Intraproboscis

Intraproboscis is a genus of Acanthocephala (thorny-headed or spiny-headed parasitic worms) that infest the black-bellied pangolin and the tree pangolin in central Africa. The genus contains a single species, Intraproboscis sanghae described from several females and one incomplete male. The body consists of a long, thin trunk and a tubular feeding and sucking organ called the proboscis which is covered with hooks. There are 34 to 36 rows of 6 to 7 hooks on the front of the proboscis and 15 to 17 spinelike hooks on the back that are used to pierce and hold the intestinal wall of its host. Female worms reach up to 180 mm long (mostly trunk) and 2 mm while males are smaller in all dimensions (based off an incomplete specimen). Infestation by I. sanghae can cause intestinal perforation and death.

Intraproboscis
Scientific classification
Domain:	Eukaryota
Kingdom:	Animalia
Phylum:	Rotifera
Class:	Archiacanthocephala
Order:	Gigantorhynchida
Family:	Giganthorhynchidae
Genus:	Intraproboscis Amin, Heckmann, Sist, and Basso 2021
Species:	I. sanghae
Binomial name
Intraproboscis sanghae Amin, Heckmann, Sist, and Basso 2021
I. sanghae class=notpageimage| The type locality for I. sanghae is Dzanga-Sangha Complex of Protected Areas in the extreme southwest part of the Central African Republic.

This genus closely resembles the genus Mediorhynchus but differs in having a mammalian hosts instead of avian hosts, a simple proboscis receptacle that is completely suspended within the proboscis, and a complete lack of neck. This first discovery of a parareceptacle structure in Archiacanthocephala represents an important taxonomic and evolutionary bridge between different acanthocephalan groups.

Taxonomy

Intraproboscis is a monotypic genus of acanthocephalans (also called thorny-headed or spiny-headed parasitic worms). The genus Intraproboscis was circumscribed and species I. sanghae was formally described in 2021 by Amin, Heckmann, Sist, and Basso, from four female specimens extracted post-mortem from a 5-year-old black-bellied pangolin. The name Intraproboscis refers to the proboscis receptacle's unusual internal position, while sanghae derives from the Sangha tribal region where specimens were collected.

Six distinct morphological features support Intraproboscis's classification within Giganthorhynchidae and distinguish it from the similar genus Mediorhynchus. Intraproboscis is characterized by: infesting a mammal instead of birds, a simple proboscis receptacle (a complex structure for housing the proboscis when retracted) that is completely suspended within the proboscis, proboscis retractor muscles that pass through the proboscis receptacle and into the body cavity posteriorly, no neck, and a parareceptacle structure and a uterine vesicle which are both absent in Mediorhynchus. In addition to morphological differences, a 18S rDNA analysis further confirms the status of Intraproboscis as a distinct genus forming a separate lineage from Mediorhynchus. The discovery of a parareceptacle structure in Archiacanthocephala is novel, representing an important taxonomic and evolutionary discovery that bridges understanding between different acanthocephalan groups. Several phylogenetic studies have been performed confirming its position in the order Giganthorhynchidae.

Archiacanthocephala

Archiacanthocephala Oligacanthorhynchidae Macracanthorhynchus ingens Oncicola venezuelensis Oligacanthorhynchus tortuosa Nephridiacanthus major Moniliformidae Moniliformis moniliformis Gigantorhynchida Mediorhynchus grandis Gigantorhynchus echinodiscus Intraproboscis sanghae

Cladogram for select taxa in the class Archiacanthocephala based on a 28S rRNA gene comparison from Gomes et. al (2019) and a 18S rDNA gene comparison from Amin et al. (2020) and Rodríguez et al. (2022).

Description

Anatomical measurements of I. sanghae

Measurements	Female (mm)	Male (mm)
Length of proboscis	1.56–1.87	1.37
Width of proboscis	0.27–0.41 (anterior) 0.58–0.74 (posterior)	0.29 (anterior) 0.44 (posterior)
Length of proboscis receptacle	0.77–1.04	0.68
Width of proboscis receptacle	0.26–0.36	0.21
Length of trunk	63.75–180.00	94.25
Max width of trunk	1.12–2.00	1.5
Cephalic ganglion l	166–229 x 60–100	208 x 94
Length of lemnisci	2.08–3.28	4.00
Width of lemnisci	0.22–0.38	0.42
Size of eggs	0.068–0.083 x 0.038–0.052
Size of testes		2.90 x 0.60 (anterior) 1.32 x 0.55(posterior)
Anterior trunk to anterior testis		88.25

Intraproboscis sanghae consists of a proboscis (a tubular organ for attachment to the host's intestinal wall), proboscis receptacle, and a long and narrow trunk that lacks spines and shows noticeable pseudosegmentation (false divisions resembling segments). The original description is based on a sample of four pregnant female worms, and was confirmed with a second which included both females and a single incomplete male. The worms are up to 180 mm long, virtually all of which is the trunk, and 2 mm wide. There is pronounced sexual dimorphism with the female being larger in all measurements: the male body is 94.25 mm long and 1.5 mm wide. The body wall is much thicker on the dorsal side compared to the ventral side, containing many fragmented nuclei and a few large nuclei located at the front.

The proboscis has a truncated cone shape—cylindrical at the front and conical at the back. The anterior proboscis has two sensory pores at the tip has two sensory pores (small openings for detecting stimuli) at the tip and numerous hooks arranged in longitudinal rows, while the posterior part also has hooks, with spines forming dome-shaped folds in the tegument (outer body covering). The roots of the hooks (anchor-like extensions) are about as long as the hook blades. Specifically, the proboscis is armed with 34 to 36 rows (32 in the male sample) of 6 to 7 tightly packed hooks anteriorly and 15–17 more widely spaced spinelike hooks posteriorly which are used to attach themselves to the intestines of the host. The hooks in the anterior proboscis increase in size as they go down the proboscis. At the apex in the female samples, they are 38–44 μm long by 9–11 μm wide whereas they are 40–50 μm long by 12–14 μm wide in the middle of the proboscis, and 47–54 μm long by 15–16 μm wide at base of the proboscis. The spinelike hooks in the posterior proboscis are more or less similar in size being 20–25 μm long by 5–7 μm wide. In the male sample, the anterior hooks are 33 μm long by 8 μm wide, the middle hooks are 37 μm long by 11 μm wide, and the posterior hooks are 42 μm long by 13 μm wide. The spinelike hooks in the posterior proboscis are 18 μm long by 4 μm wide.

The proboscis receptacle (a sac holding the proboscis) is simple in structure, entirely contained within the proboscis, and has a single layer that is thicker on the dorsal side. It is cylindrical but becomes narrower at the back and widens at the front, attaching at the division between the anterior and posterior portions of the proboscis. Retractor muscles (muscles used to pull the proboscis back) pass through its back end. A large, elliptical cerebral ganglion (a mass of nerve cells acting as a brain) is located near the rear of the receptacle. There is one parareceptacle structure (a secondary attachment structure that is 520–624 μm long) connecting the ventral body wall at the front and the receptacle at the back.

The organism has no neck. The lemnisci (bundles of sensory nerve fibers) are long, flat, and wide, located at the front of the body within the posterior proboscis, and contain 8 or 9 large nuclei.

The reproductive system is compact but well-developed, featuring a round uterine vesicle (a sac involved in egg storage and transport that is 387 μm long x 322 μm wide) with anterior and lateral lobes encircled by complex uterine tubules and connected to a tubular structure, a large uterine bell (a funnel-like opening continuous with the uterus for directing eggs) that lacks the glandular structures typically found in related species, and a terminal gonopore (external opening for reproductive discharge). The eggs are oval, with concentric shells (layered coverings); the outer shell is thinner at the poles and is always enclosed within a ligament sac (a protective sac) supported by prominent ligament strands.

Distribution

Range of the black-bellied pangolin (left) and the tree pangolin (right), hosts of I. sanghae

The distribution of I. sanghae is determined by that of its two known hosts. The black-bellied pangolin is a vulnerable species which is at high risk of extinction in the wild. An infested specimen was found in Dzanga-Sangha Complex of Protected Areas, the type locality, located in the extreme southwest part of the Central African Republic. This host is native to parts of western and central Africa, having been found as far west and north as Senegal, across the continent to Western border of Uganda, and south into the northern border of Angola. They are found in areas such as the Congo Basin and Guinean forests. There is a distinct gap in the populations with no record of individuals from southwest Ghana through to western Nigeria.

The tree pangolin (Phataginus tricuspis), which is an endangered species at high risk of extinction, is also a host. This host is native to large portions of central Africa south of the Sahara desert, as far west as Guinea-Bissau in west Africa, as far east as south-western Kenya and north-western Tanzania, and as far south as north-western Zambia and northern Angola.

Hosts

Life cycle of Acanthocephala.

The specific life cycle of Intraproboscis is unknown, but the life cycle of thorny-headed worms, or acanthocephala, in general unfolds in three distinct stages. It begins when an egg develops into an infective form known as an acanthor. This acanthor is released with the feces of its definitive host, typically a vertebrate, and must be ingested by an intermediate host, an arthropod such as an insect, to continue its development. Although the specific intermediate hosts for the genus Intraproboscis are unidentified, it is generally accepted that insects serve as the primary intermediaries as they make up the diet of the host.

Inside the intermediate host, the acanthor molts its outer layer, becoming an acanthella. At this stage it burrows into the host's intestinal wall and continues to grow. The life cycle culminates in the formation of a cystacanth, a larval stage that retains juvenile features (differing from the adult only in size and stage of sexual development) and awaits ingestion by the definitive host to mature fully. Once inside the definitive host, these larvae attach themselves to the intestinal walls, mature into sexually reproductive adults, and complete the cycle by releasing new acanthors into the host's feces.

I. sanghae parasitizes two species of pangolin: black-bellied pangolin (Phataginus tetradactyla) and the tree pangolin (Phataginus tricuspis). The black-bellied pangolin, the type host, by using their proboscis hooks to pierce and hold the wall of the intestines. They have been found perforating the intestine and invading the body cavity and causing secondary septic peritonitis (an infection of the peritoneum, the thin tissue lining the abdomen, that's caused by the parasite). The cause of death for the sampled host was intestinal perforation. There are no reported cases of I. sanghae infesting humans in the English language medical literature.

• Hosts for Apororhynchus species
• 
  The black-bellied pangolin is the definitive host of I. sanghae.
• 
  The tree pangolin is the second host of I. sanghae discovered.