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The last two moulting processes of Parafronurus youi and possible emergence evolution of (Ephemeroptera: )

Juan-Yan Luo, Ze Hu, Zhen-Xing Ma & Chang-Fa Zhou

To cite this article: Juan-Yan Luo, Ze Hu, Zhen-Xing Ma & Chang-Fa Zhou (2017): The last two moulting processes of Parafronurus youi and possible emergence evolution of Mayflies (Ephemeroptera: Heptageniidae), Oriental Insects, DOI: 10.1080/00305316.2017.1415172 To link to this article: https://doi.org/10.1080/00305316.2017.1415172

Published online: 21 Dec 2017.

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The last two moulting processes of Parafronurus youi and possible emergence evolution of Mayflies (Ephemeroptera: Heptageniidae)

Juan-Yan Luo , Ze Hu, Zhen-Xing Ma and Chang-Fa Zhou

The Key Laboratory of Jiangsu and Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing, China

ABSTRACT ARTICLE HISTORY Moulting processes of last instar and subimago, Received 10 February 2017 longevity of subimago and imago of Parafronurus youi is Accepted 6 December 2017 observed and filmed in laboratory for the first time in China. KEYWORDS The videos show clearly this emerges in the afternoon ; emergence; moult; (ca. 5:30 PM to 9:30 PM) on the object surface in water. The subimago; Heptageniidae subimagos moult 14–19 h later before noon. Imago can survive for 3 to 4 days in lab. The data in the present paper and others as well as phylogeny do not provide clear evolutionary pattern of mayfly emergence location or time but a possibility maybe present: both the primitive mayfly nymph and adult can live and emerge on moist land, then adapt to aquatic habitats.

Introduction

Mayflies are unique winged insects because of their two adult instars (subimago and imago). However, the ecdysis of aquatic mayfly nymphs are difficult to observe in the field and their subimaginal stage is very brief. So there are few detailed reports on metamorphic pattern of mayflies although some researchers sum- marised this process. Kimmins (1941) reported the lateralis nymph (now in the ) can emerge underwater or on the surface of water. Minshall (1967) and Hall et al. (1975) observed, respectively, the pleralis and atratus can moult in water too. Peters and Peters (1977) show the species americana life history. Russev (1987) took some pictures about moulting behaviour and process of . The latter two species emerge on the water surface. Generally, Edmunds and McCafferty (1988) pro- posed some mayflies (like and Coloburiscus) can emerge on the surface of water or on the land but most mayflies emerged at surface of the water, such as

CONTACT Chang-Fa Zhou [email protected] © 2017 Informa UK Limited, trading as Taylor & Francis Group

Published online 21 Dec 2017 2 J.-Y. LUO ET AL. some species of and . Brittain (1982) and Bauernfeind and Soldán (2012) indicated mayflies can emerge at surface of water, under water or above water. For instance, , Isonychia and mayflies will climb out of water to moult. But the evolutionary trends of them have not been hypothesised so far. According to Kukalová-Peck (1978, 1991), the original mayflies probably lived in the moist environment and then became aquatic. That means living in the water of mayfly larvae is secondary. So in our own opinion, if more species emergence processes are detailed, they can help us solve some phylogenetic and evolutionary puzzles of Ephemeroptera. In China, only few mayfly species biology was mentioned and discussed briefly (Zhou and Peters 2003, 2004; Wang et al. 2011), but no specific research on this issue. In 2015, the Parafronurus youi Zhou and Braasch (2003) were reared, observed and recorded in lab. Therefore, the biology of this species, such as emer- gence of nymph, moulting of subimago, longevities of subimago and imago are clear to us and described here. Their possible phylogeny and evolutionary value are discussed.

Methods Mayfly rearing (Fig. 1) Nymphs are collected with a hand net (40 um) or a hand nylon mesh (35 um) in the ponds and creeks of Zijin Mountain, Nanjing, Eastern China. Mature nymphs (with black wingpads) were taken back to laboratory and reared in the white plastic trays (size 40 × 25 × 8 cm) which were filled with stones (some parts above water), withered leaves and water gathered in the creek where the insects live. The rearing water depth is about 5 cm under the temperature 18–25 °C. Those trays were covered with mosquito nets to catch the adults (Fig. 1).

Video taking

In order to observe and see clearly the moulting process, we took videos with smartphones. When we find mature nymphs show some abnormal behaviour like moving fast and irregularly, we focus on them and record. The videos will replay on laptop and key information will be written down. Totally 22 emergence videos of nymphs and 3 moulting episodes of subimagos are filmed. They show exactly the last two moulting process of the mayfly P. y oui and some information of its life history. ORIENTAL INSECTS 3

Figure 1. The rearing equipment.

Results Moulting of the nymph (Fig. 2A–C) The last instar nymphs of Parafronurus youi moult at about 5:30 PM to 9:30 PM (Beijing time). Just before that, the nymphs will climb to or grasp the stone surface in the water (Fig. 2A). This phenomenon can happen several times. At the same time, the colour of ongoing moulting nymphs becomes conspicuously darker and the vibrations of gills are quicker than normal. Before moulting, the gas bubbles can be seen in head, thorax and wingpads first. This process lasts several minutes. During this period, they will move forth and back if they are touched by other larvae or be shaken. Also in this process, the nymphs can climb to stone tips above the water one to several times, expose their dorsal head or half body into the air 1–2 s and move back down to the water. Just before the emergence, three caudal filaments of nymphs will put together quickly. After the gas bubbles appeared in the body about 6 min, pro- and mesonotum will split in the middle, and then extend to vertex. Soon the head and thorax of subimago come out of nymphal exuviae and pull forward slowly, and then legs, wings, abdomen and caudal fila- ments appeared progressively. This emergence process can last 11s–126s (Table 1). During this process, the packed wings show silver white appearances. After they take off their exuviae, the subimagos will move to the water surface immediately. As soon as they touch the air, the wings of them stretched out fully and became brown to black immediately. 4 J.-Y. LUO ET AL.

Figure 2 A–H. Different stages of Parafronurus youi; A, nymph; B–C, nymph moulting to subimago; D, female subimago; E–G, moulting subimago; H, male imago.

Longevity of the subimago

Under laboratory conditions (20–25 °C), the observed living time of three subima- gos (Fig. 2D) (from coming out of nymphal skin to next moult) is about 14–19 h.

Moulting of the subimago (Fig. 2E–G)

Before subimagos begin to moult, their vertically positioning wings will flap down and hold laterally step by step. When wings are at horizontal position, they bend backwards slightly. The whole body, meanwhile, is shaking quickly. Then the head and thorax of imago come out from their shells and move forward slowly or roll over to pull abdomen and caudal filaments out of cuticle. The average lasting time ORIENTAL INSECTS 5

Table 1. The moulting time of the Parafronurus youi nymph.

Video The start time of moulting The time of metamorphosis 1 19:22:57 112s 2 21:12:26 11s 3 19:33:25 119s 4 17:47:11 111s 5 18:05:58 126s 6 18:01:12 95s 7 18:39:41 88s 8 18:47:21 94s 9 18:59:09 81s 10 19:01:01 87s 11 19:16:08 98s 12 19:24:21 86s 13 19:40:31 107s 14 18:37:14 110s 15 18:57:31 93s 16 19:10:23 108s 17 19:17:51 113s 18 18:07:32 111s 19 18:20:11 121s 20 19:19:41 109s 21 20:32:20 99s of this moulting is 233 s. The time of subimaginal moulting is from about 10:00 to 12:00 AM (Beijing Time) (Table 2).

Longevity of the imago

The imagos (Fig. 2H) in mosquito net can live 3–4 days under laboratory condi- tions. Mating, swarming and oviposition were not seen.

Discussion

In order to compare the emergence patterns of mayflies, we list the related infor- mation in the literatures we can find (Table 3). From it, besides most mayflies emerge at the water surface, no other obvious and congruent evolutionary trend can be summarised generally, either the emergence location or time. For exam- ple, the heptageniid and leptophlebiid nymphs have three moulting types: at the surface of water, under water or above water. The ephemerellid and leptohyphid species have two types. Furthermore, the species in same genus can have more than one moulting type, like , Habroleptoides and . Even

Table 2. The moulting time of the Parafronurus youi subimago.

The time of the The start time of The preparation The time of meta- whole moulting Video moulting time of moulting morphosis process A 10:15:28 81s 203s 284s B 11:30:57 – 153s 153s C 11:47:15 81s 180s 261s Average time 81s ≈179s ≈233s 6 J.-Y. LUO ET AL. oldán oldán oldán oldán oldán oldán oldán oldán oldán oldán oldán dmunds et al. dmunds et al. Literature dmunds et al. ( 1976 ) dmunds et al. ( 2012 ), E ( 1976 ) 2012 ; E ( 2012 ) ( 2012 ) ( 2012 ) ( 2012 ) ( 2012 ) ( 2012 ) ( 2012 ) ( 2012 ) ( 2012 ) ampbell ( 1986 ) dmunds et al. ( 1976 ) dmunds et al. dmunds et al. ( 1976 ) dmunds et al. dmunds et al. ( 1976 ) dmunds et al. Bauernfeind and S Bauernfeind I de ( 1930 ) and S Bauernfeind E ( 1973 ), Pescador ( 1977 ) and Peters Peters and S Bauernfeind C ( 1935 ) N eedham et al. E and S Bauernfeind and S Bauernfeind and S Bauernfeind E and S Bauernfeind and S Bauernfeind Bauernfeind and S Bauernfeind and S Bauernfeind and S Bauernfeind – – – – – – – – – – – – – – – – subimago The living longevityThe of 8–10 h A bout 24 h 12 h 7 to L ast from - – – – – – – – – – – – – – gence econds (rapidly) econds ake a shortake time mmediately n 5 or 10 s mmediately The longevityThe of emer I T I I S 15 min B B B B B B B B B B B B B A A A A A A Location of emergence Location M and – – – – – – – – – emergence 2:30 PM ing fternoon fternoon vening and mid-morn - vening wilight to dusk to wilight The beginning time of beginning The n the afternoon n the afternoon A I Between 8:30 A I During daylight hours During daylight Between 10:00 and 16:00 E T A During daytime Species Centroptilum convexum Centroptilum Baetis rhodani Pseudocloeon rogersi Baetisca Dolania americana Behningia ulmeri Callibaetis fluctuans Callibaetis Baetis parvus Baetis fascicaudale Procloeon Procloeon Cloeon Metreletus Ametropus aapta Mirawara Arthroplea Ameletus inopinatus Ameletus subnotatus Ameletus validus he moulting processes of reported mayflies. he moulting processes Baetidae Baetidae Baetidae Behningiidae Baetidae Baetidae Baetidae Baetidae Baetidae Baetidae Table 3. T Table Family A meletidae A metropodidae A meletopsidae A rthropleidae A meletidae A meletidae A meletidae ORIENTAL INSECTS 7 afferty oldán oldán oldán oldán oldán ) ( Continued Literature ( 1988 ) ( 1926 ) ( 2012 ) ( 2012 ) ( 2012 ) eedham et al. ( 2012 ), N eedham et al. ( 1935 ) ( 2012 ) ampbell ( 1986 ) dmunds and Mc C ( 1976 ) dmunds et al. dmunds et al. ( 1976 ) dmunds et al. dmunds et al. ( 1976 ) dmunds et al. dmunds et al. ( 1976 ) dmunds et al. E E Kennedy ( 1926 ) and Whitehead Percival and S Bauernfeind Funk et al. ( 2008 ) et al. Funk E Funk et al. ( 2008 ) et al. Funk and S Bauernfeind E ( 2008 ) et al. Funk and S Bauernfeind ( 2008 ) et al. Funk Funk et al. ( 2008 ) et al. Funk Wisely ( 1965 ) Wisely Bauernfeind and S Bauernfeind E and S Bauernfeind C – – – – – – – – – – subimago everal days everal The living longevityThe of 24–48 h A bout 24–36 h 22–30 h 22–30 h hours A few S immediately 5–6 min 1–2 h - – – – – – – – – – gence this position everal minutes to ½ h in to minutes everal mmediately mmediately mmediately The longevityThe of emer I 10 s I 10–20 s I hours A few seconds A few S 1–2 h 10–12 s B B B B B B B B B B B B B B B B B A A Location of emergence Location - - – – – – – – – – emergence sunset times occurs in evening times occurs times occurring after times occurring sunset afternoon late ing to species morning night fternoon The beginning time of beginning The n the late afternoon or at afternoon or at n the late n the afternoon some n the afternoon some n the afternoon n the evening or early n the evening n the afternoon or at n the evening I A I I mid-morn - from A nytime I ate afternoon in most L ate During the night I I I Species Ephemerella species n some species of n others of Ephemerella Hexagenia limbata Hexagenia simulans danica Ephemera Ephemera I bilineata Hexagenia Ephemerella ignita Ephemerella I Eurylophella oviruptis Torleya Eurylophella dorothea Eurylophella invaria Eurylophella verisimilis Most other Eurylophella Coloburiscoides giganteus Coloburiscoides bumeralis Coloburiscus Caenis diminuta Caenis japonicus Brachycercus aenidae aenidae aenidae oloburiscidae oloburiscidae E phemeridae E phemeridae E phemeridae E phemeridae E phemerellidae E phemeridae E phemerellidae E phemerellidae E phemerellidae E phemerellidae E phemerellidae E phemerellidae ). 3. ( Continued Table Family E phemerellidae E phemerellidae C C C C C 8 J.-Y. LUO ET AL. oldán oldán oldán oldán oldán oldán oldán oldán oldán oldán oldán oldán ( 2012 ) dmunds et al. dmunds et al. dmunds et al. Literature ( 1980 ) (1978) ( 2012 ) ( 2012 ) ( 2012 ) and S feind ( 2012 ) ( 2012 ), E ( 1976 ) ( 2012 ), E ( 1976 ) ( 2012 ) ( 2012 ) ( 2012 ) ( 2012 ) ( 2012 ) dmunds et al. ( 1976 ) dmunds et al. ( 1976 ) dmunds et al. dmunds et al. ( 1976 ) dmunds et al. dmunds et al. ( 1976 ) dmunds et al. ehmkuhl ( 1968 ) E E Voshell Kondratieff and and Hilsenhoff Flowers Bauernfeind and S Bauernfeind and S Bauernfeind and S Bauernfeind Kimmins ( 1941 ), Bauern - Bauernfeind and S Bauernfeind and S Bauernfeind Minshall ( 1967 ) and S Bauernfeind Bauernfeind and S Bauernfeind L E Bauernfeind and S Bauernfeind Bauernfeind and S Bauernfeind and S Bauernfeind and S Bauernfeind E – – – – – – – – – – – – – – – subimago The living longevityThe of 20–36 h 24 h 2–21/2 days in laboratory 2–21/2 days 3–4 days A bout 2 days - – – – – – – – – – – – – – – – – – – gence akes only a few seconds only a few akes The longevityThe of emer T pparently quite long quite A pparently B B B B B B B B B B C C C C C C C C A C /B Location of emergence Location – – – – – – – – – – – – － emergence afternoon t dusk The beginning time of beginning The n the evening 6:30 PM to 8:00 PM to 6:30 PM A round noon and early A round During daytime afternoon During the late dusk A round I Species smithae Stenonema modestum Stenonema terminatum Stenonema Ephemera uulgata Ephemera insignis Ecdyonurus torrentis Ecdyonurus lateralis Electrogena kugleri Afronurus Epeorus Heptagenia Heptagenia fuscogrisea Epeorus nitidus Rhithrogena loyolaea Rhithrogena semicolorata Rhithrogena morrisoni Rhithrogena canadense ). 3. ( Continued Table Family Heptageniidae Heptageniidae Heptageniidae E phemeridae Heptageniidae Heptageniidae Heptageniidae Heptageniidae Heptageniidae Heptageniidae Heptageniidae Heptageniidae Heptageniidae Heptageniidae Heptageniidae Heptageniidae Heptageniidae Heptageniidae Heptageniidae Heptageniidae ORIENTAL INSECTS 9 oldán oldán oldán oldán oldán oldán oldán oldán oldán oldán oldán oldán ) ( Continued artori ( 1994 ) dmunds et al. dmunds et al. Literature dmunds et al. ( 1976 ) dmunds et al. ( 2012 ) ( 2012 ) ( 2012 ) ( 2012 ) ( 2012 ), E ( 1976 ) E ( 2012 ) ( 2012 ) ( 2012 ) ( 2012 ) ( 2012 ) ( 2012 ) ( 2012 ) dmunds et al. ( 1976 ) dmunds et al. dmunds et al. ( 1976 ) dmunds et al. ( 1976 ) dmunds et al. ubini and S akemon ( 1993 ) akemon E and S Bauernfeind and S Bauernfeind and S Bauernfeind L T and S Bauernfeind and S Bauernfeind ( 1975 ), Hall et al. E and S Bauernfeind and S Bauernfeind ( 1972 ) Kjellberg E and S Bauernfeind and S Bauernfeind and S Bauernfeind and S Bauernfeind and S Bauernfeind – – – – – – – – – – – – – – subimago female is briefer female The living longevityThe of 12–14 h Between 22 and 31 h of the 5–7 h but that 5–6 h 8–10 h - – – – – – – – – – – – – – – – gence stayed about 30 s stayed he process had been he process The longevityThe of emer mmediately A moment Within 2 h Within I T B B B B C C A A A A A A A A A A A A A Location of emergence Location – – – – – – emergence afternoon to the night to night night shortly early evening (ca.12:00 to 13:30) to (ca.12:00 fter sunset and continue fter sunset and continue fter dark The beginning time of beginning The n the early morning n the morning or early n the afternoon n the afternoon or A dusk A round During the morning A dusk A round dusk or in the A round dusk or in the A round I – I I I merged at noon at E merged Species neipennis ome other Tricorythodes Habroleptoides confusa Habroleptoides Tricorythodes atratus Tricorythodes S vespertina Leptophlebia oklahoma picteti Choroterpes Choroterpes Thraulus bellus Thraulus humilis Calliarcys brun - Epeorus ikanonis ignota Isonychia Isonychia Rhithrogena eptophlebiidae eptophlebiidae eptophlebiidae eptohyphidae eptohyphidae eptophlebiidae eptophlebiidae eptophlebiidae eptophlebiidae eptophlebiidae eptophlebiidae eptophlebiidae eptophlebiidae eptophlebiidae eptophlebiidae L L L ). 3. ( Continued Table Family Heptageniidae I sonychiidae I sonychiidae L L L L L L L L L L L L Heptageniidae 10 J.-Y. LUO ET AL. oldán oldán oldán oldán oldán oldán oldán oldán oldán oldán oldán ( 2012 ) dmunds et al. dmunds et al. dmunds et al. dmunds et al. Literature ( 2012 ), E ( 1976 ) ( 2012 ) ( 2012 ) ( 2012 ) ( 2012 ) ( 2012 ), E ( 1976 ) ( 2012 ) ( 2012 ) ( 2012 ) and S feind ( 2012 ) ampbell ( 1986 ) dmunds et al. ( 1976 ) dmunds et al. ( 1976 ) dmunds et al. ( 1976 ) dmunds et al. dmunds et al. ( 1976 ) dmunds et al. iensuu ( 1935 ) Bauernfeind and S Bauernfeind and S Bauernfeind and S Bauernfeind ( 1935 ) N eedham et al. E E E and S Bauernfeind T Bauernfeind and S Bauernfeind and S Bauernfeind E C Bauernfeind and S Bauernfeind and S Bauernfeind and S Bauernfeind R ussev ( 1987 ), Bauern - and S Bauernfeind – – – – – – – – – – – – – – – subimago south to as much south to 48 h in the north The living longevityThe of A bout 48 h ast from 12 h in the L ast from N o longer than 2 h - – – – – – – – – – – – – – – gence The longevityThe of emer mmediately I few moments A few Within seconds Within 2 min B B B B B B B B C A A A A A A A A B/ A Location of emergence Location – – – – – – M emergence time is in late morning time is in late in the morning t 10:00 A t night, before dawn, or dawn, before t night, t dusk he whole day vening The beginning time of beginning The n the evening n the late afternoon n the late n the evening I A – but the most A ll the day T E A A I Between 15:30~17:00 I - - Species ginata lacus T. nigrescens, T. coerulei Prosopistoma pennigerum Prosopistoma Prosopistoma alternatus Siphlonurus Edmundsius Siphlonisca Parameletus armatus Siphlonurus Ephoron submar Paraleptophlebia Paraleptophlebia Neoephemera purpurea Neoephemera lacustris, Tasmanophlebia Oligoneuriella rhenana Potamanthus luteus Potamanthus Potamanthus longicauda Palingenia Palingenia nigridorsum Ephoron eptophlebiidae eptophlebiidae Prosopistomatidae S iphlonuridae S iphlonuridae S iphlonuridae S iphlonuridae S iphlonuridae ). 3. ( Continued Table Family L L N eoephemeridae Oniscigastridae Potamanthidae Palingeniidae Polymitarcyidae ORIENTAL INSECTS 11 oldán oldán Literature ( 2012 ) ( 2012 ) dmunds et al. ( 1976 ) dmunds et al. Bauernfeind and S Bauernfeind and S Bauernfeind E – – subimago The living longevityThe of ast from 26 to 53 h 26 to L ast from - – – – gence The longevityThe of emer A A A Location of emergence Location – – emergence afternoon The beginning time of beginning The n morning or early I Species Siphlonurus aestivalis Siphlonurus Siphlonurus ). 3. ( Continued Table Family S iphlonuridae S iphlonuridae S iphlonuridae of subimago under water. surface, C : emergence the water of subimago at B: emergence the waterline, of subimago above A : emergence N otes: 12 J.-Y. LUO ET AL. the same species (such as Leptophlebia vespertina and Eletrogena lateralis) has two moulting places. Kimmins (1941) and Bauernfeind and Soldán (2012) pointed out that the mayfly moulting may be affected greatly by the environmental factors. The data we gathered here also show the diverse moulting of mayflies. The moulting time and longevity of subimagos are more affected by ecological factors and more flexible than the moulting place (Riederer 1985; Perng et al. 2005). However, from Table 3, if we put aside the ephemerellid, heptageniid and lep- tophlebiid data (all three families are very diverse), we can see all nymphs who can emerge above the water (Ameletidae, Baetiscidae, Isonychiidae, Oniscigastridae, ) are fall into the more plesiomorphic lineages [the phylogeny can be seen in Kluge et al. (1995), Kluge (1998), McCafferty (1997) and Ogden et al. (2009)]. For instance, the Australian Tasmanophlebia (Oniscigastridae) is an old clade, Baetisca (single genus of Baetiscidae) leaves other lineages very early, Siphlonuridae, Isonychiidae and Ameletidae are primitive families generally. On the other hand, only some Heptageniidae and all Oligoneuriidae, and (very derived) mayfly nymphs can become subimagos in the water. Upon these, it is assumed that the evolution trend of mayfly emergence is from above water to water surface then to underwater. Kukalová-Peck (1978, 1991) assumed that the original mayflies (imago, several stages of subimago and ) can live in moist habitats then became aquatic. The preliminary results here support this hypothesis. It is hoped that more researches on mayfly subimagos will verify this issue.

Conclusion

The last instar Parafronurus youi nymphs moult on substrate surface in the water. Before to ecdysis, the nymphs show some active movements. The moulting time and longevity of subimago as well as imago can change remarkably. The moulting places of selected mayflies show diverse types of same family, genus or species, but the possible evolutionary trend is still present: the plesiomorphic families usually prefer moulting above water. This may be a relic of an ancient character of their ancestor.

Disclosure statement

No potential conflict of interest was reported by the authors.

Funding

This work was supported by the National Natural Science Foundation of China [grant number 31172124] and [grant number 31472023], Project Funded by the Priority Academic Program, Development of Jiangsu Higher Education Institutions (PAPD) and project supported by key project of Science-technology basic condition platform from The Ministry of Science and ORIENTAL INSECTS 13

Technology of the People’s Republic of China [grant number 2005DKA21402]. Some data in this research comes from the database of National Digital-Museum of Specimens.

ORCID

Juan-Yan Luo http://orcid.org/0000-0001-8785-5228

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