The Chemoreceptive Lattice Organs in Cypris Larvae Develop from Naupliar Setae (Thecostraca: Cirripedia, Ascothoracida and Facetotecta)

Lattice organs are peculiar chemoreceptors found only in the Crustacea Thecostraca (Facetotecta, Ascothoracida, Cirripedia). In these taxa, five pairs occur in the head shield (carapace) of the terminal larval instar (y-cyprid, ascothoracid larva, cyprid), which is the settlement stage. Lattice organs represent an autapomorphy for the Thecostraca but their evolutionary origin and possible homologues in other Crustacea remain obscure. We have used scanning electron microscopy to describe the setation pattern of the head shield in late nauplii of one species of Ascothoracida, one species of Facetotecta and several species of the Cirripedia Thoracica, Acrothoracica, and Rhizocephala. The naupliar head shield always carries two pairs setae situated anteriorly near the midline. Each of these setae carry a single pore, and positional, structural and ontogenetic evidence show that these setae are homologous in all the examined species and that they represent precursors of the two anterior pairs of lattice organs of the succeeding larval stage, viz., the ascothoracid larva (Ascothoracida), y-cyprid (Facetotecta), and cyprid (Cirripedia). This leads us to infer that lattice organs are among the most highly modified sensilla in all Crustacea and they have in most cases lost all external resemblance to a seta. The nauplii of the Rhizocephala carry an additional three pairs of setae situated more posteriorly on the head shield and they could be precursors of the three posterior pairs of lattice organs. All other species examined lack these posterior setae, except the Facetotecta which have one posteriorly situated pair.     

A new species of Tigriopus (Copepoda, Harpacticoida, Harpacticidae) from Thailand with the description of its naupliar development

Both genders of Tigriopus thailandensis sp. nov. are described from a laboratory stock raised from individuals collected from the seaweed Enteromorpha clathrata in Thailand (Bangsaen Beach, Chonburi Province). Tigriopus thailandensis sp. nov. shares with its closest relative T. japonicus Mori, 1932 two setae on the third exopodal segment of leg 4 while other congeners bear 3 inner setae. However, allobasis and exopod of antenna in both genders are much more slender and elongate than in T. japonicus. All six naupliar stages of T. thailandensis are described from the offspring of isolated females. In comparison with nauplii of T. japonicus, T. thailandensis nauplii are characterized by the following: a smaller body size throughout the naupliar phase; first antennular segment without seta, second antennular segment with only one small seta plus two longer setae; third antennular segment with additional spinules from naupliar stage II onwards; antenna bears three small spinules on the terminal exopodal segment; one additional seta on the anterior surface of the antennary basis, tubular endopod of antenna with one tiny seta midlength at naupliar stage III that increases in size; mandibular basis with several spinules on anterior surface; mandibular coxa with one spinulose seta that is smooth in T. japonicus.     

Larval development of the rhizocephalan cirripede Briarosaccus tenellus (Maxillopoda: Thecostraca) reared in the laboratory: a scanning electron microscopy study

SEM investigations of laboratory-reared larvae of Briarosaccus tenellus Boschma, 1970, revealed five naupliar instars, one more than previously described for the Rhizocephala. The external features of these and the cypris larva are described in detail. The youngest instar (NO) is characterised by a better developed furca than in subsequent stages and one additional antennulary seta. Differences in outline, shape of antennulae, and hind-body denticulation, offer the potential of individual discrimination. All the nauplii possess a transparent, hollow cuticular ring around their body. This flotation collar represents the bulged margin of the larval head shield and is attached to the body along a delicate ridge. Three pairs of tiny pores in contact with the ridge possibly regulate inflation of the ring, but details of this mechanisms remain unknown. Due to total lecithotrophy, the nauplii of B. tenellus have limbs setation reduced to that needed for swimming only, and other feeding structures such as the labrum are also highly reduced. In the antennulae, the morphological changes in form and setation were followed from nauplius to cypris and shown to largely resemble events in ontogeny of the thoracican barnacle Semibalanus balanoides. On this basis we establish a homology scheme between antennulary setae in these two species. In both B. tenellus and S. balanoides, a naupliar seta, apically on the fourth antennulary segment develops into a conspicuous aesthetasc while one (B. tenellus) or two (S. balanoides) subapical and postaxially sited setae on the same segment develops into into four short setae in the cypris. Our study reveals that the terminology used in describing cirripede nauplius and cypris larvae is often misleading or even erroneous and improvements are suggested. Notably replacing cypris carapace with the ontogenetically and phylogenetically more informative term head shield.     

Larval development of the pedunculate barnacles Octolasmis angulata Aurivillius 1894 and Octolasmis cor Aurivillius 1892 (Cirripedia: Thoracica: Poecilasmatidae) from the gills of the mud crab,Scylla tranquebarica Fabricius, 1798

Detailed studies of larval development of Octolasmis angulata and Octolasmis cor are pivotal in understanding the larval morphological evolution as well as enhancing the functional ecology. Six planktotrophic naupliar stages and one non-feeding cyprid stage are documented in details for the first time for the two species of Octolasmis. Morphologically, the larvae of O. angulata and O. cor are similar in body size, setation patterns on the naupliar appendages, labrum, dorsal setae-pores, frontal horns, cyprid carapace, fronto-lateral gland pores, and lattice organs. Numbers of peculiarities were observed on the gnathobases of the antennae and mandible throughout the naupliar life-cycle. The setation pattern on the naupliar appendages are classified based on the segmentation on the naupliar appendages. The nauplius VI of both species undergoes a conspicuous change before metamorphosis into cyprid stage. The cyprid structures begin to form and modify beneath the naupliar body towards the end of stage VI. This study emphasises the importance of the pedunculate barnacle larval developmental studies not only to comprehend the larval morphological evolution but also to fill in the gaps in understanding the modification of the naupliar structures to adapt into the cyprid life-style.     

Effects of temperature and salinity on the larvae of two species of rhizocephalan (Crustacea: Cirripedia)

Summary

Responses of larvae of two rhizocephalan species to changes in seawater temperature and salinity were studied under laboratory conditions. Peltogasterella gracilis parasitizes the hermit crab Pagurus pectinatus, which occurs at stable salinity and gradually changing temperature in summer. Sacculina polygenea is a parasite of the crab Hemigrapsus sanguineus, which lives in the intertidal zone in summer where salinity and temperature can fluctuate during the day. The development of both species is comprised of five naupliar stages and the cyprid stage, and it was considered successful if more than 50% of the nauplii attained the cyprid stage. P. gracilis nauplii successfully developed at 12–20°C and 30–34‰, but at 22°C successful development occurred in a narrower salinity range (32–34‰). All nauplii died both at 25°C and in 26‰. S. polygenea nauplii successfully reached the cyprid stage at higher temperatures (18–25°C) and a wider salinity range (18–34‰) than P. gracilis nauplii, but at 12°C and 16‰ larval development of S. polygenea was suppressed. Under favorable conditions, naupliar development lasted 3.5 days in P. gracilis and 2–3 days in S. polygenea. The cyprids of both rhizocephalan species demonstrated a greater resistance to temperature and salinity changes than nauplii. However, P. gracilis cyprids were active in a narrower salinity range (16–34‰), as compared to S. polygenea cyprids (8–34‰). Under favorable conditions the cyprids of both species survived for 6 to 10 days.     

Larval development of the rhizocephalanSacculina polygenea (Crustacea: Cirripedia)

Larval development of the rhizocephalanSacculina polygenea (Crustacea: Cirripedia: Rhizocephala) parasitizing the coastal crabHemigrapsus sanguineus was studied in Vostok Bay, the Sea of Japan. At 22–23°C, the entire cycle of larval development takes 2.5 days and includes five naupliar stages and one cypris stage. Like other rhizocephalans, the larvae ofS. polygenea are lecithotrophic and only grow slightly in size in the course of development, and like all sacculinids, they have no flotation collar. The naupliar stages IV and V have a tubercle between the furcal rami; this tubercle is absent in the larvae of the genusPeltogasterella, but it has been described inS. carcini. The first seta of the antennule only disappears completely at the fourth stage, although it is markedly reduced at the third stage. No morphological differences, except differences in size, are found between male and female nauplii.     

Naupliar and Metanaupliar Development of Thysanoessa raschii (Malacostraca,Euphausiacea) from Godth?bsfjord,Greenland, with a Reinstatement of the Ancestral Status of the Free-Living Nauplius in Malacostracan Evolution

The presence of a characteristic crustacean larval type, the nauplius, in many crustacean taxa has often been considered one of the few uniting characters of the Crustacea. Within Malacostraca, the largest crustacean group, nauplii are only present in two taxa, Euphauciacea (krill) and Decapoda Dendrobranchiata. The presence of nauplii in these two taxa has traditionally been considered a retained primitive characteristic, but free-living nauplii have also been suggested to have reappeared a couple of times from direct developing ancestors during malacostracan evolution. Based on a re-study of Thysanoessa raschii (Euphausiacea) using preserved material collected in Greenland, we readdress this important controversy in crustacean evolution, and, in the process, redescribe the naupliar and metanaupliar development of T. raschii. In contrast to most previous studies of euphausiid development, we recognize three (not two) naupliar (= ortho-naupliar) stages (N1-N3) followed by a metanauplius (MN). While there are many morphological changes between nauplius 1 and 2 (e.g., appearance of long caudal setae), the changes between nauplius 2 and 3 are few but distinct. They involve the size of some caudal spines (largest in N3) and the setation of the antennal endopod (an extra seta in N3). A wider comparison between free-living nauplii of both Malacostraca and non-Malacostraca revealed similarities between nauplii in many taxa both at the general level (e.g., the gradual development and number of appendages) and at the more detailed level (e.g., unclear segmentation of naupliar appendages, caudal setation, presence of frontal filaments). We recognize these similarities as homologies and therefore suggest that free-living nauplii were part of the ancestral malacostracan type of development. The derived morphology (e.g., lack of feeding structures, no fully formed gut, high content of yolk) of both euphausiid and dendrobranchiate nauplii is evidently related to their non-feeding (lecithotrophic) status.     

The Morphology of the Naupliar Stages of Sacculina carcini(Crustacea: Cirripedia: Rhizocephala)

A morphological study was carried out on the fournaupliar stages of Sacculina carciniusing mainly scanning electron microscopy. Frontal horns were present and throughout development the typical nauplius limbs remained simple and gnathobases were lacking. Such features are characteristic of other lecithotrophic barnacle nauplii. The presence of a vestigial ventral thoracic process was evident on the stage III nauplius and was even more prominent on the stage IV nauplius. These observations confirm that the rhizocephalan nauplius is close to the thoracican nauplius form and lend strong support for the retention of the Rhizocephala within the Cirripedia.     

The larval development of an Australian limnadiid clam shrimp (Crustacea, Branchiopoda, Spinicaudata), and a comparison with other Limnadiidae

The adult morphology of the Australian Limnadopsis shows some remarkable differences to that of other Limnadiidae. These differences are not reflected in its larval development. In Limnadopsis parvispinus, larval development comprises six stages. In stages I and II only the three naupliar appendages are present: the antennule as a small bud, the biramous antenna as the main swimming organ, and the mandible. The antennal protopod bears two endites, the proximal naupliar process and a more distal endite. In stage III a bifid naupliar process (in earlier stages not bifid) and the first signs of the carapace and trunk limb anlagen (undifferentiated rudiments) appear. In stage IV the carapace anlagen become more pronounced. The number of trunk limb anlagens increases to five, and differentiation has commenced. In stage V the first five pairs of trunk limbs are differentiated to varying degrees. The anterior-most four pairs of trunk limbs are subdivided into five endites, a small endopod, an exopod and an epipod. The bivalved carapace covers the anterior-most limbs. In larval stage VI the carapace is larger and the trunk limbs are further differentiated. A general pattern in the sequence of larval stages is the increasing number of sensilla on the antennules. From the last larval to the first postlarval stage, a significant change in morphology takes place. The trunk limbs are now used for swimming. Typical larval organs are much smaller than in the last larval stage. A comparison with other representatives of the Limnadiidae shows a high degree of correspondence, with most differences explained by the heterochronous appearance of characters during development. Five to seven stages are described for all studied Limnadiidae, including one particular stage in which four fully developed setae, a bifid naupliar process and the first signs of carapace anlagen are present. These characters are found in stage III in L. parvispinus, Limnadia stanleyana, Eulimnadia texana, and Imnadia yeyetta but in stage IV in E. braueriana and L. lenticularis. Based on a comparison of the larval stages of six limnadiid and one cyzicid species, we conclude that at least six naupliar stages belong to the limnadiid ground pattern.     

Larval Development in the Rhizocephalan Barnacle Sacculina pilosella

We studied, under laboratory conditions, the larval development of a rhizocephalan barnacle Sacculina pilosellaVan Kampen et Boschma, 1925, which parasitizes the kelp crab Pugettia quadridens(de Haan) in Vostok Bay, Sea of Japan. It is shown that at 22–23°C, the whole cycle of larval development takes about 3 days. The larvae of S. pilosellaare lecithotrophic; their development, like in other rhizocephalans, comprises five naupliar instars. Like the larvae of all sacculinids, the nauplii of S. pilosellahave no flotation collar. In their structure, the larvae of S. pilosellaare similar to the nauplii of the typical sacculina, S. carcini(elongated body outline, long furcal branches, and weakly pronounced segmentation of the abdomen). On the other hand, the characteristic outgrowth inbetween the furcal branches that is characteristic of stages IV and V in S. carciniand S. polygeneais absent in the larvae of S. pilosella.The first seta on the antennula of S. pilosellacompletely disappears only at stage IV; however, at stage III, it is already significantly reduced. No morphological differences have been revealed between male and female larvae of S. pilosellaexcept certain size differences.     

Haplostomides hawaiiensis,new species (Copepods: Cyclopoida: Ascidicolidae), associated with the ascidian Polyclinum constellatum at Honolulu,Hawaii

An ascidicolid copepod, Haplostomides hawaiiensis, is described on the basis of females obtained from the compound ascidian Polyclinum constellatum collected in Keehi Lagoon, Honolulu, Hawaii. The features that separate H. hawaiiensis from other species of the genus include an elongate body with dorsal curvature and indistinct tagmosis, and a combination of characters of cephalic appendages (antenna with 2 spines, mandible with 3 setae, maxillule with 7 setae and maxilla with 2 setae) and thoracic appendages (legs 1–4 with 1 seta on protopod and 2 spines and 1 seta on exopod). Haplostomides hawaiiensis appears to be most closely related to H. hibernicus (T. & A. Scott, 1895) which occurs in compound ascidians from European seas. This is the first copepod associate of an ascidian to be reported from Hawaii.     

Deep sequencing of naupliar-, cyprid- and adult-specific normalised Expressed Sequence Tag (EST) libraries of the acorn barnacle Balanus amphitrite

In order to improve the genetic characterisation of the barnacle Balanus amphitrite, normalised EST libraries for the developmental stages, viz. nauplius (a mix of instars I and II), cyprid and adult, were generated. The libraries were sequenced independently using 454 technologies and 575,666 reads were generated. For adults, 4843 unique isotigs were estimated and 6754 and 7506 in the cyprid and naupliar stage, respectively. It was found that some of the previously proposed cyprid-specific bcs genes were also expressed during the naupliar and adult stage. Furthermore, as lectins have been hypothesised to influence settlement cue recognition in barnacles, the database was searched for lectin-like isotigs. Two proteins, uniquely expressed in either the cyprid or the adult stage, matched a mannose receptor, and their nucleotide sequences were 33% and 31% identical to a lectin (BRA-3) isolated from Megabalanus rosa. Further characterisation of these genes may suggest their involvement in settlement.     

Postembryonic development of Drescheriella glacialis Dahms & Dieckmann (Copepoda,Harpacticoida) reared in the laboratory

Summary All 6 naupliar and 5 copepodite stages of Drescheriella glacialis, a tisbid from Antarctic fast ice, are described. A key for the identification of the naupliar stages is given. Sexual dimorphism makes its first appearance in the copepodid IV. The setae configuration of the exopod of the second antenna in copepodid I is considered to be an ancestral state, and subsequent ontogenetic reductions are proposed to be apomorphic processes.     

Larval development of Japanese 'conchostracans': part 2, larval development of Caenestheriella gifuensis (Crustacea, Branchiopoda, Spinicaudata, Cyzicidae), with notes on homologies and evolution of certain naupliar appendages within the Branchiopoda

As part of a larger project examining and comparing the ontogeny of all major taxa of the Branchiopoda in a phylogenetic context, the larval development of Caenestheriella gifuensis (Ishikawa, 1895), a Japanese spinicaudatan ‘conchostracan’, is described by scanning electron microscopy. Seven different larval stages are recognised, in most cases based on significant morphological differences. They range in length from about 200 to 850 μm. Nauplius 1 has a plumb and lecithotrophic appearance with a rounded hind body and a labrum with an incipient medial spine. Limb segmentation is mostly unclear but the second antennae have more putative segments delineated than are expressed in the later stages. Feeding structures such as the mandibular coxal process and antennal coxal spine are only weakly developed. Nauplius 2 is very different from nauplius 1 and has three large spines on the labral margin and two long caudal spines. Feeding structures such as the mandibular coxal process and various spines and setae are developed, but whether feeding begins at this stage was not determined. The mandible has developed an ‘extra’ seta on endopod segment 1, absent in Nauplius 1. The segmentation of the second antenna has changed significantly due to fusions of various early segments. Nauplius 3 is like nauplius 2 in morphological detail, but larger and more elongate. Nauplius 4 has developed a pair of small anlagen of the carapace and rudiments of the first five pairs of trunk limbs, and the coxal spine of the antenna has become distally bifid. Nauplius 5 has a larger carapace anlage, externally visible enditic portions of the elongate trunk limbs, and a pair of primordial dorsal telson setae. Nauplius 6 has a larger and partly free carapace and better-developed, partly free trunk limbs with incipient enditic, endopodal, and exopodal setation. A pair of caudal spines, dorsal to the large caudal spines, has appeared. Nauplius 7 is quite similar to nauplius 6 but is larger and has slightly longer caudal and labral spines; also, the setation of the most anterior trunks limbs is better developed. The larval development is largely similar to that of other spinicaudatans. The larval mandible, which is evolutionarily conservative within the Branchiopoda, reveals a setation pattern similar to that of the Anostraca and Notostraca (two setae on mandibular endopod segment 1). Most other spinicaudatans and all examined laevicaudatans share another setal pattern (one seta on mandibular endopod segment 1), which could indicate a close relationship among these taxa. The second antenna undergoes a special development, which provides an insight into the evolution of this limb within the Branchiopoda. In nauplius 1 the basipod, endopod, and exopod are all superficially divided into a relatively high number of segments. In later nauplii some of these have fused, forming fewer but larger segments. We suggest that this ontogeny reflects the evolution of antennae in the conchostracans. Various aspects of the morphology of the antennae are discussed as possible synapormorphies for either the Diplostraca or subgroups of the Conchostraca.     

The naupliar stages of Cyclopina yutimaete Lotufo (Cyclopinidae,Cyclopoida)

The six naupliar stages of Cyclopina yutimaete Lotufo are described and compared to other cyclopoid nauplii. They seem more similar to freshwater cyclopoid nauplii than to marine species. The hirsute aspect of the last segment of the antennule is of diagnostic value for these nauplii.     

Isethionic Acid and Floridoside Isolated from the Red Alga,Grateloupia turuturu,Inhibit Settlement of Balanus amphitrite Cyprid Larvae

Isethionic acid (2-hydroxyethane sulfonic acid) and floridoside (2-O-α-D-galactopyranosylglycerol) were extracted from the red alga, Grateloupia turuturu, and tested for anti-settlement activity against cyprid larvae of the tropical barnacle, Balanus amphitrite and for their toxicity to nauplius larvae. Isethionic acid was active for anti-settlement but had the disadvantage of being toxic to nauplius larvae. Floridoside was a potent inhibitor of cyprid settlement at non-toxic concentrations to nauplii (0.01 mg ml^?1).     

Early Developmental Stages of the Green Tiger Prawn, Penaeus semisulcatus de Haan (Crustacea, Decapoda, Penaeidae)

Gravid females of Penaeus semisulcatus were spawned in the laboratory by natural means. The embryos were documented and the larvae were reared from hatching to postlarval stage at 28.2–30.0 °C and 33.5–34.5 g kg⁻¹ salinity for about 10 days (223 h 55 min). Six naupliar stages, three protozoea stages, three mysis stages and the first postlarval stage were described and illustrated. The larvae were fed only with microalgae Tetraselmis tetrathele and Chaetoceros gracilis from first protozoea until the second mysis, with about 90% survival rate; from the third mysis until the first postlarva they were fed with similar microalgae coupled with rotifer Brachionus plicatilis and Artemia nauplii. The embryonic and larval stages of P. semisulcatus are generally similar to those of other closely related species in the family Penaeidae, such as Melicertus canaliculatus, Fenneropenaeus merguiensis, and Marsupenaeus japonicus, except for the size and structure of diagnostic characters, setation of appendages and duration of metamorphoses. The change in the feeding habit during ontogeny was related to morphological transformation of the feeding apparatus of larvae and postlarvae. This paper is the first comprehensive and complete account of the early developmental stages of P. semisulcatus.     

When similar beginnings lead to different ends: Constraints and diversity in cirripede larval development

Summary

Cirripedes are fascinating models for studying both functional constraints and diversity in larval development. Adult cirripedes display an amazing variation in morphology from sessile suspension feeders that still retain many crustacean characters to parasites that have lost virtually all arthropod traits. In contrast, cirripede larval development follows a common scheme with pelagic larvae comprising a series of nauplii followed by a cyprid. Variations are mostly concerned with whether or not the nauplii are feeding and the degree of abbreviation of development, culminating in species where the larvae hatch as cyprids. The cypris larvae are very similar among the ingroups of the Cirripedia, but interesting variations occur in structures used for substrate location and attachment. The cyprid is specialized to both swim through the water and actively explore the substratum by walking on the antennules and using an array of sensory organs in search for a suitable site to attach. This unique morphology and behavior of the cyprid have enabled the Cirripedia to colonize widely different habitats ranging from hard rock to soft animal tissue. Yet, the cyprid can metamorphose into juveniles as different as a setose feeding barnacle and the vermiform stages of the parasitic forms. This emphasizes the importance of the cyprid as one of the key features for the evolutionary success of the Cirripedia.