Histological, histochemical, and ultrastructural investigation of the male copulatory apparatus of Haminoea navicula (Gastropoda, Cephalaspidea)

Abstract

Due to its biological and systematic importance, the morphology and function of the male copulatory apparatus of Haminoea navicula, a Cephalaspidea gastropod mollusk, was investigated by light and electron microscopy. These systems are poorly understood in haminoids, but are often used in the taxonomy of the genus. In H. navicula, the male copulatory apparatus comprises the penis within a penial sheath, a seminal duct and the prostate with two lobes. The penis is a muscular structure with a tip covered by spikes formed by muscular cells. The penial sheath consists of muscular tissue folds lined by an epithelium. Below this epithelium, polysaccharide-secreting cells and pigment cells were observed. A large number of vacuolar cells were found below the ciliated epithelium of the seminal duct. The proximal lobe of the prostate was formed by tubules that could be divided in basal, middle and apical zones, containing cells that secrete polysaccharides and proteins. The tubules of the prostate distal lobe contained a single type of secretory cells with vesicles that were stained by histochemical techniques for detection of polysaccharides and proteins. Ciliated cells were present along the tubules in both lobes of the prostate. This study revealed a complex prostate with five types of secretory cells, which secrete substances that should be involved in the maintenance and eventually also in the maturation of spermatozoa. A comparison with previous publications, shows that the male copulatory apparatus can differ substantially among cephalaspideans, even between H. navicula and non-European species attributed to this genus.

The copulatory apparatus of the marine gastropod Haminella solitaria (Heterobranchia: Cephalaspidea) and its phylogenetic relevance

“…Because of its taxonomic relevance, the general anatomy of the copulatory apparatus of cephalaspideans is usually mentioned in species and genus descriptions. However, histological and ultrastructural data are available only for a very limited number of species (Amorim et al, ; Kress, ; Lobo‐da‐Cunha et al, ). Deeper investigations of this apparatus are currently more interesting because it is now possible to analyze correlations between the morphofunctional features of the copulatory apparatus and species positions in more robust molecular phylogenetic trees.…”

“…The histological studies revealed substantial differences between the copulatory apparatus in Haminoea navicula and Haminella solitaria . In Haminoea navicula the penial sheath surrounds a muscular penis containing a penial duct, which is continuous with the seminal duct (Lobo‐da‐Cunha et al, ). In Haminella solitaria a real penis is absent.…”

“…Instead, a muscular papilla without a duct was found inside an atrium, and spermatozoa must travel around it to enter into the seminal duct and reach the prostate. Furthermore, the prostate in Haminoea navicula has two lobes and contains five types of secretory cells (Lobo‐da‐Cunha et al, ), whereas in Haminella solitaria only one type of secretory cell was found in the single‐lobed prostate, with additional types of secretory cells in the atrium wall and papilla. These substantial differences in the copulatory apparatus support the placement of these two species in different genera, as established by recent molecular studies (Oskars et al, ).…”

“…The histological, histochemical, and ultrastructural studies reveal the complexity of the copulatory apparatus of cephalaspideans, with many types of mucous‐ and glycoprotein‐secreting cells that must have specific functions not yet known. In the penial sheath in Haminoea navicula a single type of polysaccharide‐secreting cell was observed (Lobo‐da‐Cunha et al, ). On the other hand, the atrium wall of the copulatory apparatus in Haminella solitaria contains two cells types secreting acid polysaccharides and glycoproteins, plus an additional type of glycoprotein‐secreting cell in the distal zone of the papilla.…”

“…In these hermaphroditic animals the gonad (ovotestis) is embedded in the digestive gland. Mature sperm cells emerge through the common genital pore located on the right side at the midpoint of the body, travel along the external seminal groove and enter into the copulatory apparatus, where spermatozoa are stored in the prostate until copulation (Amorim, Oliveira, Malaquias, & Lobo‐da‐Cunha, ; Gosliner, ; Lobo‐da‐Cunha, Alves, Oliveira, & Malaquias, ).…”