Boulengerula taitana

''Boulengerula taitana'' (common names: Taita African caecilian, Taita Hills caecilian, Taita Mountains caecilian) is a species of caecilian. It is endemic to the Taita Hills region of southeast Kenya. ''Boulengerula taitana'' are unique caecilians in appearance, fertilization type, and parental care. From their similar shape and presentation to worms, and their internalized fertilization, they set themselves apart from many other amphibians. ''D. taitana'' interactions between mothers and newly hatched young is unique in that the mother uses her own skin as a food resource for offspring. This species also has physiological adaptations in place to increase oxygen uptake and affinity to fit their underground lifestyle. The ''Boulengerula taitana'' differentiates itself from its close relatives in ways rarely documented and researched before.

Description

As stated above, ''B. taitana'' are caecilians, which are amphibians who are limbless and long in length; this amphibians’ skin is divided into ring shapes, which gives the animal a similar appearance to that of an earthworm. Hatchling ''B. taitana'' are about 28mm in length and have an inadequately ossified axial and skull skeleton in contrast to other direct-developing species. Hatchling ''B. taitana'' also have weakly developed body musculature and external annulation, which negatively affects their mobility – essentially restricting it. When offspring are at the stage in their life where they become independent, they total about 86mm in length.

Compared to hatchlings, adult ''B. taitana'' are typically seen as predators, exhibiting two rows of pointed teeth in the premaxillary- maxillary parts of the jaw and vomer palatine in the dentary and splenial parts of the jaw, which have one to two distinct cusps. The monocuspid teeth of the ''B. taitana'' are the three or four most anterior teeth and the vomer palatine teeth. There is then the combination of noticeable labial cusps with a lingual cusp made up of two to three supplemental cusps that make up the rest of the teeth and are multicusped. These teeth are either more pointed and elongated or are shorter and blunter.

Habitat and Distribution

Habitat

''B. taitana'' are found to occupy forest environments more often than agricultural environments in east Africa. ''B. taitana'' has also been found to be longer in length when found in forest settings compared to agricultural settings – with forest-inhabiting ''B. taitana'' averaging 285.9 mm and agriculture-inhabiting ''B. taitana'' averaging 219.3 mm. ''B. taitana'' are typically found only a couple centimeters under the soil beneath rotting logs and in soil that gradually builds up around static rocks.

In this environment, ''B. taitana'' exhibit horizontal movements, which is demonstrated by them moving closer to parts of the soil that are closest to permanent water sources after the area dries out, then they move away after rainfall when the soil has become too moist. ''B. taitana'' is dependent on minimal moisture in the soil; this limits them, during drier periods, to soils near water bodies or deeper soils. In order to feed on their prey, ''B. taitana'' migrate to surface soil.

Geographic Distribution

Endemic to the Taita Hills of Kenya, ''B. taitana'' is currently the only caecilian amphibian that inhabits this area. In the Taita Hills, the ''B. taitana'' are called “ming’ ori,” which is a term commonly used for earthworms. This misnomer heavily affects the false understanding of caecilians as earthworms. ''B. taitana'' is commonly found in agricultural social ecosystems or forests.

Initially, the Taita Hills were mainly forest grounds, but now the area is primarily low-intensity, small-scale agricultural units, with the majority of the area uncultivated. The climate of the area is described as having varying seasonal precipitation. Throughout the year, the rainfall is characterized as monsoonal, with April to October having wetter south-easterly monsoons and November to March having north-easterly monsoons that are drier. Furthermore, there are two distinct rainy seasons: 'masika' season from March to May with long rains and 'vuli' season from October to December with short rains.

Conservation

As of 2020'', B. taitana'' is classified as endangered according to the IUCN Red List. It tolerates low-intensity agricultural practices, but is threatened by intensification of agriculture and deforestation. The overall population is believed to be declining. The forest fragments on the Taita Hills are protected by the Kenya Forest Service, but habitat disturbance still takes place. There are some plans for habitat rehabilitation.

Diet

Juvenile

Following the dentitional metamorphosis stage of development, ''B. taitana'' transitions into a generalist predator. Their diet typically consists of social macrofauna, including termites, ants, and earthworms.

Adult

As with other caecillians, Boulengerula taitana are generalist predators. Adults primarily eats termites, dipteran larvae, ants, antlions, slugs, thrips, centipedes, and earthworms. Still, it has been documented that ''B. taitana'' eats more termites and earthworms compared to the other macrofauna they typically consume. Rather than large jaw muscles and bite forces, they utilize long-axis rotations to reduce prey. Feeding events in the wild are difficult to observe due to their underground dwelling habits. Therefore, most diet studies are done on individuals above-ground laboratory conditions. The feeding process is notably slower in ''B. taitana'' compared to other terrestrial amphibian species. In ''B. taitana'', the prey must be contacted and jaw openings modified via sensory feedback before feeding is initiated. Despite their slow feeding, their predation movements are rapid - with an average peak lunge velocity of 7.4 cm sec^-1 and similar jaw closure speed.

Reproduction and Life Cycle

Fertilization

In ''B. taitana'', fertilization takes place internally, making it a direct-developing oviparous caecilian, and the females of the species take responsibility for guarding their eggs. Cell proliferation and degeneration are functional and morphological changes of the oviducts that occur during the ovarian cycle and pregnancy to be where fertilization and early embryonic development occur.

The oviducts of ''B. taitana'' are more elongated and lie laterally to the ovaries and kidneys. The anterior part, which consists of the ostium, is located near the heart. The posterior part of the oviduct is stops at the cloaca. The oviduct is split and differentiated into three segments: anterior, middle, and posterior. Each segment comprises a serosa, mucosa, and a thin muscular layer. The folded section of the mucosal layer is sheathed in the pseudo-stratified epithelium and reinforced by the tissue of the lamina propria.

The sexual cycle is annual and is divided into three periods: from September to October is preparation, from November to February is ovulation, and from March to August is a rest period. Between March and August, the oviduct diameter of the ''B. taitana'' varied from 120-170 μm. The epithelium, which is somewhat developed, borders a narrow lumen. At the same time, the lamina propria is narrow and contains very little blood vessels. At this point, the para recta (the anterior segment) has a limited amount of shallow crypts, and the surface epithelium contains a multitude of clusters of ciliated and secretory cells. The par utera (the posterior segment) section of the oviduct is the most folded at this time.

From September to October, the environment of the oviduct becomes more complex and more extended. At this time, the diameter of the lumen increases, the thickness of the lamina propria increases, and the epithelium are at its thickest. The pars recta secretory cells increase in size, and there are significant developments in the ciliature and secretory cells of the pars convolute (the middle segment). In the cytoplasm of ciliated cells, acidic carbohydrates are also detected.

These changes allow the oviduct of the ''B. taitana'' to be a perfect environment for ovulation and fertilization. At the end of ovulation in February, the para recta contain very few ciliated cells and a large number of glandular cells. The pars convolute contains secretory, goblet, and ciliated cells, and the par utera only has one type of glandular cell. The epithelial mucosa is more secretory at this time, and there is a greater abundance of cilia cells.

Brood Size

Broods of ''B. taitana'' range from two to nine young. They have the smallest clutch sizes compared to all other caecilians. For pregnant females, smaller clutches allow them to continuously burrow within rigid substrates and feed on prey due to minimal changes of the thin body.

Life Cycle

Once the tadpoles metamorphosize to become juvenile adults, they mature into adults after one year, reaching a size of 240mm or more.

Parental Care

Site Selection for Egg Laying

The eggs of ''B. taitana'' are laid in terrestrial chambers constructed by females, negating development through an aquatic larval stage. Prior to or following the hatching of their eggs, ''B. taitana'' mothers typically occupy areas close to other nesting females. By doing so, females increase their own and their offspring, chances of social interactions, and the prospect of communal breeding.

Feeding Young

''B. taitana'' is an oviparous caecilian, and there is a parent-offspring transfer of nutrients after birth. ''B. taitana'' offspring are born in an undeveloped state, thus requiring feeding and care by the parents. The dentition of offspring includes ‘fetal-like’ teeth, which they use to peel and eat the modified skin of their mothers after birth. The peculiar dentition of dermatophagous (skin feeding) may be the result of a pre-adaptation to fetal viviparous caecilians eating the oviduct lining of their mothers. After their birth, the young position themselves on different parts of their mother’s body and repeatedly use their lower jaws to lift and peel the outer lays of the skin, which are rich in lipids. Within one week of care, juvenile ''B. taitana'' substantially increase in total length, averaging growth of about 1 mm per day. This is because the ingested skin provides a copious amount of nutrients to the offspring. At the same time, weight loss is exhibited by the mother, which is consistent with continuous feeding by their offspring, and imposes a high cost onto the mother. Researchers suggest a similarity between skin feeding and adult feeding in terms of bite forces over different gape angles.

The skin color of nurturing mothers is considerably lighter than other females and males due to the differences in composition at the cellular and tissue level. This difference is most likely due to the role of skin in nutrition for the young. The stratum corneum, the outermost layer of the epidermis, consists of flattened, keratinized cells. The cells of brooding females are lengthy and full of vesicles, and, as a result, the epidermis is double the thickness of non-brooding females. Brooding females are shown to have lower amounts of body fat and negatively impacted body conditions, with the condition of body fat and overall bodily health decreasing significantly throughout the time of caring for their young.

Mutualism

Beneficial Interspecific Relationships

Observations of the species show that it is typical for two fathers to sire a single litter. There is also a high probability of offspring not being cared for by their biological mothers, which showcases an example of alloparenting.

Physiology

Respiration

''B. taitana'' are fossorial species, meaning their habitat consists of burrowing into moist and hard packed soil. Due to this, ''B. taitana'' often encounters hypercarbic and hypoxic conditions, which showcases that blood respiratory properties may be a result of adaptive features to its environment and behavior. Oxygen uptake levels of ''B. taitana'' are significantly higher than those of other caecilians, but they fall within the ranges of other amphibians. The O2 capacity of ''B. taitana'' is 14% volume, which is very high. Compared to other amphibians, the erythrocytes are smaller in size, their red cell count is significantly higher, and their oxygen affinity overall is higher.

References

{{Taxonbar, from=Q677689

taitana
Endemic fauna of Kenya
Amphibians of Kenya
Taxa named by Arthur Loveridge
Amphibians described in 1935