Fsuns of New Zealand 72: Micropterigidae (Insecta: Lepidoptera) - Life history and biology
Gibbs, G W 2014. Fauna of New Zealand. 72, 127 pages.
(
ISSN 0111-5383 (print),
ISSN 1179-7193 (online)
;
no.
72.
ISBN 978-0-478-34759-3 (print),
ISBN 978-0-478-34760-9 (online)
).
Published 30 Jun 2014
ZooBank: http://zoobank.org/References/D6BC8C34-6D93-4EC7-BCB3-5670B2CFE744
DOI: 10.7931/J2/FNZ.72
Life history and biology
Egg
Large for a moth of this size, with the implication that fecundity must be relatively low in this family. This is confirmed by a study of the ovarian morphology in a Japanese species of Neomicropterix (Kobayashi 1994), which indicates that 30–40 mature eggs are present at eclosion. The eggs are spherical or slightly ovoid in shape and characterised by the development of large numbers of gelatinous processes which come to smother the surface a few hours after oviposition (Fig. 63). They result from an exudate from the oocyte and are not secreted by the follicle (Chauvin & Chauvin 1980).
Larva
Larval morphotypes. Two distinctive types of micropterigid larva occur in the New Zealand fauna and indeed in the world fauna at large. In New Zealand, all but one species conform to the ‘sabatincoid’ morphotype (Gibbs & Lees 2014). These look nothing like the typical caterpillars of other lepidopterans. Instead, they are hunch-backed and slug-like, more-or less hexagonal in cross-section (Fig. 59) and lack abdominal prolegs. In common with the alternative morphotype, the prognathous head capsule is capable of being retracted entirely within the prothorax. They are free-living, feeding on foliose liverworts. Their setae are distinctive and well-developed, especially the dorsal series, and the cuticle is pigmented in various shades of green, brown and black, rendering them highly cryptic. This type, with 8 pairs of abdominal spiracles, is found around the southern hemisphere and also in Asia and North America and has recently been reviewed by Hashimoto (2006). The alternative ‘micropteroid’ morphotype, modelled on the European Micropterix-clade and described most recently by Klausnitzer et al. (2002), and Hasenfuss & Kristensen (2003) are subterranean and unpigmented with short clubbed setae. Their trunk is round or oval in cross-section, with 7 pairs of functional abdominal spiracles, and small abdominal prolegs on segments A1-8. They have been extracted from soil, grass roots and rotten logs and are deemed to be fungal or detrital feeders, although some are capable of eating seedling angiosperms (Carter & Dugdale 1982). In the southern hemisphere, this type of larva occurs only in the Australian group species, which includes Zealandopterix zonodoxa.
The trunk cuticle of micropterigid larvae is uniquely specialised (Kristensen 1998) with liquid-filled chambers (each corresponding to one epidermal cell) in a honeycomb pattern, the exo- and endocuticle separated by fluid-filled spaces. This structure suggests it might have a role in the semi-aquatic lifestyles of these larvae where all conditions from total immersion to the threat of desiccation are likely. The threat of submergence in water is further ameloriated by the development of a complex micro-sculptured plastron surface (Davis & Landry 2012). The larval cuticle is overlain with a sticky pellicle to which foreign bodies often adhere.
Larval chaetotaxy. Before discussing larval taxonomy, it should be stressed that establishing a direct link between a larval type and a corresponding species of adult can present a challenge. To my knowledge, although larvae of virtually all New Zealand species have been collected, only four species have been successfully reared to adult from larvae (unpublished data) in order to establish their identity. The result is that the majority of larval determinations made for this study have been confirmed with the aid of molecular barcoding.
Chaetotaxy, a system for describing the numbers and position of setae on the head and trunk of larvae, has become an integral part of lepidopteran taxonomy (Hasenfuss & Kristensen 2003). It is included here because micropterigid larvae are likely to be encountered, sometimes quite commonly, in samples of litter or periphyton and are seldom recognised as lepidopteran, let alone identified to species. However, it is now known that trunk chaetotaxy can be used to discriminate between species clades, while pigmentation can often define species. Although all setae are shown on the setal maps presented here (Fig. 88–95), only the larger macrosetae are included in species descriptions. The benchmark publication by Hinton (1946), which established a nomenclature for homologous setae in lepidopteran larvae, unfortunately excluded the Micropterigidae, since he believed them worthy of their own order, Zeugloptera. Once Micropterigidae had been restored to the Lepidoptera (Kristensen 1971) there was a strong incentive to establish a system of setal nomenclature that reflected their lepidopteran heritage. Davis (1987), accepting that Micropterigidae represent the most archaeic lineage of Lepidoptera, made the first attempt to assign Hinton-based nomenclature to larval chaetotaxy. His study was based on the North American Epimartyria. An extensive review of Japanese micropterigid larvae by Hashimoto 2001, 2006, has modified Davis’ scheme further. I have adopted Hashimoto’s nomenclature here, but with reconsideration of the dorsum of the prothorax as discussed below.
The prothorax carries by far the most setae and some of these are the most difficult to locate. Three pairs of minute setae that occur on the ventral region, around the cuticular invagination for the retractable head capsule, have often escaped the attention of previous workers and may require special preparation to reveal them. This is best done by dissecting off the whole ventral area of cuticle from segment A1 to the head capsule, extending laterally to the level of the spiracle, and clearing in KOH. Alternatively, especially with small forms, it is preferable to treat the whole larva, complete with head capsule, in KOH until cleared of internal tissues, stain in chlorazol black and mount in glycerol using a coverglass supported on wax pads so the larva remains inflated. This way it is a simple matter to roll the specimen in order to examine all surfaces and also find landmark internal epidermal organs such as tracheal trunks.
In New Zealand larvae, the frontal row of macro-setae on the prothorax has important taxonomic significance. These setae vary from a maximum of seven pairs to minimum of five but agreement on their respective homologies has never been achieved. I regard the two setae closest to the mid-dorsal line as D1 and D2, which is in agreement with the conclusions of Hashimoto, 2006. Seta D1 is well back from the anterior cuticular ridge (which marks the head invagination fold). Seta D2 is the most median of the frontal row which in total comprises 4–6 near equal-sized pairs of setae that project forward over the head (if extended) or over the recess into which the head is retracted. In sabatincoid larvae these anterior prothoracic setae are situated on raised bases along the antero-lateral cuticular ridges. From a world-wide investigation of larval diversity (unpublished data) I have come to interpret this row of setae that extend laterally from D2, as follows: the next in line are XD1 and XD2. This terminology reflects that they are unique to the dorsum of the prothorax, not represented on T2 or T3. Hinton (1946) established the XD notation on this basis. Hashimoto (2001, 2006) has disregarded the XD setae, naming them instead as part of the L group, but I find that both are universally present on all micropterigid larvae. Beyond XD2, on the more lateral part of the segment, are a maximum of three setae (in a triangle), minimum one. Based on the New Zealand Sabatinca larvae these three setae appear almost identical in configuration (and therefore homologous?) to those normally interpreted as L1, L2, and L3 on the meso- and metathorax. Moreover, in this latter situation, losses of L group setae are commonplace in different micropterigid lineages (see Table 1 below) and I would argue that this principle also applies to the prothoracic L setae. Thus, I am suggesting that all variability in the number of dorsal prothoracic macro-setae is taking place within the L group. In New Zealand taxa, the prothoracic L group can retain all three setae (incongruella and calliarcha-group species), or be reduced to two (Zealandopterix and the chrysargyra-subgroup species) or be further reduced to a single L seta (chalcophanes-subgroup species). This separation of chrysargyra-group species into two subgroups on the basis of a larval setal character is confirmed by the CO1 sequences employed for bar-coding and in the male phallus morphology.
New Zealand larvae of the Sabatinca-clade can be distinguished from those in New Caledonia by the presence of a D2 seta on the mesothorax which is absent in all known New Caledonian taxa. Note that the SD setal group of higher Lepidoptera is not found on micropterigid larvae. The L group is consistently present on all segments but where only a single seta occurs it is not always clear which it represents. Hinton (1946) regarded the longest as L1. If we adopt this principle then, based on the setation of calliarcha-group larvae (Fig. 89), where a single seta remains on abdominal segments, it is situated on the more posterior of a double lateral lobe, the conclusion is that it represents L2. Thus, I have labelled the lateral abdominal seta of New Zealand larvae as L2.
Interestingly, while most attention in the chaetotaxy literature focuses on the anterior parts of the body, it is the setation of the anal segment (A10) that distinguishes the two major lineages of larvae in New Zealand. Here, the Australian-group species Z. zonodoxa bears three pairs of conspicuous setae on A10, two above the anus and one below (Fig. 90) (a larva of this group from Australia has two pairs only (Gibbs 2010)). Other New Zealand micropterigid larvae (all Sabatinca clade) lack all setae on A10, although two pairs occur on A9. The anal segment (A10) of calliarcha-group species is distinctively modified with an acute median anal cone above the anus flanked by a pair of comb-bearing paraproct lobes (not observed in S. pluvialis) which evidently serve to separate the larva from its faecal pellets, hence possibly distancing itself from potential parasites or predators which utilise frass pellets to find hosts.
The insertion points of segmental muscles are often visible externally and can have taxonomic value in New Zealand larvae. Referred to as ‘platelets’, they are marked on the trunk segments by small sclerites situated near the dorsal mid-line in the middle of each segment, or dorsolaterally by elongate sclerites in the intersegmental furrows, between the D and L setae but closer to the former. The dorsal platelets provide a binary character for discriminating aurella-subgroup species (with a single platelet on mid-line of segments T3 and A1–8) from chalcophanes-subgroup species (with paired separated platelets on all segments). Dorsal platelets are difficult to see on larvae of the incongruella and calliarcha-group, due to greater folding of the cuticle, and hence not taxonomically useful.
Cranial chaetotaxy of micropterigid larvae is difficult to resolve, difficult to homologise with other Lepidoptera and is not as useful for identifying larvae as trunk setation. All that need be said here is that they all possess a unique median seta (Davis 1987) in the middle of the frontal area. Thus, although head capsules of the two morphotypes present in New Zealand are illustrated to stress their overall differences, little attention is given to their setal detail.
The retractable head capsule of micropterigid larvae is notable for its near-prognathous form, long antennae (for a lepidopteran larva), and an occipital foramen that is separated from the base of the maxillolabium by a broad hypostomal bridge. In cleared preparations, the antero-ventral part of the occipital foramen has the appearance of an isolated oval foramen due to the presence of an exceptionally broad tentorial bridge toward the posterior of the head capsule. Facial ecdysial sulci (adfrontal) are present in sabatincoid larvae but not in Zealandopterix. A tight cluster of 5 stemmata, enclosed in a melanised ‘basket’, is situated ventral to the antennal base in sabatincoid forms but it should be noted that the subterranean larvae of the Australian-group (Zealandopterix) lack any external sign of stemmata. However, until histological sectioning is done it cannot be categorically stated that stemmata are absent in this lineage.
Larval micropterigid legs play little role in locomotion. The larvae creep along or rotate, snail-like, in a film of moisture, driven by the trunk muscles and internal fluid pressures, often with help from the mandibles as a grasping organ. Particularly intriguing is their way of inflating a large bulge on the ventral surface to accommodate uneven surfaces or revolve around on the spot. With their minimal locomotory function, the thoracic legs have become greatly reduced and all traces of the abdominal legs lost in the Sabatinca lineage. Eight pairs of short legs, with acutely pointed tips, are present on A1–8 of larval Zealandopterix (Fig. 82). Sabatincoid larval thoracic legs (Fig. 96, 97) comprise a maximum of four sclerites only; a coxa represented by two small crescent-shaped sclerites (absent in some); a cylindrical fused trochanter + femur; and a fused tibiotarsus, which carries a single hooked pretarsal claw. Thoracic legs of Zealandopterix and Sabatinca calliarcha-group larvae are more elongate (Fig. 97) (3× longer than basal diam.) than those of S. chrysargyra-group larvae (Fig. 96) (1.5× longer than basal diam.). The Sabatinca larval leg possesses a curious inflatable bladder-like sac which arises from a mesal desclerotised region of the femur.
Marked differences exist between the setal types on the trunk of different micropterigid larvae and can assist with taxonomic resolution. In New Zealand, only the calliarcha-group of Sabatinca species has ‘conventional’ acutely-pointed macro-setae (Fig. 86). In all other species, the trunk macrosetae are thickened in some way and distinctively ridged (Fig. 83–87), giving the appearance of a compound structure. The relative lengths of these setae has taxonomic significance and is thus cited here in terms of an overall length measurement and the ratio of setal length/length of a mid-abdominal segment, as measured along the dorsal mid-line. The cranial setae are very small, as are those of the more ventral parts of the trunk where they are camouflaged amongst the coarse honeycomb texture of the cuticle. In some cases a small raised papilla is present but lacks a seta (e.g., the SV group of chrysargyra-group larvae). These minor setal features are shown on the chaetotaxy maps but not discussed in the descriptions.
Pupa
Pupae are known for Sabatinca lucilia, S. heighwayi, S. weheka, S. pluvialis, S. chrysargyra and S. chalcophanes, but not for Zealandopterix. They are formed within a thin-walled oval silk cocoon, concealed amongst the foliage of the liverworts on which the larvae have been feeding (Fig. 61). Leaves are drawn together and fragments of leaves and other particles may be incorporated to render the structure highly cryptic. These New Zealand examples conform closely to the published descriptions of Micropterigid pupae (Tillyard, 1922; Lorenz, 1961; Yasuda, 1962; Hashimoto, 2006) differing mainly in the numbers and relative sizes of certain setae.
The pupa is of the type referred to as decticous exarate (Fig. 62, 102–105). Decticous denotes the presence of functional mandibles: a pair of sharp sclerotised mandibles, operated by the mandibles of the pharate adult and used for opening the cocoon prior to emergence of the adult moth. The mandibles of micropterigid pupae are conspicuous as the only melanised part of the pupa (Fig. 105), but are not markedly asymmetrical or hypertrophied as in Agathiphaga, Heterobathmia, Eriocrania, or Acanthopteroctetes. Their sharply pointed apices overlap slightly in the mid-line and there is a small supernumery tooth about half way along the inner margin of the right mandible. The distal mandible, beyond the supernumery tooth, is heavily sclerotised and finely serrate along its inner margin. Sheaths for the long maxillary palps are free, elbowed around the mandibles with the distal joints passing across the ventral surface of the eyes.
The clypeus and labrum are clearly demarcated in sabatincoid pupae and Asian/North American micropterigids but not in Micropterix (Hasenfuss & Kristensen, 2003). The antennae arise above the eye-piece and extend dorsally around the eye and along the forewing to terminate on the ventral side midway between the end of leg 2 and leg 3. The leg sheaths overlap each other along the mid-ventral region between the wings, with leg 3 bent into an ‘S’-shape leaving the tarsus projecting clear of the abdomen as a free and mobile appendage, with the first tarsal joint bent into a right-angle.
The term exarate refers to the moveable appendages of these pupae when compared with the obtect ‘soldered’ pupae of higher Lepidoptera. There is a considerable degree of mobility possible resulting from the combined action of leg 3 and wriggling of the abdominal segments. The right-angled tibia and tarsus of leg 3 projects freely from the ventral surface of the pupa. The wing sheaths are readily detached from the abdomen during preservation but to what extent this can occur in living pupae is unknown. Sheaths of palps and legs become detached when the pupa is active on emergence and are thus separated on the exuviae.
Relatively long robust macro-setae occur on the head, and thorax (Fig. 105). In S. heighwayi, which can be regarded as a groundplan Sabatinca form, these setae are distributed as follows: a trio of long setae on the lower facial region between the eyes, in the positions of the single M and pair of C1 setae of the larval stage. Directly dorsal to these and forming an overall cluster of five setae on the fronto-clypeal area, is another pair, equivalent to the AF setae of the larva. These five setae seem to be universally present in all micropterigid pupae that have been studied, as are a pair of long setae between the antennal bases on the dorsum of the head. More laterally, on the occipital region of the head, is a group of long setae close together, three in the case of S. heighwayi. Much smaller macrosetae occur on the clypeus and labrum. In addition to the long seta dorsally on the clypeus (as above) is a pair of two very small setae towards each lateral angle. Six equal small setae occur in two rows on the labrum, as in the larva, a dorsal row of two with four along the ventral margin.
On the thorax, the dome of the mesoscutum carries a pair of long setae on each side and in a similar position on the metascutum is a pair of equally long setae. The abdominal segments of all micropterigid pupae bear a pair of very short setae subdorsally on each segment, the inner one being about twice the length of the outer in S. heighwayi. These setae are absent on A8, replaced by a pair of small sclerotised tooth-like spines which point posteriorly. The terminal piece of the abdomen, representing segments 9 and 10 and enclosing the external genitalia, is devoid of setae.
Any thorough comparative treatment between New Zealand taxa is premature since very few specimens exist and only few species are represented. However, it can be noted that quite major species differences in the dimensions of the head setae and in the number of long setae in the thoracic clusters can occur. Thus, while in calliarcha-group species and S. chrysargyra, the six labral setae on each side are all relatively short and equal, those of S. chalcophanes are represented by four short medial setae (one in dorsal pair, three in ventral row) and two very long setae at the outer end of each row, equivalent to those of the clypeus. On the thorax, S heighwayi with two equally long setae on the metascutum differs from S. weheka where the same group consists of a single much shorter seta. On the abdomen the pair of spines on A8 of S. heighwayi and S. weheka is represented by only a single spine in S. chalcophanes and there are no spines on S. chrysargyra pupae.
Northern hemisphere pupae are described for Micropterix calthella (Lorenz 1961) and Neomicropterix nipponensis (Yasuda 1962) and N. matsumurana (Hashimoto 2006). Hashimoto (2006) records that the number of setae is frequently variable on both sides of the body, also noted in New Zealand pupae. While it is not practical to make detailed comparison with Micropterix on the basis of the Lorenz drawings, other than to note that the long head setae concur with New Zealand species, a single seta is figured for the proscutum and mesoscutum, and the abdominal pairs of setae are shown as in New Zealand taxa apart from an absence of spines on A8. In both M. calthella and M. aruncella the long head and thoracic setae are furcate (Carter & Dugdale 1982). Pupal chaetotaxy of Neomicropterix and Sabatinca are in general agreement for the head and thorax, but differ on the abdomen, where the Japanese species exhibit a greater complement of setae than New Zealand species, with pairs of microsetae in both dorsal and lateral positions (Hashimoto 2006).
Phenology
Table 2 shows the seasonal distribution of collection records for New Zealand Micropterigidae. The reliability of any interpretations concerning the relationship between seasonal flight records and the life cycle of a species will depend on the geographic range of the sampling and the number of samples. Thus, the following generalised comments must be regarded as provisional, especially for the rarer species.
Based on the occurrence of adult moths and larvae of each species throughout the year, it appears that in general, New Zealand micropterigids have an annual life cycle with spring to early summer flight periods. Peak months for adults are November and December but the first species to appear in early spring is S. aurantissima in which almost the entire known flight period takes place during September, followed by S. bimacula andS. quadrijuga in October. These three species are all restricted to South Island. By March, only S. chalcophanes and Z. zonodoxa are still on the wing.
When we look in more detail we find two distinct types of seasonal strategy, distinguished by the immature stage in which they overwinter—the majority, as above, spend autumn and winter as active larvae. From what is known, it appears that all incongruella- and chrysargyra-group species belong to this group, which reaches larval maturity sometime during winter or spring, and spends one or two months in the pupal stage before emerging for their flight period. There is no evidence of pupal dormancy (diapause) in this group. Small, early instar larvae can be collected in the field during late summer months after their flight season, and large larvae in late winter or early spring. There is a possibility that the common species with 5 or 6-month flight records (e.g., chalcophanes and aurella respectively), might be double-brooded over the summer, at least in some favourable locations, but this has yet to be confirmed.
In contrast to the above predominant type, adults of calliarcha-group species, are characterised by the spasmodic appearance of individuals over many months. These species can occasionally be found in large numbers at a very restricted locality, at the peak of their flight season, but otherwise their appearance is erratic and unpredictable. There is evidence that at least some of them undergo an extended pupal period, implying a pupal diapause. This pattern is clearly demonstrated by the South Island sister species S. heighwayi and S. weheka where mature larvae have consistently occurred at the end of December, reaching the pupal stage during January. Instead of emerging after the normal pupal development period (i.e., in autumn), they remain until the following spring, 9-10 months later. Not all larvae follow this pattern. For instance, seemingly mature larvae of S. heighwayi have been maintained under ambient conditions in captivity throughout winter. Any conclusions are tentative since these alternative strategies have only been recorded from a few captive individuals and field sampling is far from sufficient to substantiate these seasonal hypotheses.
It is tempting to speculate that the early New Zealand lepidopterists, who made such a significant contribution towards our knowledge of Micropterigidae between 1900 and 1930, failed to locate three of the new species described here simply because they were not in the field sufficiently early in the season (aurantissima (Sept), bimacula (Oct), weheka (Oct)) to encounter them.