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Sternal Keel Affects Swimming Speed in Giant Water Scavenger Beetles (Coleoptera: Hydrophilidae: Hydrophilini)

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Sternal Keel Affects Swimming Speed in Giant Water Scavenger Beetles (Coleoptera: Hydrophilidae: Hydrophilini) Canadian Journal of Zoology Evidence of morphological adaptation to life underwater: Sternal keel affects swimming speed in giant water scavenger beetles (Coleoptera: Hydrophilidae: Hydrophilini) Journal: Canadian Journal of Zoology Manuscript ID cjz-2020-0247.R1 Manuscript Type: Article Date Submitted by the 23-Dec-2020 Author: Complete List of Authors: Matsushima, Ryosuke; University of Tsukuba Is your manuscript invited for consideration in a Special Not applicableDraft (regular submission) Issue?: Aquatic beetles, gas gill, motion analysis, oscillatory movement, Keyword: submergence, water scavenger beetles, Hydrophilus acuminatus © The Author(s) or their Institution(s) Page 1 of 22 Canadian Journal of Zoology Evidence of morphological adaptation to life underwater: Sternal keel affects swimming speed in giant water scavenger beetles (Coleoptera: Hydrophilidae: Hydrophilini) Ryosuke MATSUSHIMA1 1Laboratory of Conservation Ecology, Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan Draft Correspondence: Ryosuke Matsushima, Laboratory of Conservation Ecology, Graduate School of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8572, Japan E-mail: [email protected] ORCID: https://orcid.org/0000-0001-5131-4147 1 © The Author(s) or their Institution(s) Canadian Journal of Zoology Page 2 of 22 Abstract Fundamentally, insects evolved on land and secondarily inhabited aquatic environments multiple times. To live underwater, aquatic insects have acquired enormously variable morphological, developmental, physiological, and ecological traits, such as gas exchange systems and swimming-related characteristics. Giant water scavenger beetles of the tribe Hydrophilini (Coleoptera: Hydrophilidae) are characterised by the presence of sternal keel, which often extends posteriorly. Despite being a conspicuous morphological trait, its function remains unclear. Here, I verified two hypotheses: keel affects (1) submergence time following air replacement as well as (2) speed and oscillatory movement during forward swimmingDraft in Hydrophilus acuminatus Motschulsky, 1854. Submergence time was affected by body mass rather than keel removal; in other words, larger individuals replaced their gas gills more frequently. Keel removal reduced swimming speed by 12.5%. These observations support hypothesis (2) and are also consistent with previous speculations that sternal keel is a key adaptation to swim, but the results showed that the degree of oscillation was closely related to body mass but not keel removal. Further studies are warranted to elucidate precise factors through which the presence of keel increases swimming speed. Such studies would provide clues into understanding the associations amongst body size, swimming methods, and morphological traits. Keywords: Aquatic beetles; gas gill; Hydrophilus acuminatus; motion analysis; oscillatory movement; submergence; water scavenger beetles 2 © The Author(s) or their Institution(s) Page 3 of 22 Canadian Journal of Zoology INTRODUCTION Fundamentally, insects evolved on land, and some orders, including Diptera, Hemiptera, and Coleoptera, secondarily inhabited aquatic environments multiple times (e.g. Andersen 1995; Jäch and Balke 2008). To live underwater, these insects have acquired enormously variable morphological, developmental, physiological, and ecological traits (Lancaster and Downes 2013; Bilton et al. 2019). One of the most specialised traits in aquatic insects is gas exchange system. For instance, most adult diving beetles (Dytiscidae) and water boatmen (Corixidae) use gas gills: they hold air bubblesDraft under elytra and hemielytra or trap them using a layer of hydrophobic hair (Rahn and Paganelli 1968). The water bug Aphelocheirus sp. (Aphelochiridae) possess plastron gills, which can fully satisfy body’s oxygen demand by diffusion of oxygen from water into the gas store (Thorpe 1950; Flynn and Bush 2008; Seymour et al. 2015). Moreover, swimming-related traits of aquatic insects, such as body shape and limb structure, are evidently modified in various ways. For instance, adult dytiscids and gyrinids show dorso-ventrally flattened or streamlined bodies and oar-like legs possessing swimming hair. These specialised morphological traits help energy-efficient swimming by minimising drag as well as increasing stability and manoeuvrability (Nachtigall 1961; Ribera and Foster 1997). Water scavenger beetles (Coleoptera: Hydrophilidae) comprise over 3000 described species that show nearly global distribution (Short and Fikáček 2013). Many of these species are well-known as aquatic beetles inhabiting 3 © The Author(s) or their Institution(s) Canadian Journal of Zoology Page 4 of 22 various environments, including small ponds, stream margins, and wetlands. Some species inhabit both semiaquatic and terrestrial environments. Aquatic hydrophilids hold air bubbles on their ventral thorax and/or abdomen in addition to under wings, namely, gas gill breathers. Under air deficiency, these insects extend their antennae above water and send fresh atmospheric air to the gas store (Lancaster and Downes 2013). However, the air bubbles on the ventral side would make it difficult for them to maintain posture in the water. Indeed, several groups with smaller body sizes (e.g., Amphiops) move through the water with their ventral side above (Angus 1966). As for their swimming method, they follow alternate-leg swimming (legs on either side are paddled alternately), producing a distinct side-to-sideDraft body movement, similar to the members of Haliplidae and Curculionidae (Hughes 1958; Barr and Smith 1980). Majority of hydrophilids bear swimming hair on the tibiae and/or tarsi (Hughes 1958; Short and Fikáček 2013). Overall, the gas exchange system and swimming-related traits of hydrophilids play pivotal roles in enabling life underwater. The tribe Hydrophilini contains some of the largest aquatic insects in the world, with some species exceeding a body length of 50 mm (Short 2010; Short and Fikáček 2013). Importantly, all members of this tribe are characterised by the presence of sternal keel, resulting from the fusion of meso- and metaventral elevations, which often extends posteriorly over the abdominal ventrites as a sharp spine (Hansen 1991; Short and Fikáček 2013). Interestingly, it is similar to the structure at the bottom of a ship—also called the keel. Although the genus Hydrophilomima (Hydrophilidae: Laccobiini) also has the sternal keel, it is not extend to the same extent 4 © The Author(s) or their Institution(s) Page 5 of 22 Canadian Journal of Zoology as in most Hydrophilini, indicating the sternal keel is unique to this tribe of aquatic beetles. However, despite being a conspicuous morphological trait, its function remains unclear. Typically, larger animals show higher oxygen requirements, and increase in oxygen storage capacity allows them to submerge longer (Zeuthen 1953; Verberk et al. 2020). Therefore, members of Hydrophilini, which are amongst the largest aquatic beetles, may exhibit specific traits to meet high oxygen demand. Additionally, since they store air bubbles ventrally, where the keel is located, this structure may affect the ability to hold air bubbles (Watanabe 1982; Dettner 2019). Previously, Barr and Smith (1980) hypothesized that sternal keel damps out wobble, providing a more stable forward trajectory.Draft In the present study, to clarify the functions of sternal keel in Hydrophilini, I examined the effects of keel removal on (1) submergence time following air replacement as well as (2) speed and oscillatory movement during forward swimming. MATERIAL AND METHODS Study animal Hydrophilius acuminatus Motschulsky, 1854 (body length, 33–40 mm) belongs to the family Hydrophilidae and is distributed in China, Japan, Russia, Korea, Myanmar, Indonesia, and Taiwan (Hansen 1999). This species usually inhabits lentic water systems, such as ponds and paddy fields (Satô and Yoshitomi 2018). From late July to early August 2020, six males and six females of adult H. acuminatus were collected from paddy fields in 5 © The Author(s) or their Institution(s) Canadian Journal of Zoology Page 6 of 22 Tsukuba, Ibaraki Prefecture, Japan (36°11′33″N, 140°06′42″E, ca. 52 m above sea level). The individuals were not fed and maintained in plastic containers (31 cm × 16 cm basal width × 22 cm height) with moistened filter paper in the laboratory at approximately 25 °C. Within 12 h of collection, the keel of three males and three females was cut and filed using a nail clipper and a nail file. The ridge on the head side and the spine were cut and filed, and the raised section between the middle and hind legs was filed (Fig. 1a). The experiments were conducted within at least 48 h of collection, after confirming that their activity levels had not decreased. Draft Experiment 1. Submergence time following air replacement One individual with or without keel was placed into a plastic container (19.5 cm × 17.5 cm basal width × 10 cm height) filled with water up to 2.5 cm and containing a plastic net (13 cm × 10 cm) on the bottom (Fig. 1b). Air-replacing behaviour was observed, and submergence time, defined as is the duration from when the insects extended their antennae above water surface and replaced gas gills to when they did so again, was recorded after every air replacement event. Ten consecutive observations were recorded for twelve individuals (with keel: three males and three females, without keel: three males
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