SciCombinator

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Concept: Crustacean

1570

Global declines in insects have sparked wide interest among scientists, politicians, and the general public. Loss of insect diversity and abundance is expected to provoke cascading effects on food webs and to jeopardize ecosystem services. Our understanding of the extent and underlying causes of this decline is based on the abundance of single species or taxonomic groups only, rather than changes in insect biomass which is more relevant for ecological functioning. Here, we used a standardized protocol to measure total insect biomass using Malaise traps, deployed over 27 years in 63 nature protection areas in Germany (96 unique location-year combinations) to infer on the status and trend of local entomofauna. Our analysis estimates a seasonal decline of 76%, and mid-summer decline of 82% in flying insect biomass over the 27 years of study. We show that this decline is apparent regardless of habitat type, while changes in weather, land use, and habitat characteristics cannot explain this overall decline. This yet unrecognized loss of insect biomass must be taken into account in evaluating declines in abundance of species depending on insects as a food source, and ecosystem functioning in the European landscape.

Concepts: Biodiversity, Insect, Ecology, Crustacean, Ecosystem, Taxonomic rank, Ant, Ecological economics

180

We investigated the navigational capabilities of the world’s largest land-living arthropod, the giant robber crab Birgus latro (Anomura, Coenobitidae); this crab reaches 4 kg in weight and can reach an age of up to 60 years. Populations are distributed over small Indo-Pacific islands of the tropics, including Christmas Island (Indian Ocean). Although this species has served as a crustacean model to explore anatomical, physiological, and ecological aspects of terrestrial adaptations, few behavioral analyses of it exist. We used a GPS-based telemetric system to analyze movements of freely roaming robber crabs, the first large-scale study of any arthropod using GPS technology to monitor behavior. Although female robber crabs are known to migrate to the coast for breeding, no such observations have been recorded for male animals. In total, we equipped 55 male robber crabs with GPS tags, successfully recording more than 1,500 crab days of activity, and followed some individual animals for as long as three months. Besides site fidelity with short-distance excursions, our data reveal long-distance movements (several kilometers) between the coast and the inland rainforest. These movements are likely related to mating, saltwater drinking and foraging. The tracking patterns indicate that crabs form route memories. Furthermore, translocation experiments show that robber crabs are capable of homing over large distances. We discuss if the search behavior induced in these experiments suggests path integration as another important navigation strategy.

Concepts: Crustacean, Coconut crab, Coenobitidae, Anomura, Christmas Island, Caroline Island, Chagos Archipelago

176

Carbonated hydroxyapatite is the mineral found in vertebrate bones and teeth, whereas invertebrates utilize calcium carbonate in their mineralized organs. In particular, stable amorphous calcium carbonate is found in many crustaceans. Here we report on an unusual, crystalline enamel-like apatite layer found in the mandibles of the arthropod Cherax quadricarinatus (freshwater crayfish). Despite their very different thermodynamic stabilities, amorphous calcium carbonate, amorphous calcium phosphate, calcite and fluorapatite coexist in well-defined functional layers in close proximity within the mandible. The softer amorphous minerals are found primarily in the bulk of the mandible whereas apatite, the harder and less soluble mineral, forms a wear-resistant, enamel-like coating of the molar tooth. Our findings suggest a unique case of convergent evolution, where similar functional challenges of mastication led to independent developments of structurally and mechanically similar, apatite-based layers in the teeth of genetically remote phyla: vertebrates and crustaceans.

Concepts: Arthropod, Calcium, Crustacean, Mineral, Calcium carbonate, Teeth, Crayfish, Aragonite

170

Brine shrimp are primitive crustacean arthropodal model organisms, second to daphnia, which can survive in high-salinity environments. Their oviposited cysts, cuticle-covered diapausing eggs, are highly resistant to dryness. To elucidate specialties of brine shrimp, this study characterized glycosphingolipids, which are signal transduction-associated material. A group of novel and complex fucosyl glycosphingolipids were separated and identified from cysts of the brine shrimp Artemia franciscana by repeated lipid extraction, alkaline methanolysis, acid treatment, successive column chromatography, and post-source decay measurements by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Structures of the glycosphingolipids were elucidated by conventional structural characterization and mass spectrometry, and the compounds were identified as GlcNAcβ1-3GalNAcβ1-4(GlcNAcα1-2Fucα1-3)GlcNAcβ1-3Manβ1-4Glcβ1-Cer, GalNAcβ1-4(Fucα1-3)GlcNAcβ1-3GalNAcβ1-4(GlcNAcα1-2Fucα1-3)GlcNAcβ1-3Manβ1-4Glcβ1-Cer, and GalNAcβ1-4(GlcNAcα1-2Fucα1-3)GlcNAcβ1-3GalNAcβ1-4(GlcNAcα1-2Fucα1-3)GlcNAcβ1-3Manβ1-4Glcβ1-Cer. These compounds also contained a branching, non-arthro-series disaccharide with an α-GlcNAc terminus, similar to that found in a previously reported ceramide hexasaccharide (III(3)(GlcNAcα2Fucα)-At4Cer). The glycans within these complex GSLs are longer than reported glycans of the animal kingdom containing α-GlcNAc terminus. These complex GSLs as well as the longest GSL with ten sugar residues, ceramide decasaccharide (CDeS), contain the fucosylated LacdiNAc sequence reported to associate with parasitism/immunosuppression and the α-GlcNAc terminus reported to show a certain antibacterial effect in other reports. CDeS, the longest GSL of this species, was found in the highest amount, which indicates that CDeS may be functionally important.

Concepts: Mass spectrometry, Arthropod, Crustacean, Brine shrimp, Branchiopoda, Time-of-flight, Artemia salina, Fairy shrimp

170

BACKGROUND: Sexual system is a key factor affecting the genetic diversity, population structure, genome structure and the evolutionary potential of species. The sexual system androdioecy – where males and hermaphrodites coexist in populations – is extremely rare, yet is found in three crustacean groups, barnacles, a genus of clam shrimps Eulimnadia, and in the order Notostraca, the tadpole shrimps. In the ancient crustacean order Notostraca, high morphological conservatism contrasts with a wide diversity of sexual systems, including androdioecy. An understanding of the evolution of sexual systems in this group has been hampered by poor phylogenetic resolution and confounded by the widespread occurrence of cryptic species. Here we use a multigene supermatrix for 30 taxa to produce a comprehensive phylogenetic reconstruction of Notostraca. Based on this phylogenetic reconstruction we use character mapping techniques to investigate the evolution of sexual systems. We also tested the hypothesis that reproductive assurance has driven the evolution of androdioecy in Notostraca. RESULTS: Character mapping analysis showed that sexual system is an extremely flexible trait within Notostraca, with repeated shifts between gonochorism and androdioecy, the latter having evolved a minimum of five times. In agreement with the reproductive assurance hypothesis androdioecious notostracans are found at significantly higher latitudes than gonochoric ones indicating that post glacial re-colonisation may have selected for the higher colonisation ability conferred by androdioecy. CONCLUSIONS: In contrast to their conserved morphology, sexual system in Notostraca is highly labile and the rare reproductive mode androdioecy has evolved repeatedly within the order. Furthermore, we conclude that this lability of sexual system has been maintained for at least 250 million years and may have contributed to the long term evolutionary persistence of Notostraca. Our results further our understanding of the evolution of androdioecy and indicate that reproductive assurance is a recurrent theme involved in the evolution of this sexual system.

Concepts: Evolution, Biology, Organism, Species, Crustacean, Hermaphrodite, Branchiopoda, Notostraca

170

Biogenic amines, particularly serotonin, are recognised to play an important role in controlling the aggression of invertebrates, whereas the effect of neurohormones is still underexplored. The crustacean Hyperglycemic Hormone (cHH) is a multifunctional member of the eyestalk neuropeptide family. We expect that this neuropeptide influences aggression either directly, by controlling its expression, or indirectly, by mobilizing the energetic stores needed for the increased activity of an animal. Our study aims at testing such an influence and the possible reversion of hierarchies in the red swamp crayfish, Procambarus clarkii, as a model organism. Three types of pairs of similarly sized males were formed: (1) ‘control pairs’ (CP, n = 8): both individuals were injected with a phosphate saline solution (PBS); (2) ‘reinforced pairs’ (RP, n = 9): the alpha alone was injected with native cHH, and the beta with PBS; (3) ‘inverted pairs’ (IP, n = 9): the opposite of (2). We found that, independently of the crayfish’s prior social experience, cHH injections induced (i) the expression of dominance behaviour, (ii) higher glycemic levels, and (iii) lower time spent motionless. In CP and RP, fight intensity decreased with the establishment of dominance. On the contrary, in IP, betas became increasingly likely to initiate and escalate fights and, consequently, increased their dominance till a temporary reversal of the hierarchy. Our results demonstrate, for the first time, that, similarly to serotonin, cHH enhances individual aggression, up to reverse, although transitorily, the hierarchical rank. New research perspectives are thus opened in our intriguing effort of understanding the role of cHH in the modulation of agonistic behaviour in crustaceans.

Concepts: Arthropod, Hierarchy, Crustacean, Procambarus clarkii, Crayfish, Decapoda, Cambaridae, Procambarus

166

BACKGROUND: The gene doublesex (dsx) is known as a key factor regulating genetic sex determination in many organisms. We previously identified two dsx genes (DapmaDsx1 and DapmaDsx2) from a freshwater branchiopod crustacean, Daphnia magna, which are expressed in males but not in females. D. magna produces males by parthenogenesis in response to environmental cues (environmental sex determination) and we showed that DapmaDsx1 expression during embryonic stages is responsible for the male trait development. The D. magna dsx genes are thought to have arisen by a cladoceran-specific duplication; therefore, to investigate evolutionary conservation of sex specific expression of dsx genes and to further assess their functions in the environmental sex determination, we searched for dsx homologs in four closely related cladoceran species. RESULTS: We identified homologs of both dsx genes from, D. pulex, D. galeata, and Ceriodaphnia dubia, yet only a single dsx gene was found from Moina macrocopa. The deduced amino acid sequences of all 9 dsx homologs contained the DM and oligomerization domains, which are characteristic for all arthropod DSX family members. Molecular phylogenetic analysis suggested that the dsx gene duplication likely occurred prior to the divergence of these cladoceran species, because that of the giant tiger prawn Penaeus monodon is rooted ancestrally to both DSX1 and DSX2 of cladocerans. Therefore, this result also suggested that M. macrocopa lost dsx2 gene secondarily. Furthermore, all dsx genes identified in this study showed male-biased expression levels, yet only half of the putative 5' upstream regulatory elements are preserved in D. magna and D. pulex. CONCLUSIONS: The all dsx genes of five cladoceran species examined had similar amino acid structure containing highly conserved DM and oligomerization domains, and exhibited sexually dimorphic expression patterns, suggesting that these genes may have similar functions for environmental sex determination in cladocerans.

Concepts: DNA, Evolution, Amino acid, Crustacean, Branchiopoda, Penaeus monodon, Cladocera, Daphnia

164

INTRODUCTION: One of the most interesting riddles within crustaceans is the origin of Cladocera (water fleas). Cladocerans are morphologically diverse and in terms of size and body segmentation differ considerably from other branchiopod taxa (Anostraca, Notostraca, Laevicaudata, Spinicaudata and Cyclestherida). In 1876, the famous zoologist Carl Claus proposed with regard to their origin that cladocerans might have evolved from a precociously maturing larva of a clam shrimp-like ancestor which was able to reproduce at this early stage of development. In order to shed light on this shift in organogenesis and to identify (potential) changes in the chronology of development (heterochrony), we investigated the external and internal development of the ctenopod Penilia avirostris and compared it to development in representatives of Anostraca, Notostraca, Laevicaudata, Spinicaudata and Cyclestherida. The development of the nervous system was investigated using immunohistochemical labeling and confocal microscopy. External morphological development was followed using a scanning electron microscope and confocal microscopy to detect the autofluorescence of the external cuticle. RESULTS: In Anostraca, Notostraca, Laevicaudata and Spinicaudata development is indirect and a free-swimming nauplius hatches from resting eggs. In contrast, development in Cyclestherida and Cladocera, in which non-swimming embryo-like larvae hatch from subitaneous eggs (without a resting phase) is defined herein as pseudo-direct and differs considerably from that of the other groups. Both external and internal development in Anostraca, Notostraca, Laevicaudata and Spinicaudata is directed from anterior to posterior, whereas in Cyclestherida and Cladocera differentiation is more synchronous. CONCLUSIONS: In this study, developmental sequences from representatives of all branchiopod taxa are compared and analyzed using a Parsimov event-pairing approach. The analysis reveals clear evolutionary transformations towards Cladocera and the node of Cladoceromorpha which correspond to distinct heterochronous signals and indicate that the evolution of Cladocera was a stepwise process. A switch from a strategy of indirect development to one of pseudo-direct development was followed by a shift in a number of morphological events to an earlier point in ontogenesis and simultaneously by a reduction in the number of pre-metamorphosis molts. A compression of the larval phase as well as a shortening of the juvenile phase finally leads to a precocious maturation and is considered as a gradual progenetic process.

Concepts: Developmental biology, Larva, Crustacean, Branchiopoda, Cladocera, Daphnia, Clam shrimp, Phyllopoda

161

The amphipod crustacean Parhyale hawaiensis is a blossoming model system for studies of developmental mechanisms and more recently regeneration. We have sequenced the genome allowing annotation of all key signaling pathways, transcription factors, and non-coding RNAs that will enhance ongoing functional studies. Parhyale is a member of the Malacostraca clade, which includes crustacean food crop species. We analysed the immunity related genes of Parhyale as an important comparative system for these species, where immunity related aquaculture problems have increased as farming has intensified. We also find that Parhyale and other species within Multicrustacea contain the enzyme sets necessary to perform lignocellulose digestion (‘wood eating’), suggesting this ability may predate the diversification of this lineage. Our data provide an essential resource for further development of Parhyale as an experimental model. The first malacostracan genome will underpin ongoing comparative work in food crop species and research investigating lignocellulose as an energy source.

Concepts: DNA, Gene, Gene expression, RNA, Developmental biology, Model organism, Crustacean, Malacostraca

161

Clam shrimps are freshwater branchiopod crustaceans which often present complicated breeding systems including asexual reproduction (parthenogenesis) and mixed mating systems (in androdioecious species both selfing and outcrossing occurs due to the co-presence of hermaphrodites and males). Reproductive patterns of Spinicaudata, which contains most clam shrimp species, have received much attention. Another group of clam shrimps, Laevicaudata, which holds a key position in branchiopod phylogeny, has practically not been studied. As a part of the mating process, males clasp to the carapace margin of the females with a pair (or two pairs) of anterior trunk limbs modified as claspers. Previous studies have shown that clasper morphology is important in a phylogenetic context, and that some parts of the claspers in Spinicaudata and Laevicaudata may have undergone a remarkable parallel evolution. Here we have used video microscopy to study aspects of the mating behaviour, egg extrusion, and fertilization in Lynceus brachyurus (Laevicaudata). It is shown that fertilization is likely to be external and that the peculiar tri-lobed lateral lamellae of female’s hind body assist in guiding the egg mass to the exopodal egg carriers where they are collected by their distal setation. The functional morphology of the male claspers was studied in detail by close-up video recordings. The movable “finger” of the clasper bends around the female’s carapace edge and serves to hold the female during mating. The larger palp grasps around the female carapace margin in a way very similar to the movable “finger”, possibly indirectly providing sensory input on the “finger” position. A brief comparative study of the claspers of a spinicaudatan clam shrimp showed both similarities and differences to the laevicaudatan claspers. The presence of two pairs of claspers in Spinicaudata seems to give males a better hold of the female which may play a role during extended mate guarding.

Concepts: Male, Reproduction, Female, Arthropod, Crustacean, Sex, Branchiopoda, Clam shrimp