Research Article |
Corresponding author: Ryoichi B. Kuranishi ( cji0820@kmd.biglobe.ne.jp ) Academic editor: Astrid Schmidt-Kloiber
© 2023 Ryoichi B. Kuranishi, Ryo Sato, Masashi Murakami.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Kuranishi RB, Sato R, Murakami M (2023) Functional morphology of the genitalia of Rhyacophila lezeyi Navas, 1933 (Trichoptera, Rhyacophilidae). Contributions to Entomology 73(2): 195-199. https://doi.org/10.3897/contrib.entomol.73.e109843
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We collected seven fixed pairs of Rhyacophila lezeyi during mating copulation and observed four different states of copulation. We investigated the underlying mechanism for the variations in the morphology of each copulating device, based on the copulation state. Notably, the male anal sclerites underwent considerable changes from the early stages of copulation. Initially, the female segment VIII approached the male anal sclerites, which were pushed downwards by the female VIII and IX segments, extending from IX. With the progression of mating stage, the distended end of the female’s segment VIII covered the anal sclerites, pushing them further down. The male parameres were initially folded in bellows-like shapes under the aedeagus before copulation initiation. However, as the copulation stage advanced, they extended to about 3.2 times of their original length. Distended ends of both parameres adhered to the position of the spiracles at the anterior margin of the lateral part of the female’s VII abdominal sternite. The attachment site was the external surface of the hair bulb of the male parameres. During the middle stage of copulation, movements involving the opening and closing of the male gonopods started. The gonoslylus made strong contact with the female’s abdominal segment VIII, resulting in the deformation of segment VIII due to the contact pressure.
anal sclerites, copulatory organ, female segment VIII, fixed pairs, mating copulation, parameres
The identification of species is often based on the morphology of the copulatory organ, which is the most extensively studied morphological trait in caddisflies. The diversity of morphological characters of copulatory organs is well recognised in Trichoptera (
While discussing the ground plan and basic evolutionary trends of male copulatory organs in caddisflies,
It is not difficult in itself for us to find mating caddisflies. We can often find mating pairs, especially in the diurnally active rhyacophilid caddisfly. However, it is difficult to observe pre-mating behaviour or examine how the copulatory apparatus functions during mating, even if many mating individuals can be seen. Parallelly-positioned females and males perform the so-called “mating turn”, in which their heads face in the opposite directions, as soon as their respective abdominal ends are in contact. After the mating turn, the abdominal ends of the female and male are completely hidden under their respective wings, making it difficult to directly observe the way copulation proceeds and function of various parts of the copulatory apparatus. A reasonable way to observe the positioning and relationships between each part of the copulatory apparatus during the mating copulation is by capturing mating pairs at the copulation. In this study, rhyacophilid caddisfly pairs were frozen and fixed during the mating copulation in the field and the copulating state was comprehensively examined to clarify how the various parts of the copulation apparatus were related to each other between pairs.
Rhyacophila lezeyi Navas, 1933 belongs to the R. acropedes species group (
Adults of R. lezeyi were collected on 8 June 2021 from Kosuge-gawa (35°45'16"N, 138°53'57"E), a mountain stream in Kosuge-mura, Yamanashi Prefecture in central Japan. As copulating pairs of the rhyacophilid caddisflies can be easily separated from each other due to external stress or disturbance, we took the following steps to preserve them in a mating state: 1) drop the mating pair very gently into an insect net, 2) freeze it instantaneously, with a cooling spray (the active ingredients are listed as HFO-1234ze and DME), 3) wrap the mating individuals in Kimwipe (Kimberly Clark Corp.), 4) soak the wrapped specimens in boiling water for a few seconds, 5) put them in plastic tubes filled with 75% ethanol, 6) take the samples to the laboratory, 7) observe the appearance of the mating state and 8) detach the abdomen from the body and treat it with 5% potassium hydroxide for transparency. Mating pairs and reproductive organs were dissected under a stereomicroscope and micrographs were taken with a digital camera attached to the stereomicroscope.
Fig.
Seven pairs of R. lezeyi were collected in a copulating state that had completed the mating turn. The mating status of each pair was classified into four states as follows. State A (four of the seven pairs) was defined when the mating had been dissolved and the pairs were separated from each other (Fig.
Although the paired specimens in this study were not strictly fixed at a specific time series after the male and female met and initiated copulation, the overall condition of the female VIII segment, anal sclerites, parameres and gonopods suggested a time elapsed during the progression from State A to State B to State C to State D. The present results clearly showed the sequence of mating behaviour of R. lezeyi after the mating turn. Based on these findings, it can be assumed that State A, when mating was not established, represented the very early stage of mating. It was found that, after the mating turn, genital locking does not first occur before the progression of mating situation. Before mating commenced, the male was observed to bend his abdomen in a U-shape and open and close his gonopods to approach the female. Despite conspicuous movement of the gonopods, the gonopodal lock was not completed during the early stages of copulation. Conversely, the state of the anal sclerites markedly changed immediately after the onset of the mating state following the mating turn. The female’s abdominal end made direct contact with the male’s anal sclerites, causing them to fold substantially in the downward direction. At this point, instead of the male phallic organ ejecting and approaching the female, the female’s abdominal end extended and entered the male’s copulatory apparatus. Before the mating began, the parameres were folded and stored under the phallic organ in a bellows-like shape. In the early stages of mating (States A and B), they were extended to about 1.5 times their normal length. In States C and D, the state of the parameres changed drastically, i.e. the parameres were elongated to approximately 2.7–3.2 times the length of the precopulating state and one or both of the parameres reached and contacted the female’s abdomen.
Observations of fixed Rhyacophila lezeyi copulatory organs suggested the copulating state changed even after the mating turn. In R. lezeyi, the female abdominal terminal was inserted into the male anal sclerites. Anal sclerites may support and stabilise the copulating state. The parameres were markedly elongated and in contact with the female abdomen. In rhyacophilid caddisfly, the long abdominal terminal of the female is presumed to have a function not only in egg laying, but also in exploring the male’s phallic organ during the early stages of copulation and in strengthening copulation.
We thank Yoshitaka Kamimura for his important technical advice and critical reading of the manuscript and thanks Vladimir D. Ivanov and John S. Weaver for kind advice and information. We thank Naotoshi Kuhara for providing micrographs of R. articulata.