. beringei are comparable to rates for humans (Habumremyi et al. 2016). Over the course of her pregnancy, a female G. b. beringei will gradually exhibit an increase in levels of her immunoreactive pregnanediol- 3-glucuronide profile ( Habumuremyi et al. 2016). Litter size is 1, with some reports of twins ( Yamagiwa et al. 2012). Sex ratio at birth is not significantly different than 1:1 ( Watts 1991b; A. Robbins et al. 2007). Mean age of 1st parturition (years; range) in G. b. beringei is 10.1 (8.7–12.8; n = 8— Watts 1991b) for the Virunga gorillas, and in G. b. graueri is 10.6 (9.1–12.1; n = 6) for the Kahuzi gorillas ( Yamagiwa et al. 2012). A more recent assessment of G. b. beringei age at 1st birth reports a median age of 9.9 years ( Morris et al. 2011).

The mean proximate composition of milk during early to mid-lactation (1–28 months) in G. b. beringei is 10.7% dry matter, 1.9% fat, 1.4% crude protein, 6.8% sugar, and 0.53 kcal/g ( Whittier et al. 2011). Mean ± SE age at weaning in 1-male groups of Virunga G. b. beringei is 10.3 months ± 0.78 (n = 17) and in multimale groups is 27.2 months ± 2.32 (n = 52— Eckardt et al. 2016). The interbirth interval varies as a function of maternal rank and the survival of the infant (A. Robbins et al. 2007). The mean (range) interbirth interval in the Virunga population is 4.1 years (3.2–6.1 years; n = 39— Stoinski et al. 2013). For the Bwindi population, if the offspring survives until 3 years of age, the interbirth interval is 56.4 months (31–78 months; n = 13), but when the offspring dies, it is 24.8 months (16–32 months; n = 7—M. Robbins et al. 2009).

Primiparous mothers have higher infant mortality than experienced mothers (A. Robbins et al. 2006). Long-term studies of G. b. beringei reveal that the youngest and oldest adult females have lower reproductive success than others (A. Robbins et al. 2006). The potential reproductive life span (age in years) is between 10.8 and 30.9 in males and 7.3 and 38 in females ( Langergraber et al. 2012). In her lifetime, a female within the Virunga population will produce an average (± SE) of 3.6 ± 0.58 surviving offspring (n = 13—A. Robbins et al. 2011). Lactational anestrus lasts 2.2–4.2 years, with a median of 3.2 years ( Harcourt et al. 1980; Watts 1991b) and eventually, decreased suckling frequency during the weaning process becomes a major influence on the return of the estrous cycle ( Stewart 1988).

External signs of estrus are slight, if present at all, but may include a perineal swelling in nulliparous females (Stewart and Harcourt 1987). Mean (± SE) length of ovarian cycles in Virunga G. b. beringei is 29 days ± 1.11 (n = 13 cycles— Habumuremyi et al. 2016). Follicular phases (mean ± SE) in G. b. beringei are 21 days ± 0.83 (n = 13 cycles) and luteal phases are 8 days ± 0.83 (n = 13 cycles— Habumuremyi et al. 2016). Amniogenesis occurs by cavitation and the yolk sac is small and free ( Luckett 1974).

In male gorillas, sperm are highly pleomorphic with small heads, posterior thickening (Harrison and Lewis 1986), and several fluorescent F-bodies ( Groves 1986). Spermatogenesis is less active in Gorilla than Pan or humans ( Jacobs et al. 1984; Enomoto et al. 2004) and ejaculate volume is small (Carnahan and Jensen-Seaman 2008) with slow-swimming sperm ( Rosenbaum et al. 2015).

Figures

Fig. 1.—Adult female Gorilla beringei beringei feeding on Rubus,

Fig. 2.—Juvenile male Gorilla beringei beringei, Volcanoes National Park, Virunga Mountains, Rwanda. Photograph used with permission of Alexandra Kralick.

Fig. 3.—Distribution of Gorilla beringei beringei (red) and G. b. graueri (yellow) in Equatorial Africa. Map redrawn from Das et al. (2014) with modifications.

Fig. 4.—Dorsal, ventral, and lateral views of skull and lateral view of mandible of an adult male Gorilla beringei beringei (United States National Museum of Natural History [USNM] 395636) from Mt. Visoke, Virunga Mountains, Rwanda; collected by Dian Fossey, 1968. Photograph by James Di Loreto, Smithsonian Institution used with permission.