Early leaf miners and the ground plan of the lepidopteran larval trunk: Caterpillar morphology of the basal moths Heterobathmia,Eriocrania, and Acanthopteroctetes

The larval trunk morphology including chaetotaxy, locomotory structures, and trunk musculature of Heterobathmia pseuderiocrania, Eriocrania cicatricella, and Acanthopteroctetes unifascia is described using conventional light, polarization, and scanning electron microscopy. The ground plan morphology of the lepidopteran larva and neolepidopteran caterpillar is discussed in light of the life history succession from free soil dwelling organism to endophagous and finally to a primarily free living, angiosperm associated organism. I suggest that the larval morphology is argued to be strongly influenced by the shift in number of surfaces present in the larval environment. Especially the environment of the endophagous species, where the upper surface of the leaf mine is linked to the presence of dorsal locomotory structures such as the retractable calli and dorsal friction patches is proposed to have had a significant impact on the morphology and locomotory mechnism of the lepidopteran caterpillar. The chaetotaxy of the lepidopteran ground plan is found to be simple, consisting only of primary and secondary tactile setae and segmental proprioceptors. The presumption of Gerasimov ([1935] Zool Anz 112:177–194) that MXD1 of the prothorax is a shifted mesothoracic MD setae is supported. I suggest that the serial arrangement of the proprioceptors MD1, present on all trunk segments except the prothorax, and a trisetous MV group on all the thoracic segments is part of the lepidopteran larval ground plan. The absence of apodeme structures associated with trunk musculature in the nonglossatans suggests that this is an autapomorphic character of the Lepidoptera and it is further found to have been influential in the evolution of the typical caterpillar trunk. The attachments of the thoracic muscles directly to the trunk integument, suggest that the apodemal structures ancestral to the Amphiesmenoptera have been reduced in the Lepidoptera. Within the non‐Neolepidoptera, the lifehistory shift may have resulted in reduction of the dorsal locomotory structures, such as calli. The abdominal musculature and structural similarities further suggest that the ventral calli are structural predecessors to the crotchet bearing proleg of the “typical caterpillar.” J. Morphol. 274:1239–1262, 2013. © 2013 Wiley Periodicals, Inc.     

External proprioceptors of locust locomotor organs and their change in the course of early larval ontogenesis

This work studies topography and structure of such important insect external proprioceptors as campaniform sensillae (CS). These mechanoreceptors are essential components of insect posture and locomotion regulation and participate in control of various forms of insect motor behavior (walking, jump, flight). There are traced their quantitative changes as well as differences in distribution of groups of these leg receptors at consecutive stages (from the 1st to the 4th instar) of ontogenetic development of larva of the locust Locusta migratoria L. The presence of groups of CS in proximal parts of extremities has been noted as early as in the 1st instar larvae. The CS groups in the wing pads were revealed only in the 4th instar larvae. The presented data allow connecting changes in structure and distribution of these proprioceptors with differences in locomotion of imagoes and larvae. A possible effect of these insect larval proprioceptors on central generators of the locomotion rhythms is discussed.     

Three‐dimensional reconstruction of the musculature of various life cycle stages of the cycliophoran Symbion americanus

Cycliophora is a very recently described phylum of acoelomate metazoans with a complex life cycle and a phylogenetic position that has been under debate ever since its discovery in 1995. Symbion americanus, which lives attached to the mouthparts of the American lobster, Homarus americanus, represents the second species described for the phylum. Aiming to increase the morphological knowledge about this cryptic clade, the present study describes the muscle arrangement of the feeding stage, the attached Prometheus larva with the dwarf male inside, the free living male, the Pandora larva, and the chordoid larva of S. americanus using actin staining and confocal laser scanning microscopy. 3D reconstructions of the muscular systems are presented. In the feeding stage, circular muscles compose the buccal funnel aperture. In addition, a pair of muscles runs longitudinally in the buccal funnel. A complex sphincter was found just proximally to the anus, and six longitudinal muscles run from the trunk constriction (“neck”) in basal direction. The musculature of the larval stages and the dwarf male is very complex and includes longitudinal muscles that run dorsally and ventrally. In addition, we found dorso‐ventral muscles. The male has a complex posterior muscle apparatus in the vicinity of the penis. In this stage, X‐ and V‐shaped structures were identified on the dorsal and the ventral side, respectively. Pandora and chordoid larvae possess additional circular muscles. We discuss our findings with respect to muscle elements of other metazoan groups and the chordoid larva of Symbion pandora. J. Morphol., 2009. © 2008 Wiley‐Liss, Inc.     

Comparative myoanatomy of cycliophoran life cycle stages

The metazoan phylum Cycliophora includes small cryptic epibionts that live attached to the mouthparts of clawed lobsters. The life cycle is complex, with alternating sexual and asexual generations, and involves several sessile and free‐living stages. So far, the morphological and genetic characterization of cycliophorans has been unable to clarify the phylogenetic position of the phylum. In this study, we add new details on the muscular anatomy of the feeding stage, the attached Prometheus larva, the dwarf male, and the female of one of the two hitherto described species, Symbion pandora. The musculature of the feeding stage is composed of myofibers that run longitudinally in the buccal funnel (two fibers) and in the trunk (variable number of fibers). The mouth opening is lined by a myoepithelial ring musculature. A complex myoepithelial sphincter is situated proximal to the anus. In the attached Prometheus larva, three longitudinal sets of myofilaments run dorsally, laterally, and ventrally along the entire anterior‐posterior body axis. The muscular architecture of the dwarf male is complex, especially close to the penis, in the posterior part of the body. An X‐shaped muscle structure is found on the dorsal side, whereas on the ventral side, longitudinal muscles and a V‐shaped muscle structure are present. These muscles are complemented by additional dorsoventral muscles. The mesodermal muscle fibers attach to the cuticle via the epidermis in all life cycle stages studied herein. The musculature of the female is similar to that of the Pandora larva of Symbion americanus and includes dorsoventral muscles and longitudinal muscles that run in the dorsal and ventral body region. Overall, our results reveal striking similarities in the muscular arrangement of the life cycle stages of both Symbion species. J. Morphol., 2010. © 2009 Wiley‐Liss, Inc.     

Caudal Musculature of the South Indian Flying Lizard Draco dussumieri Dum. and Bibr.

The modifications noticed in the caudal musculature of the South Indian Flying Lizard, Draco dussumieri, are described. The caudal musculature consists of the superficial ilio-caudalis and ischio-caudalis and the deeper ventral caudo-femoralis brevis and caudo-femoralis longus. There is an accessory tendon extending between the outer border of the tendon of the caudo-femoralis longus and the tendinous origin of the gastrocnemius. In the male the copulatory organ is provided with a retractor muscle. Attached to the ventral surface of the penis sheath is another muscle which helps in everting the penis. This latter muscle is present in the female also as a vestigeal one attached to the postero-lateral corners of the cloacal chamber. The modifications in the caudal musculature are attributable to the gliding habits of this lizard. Draco dussumieri, the South Indian Flying Lizard is unique in having a patagium for gliding from tree to tree. Associated with the development of the patagium, the musculature has undergone a number of adaptive modifications. The modifications of the trunk musculature have been published elsewhere (John 1970). The present communication is a study of the caudal musculature of this lizard.     

Growth of organ systems of Dentex dentex(L) and Psetta maxima(L) during larval development

Growth in volume of common dentex Dentex dentex and turbot Psetta maxima during larval development was studied by means of a quantitative histological method. A two‐phase pattern of volume increase was recorded for both species, turbot volume being always higher than dentex volume. During the first phase, the increase was small but during the second phase volume rose sharply from 22 days post hatch (dph) and 17 dph onwards in dentex and turbot, respectively. In dentex, the specific growth rate ( G ) of the whole larva as well as that of all the structures studied (nervous tissue, trunk musculature, digestive tract, liver, pancreas, spleen and thymus) was always higher during the second phase, whereas in turbot, only total volume of the larva, trunk musculature and nervous tissue had a higher G during the same period. The pattern of allometric growth of digestive organs was similar for both species. These organs showed an initial positive allometric growth that later became near‐isometric (digestive tract and liver) or negative (pancreas). In dentex, nervous tissue and trunk musculature showed near‐isometry throughout the period studied. In turbot, nervous tissue exhibited negative allometry and trunk musculature changed from negative to positive allometry. In both species studied, the highest allometry coefficients were recorded for digestive organs before the larva switched to strict exotrophy. This would indicate the importance of the development of these organs for survival.     

Structure and metamorphic remodeling of the larval nervous system and musculature of Phoronis pallida (Phoronida)

The structure of the larval nervous system and the musculature of Phoronis pallida were studied, as well as the remodeling of these systems at metamorphosis. The serotonergic portion of the apical ganglion is a U-shaped field of cell bodies that send projections into a central neuropil. The majority of the serotonergic cells are (at least) bipolar sensory cells, and a few are nonsensory cells. Catecholaminergic cell bodies border the apical ganglion. The second (hood) sense organ develops at competence and is composed of bipolar sensory cells that send projections into a secondary neuropil. Musculature of the competent larva includes circular and longitudinal muscle fibers of the body wall, as well as elevators and depressors of the tentacles and hood. The juvenile nervous system and musculature are developed prior to metamorphosis and are integrated with those of the larva. Components of the juvenile nervous system include a diffuse neural net of serotonergic cell bodies and fibers and longitudinal catecholaminergic fibers. The juvenile body wall musculature consists of longitudinal fibers that overlie circular muscle fibers, except in the cincture regions, where this pattern is reversed. Metamorphosis is initiated by the larval neuromuscular system but is completed by the juvenile neuromuscular system. During metamorphosis, the larval nervous system and the musculature undergo cell death, and the larval tentacles and gut are remodeled into the juvenile arrangement. Although the phoronid nervous system has often been described as deuterostome-like, these data show that several cytological aspects of the larval and juvenile neuromuscular systems also have protostome (lophotrochozoan) characteristics.     

Chambered cuticle,pellicles, strange sensilla,and extraordinary muscle arrangements: A study of the micropterigid larval trunk (Lepidoptera: Micropterigidae)

The larvsal trunk wall of Sabatinca chalcophanes (Meyrick, 1885), representing the “sabatincoid morphotype,” is described (brightfield and polarization microscopies, scanning and transmission electron microscopies). Eight sensillum types are identified, including four previously undescribed subventral and ventral kinds. The cuticle is nonsolid, the exocuticle being chambered in a honeycomb‐like fashion with chamber walls apparently secreted along epidermal cells boundaries. The chamber contents open to the exterior via minute pores in the chamber roofs. A space between endo and exocuticle communicates with the chamber interiors via pores in the chamber floors; the dense endocuticular surface in places form thickened domes. On the lower trunk region, lateral chamber walls are highly porous (lattice like), hence their contents are continuous; individual chamber roofs here are markedly convex, and the external trunk surface, therefore, papillate. The trunk surface is more or less completely covered by a pellicle, likely formed by exudates from the exocuticular chambers. Unusually for Lepidoptera all trunk muscles are slender strands covering a modest proportion of the inner trunk surface. Conspicuous insertion “nodes” are located at lateral and ventral segmental boundaries, ventromedially near segmental midlengths, and paramedially on the dorsum behind segmental midlengths. Overall similar cuticular specializations are also present in the distantly related Micropterix, strongly supporting micropterigid monophyly. J. Morphol. 275:797–821, 2014. © 2014 Wiley Periodicals, Inc.     

SEM studies on the early larval development of Triops cancriformis (Bosc)(Crustacea: Branchiopoda, Notostraca)

We investigated early larval development in the notostracan Triops cancriformis (Bosc, 1801–1802) raised from dried cysts under laboratory conditions. We document the five earliest stages using scanning electron microscopy. The stage I larva is a typical nauplius, lecithotropic and without trunk limbs. The stage II larva is feeding and has trunk limb precursors and a larger carapace. Stage III larvae have larger trunk limbs and a more adult shape. Stage IV larvae have well developed trunk limbs, and stage V larvae show atrophy of the antennae. We describe the ontogeny of selected features such as trunk limbs and carapace, discuss ontogeny and homologization of head appendages, follow the development of the feeding mechanism, and discuss trunk limb ontogeny.     

Musculature of the ovipositor of Lenitovena trigona (Matsumura) (Diptera, Tephritidae) with reference to the larval saprophagy

The larvae of most Tephritidae are endobiotic in various living plants and are therefore convenient objects for analysis of the associations of this dipteran family with seed plants. The structure of the sclerites and musculature of the ovipositor of Lenitovena trigona (Matsumura) a Far Eastern tephritid of the tribe Acanthonevrini with initially saprobiont larva, was investigated to facilitate understanding of the morphological changes in the adults associated with larval shift from saprophagous to herbivorous habit. Differences between the ovipositor of L. trigona and those of species of the genera Urophora, Ceratitis, and Rhagoletis with endophytic larvae have been found; the ovipositor musculature of these genera has been described by Dean (1935), Nanna (1938), and Berube and Zacharuk (1983).     

Anatomy and innervation of the abdominal segmental muscles in larval and adult Tenebrio molitor (Coleoptera)

The external morphology, musculature, and the innervation of the abdominal segments were examined in larvae and adult Tenebrio molitor. In the larva, there are 26 pairs of muscles arranged at four different levels in the ventral, lateral, and dorsal region of each segment. In the adult, the number of muscles has been dramatically reduced and is limited to six pairs of muscles located at the dorsal and lateral region of the segment. These muscles, in either larval or adult stages, are innervated by two main nerves, n1 and n2, which originate from the segmental ganglia. The cell bodies of the motoneurons innervating the muscles of the 3rd abdominal segment are located in the 3rd and 2nd abdominal ganglia. Some cell bodies are retained throughout metamorphosis, but others disappear during the larva-pupa transition.     

Mapping of serotonin-immunoreactive neurons in the larval nervous system of the flies Calliphora erythrocephala and Sarcophaga bullata

Summary Serotonin-immunoreactive (5-HTi) neurons were mapped in the larval central nervous system (CNS) of the dipterous flies Calliphora erythrocephala and Sarcophaga bullata. Immunocytochemistry was performed on cryostat sections, paraffin sections, and on the entire CNS (whole mounts).The CNS of larvae displays 96–98 5-HTi cell bodies. The location of the cell bodies within the segmental cerebral and ventral ganglia is consistent among individuals. The pattern of immunoreactive fibers in tracts and within neuropil regions of the CNS was resolved in detail. Some 5-HTi neurons in the CNS possess axons that run through peripheral nerves (antenno-labro-frontal nerves).The suboesophagealand thoracico-abdominal ganglia of the adult blowflies were studied for a comparison with the larval ventral ganglia. In the thoracico-abdominal ganglia of adults the same number of 5-HTi cell bodies was found as in the larvae except in the metathoracic ganglion, which in the adult contains two cell bodies less than in the larva. The immunoreactive processes within the neuropil of the adult thoracico-abdominal ganglia form more elaborate patterns than those of the larvae, but the basic organization of major fiber tracts was similar in larval and adult ganglia. Some aspects of postembryonic development are discussed in relation to the transformation of the distribution of 5-HTi neurons and their processes into the adult pattern.     

Changes in chloride cell distribution during early larval stages of Clupea harengus

A non-uniform distribution of cutaneous chloride cells was found in the early, pre-feeding larval stages of herring Clupea harengus . Chloride cells on the head, yolk-sac and trunk regions were unevenly distributed, whereas more densely packed chloride cells were observed in the pericardial and prebranchial regions. The pattern of chloride cell distribution changed during development and two distinct changes are described. The density of choride cells on the ventral trunk increased substantially during the period of yolk absorption, presumably due to contraction of the yolk sac and selective retention of yolk-sac chloride cells. Also during this period the cells on the lateral body wall increased in number and became distributed in segmental bands overlying the myosepta. Most chloride cells were found in association with the haemocoel or primordial blood vessels. Superficial segmental blood vessels were not found in the early larva, but the segmental bands of chloride cells overlay nerve tracts in the myosepta which were tentatively identified as the focal innervation of myotomes. It is concluded that both the circulatory system and the peripheral nervous system may play a role in determining chloride cell distribution in early larvae.     

Larval Behavior and Post-Larval Development in Parasmittina nitida Morphotype B (Bryozoa: Cheilostomata)

Larval behavior and metamorphosis in Parasmittina nitida morphotypeB from the Gulf of Mexico has been studied. The larvae havetwo basic types of movement: (1) a clockwise-counterclockwisemovement about the aboral-oral axis of the lobular larval formresulting in either slow horizontal or rapid vertical movement,and (2) a directed horizontal movement of the creeping larvalform, whereby either the oral lobe is pressed against the substrateor the aboral-oral axis is tilted forward. In both forms, thevibratile plume of the pyriform organ complex extends the leadingedge of the larva. Metamorphosis was observed with Nomarskidifferential interference microscopy in living specimens andwith scanning electron microscopy in fixed specimens. Polypidedevelopment— in particular, the formation and diminutionof the nutritive mass, the differentiation of the polypide rudiment,diaphragm, vestibular glands, operculum, major components ofthe musculature and alimentary canal, and the early stages ofastogenetic growth—is described. The tata ancestrula ofthis species is characterized by a frontal wall calcified distallyto the aperture, which is surrounded by nine erect spines. Thepolypide feeds actively within seven to eight days after theonset of larval attachment and metamorphosis under laboratoryconditions of 22°C.     

Embryonic and larval development of the peanut worm Phascolosoma agassizii (Keferstein 1867) from the Sea of Japan (Sipuncula: Phascolosomatidea)

All stages of the embryonic and larval development of Phascolosoma agassizii from Peter the Great Bay (Sea of Japan) were studied and illustrated using light and electron microscopy. The eggs of P. agassizii have the form of an ellipsoid (long and short axes about 100 and 70?µm, respectively). Egg cleavage is typical, spiral, and unequal. Gastrulation occurs by epiboly. This species possesses two pelagic larval stages, a lecithotrophic trochophore and a planktotrophic pelagosphera. The transformation of trochophore into pelagosphera occurs 80–90?h after fertilization. After 120–180?h, the larva has developed all systems of organs characteristic of the pelagosphera and is capable of feeding. At day 10, pelagospheras can settle, for some time, on the aquarium bottom and move on a ciliated lip, collecting food with the aid of a buccal organ. In addition, the larvae periodically attach themselves to the aquarium bottom or to the surface film of the water by means of a terminal organ. The trunk of the larva elongates by enlargement of the region behind the dorsal anal opening, which is located almost in the middle of the trunk region in the 15-day old larva. In the laboratory, 1-month old larvae spend the greater part of time in the attached state. Being attached by a glandular terminal organ to the aquarium bottom, they characteristically bend the body, actively feeding on microalgae from the substratum surface. The differences in the development of P. agassizii in the isolated West-Pacific and East-Pacific populations are shown and discussed.     

Lecithotrophic development and metamorphosis in the Indo-West Pacific brittle star Ophiomastix venosa (Echinodermata: Ophiuroidea)

Summary

The larval development of the ophiocomid ophiuroid Ophiomastix venosais described using SEM. The gastrula transforms into a uniformly ciliated early larva which progressively changes into a lecithotrophic late premetamorphic larva with a continuous bilateral ciliated band. This stage is short-lived and equivalent to a highly reduced ophiopluteus. Comparisons between O. venosa and other ophiuroid species whose development has been investigated suggest that, whatever the developmental mode (lecithotrophic or planktotrophic), a pluteus stage always occurs in ophiuroids with planktonic development. Two metamorphic stages were identified, the late metamorphic larva differing from the early one by the closure of the larval mouth. The appearance of the permanent mouth marks the end of the metamorphosis. The postlarva still possesses remnants of larval features. The transformation of the reduced ophiopluteus into a barrel-shaped metamorphic larva with transverse ciliated bands, a vitellaria larva, is followed. The possible occurrence of a unique type of metamorphic larva in non-brooding ophiuroids is discussed. Verification of this, however, needs further SEM investigations on metamorphic larva from species having “regular” planktotrophic development.     

Serotonin immunoreactivity in the nervous system of the Pandora larva, the Prometheus larva, and the dwarf male of Symbion americanus (Cycliophora)

Cycliophora is a recently described phylum of enigmatic metazoans with a very complex life cycle that includes several sexual and asexual stages. Symbion pandora and Symbion americanus are the only two cycliophoran species hitherto described, of which morphological and genetic knowledge is still deficient to clarify the phylogenetic position of the phylum. Aiming to increase the database on the cycliophoran neural architecture, we investigated serotonin immunoreactivity in the free swimming Pandora larva, the Prometheus larva, and the adult dwarf male of S. americanus. In the larval forms, serotonin is mainly expressed in a ring-shaped pattern at the periphery of the antero-dorsal cerebral ganglion. Additionally, several serotonergic perikarya emerge from both sides of the cerebral ganglion. Thin neurites project anteriorly from the cerebral ganglion, while a pair of ventral longitudinal neurites emerges laterally and runs along the anterior-posterior body axis. Posteriorly, the ventral neurites fuse and extend as a posterior projection. In the dwarf male, serotonin is found mainly in the commissural neuropil of the large anterior cerebral ganglion. In addition, serotonin immunoreactivity is present in the most anterior region of the ventral neurites. Comparative analysis of spiralian nervous systems demonstrates that the neuroanatomy of the cycliophoran larval stages resembles much more the situation of adult rather than larval spiralians, which may be explained by secondary loss of larval structures and heterochronic shift of adult components into the nervous system of the Pandora and the Prometheus larva, respectively.     

The larval nephridia of the brackish-water polychaete,Nereis diversicolor

The larval nephridia of the brackish-water polychaete Nereis diversicolor are described for the first time, and have been studied to determine if their times of development and structural characteristics are consistent with a role in the osmotic regulation of the larva. As shown in serial paraffin sections and by interference-contrast optics, the nephridia of the three-setiger larva consist of a single pair of very large metanephridia, arising in the 3rd larval setiger, but with their elongated terminal ducts and coiled ciliated tubules pushed forward into the 2nd setiger; their open metanephrostomes and anterior anchoring filaments lie dorsal to the 2nd set of setae. In contrast, the definitive or juvenile metanephridia, arising in the 4th and subsequently formed setigerous segments, have short terminal ducts and coiled ciliated tubules confined to the segments on which their external nephropores open; their nephrostomes are ventrally located and open into the rear of the next anterior segment. These findings are in contrast to the claims of Edouard Meyer (1887), who described two pairs of closed protonephridia in the 2nd and 3rd larval setigers of Perinereis cultrifera. Although it is not excluded that the single larval pair of metanephridia of N. diversicolor may arise as protonephridia, Meyer's claim of two pairs of larval protonephridia was an observational error. The larval nephridia of the marine Platynereis dumerilii resemble in form, but are considerably smaller than, those of N. diversicolor. It is concluded that the hypertrophied pair of larval metanephridia of N. diversicolor is an evolutionary adaptation to existence in habitats of low and unpredictably varying salinity. Their development occurs irrespective of the prevailing salinity; hence, it must be genetically determined.