Boulengerula taitana

Last updated

Boulengerula taitana
Boulengerula taitanus 1.jpg
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Chordata
Class: Amphibia
Order: Gymnophiona
Clade: Apoda
Family: Herpelidae
Genus: Boulengerula
Species:
B. taitana
Binomial name
Boulengerula taitana
Loveridge, 1935
Boulengerula taitana range 2.png
Range highlighted in blue
Synonyms [2]
  • Boulengerula taitanus(Loveridge, 1935)
  • Afrocaecilia taitana(Loveridge, 1935)

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. [3] 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 are 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.

Contents

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. [4] 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 86 mm 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. [5]

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. [4]

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. [6]

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", 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. [7]

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. [6] 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. [8]

Conservation

As of 2020, B. taitana is classified as endangered according to the IUCN Red List. [3] 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. [3]

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. [7]

Adult

As with other caecillians, Boulengerula taitana are generalist predators. Adults primarily eat termites, dipteran larvae, ants, antlions, slugs, thrips, centipedes, and earthworms. Still, it has been documented that B. taitana eat more termites and earthworms compared to the other macrofauna they typically consume. [8] 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 the similar jaw closure speed. [9]

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: preparation from September to October, ovulation from November to February, and a resting period from March to August. Between March and August, the oviduct diameter of the B. taitana varies 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. [10]

Brood size

Broods of B. taitana range from two to nine young. [5] 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. [6]

Life cycle

Once the tadpoles metamorphosize to become juvenile adults, they mature into adults after one year, reaching a size of 240mm or more. [6]

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. [7]

Feeding young

B. taitana is an oviparous caecilian, and there is a parent-offspring transfer of nutrients after birth. B. taitana offsprings 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. [5] Researchers suggest a similarity between skin feeding and adult feeding in terms of bite forces over different gape angles. [11]

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. [5] 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. [7]

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. [7]

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. [12]

Related Research Articles

<span class="mw-page-title-main">Amphibian</span> Class of ectothermic tetrapods

Amphibians are ectothermic, anamniotic, four-limbed vertebrate animals that constitute the class Amphibia. In its broadest sense, it is a paraphyletic group encompassing all tetrapods, excluding the amniotes. All extant (living) amphibians belong to the monophyletic subclass Lissamphibia, with three living orders: Anura (frogs), Urodela (salamanders), and Gymnophiona (caecilians). Evolved to be mostly semiaquatic, amphibians have adapted to inhabit a wide variety of habitats, with most species living in freshwater, wetland or terrestrial ecosystems. Their life cycle typically starts out as aquatic larvae with gills known as tadpoles, but some species have developed behavioural adaptations to bypass this.

<span class="mw-page-title-main">Birth</span> Process of bearing offspring

Birth is the act or process of bearing or bringing forth offspring, also referred to in technical contexts as parturition. In mammals, the process is initiated by hormones which cause the muscular walls of the uterus to contract, expelling the fetus at a developmental stage when it is ready to feed and breathe.

<span class="mw-page-title-main">Caecilian</span> Order of amphibians

Caecilians are a group of limbless, vermiform (worm-shaped) or serpentine (snake-shaped) amphibians with small or sometimes nonexistent eyes. They mostly live hidden in soil or in streambeds, and this cryptic lifestyle renders caecilians among the least familiar amphibians. Modern caecilians live in the tropics of South and Central America, Africa, and southern Asia. Caecilians feed on small subterranean creatures such as earthworms. The body is cylindrical and often darkly coloured, and the skull is bullet-shaped and strongly built. Caecilian heads have several unique adaptations, including fused cranial and jaw bones, a two-part system of jaw muscles, and a chemosensory tentacle in front of the eye. The skin is slimy and bears ringlike markings or grooves and may contain scales.

<i>Boulengerula niedeni</i> Species of amphibian

Boulengerula niedeni, the Sagalla caecilian, is a worm-like amphibian first described in 2005. The species was described from a specimen discovered on Sagala Hill, an isolated mountain block of the Taita Hills in Kenya, and is not known from other areas.

<span class="mw-page-title-main">Caecilians of the Western Ghats</span>

The Western Ghats in India are home to several species of caecilians (Gymnophiona). Caecilians are legless, burrowing amphibians which mostly live in leaf litter, loose soil, under rocks and decaying logs. They are also found in agricultural fields and only surface during the monsoon. The body is elongated and smooth with a slimy skin. The smaller caecilians superficially resemble earthworms while the larger ones are often mistaken for snakes. However, they can be told apart from earthworms by the presence of eyes, teeth and skeleton and from snakes by the lack of scales on skin. The eyes in caecilians are not well developed which is most likely to be because of their burrowing life style. They are considered as rare which is apparently due to their subterranean habits. To see them one has to search carefully and be at the right place and at the right time. There are few places where they are common, but, at least one species was reported to be abundant in agricultural fields in Kerala. The larger caecilians can resemble snakes, but their skin is smooth, not scaly.

<i>Atretochoana</i> Genus of amphibians

Atretochoana eiselti is a species of caecilian originally known only from two preserved specimens discovered by Sir Graham Hales in the Brazilian rainforest, while on an expedition with Sir Brian Doll in the late 1800s, but rediscovered in 2011 by engineers working on a hydroelectric dam project in Brazil. Until 1998, it was known only from the type specimen in the Naturhistorisches Museum, Vienna. Originally placed in the genus Typhlonectes in 1968, it was reclassified into its own monotypic genus, Atretochoana, in 1996. It was also found to be more closely related to the genus Potamotyphlus than Typholonectes. The species is the largest of the few known lungless tetrapods, and the only known lungless caecilian.

<i>Boulengerula</i> Genus of amphibians

Boulengerula is a genus of amphibians in the family Herpelidae. They are found in East Africa. They are sometimes known as Boulenger's caecilians or Usambara bluish-gray caecilians.

<i>Boulengerula fischeri</i> Species of amphibian

Boulengerula fischeri is a species of caecilian in the family Herpelidae. It is endemic to Rwanda and only known from around its type locality near Cyangugu, southwestern Rwanda. The specific name fischeri honours Eberhard Fischer, a German botanist who has worked with Rwandan fauna and flora. Common name Fischer's African caecilian has been coined for it. Live animals have the appearance of "live pink spaghetti".

<i>Dermophis mexicanus</i> Species of amphibian

Dermophis mexicanus, also known commonly as the Mexican burrowing caecilian or the Mexican caecilian, and locally as the tapalcua or tepelcua, is a species of limbless amphibian in the family Dermophiidae. The species is native to Mexico and Central America, where it burrows under leaf litter and plant debris.

<i>Herpele squalostoma</i> Species of amphibian

Herpele squalostoma is a species of caecilian in the family Herpelidae. It is also known by the common name Congo caecilian. It is found in Central and extreme easternmost West Africa.

<i>Potamotyphlus kaupii</i> Genus of amphibians

Potamotyphlus kaupii is a species of amphibian in the family Typhlonectidae. It is monotypic within the genus Potamotyphlus. It is found widely in the Amazon Basin and the Guianas in South America, and is known to occur in Brazil, Colombia, Ecuador, Peru, Venezuela, and possibly Bolivia. It is an entirely aquatic species and typically ranges between 30 and 60 cm (12–24 in) in length.

<i>Schistometopum thomense</i> Species of amphibian

Schistometopum thomense is a species of amphibian in the family Dermophiidae, endemic to São Tomé and Ilhéu das Rolas. It is found in most soils on São Tomé, from tropical moist lowland forests to coastal coconut plantations. It is absent only from the driest northern areas of the island. It is typically around 30 cm (12 in) in length, and is often bright yellow. The size of S. thomense can vary throughout São Tomé, however, and it is the only known caecilian to follow Bergmann's rule, which states that a decreasing temperature due to factors such as increasing altitude will cause an increase in the body size of endothermic vertebrate species. The island of São Tomé is a massive shield volcano, and it therefore has differing altitudes throughout the island, potentially resulting in the size diversity of S. thomense. This species may be referred to as the São Tomé caecilian, as the Agua Ize caecilian, or as the island caecilian, or by the local name of cobra bobo.

<i>Siphonops annulatus</i> Species of amphibian

Siphonops annulatus, the ringed caecilian, is a species of caecilian in the family Siphonopidae endemic to South America. It may have the broadest known distribution of any terrestrial caecilian species.

<i>Typhlonectes compressicauda</i> Species of amphibian

Typhlonectes compressicauda, the Cayenne caecilian, is a species of amphibian in the family Typhlonectidae that lives in water. It is found in Amazonian Brazil, Peru, and Colombia as well as in Guyana and French Guiana, and likely Suriname, and according to some sources, Venezuela. It is an aquatic caecilian that inhabits permanent rivers and marshes mainly in the lowland forest zone.

<i>Ichthyophis glutinosus</i> Species of amphibian

Ichthyophis glutinosus, the Ceylon caecilian or common yellow-banded caecilian, is a species of caecilian in the family Ichthyophiidae endemic to Sri Lanka. Its natural habitats are moist tropical and subtropical forests and pastures.

Indotyphlus is a small genus of caecilians in the family Grandisoniidae. As caecilians in general, they superficially resemble earthworms. The genus is endemic to the Western Ghats, India. They are sometimes known as Battersby's caecilians.

<span class="mw-page-title-main">Matriphagy</span>

Matriphagy is the consumption of the mother by her offspring. The behavior generally takes place within the first few weeks of life and has been documented in some species of insects, nematode worms, pseudoscorpions, and other arachnids as well as in caecilian amphibians.

Boulengerula spawlsi is a species of caecilian in the family Herpelidae. It is endemic to Kenya and only know from the vicinity of its type locality, Ngaia Forest Reserve, in the Nyambene Hills, Meru County; the type locality is also spelled "Ngaya" or "Ngaja". The specific name spawlsi honours Stephen Spawls who first collected this species and who has contributed substantially to African herpetology. Common name Spawls' boolee has been coined for it.

Vertebrate maternal behavior is a form of parental care that is specifically given to young animals by their mother in order to ensure the survival of the young. Parental care is a form of altruism, which means that the behaviors involved often require a sacrifice that could put their own survival at risk. This encompasses behaviors that aid in the evolutionary success of the offspring and parental investment, which is a measure of expenditure exerted by the parent in an attempt to provide evolutionary benefits to the offspring. Therefore, it is a measure of the benefits versus costs of engaging in the parental behaviors. Behaviors commonly exhibited by the maternal parent include feeding, either by lactating or gathering food, grooming young, and keeping the young warm. Another important aspect of parental care is whether the care is provided to the offspring by each parent in a relatively equal manner, or whether it is provided predominantly or entirely by one parent. There are several species that exhibit biparental care, where behaviors and/or investment in the offspring is divided equally amongst the parents. This parenting strategy is common in birds. However, even in species who exhibit biparental care, the maternal role is essential since the females are responsible for the incubation and/or delivery of the young.

Dermatotrophy is a rare reproductive behaviour in which the young feed on the skin of its parents. It has been scientifically observed in several species of caecilian, including Boulengerula taitana, and is claimed to exist in the newly discovered unpublished species Dermophis donaldtrumpi.

References

  1. ↑ IUCN SSC Amphibian Specialist Group (2013). "Boulengerula taitana". IUCN Red List of Threatened Species . 2013: e.T59498A16944134. doi: 10.2305/IUCN.UK.2013-2.RLTS.T59498A16944134.en . Retrieved 20 November 2021.
  2. ↑ Frost, Darrel R. (2018). "Boulengerula taitana Loveridge, 1935". Amphibian Species of the World: an Online Reference. Version 6.0. American Museum of Natural History. Retrieved 22 May 2018.
  3. 1 2 3 IUCN (2013-07-02). "Boulengerula taitana: IUCN SSC Amphibian Specialist Group: The IUCN Red List of Threatened Species 2013: e.T59498A16944134". doi: 10.2305/iucn.uk.2013-2.rlts.t59498a16944134.en .{{cite journal}}: Cite journal requires |journal= (help)
  4. 1 2 Measey, G. John (January 2004). "Are Caecilians Rare? An East African Perspective". Journal of East African Natural History. 93 (1): 1–21. doi: 10.2982/0012-8317(2004)93[1:ACRAEA]2.0.CO;2 . ISSN   0012-8317.
  5. 1 2 3 4 Kupfer, Alexander; Müller, Hendrik; Antoniazzi, Marta M.; Jared, Carlos; Greven, Hartmut; Nussbaum, Ronald A.; Wilkinson, Mark (April 2006). "Parental investment by skin feeding in a caecilian amphibian". Nature. 440 (7086): 926–929. doi:10.1038/nature04403. hdl: 2027.42/62957 . ISSN   0028-0836. PMID   16612382. S2CID   4327433.
  6. 1 2 3 4 Malonza, P. K.; Measey, G. J. (July 2005). "Life history of an African caecilian: Boulengerula taitanus Loveridge 1935 (Amphibia Gymnophiona Caeciilidae)". Tropical Zoology. 18 (1): 49–66. doi: 10.1080/03946975.2005.10531214 . ISSN   0394-6975. S2CID   84191348.
  7. 1 2 3 4 5 Kupfer, Alexander; Wilkinson, Mark; Gower, David J.; Müller, Hendrik; Jehle, Robert (October 2008). "Care and parentage in a skin-feeding caecilian amphibian". Journal of Experimental Zoology Part A: Ecological Genetics and Physiology. 309A (8): 460–467. doi:10.1002/jez.475. PMID   18618577.
  8. 1 2 Measey, G. John; Gaborieau, Olivier (2004). "Termitivore or detritivore? A quantitative investigation into the diet of the East African caecilian Boulengerula taitanus (Amphibia: Gymnophiona: Caeciliidae)". Animal Biology. 54 (1): 45–56. doi:10.1163/157075604323010042. ISSN   1570-7555.
  9. ↑ Herrel, Anthony; Measey, G. John (August 27, 2012). "Feeding Underground: Kinematics of Feeding in Caecilians: CAECILIAN FEEDING KINEMATICS". Journal of Experimental Zoology Part A: Ecological Genetics and Physiology. 317 (9): 533–539. doi:10.1002/jez.1745. PMID   22927194.
  10. ↑ Brun, C.; Raquet, M.A.; Measey, G.J.; Exbrayat, J.M. (2017-07-03). "Cyclic variation of the oviduct structure of Boulengerula taitana , an oviparous species of Gymnophiona: morphological changes, proliferation and apoptosis". African Journal of Herpetology. 66 (2): 93–105. doi:10.1080/21564574.2017.1365098. hdl: 10019.1/117327 . ISSN   2156-4574. S2CID   90577065.
  11. ↑ Kleinteich, Thomas (2010-10-01). "Ontogenetic differences in the feeding biomechanics of oviparous and viviparous caecilians (Lissamphibia: Gymnophiona)". Zoology. 113 (5): 283–294. doi:10.1016/j.zool.2010.05.002. ISSN   0944-2006. PMID   20952171.
  12. ↑ Wood, S.C.; Weber, R.E.; Maloiy, G.M.O.; Johansen, K. (September 1975). "Oxygen uptake and blood respiratory properties of the caecilian Boulengerula taitanus". Respiration Physiology. 24 (3): 355–363. doi:10.1016/0034-5687(75)90024-9. PMID   242053.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.