Research Article |
Corresponding author: Grzegorz K. Wagner ( karol.wagner@wp.pl ) Academic editor: Jan Klimaszewski
© 2018 Bernard Staniec, Mirosław Zagaja, Ewa Pietrykowska-Tudruj, Grzegorz K. Wagner.
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:
Staniec B, Zagaja M, Pietrykowska-Tudruj E, Wagner GK (2018) Comparative larval ultramorphology of some myrmecophilous Aleocharinae (Coleoptera, Staphylinidae), with a first description of the larvae of Amidobia talpa (Heer O, 1841) and Oxypoda haemorrhoa (Mannerheim C.G., 1830), associated with the Formica rufa species group. ZooKeys 808: 93-114. https://doi.org/10.3897/zookeys.808.29818
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The paper describes the external structures of the late larval stages of two Palearctic myrmecophilous staphylinids: Amidobia talpa and Oxypoda haemorrhoa associated with the Formica rufa species group. This is the first-ever description of the larva of Amidobia, and the only complete, detailed account of the morphology of this developmental stage in the genus Oxypoda currently available. For the first time in these two genera, 13 and 10 larval diagnostic features, respectively, are proposed. Morphological differences have been established between known and the newly described larvae of five species (genera) of myrmecophilous and one non-myrmecophilous Aleocharinae, belonging to three tribes. Amidobia talpa and O. haemorrhoa are probably typical, tiny predators, like most other Aleocharinae, including non-myrmecophilous ones. Being very small and highly mobile, they are ignored by worker ants. Not surprisingly, no particular larval morphological modifications were found to enable them to survive among ants. Such features have, however, evolved in the larvae of larger aleocharines, that is, those that are perceived by ants and are wholly integrated with their hosts in the ant nest (e.g. Lomechusa). This comparative analysis of the functional morphology of the larvae of known myrmecophilous Aleocharinae is a springboard to further such studies of these interesting insects.
Aleocharines, Red wood ants, Coleoptera , developmental stages, ecological preferences, external structure, late larval instars, larva, morphology, myrmecophile, rove beetles, symbionts
Red wood ants from the Formica rufa Linnaeus, 1761 species group are regarded as key insect species in European woodlands because of their vast numbers and the invaluable biocoenotic contribution they make to the ecosystems they inhabit. Being polyphagous predators, they have a major, multidimensional effect on the invertebrate fauna in that they limit the numbers of many harmful woodland phytophages. On the other hand, the presence of ants has a very positive effect on a range of tiny woodland creatures, such as aphids, which ants protect and defend, obtaining honeydew in return (
Among the insects associated with ants, beetles (Coleoptera) are the richest and the most diverse in form. According to
The genus Amidobia Thomson C.G., 1858 (Athetini) contains eight Palearctic species, of which only A. talpa (Heer O., 1841) occurs in Europe (
The genus Oxypoda Mannerheim, 1830, one of the most species rich aleocharine genera, has a worldwide distribution (
Myrmecophilous Aleocharinae, like other beetles associated with ants, are fascinating organisms for research because of their highly interesting morphological, ecological and behavioural adaptations to the distinctive conditions found in ant nests (
Presumably, the larval structure of these myrmecophiles, among other characteristics, which actively live and forage in the anthill throughout their development, should well reflect the extent and nature of their integration with their hosts. Therefore, detailed morphological data of the larval forms should prove useful for discovering the distinctive adaptations of myrmecophilous species to life in ant nests and also the relations between them and their hosts.
The links of numerous Staphylinidae with such a characteristic habitat like ant nests are reflected in various degrees of specialization. In the context of host-guest interactions,
It is apposite, therefore, to pose the following questions: 1) Does the myrmecophily of A. talpa and O. haemorrhoa have any effect on the external structure of their larvae? 2) Are their ecological preferences of no great importance in this respect, as in the case of T. angulata? 3) How does the extent of guest-host integration affect the morphology of aleocharine larvae so far examined?
The chief aim of this paper is therefore to describe in detail the morphology, including the chaetotaxies and external ultrastructure, of the larval stages of Amidobia talpa and Oxypoda haemorrhoa and to compare them with the external larval structures of other, well-known myrmecophilous aleocharines.
Larval stages were obtained by rearing 34 adults of Amidobia talpa and 9 adults of Oxypoda haemorrhoa. Specimens of both species were collected on May 5, 2017, at Lake Moszne (51°26'57.4"N, 23°07'34.0"E) and Lake Długie (51°27'04.0"N 23°09'39.9"E), situated in the Polesie National Park near Lublin (SE Poland). The insects were sifted from the nest material of Formica polyctena. Live beetles of A. talpa and O. haemorrhoa were placed in transparent plastic containers (diameter 10 cm, height 4 cm) filled with nest substrate and observed in the laboratory from May 9 to June 24, and from May 11 to June 21, respectively, at room temperature (22–25 °C). Adults and larvae of various species of ants, including F. rufa and small springtails, were supplied as a source of adult food.
Larvae of both species were killed in boiling water and preserved in ethanol (75%).
To prepare temporary microscope slides, some larvae were macerated in cold 10% KOH for two to three hours, immersed in lactic acid for subsequent preparation and mounting of antennae, mouthparts, sensory structures, chaetotaxy of the body, legs and urogomphi. They were then traced from photos taken with an Olympus DP72 or Olympus DP21 digital camera mounted on a binocular Olympus SZX16 or Olympus BX63 compound microscope (Figs
Habitus illustrations of larvae, structure of setae, chaetotaxy of head, functional position of mouthparts, structural details of antennae, microstructure, spiracles and various details of their external structure were recorded using SEM, type VEGA3 TESCAN (Figs
Measurements of the larvae of both species, made using an Olympus BX63 compound microscope in cellSens Dimension v1.9 software, are given in millimetres, as explained in detail in
Measurements of larval instars of Amidobia talpa and Oxypoda haemorrhoa. Symbols and abbreviations: larval instars, A – average, N – number of specimens examined, M – measurement, R – range, SV – standard variation.
Species (larval instars/N) | M | R | A | SV |
---|---|---|---|---|
Amidobia talpa (all larval instars/28) | Body length | 1.00–2.55 | 1.99 | 0.45 |
Thorax length | 0.38–0.69 | 0.55 | 0.09 | |
Head width | 0.16–0.23 | 0.20 | 0.02 | |
Prothorax length | 0.15–0.30 | 0.21 | 0.40 | |
Prothorax width | 0.18–0.27 | 0.23 | 0.03 | |
Oxypoda haemorrhoa (all larval instars/17) | Body length | 2.46–3.32 | 2.79 | 0.37 |
Thorax length | 0.40–0.80 | 0.68 | 0.09 | |
Head width | 0.22–0.27 | 0.25 | 0.02 | |
Prothorax length | 0.19–0.33 | 0.27 | 0.03 | |
Prothorax width | 0.23–0.32 | 0.28 | 0.02 |
The combination of characteristics distinguishing mature larvae of Amidobia and Oxypoda from known larvae of other genera within the subfamily Aleocharinae are as follows (
Body narrow, elongate, semi-cylindrical, segments IX and X distinctly narrower than the others; A. p. (Figs
A. talpa (1, 3, 5, 8, 8a, 10), O. haemorrhoa (2, 4, 6, 7, 9, 11), mature larva. 1–4 habitus in dorsal (1, 2) and lateral (3, 4) aspect 5–7 abdominal setae 8–11 head in dorsal (8, 9) and lateral (10, 11) aspect. Abbreviations: I-X, abdominal segments; At, antenna; Ec, epicranial campaniform sensilla; Ed, epicranial dorsal setae; Eg, epicranial gland; El, epicranial lateral setae; Em, epicranial marginal setae; Es, epicranial suture; F, frons; Fd, frontal dorsal setae; Fl, frontal lateral setae; L, lateral setae; P, posterior setae; T, temporal setae; V, ventral setae; Vl, ventral lateral setae.
Head. Shape: A. p. (Fig.
A. talpa (12, 13, 15, 17, 19, 20), O. haemorrhoa (14, 16, 18, 21), mature larva. 12 head in fronatl aspect 13, 14 gular region 15, 16 functional position of mouthparts in frontal aspect 17–21 right antenna in dorsal aspect (17, 18), entire article III in anterior (19) and in ventral (20) aspect, entire article II and III in anterior aspect (21). Abbreviations: I-III, antennal articles; IIS, IIIS, solenidia of antennal article II or III; At, antenna; F, frons; Gu, gula; Hp, hypopharynx; Lp, labial palp; Lr, labrum; Ma, mala; Md, mandible; Mx, maxilla; Pm, maxillary palp; Oc, ocellus; Sa, sensory appendage; Smnt, submentum.
Antenna (Figs
Labrum (Figs
A. talpa (22, 24, 26, 27, 30, 31, 34, 36), O. haemorrhoa (23, 25, 28, 29, 32, 33, 35, 37), mature larva 22, 23 labrum 24, 25 epipharynx 26–29 left (L) and right (R) mandible, in dorsal aspect; 30–33 anterior region of left (L) and right (R) mandible, in dorsal aspect 34, 35 right maxilla in ventral aspect 36, 37 right mala in ventral aspect. Abbreviations: I-III, articles of maxillary palp; 1, 2, mandibular setae; Ad, additional setae; Cp, cuticular processes; Cdo, cardo; La, labral anterior setae; Ld, labral dorsal setae; Lm, labral marginal setae; Mi, microtrichia; Ma, mala; Pf, palpifer; Pm, maxillary palp; Stp, stipes.
Epipharynx (adoral surface of labrum) membranous (Figs
Mandibles (Figs
Maxilla (Mx) (Figs
Hypopharynx (Hp) (Figs
A. talpa (38, 40, 42, 42a, b, 44, 44a), O. haemorrhoa (39, 41, 43, 43a, 45, 46, 47, 47a), mature larva. 38, 39 hypopharynx 40, 41 labium 42, 43 prementum with labial palp, apex of ligula (42a) and labial palp (42b, 43a), 44, 45 legs and tarsungulus (44a), 46 pre- and mesosternum 47 anterior portion of presternum and microstructure (47a). Abbreviations: 1, 2, 3, 4, setae of mesosternum; 1, 2, setae of tarsungulus; Ad, anterodorsal setae; Al, anterolateral setae; Av, anteroventral setae; Cx, coxa; D, dorsal setae; Eu, eusternum; Fe, femur; Hp, hypopharynx; Lg, ligula; Lp, labial palp; Ls, laterosternum; Ma, mala; Mes, mesosternum; Mnt, mentum; Pd, posterodorsal setae; Pl, posterolateral; Pmnt, prementum; Pr, prosternum; Prehy, prehypopleuron; Prs, presternum; Smt, submentum; Sp, spiracle; St, sternellum; Tb, tibia; Tr, trochanter; Ts, tarsungulus; V, ventral setae.
Thorax. Foreleg (Figs
Pro- (Prs), meso- (Mes) and metasternum (Met) membranous (Figs
Abdomen. Chaetotaxy of tergites: I with 28 setae [2(A1, A6, Da3, Db3, Dc3, Dd2, L1–2, L4, P1–5)], II-VII with 32 setae [2(A1, A2, A4, A6, Da3, Db3, Dc3, Dd2, L1–2, L4, P1–5)] and 1 pair of paratergal glands (Pg) (Fig.
A. talpa (48, 49, 50, 52, 53, 53a, b, 55), O. haemorrhoa (51, 54, 54a, b, 56), mature larva. Thoracal (48) and abdominal segment I–II (49), VIII (52), VIII–X (53, 54) and urogomphus (55, 56) in lateral aspect. Abbreviations: 1, 2, article of urogomphi; VII – X, abdominal segments; A, anterior setae; Ah, anal hooks; Asp, atrophied spiracles; C, campaniform sensilla; Cx, coxa; D, Da-c, discal setae; L, lateral setae; Msn, mesonotum; Mtn, metanotum; Op, opening of gland reservoir; P, posterior setae; Pg, pretergal gland; Pnt, pronotum; Ps, presternal sensilla; R, gland reservoir; Sp, spiracle; Ste, sternite; Te, tergite; Ug, urogomphus.
Table
This paper gives a detailed description of the external structure of the hitherto unknown larval stage of Amidobia talpa and Oxypoda haemorrhoa – Palearctic, myrmecophilous staphylinids belonging to the subfamily Aleocharinae – which are associated with the Formica rufa species group. It also gives the first description of the larva of Amidobia, and at present, the only complete, detailed account of the larval morphology of Oxypoda. The existing fragmentary descriptions of Oxypoda larvae, with only a few schematic drawings relating to just two species – O. spectabilis and O. longipes – were written 40–50 years ago (
Relationships between myrmecophiles and their hosts exhibit varying degrees of advancement (
Similarities and differences in external morphology between known late larval instars of some myrmecophilous and non-myrmecophilous Aleocharinae species. Abbreviations: A–article; a–anterior; arrg.–arrangement; As–apical seta of urogomphus; ang.–angulata; ap.–apical; c–central; cent. reg.–central region; cut. proc.–cuticular processes; Fe–femur; haem.–haemorrhoa; L–left mandible; l–long; Lr–length ratio; LWr–length to width ratio; Ma–mala; mod.–moderately; mic.–micro; mod.–moderately; Msn–mesonotum; Ns–number of setae; p–posterior; Pm–maxillary palp; Pnt–pronotum; preap.–preapical; poor.–poorly; pub.–pubicollis R–right mandible; S–segment; s–short; Sa–sensory appendage of antennal article II; Sas–subapical setae of urogomphus; St.–sternite; strong.–strongly; Tb–tibia; Ts–tarsungulus; Ug–urogomphus; w.–without; weak.–weakly; Wr–width ratio; ?–lack of data; *–body measurements of all known larval instars. Data based on
Ecological preferences | Myrmecophilous species | Non-myrmecophilous species | ||||
---|---|---|---|---|---|---|
Host | Lasius fuliginosus | Formica rufa group | – | |||
Tribe of Aleocharinae | Lomechusini | Oxypodini | Athetini | |||
Species | Pella laticollis | Lomechusa pub. | Thiasophila ang. | Oxypoda haem. | Amidobia talpa | Dinaraea aequata |
level of integration with host | preadaptation to integration | peak of integration (symphile) | preadaptation to integration | non-integrated? (synoics) | – | |
Character | ||||||
Body length | 4.30–4.80 | 4.99–6.70 | 2.72–4.40 | 2.46–3.32* | 1.00–2.55* | 3.01–3.78 |
Body shape | moderately elongate | dumpy | elongate | elongate | elongate | elongate |
Cuticle | mod. sclerotized | membranous | mod. sclerotized | poor. sclerotized | poor. sclerotized | mod. sclerotized |
Setae: structure | setose | blunt, jagged distally | setose | setose | setose | setose |
Head | ||||||
Width | 0.57–0.63 | 0.87–0.97 | 0.41–0.48 | 0.22–0.27* | 0.16–0.23* | 0.42–0.45 |
LWr | 1:1 | 1:1.4 | 1:1 | 1.1:1 | 1:1.2 | 1:1 |
Ocelli | present | absent | present | present | present | present |
Ns: dorsal side | 40 | 70 | 42 | 40 | 40 | 40 |
Sides | distinctly rounded | distinctly rounded | distinctly rounded | weakly rounded | distinctly rounded | distinctly rounded |
Wr of head and Pnt | 1:1.3 | 1:1.5 | 1:1.3 | 1:1.1 | 1.1:1 | 1:1.1 |
Antenna | ||||||
Lr of AI-III | 1.4:2.3:1 | 1.2:1.7:1 | 1.5:1.9:1 | 1.3 : 1.6 : 1 | 1.3:1.9:1 | 1:1.7:1 |
LWr of AI, AII, AIII | 1.2:1/2.4:1/2.2:1 | 1:2.8/1:1.1/1:1.6 | 1.2:1/1.4:1/2:1 | 1:1.2/1.5:1/1.6:1 | 1:1/1.5:1/1.5:1 | 1:1/1.8:1/1.4:1 |
LWr of Sa | 1.5:1 | 1.4:1 | 2.1:1 | 1.9:1 | 1.6:1 | 1.8:1 |
Lr Sa and AIII | 1:1.6 | 1.1:1 | 1:1.1 | 1:1.3 | 1.1:1 | 1:1 |
Labrum | ||||||
Shape | trapeziform | trapeziform | semi-circular | semi-circular | rectangular | trapeziform |
Anterior margin | almost straight | slightly rounded | distinctly rounded | distinctly rounded | excised in the centre | cent. reg. protruding, crenate |
Seta Ld2: structure | mic. setose | macro, setose | macro, peg shaped | mic. verrucous | mic. spiniform | mic. spiniform |
Labium and clypeus | separated | fused | separated | separated | separated | separated |
Epipharynx | ||||||
Cuticular processes: No. | well above 200 | well above 200 | 150–200 | 100–150 | about 20 | 50–80 |
Cut. proc.: length | short | short | short | short | long | short |
Cut. proc. in central area | absent | present | absent | absent | absent | present |
No. of pores of a/c/p | 2/8 (in 1 row)/ 4 | ? | 1–2/9/4 | 2/6 (in 2 rows)/2 | 0/2/0 | 2/4/4 |
Mandible | ||||||
Shape | slender, bent weakly | slender, strong, bent | slender, weak, bent | slender, strong, bent | stocky, mod., bent | slender, weak, bent |
Interior edge ap. tooth | slightly undulating | smooth | smooth | serrate | smooth | smooth |
Edge below preap. tooth | slightly undulating | smooth | smooth | serrate | smooth | serrate |
No. of preap. teeth | 1-R and 1-L | 0 | 1-R and1-L | R-1 and L-1 | R-2 and L-2 | 4-R, 5-L |
Number/length of setae | 2/almost equal | 3/almost equal | 2/almost equal | 2/different | 2/almost equal | 2/equal |
Maxilla | ||||||
Mala: ant. marg. with: | 27–31 equal teeth | 8 equal setae | 20 teeth (11 small) | 11 teeth (1 big) | 12 teeth (4 small) | 23 teeth (15 small) |
Mala: shape | wide, equilateral, sclerotized | lobar, membranous | slender, slightly dilated anteriorly | slender, slightly narrowed anteriorly | wide, distinctly dilated anteriorly | slender, distinctly dilated anteriorly |
Ma: No. cut. proc./arrg. | about 80/singly | numerous/in rows | 55–60/singly | 15/singly | 25/ singly | 40/singly |
Stipes and mala | fused | separated | separated | fused | fused | separated |
Pm: Lr A I-III | 1.7:1:2.3 | 1.4:1:2.0 | 1.6:1:2 | 1.5:1.0:2.0 | 1.1:1.0:2.0 | 1.6:1:2.2 |
Pm: LWr of AI-III | 2.2:1/1.4:1/5.2:1 | 1:1.8/1:1.9/2.4:1 | 1.5:1/1.3:1/4.7:1 | 1.4:1/1.3:1/3.8:1 | 1.3:1/1.5:1/5.2:1 | 1.8:1/1.5:1/6.8:1 |
Lr: Pm and Ma | 1.5:1 | 1:1.2 | 1.1:1 | 1.1:1 | 1.2:1 | 1.2:1 |
Labium | ||||||
Lg: shape | transverse, short, | transverse, very short | finger-like, 1.8 × as long as wide | finger-like, 1.9 × as long as wide | domelike, as long as wide | finger-like, 2.5 × as long as wide |
Lg/anterior margin | sinuate | rounded | truncated | truncated | truncated | truncated |
Lr: Lg and Lp | 1:2.2 | 1:3.9 | 1:1.9 | 1:2 | 1:1.5 | 1:1 |
Lg and Pmnt | fused | fused | separated | fused | separated | separated |
Pl: Lr A I and II | 1:1.3 | 1:1 | 1:1.6 | 1:2.1 | 1:2.4 | 1:2.1 |
Pl: LWr of AI/AII | 1.1:1/2.4:1 | 1:1/1.6:1 | 2:1/3.2:1 | 1:1/3.1:1 | 1:1.4/2.9:1 | 1.1:1/3.5:1 |
Thorax | ||||||
Ns: Pnt, Msn | 52, 40 | 110, 80 | 52, 38 | 50. 36 | 50, 36 | 50, 38 |
Lr: Fe, Tb, Ts | 2.3:2.2:1 | 2.2:1.9:1 | 2.1:2.2:1 | 2.4:2.0:1.0 | 1.8:1.7:1.0 | 1.9:2.2:1 |
LWr: Fe, Tb, Ts | 4.4:1/4.5:1/5.2:1 | 2.2:1/2.3:1/3.0:1 | 3.6:1/5.2:1/5.2:1 | 2.9:1/ 3.0:1/3.5:1 | 2..6:1/4.3:1/5.6:1 | 3.0:1/5.3:1/7.1:1 |
Ns: Fe, Tb, Ts | 8, 9, 2 | 30–34, 22–25, 2 | 8, 9, 2 | 8, 9, 2 | 8, 9, 2 | 7, 9,2 |
Abdomen | ||||||
Ns: Tergite I, II-VII | 30, 30 each | 70, 80 each | 30, 32 each | 28, 32 | 28, 32 | 32 each |
Ns: St. I, each II-VIII | 16, 20 | 100, 110 | 14, 20 each | 16, 20 | 16, 20 | 16, 20 each |
Urogomphi | present | absent | present | present | present | present |
Ug: Lr AI, AII, Sap | 1:1.1:1.2 | – | 1:2.2:2.6 | 2.4:1.0:4.8 | 1.4:1.0:3.1 | 1:1.5:1.7 |
LWr AII | 2.7:1 | – | 3.7:1 | 2.5:1 | 2.8:1 | 4.1:1 |
Lr Ug (w. As) to S X | 1:1.7 | – | 1:1 | 1:1.4 | 1:1.5 | 1:1.5 |
By far the largest number of characteristic features of the external structure, compared with other myrmecophilous and non-myrmecophilous aleocharines, were found in the larva of the symphilous genus Lomechusa Brisout de Barneville Ch.N.F., 1860 (Table
The classification of the degree of integration of the other four myrmecophilous species of Aleocharinae is not so obvious. Nonetheless, there do seem to be certain differences between them in this respect.
In view of the above it cannot be surprising that, with the exception of Lomechusa, discussed earlier, the other myrmecophilous larvae analysed here do not possess any outstanding features distinguishing them from non-myrmecophilous species (Table
Therefore, as studies to date have shown, the characteristic morphology of the aleocharine larvae examined to date is not due to their myrmecophily alone. Likewise, the larval stages of myrmecophiles, which exhibit behavioural pre-adaptations to integration with host ants (P. laticollis, T. angulata), do not possess any visible external structural features pointing to associations with ants (
This analysis of the comparative morphology of known myrmecophilous aleocharine larvae in the context of the type of interaction with hosts is merely a preamble to far more extensive research on this subject. Unfortunately, as knowledge of the larval stage, not only of myrmecophilous but of other members of this very numerous staphylinid subfamily, remains fragmentary, the formulation of more comprehensive generalizations is as yet not possible. Moreover, there is still no information whatsoever on the detailed external larval structure of a number of other interesting, symbiotic European aleocharines. This situation can be illustrated by the genus Dinarda Leach W.E., 1819. Its members exhibit behaviour testifying to quite an advanced degree of integration with hosts, including the possibility of their being fed by ants on the principle of regurgitation (
The authors gratefully acknowledge the State Forests National Forest Holding, Poland, for funding the research and the Management of the Polesie National Park for its cooperation. The project was carried out with the cooperation of the Polesie National Park and the Maria Curie-Skłodowska University in Lublin; the numbers of the relevant agreements are: EZ.0290.1.28.2017 (between PNP and SFNFH); 6, NB 520-3/2017 (between PNP and MCSU).