Description
Boulengerula boulengeri is a small, slender, subcylindrical caecilian with a total body length for males of 117 – 234 mm and for females of 117 – 208 mm. Total body length does not exceed 280mm in length (Gower et al. 2004, Jones et al. 2006). The head is subconical. There are short, globular tentacles on the lateral side of the head, halfway along the upper margin of the mouth (Gower et al. 2004), located distantly from the nostrils. The vomerine and palatine teeth are distinctly separated, and the species has no splenial teeth. The tongue is attached to the anterior of the gum. The eye orbits are covered with bone. The body is ringed by 122 - 134 primary annuli. Dermal scales and secondary annuli are absent. There is also no tail. The terminal shield is vertically keeled (Nussbaum and Hinkel1994).

From the sympatric Scolecomorphus vittatus, B. boulengeri can be differentiated by the latter being smaller, having eyes covered by bone, having a subcylindrical instead of flattened or tapered head and body, and having short, globular tentacles that are positioned away from the nostrils (Gower et al. 2004). Within Boulengerula, the species can be differentiated from each other by location and morphology. As of 2020, only B. boulengeri and B. denhardti completely lack splenial teeth, differentiating them from B. changamwensis, B. fischeri, B. spawlsi, B. taitanus, and B. uluguruensis (Wilkinson et al. 2004, Wilkinson et al. 2017). Some specimens of B. niedeni also lack splenial teeth, but others have a few indistinct teeth or teeth hidden by the gum, however, the brownish, in life, body color of B. niedeni distinguishes it from B. boulengeri’s blue-grey body color and pink head (Müller et al. 2005). Boulengerula boulengeri can be further distinguished from B. denhardti by the former having fewer primary annuli (124 - 134 vs ~161) and an anteriorly attached tongue (Wilkinson et al. 2004). Boulengerula fischeri and B. spawlsi also have more primary annuli than B. boulengeri (Wilkinson et al. 2004, Wilkinson et al. 2017). The distinct gap between the vomerine and palatine teeth in B. boulengeri also differentiate it from B. uluguruensis (Wilkinson et al. 2004).

In life, adult B. boulengeri have a light blue-gray base color with darker dorsal bands and pinkish heads. In alcohol, the adult coloration fades to a cream or light tannish yellow base with darkened dorsal bands. In older alcohol specimens, the bands fade entirely, and the body color is a uniform cream or light tannish yellow (Nussbaum and Hinkel 1994).

In life, juveniles are a uniform pink (Nussbaum and Hinkel 1994).

Males are heavier and have proportionally longer and wider jaws and wider heads than females (Jones et al. 2006). Some West Usambara, populations have a larger number of vertebrae and primary annuli than other populations, potentially indicating a cryptic species (Loader et al. 2011).

Distribution and Habitat

Country distribution from AmphibiaWeb's database: Tanzania, United Republic of

	View distribution map in BerkeleyMapper.
	View Bd and Bsal data (1 records).

Boulengerula boulengeri is known only from the Usambara mountains of the Tanga region of Eastern Tanzania. It occurs in both the West and East Usambara at elevational ranges from 180 to 1500 meters but is absent from the Lwengera valley that separates the two ranges (IUCN 2013). The climate in the Usambaras is humid year-round with bimodal distribution of rain, concentrated in light ‘Vuli’ rains from October to December and heavy, longer ‘Masika’ rains from March to May (Hamilton and Bensted-Smith 1989). They are present both in primary forest and agricultural land, preferring wetter soils under solitary trees and banana plants where leaf litter has accumulated (Measely 2004, IUCN 2013).

Life History, Abundance, Activity, and Special Behaviors
Boulengerula boulengeri are present in primary forest at relatively high densities (up to 0.87 individuals/square meter) and at lower densities (up to 0.02 individuals/square meter) in agricultural land, preferring wetter soils under solitary trees and banana plants where leaf litter has accumulated. Individuals are often found in close proximity, occasionally in direct contact or at times accumulated under cover (Measey 2004).

Boulengerula boulengeri are associated with topsoil and almost always found within the soil, which is often a quite dense sandy clay-loam that can be riddled with small tunnels (Jones et al. 2006, Measey and Barot 2006) and has a pH between 5.25 and 6.24 (Measey 2004). Individuals can be found from the contact between leaf litter and the soil surface to at least 30 cm below the surface, though most occur within the first 5 cm of soil (Gower et al. 2004, Measey and Barot 2006). The species appears to have a vertical seasonal migration related to temperature, being found more often in the top 30 cm of soil during warmer air temperatures. This may be associated with predator avoidance, food availability, finding a mate, and/or nest creation as the soil closer to the surface is warmer and more aeriated (Measey and Barot 2006).

Little is known of the reproductive behavior of B. boulengeri. Females are oviparious and likely lay their clutch in November and December (Measey and Barot 2006). Measey (2004) gives one account of a female in the Eastern Usambaras guarding a clutch of three eggs in late December, near the end of the short ‘Vuli’ season of light rains, away from water sources.

Boulengerula boulengeri are considered to be opportunistic, gape-limited predators of soil invertebrates. The diet of B. boulengeri consists primarily of earthworms, termites, ants, and insect larvae, with males preferring termites while females prefer ants. This may be related to males’ larger mouths (Jones et al. 2006).

Boulengerula boulengeri is known to be predated on by snakes. Six individuals were reported in the stomachs of Elapsoidea guentheri in 1928 by Barbour and Loveridge (Nussbaum and Hinkel 1994) and one individual was reported from the stomach of an Usambara garter snake, Elapsoidea nigra. Caecilians in general are also known to be predated on by ants and pigs in the Usambara ecosystem (Measey 2004).

Trends and Threats
Despite having a small range, B. boulengeri is locally common, tolerates disturbances from low-intensity agriculture, and appears to have a stable population. Additionally, the species is found in three reserves, Nilo Nature Reserve, Amani Nature Reserve, and the Mazumbai Forest Reserve, which are relatively well managed. As a result, it has an IUCN threat status of “Least Concern.” However, if agriculture in the region intensifies or new research shows that human activity, including gold mining, negatively affects the species, then this status will be reevaluated. Evaluations of subpopulations are also needed (IUCN 2013).

Relation to Humans
These caecilians can be common in agricultural soils and are able to tolerate low-intensity agriculture (IUCN 2013).

Comments

Maximum Likelihood analysis of 12S, 16S, and cytB mitochondrial sequences found B. boulengeri to be sister to the clade composed of B. changamwensis, B. niedeni, B. tatianus, and B. uluruguensis. This study did not include B. denhardti, which Wilkinson et al. (2004) placed as sister to B. boulengeri based on morphology, or B. fischeri, and was published before the description of B. spawlsi. The study also recovered some Western Usambara specimens of B. boulengeri as a separate clade from other Western and Eastern specimens, which, combined with morphological differences (see above) may indicate the presence of a cryptic species (Loader et al. 2011). In the same year, Gower et al. (2011) published an additional phylogenetic study of Boulengerula using Maximum Likelihood analyses of 12S, 16S, cytB, and cox1 mtDNA, and RAG1 nuclear DNA, which included B. fischeri and generally supported Loader et al’s (2011) findings. However, their placement of B. boulengeri and B. fischeri differed based on the number of outgroups they included. When the outgroup included Herpele squalostoma, Ichthyophis glutinosus, Scolecomorphis vittatus and Typhonectes natans, B. fischeri was sister to the clade composed of B. boulengeri, B. changamwensis, B. niedeni, B. taitanus and B. uluguruensis. However, when only Herpele squalostoma was used as an outgroup, B. boulengeri and B. fischeri switched positions. Both analyses had low support for the placement of the two species. Despite this unresolved relationship, it is clear that three distinct lineages are present in the genus: B. boulengeri, B. fischeri, and the other Boulengerula from Eastern Arc Mountain and Coastal Forests of Kenya and Tanzania.

Locals in the East Usambaras use the Kisamba word ‘mikudi’ to refer to B. boulengerula, but not to Scolecomorphus vittatus, a larger, mostly surface-active caecilian that occurs in the same region. They differentiate it from earthworms, called ‘vyambo’ (Measely 2004).

References

Gower, D. J., Loader, S.P., Wilkinson, M. and Moncrieff, C.B. (2004). ''Niche separation and comparative abundance of Boulengerula boulengeri and Scolecomorphus vittatus (Amphibia: Gymnophiona) in East Usambara forest, Tanzania.'' African Journal of Herpetology, 53, 183-190.

Gower, D.J., Papadopoulou, A., Doherty-Bone, T.M., Pupin, F., San Mauro, D., Loader, S.P., Wilkinson, M. (2011). ''The systematics of Boulengerula fischeri (Amphibia: Gymnophiona: Caeciliidae) based on morphological and molecular data.'' Zootaxa, 2767(1), 14-24. [link]

Hamilton, A.C., Bensted-Smith, R. (1989). ''.'' ''Forest Conservation in the East Usambara Mountains, Tanzania.'' [link]

IUCN SSC Amphibian Specialist Group. (2013). ''Boulengerula boulengeri.'' The IUCN Red List of Threatened Species 2013: e.T59494A16943488. http://dx.doi.org/10.2305/IUCN.UK.2013- 2.RLTS.T59494A16943488.en

Jones, D. T., Loader, S. P., and Gower, D. J. (2006). ''Trophic ecology of East African caecilians (Amphibia: Gymnophiona), and their impact on forest soil invertebrates.'' Journal of Zoology, 269, 117-126.

Loader, S.P., Wilkinson, M., Cotton, J.A., G. Measey, J., Menegon, M., Howell, K.M. Müller, H., Gower, D.J. (2011). ''Molecular phylogenetics of Boulengerula (Amphibia: Gymnophiona: Caeciliidae) and implications for taxonomy, biogeography and conservation.'' Herpetological Journal, 21(1), 5-16.

Measey, G. J. (2004). ''Are caecilians rare? An East African perspective.'' Journal of East African Natural History, 93, 1-21. [link]

Measey, G. J., Barot, S. (2006). ''Evidence of seasonal migration in a tropical subterranean vertebrate.'' Journal of Zoology, 269(1), 29-37. [link]

Müller, H., Measey, G.J., Loader, S.P., Malonza, P.K. (2005). ''A new species of Boulengerula Tornier (Amphibia: Gymnophiona: Caeciliidae) from an isolated mountain block of the Taita Hills, Kenya.'' Zootaxa, 1004(1), 37-50. [link]

Nussbaum, R.A. and Hinkel, H. (1994). ''Revision of East African caecilians of the genera Afrocaecilia Taylor and Boulengerula Tornier (Amphibia: Gymnophiona: Caeciliaide).'' Copeia, 1994(3), 750-760.

Wilkinson, M., Loader, S.P., Müller, H., Gower, D.J. (2004). ''Taxonomic status and phylogenetic relationships of Boulengerula denhardti Nieden, 1912 (Amphibia, Gymnophiona, Caeciliidae).'' Zoosystematic and Evolution, 80(1), 41-51. [link]

Wilkinson, M., Malonza, P.K., Campbell, P., Loader, S.P. (2017). ''A new species of Boulengerula Tornier, 1896 (Amphibia: Gymnophiona: Herpelidae) from Kenya and the ‘rediscovery’ of Boulengerula denhardti.'' Zootaxa, 4286(4), 525-534. [link]

Species Account Citation: AmphibiaWeb 2024 Boulengerula boulengeri: Boulenger's Caecilian <https://amphibiaweb.org/species/1840> University of California, Berkeley, CA, USA. Accessed Nov 22, 2024.

Citation: AmphibiaWeb. 2024. <https://amphibiaweb.org> University of California, Berkeley, CA, USA. Accessed 22 Nov 2024.

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