Developmental modularity and phenotypic novelty within a biphasic life cycle: morphogenesis of a cone snail venom gland

The venom gland of predatory cone snails (Conus spp.), which secretes neurotoxic peptides that rapidly immobilize prey, is a proposed key innovation for facilitating the extraordinary feeding behaviour of these gastropod molluscs. Nevertheless, the unusual morphology of this gland has generated controversy about its evolutionary origin and possible homologues in other gastropods. I cultured feeding larvae of Conus lividus and cut serial histological sections through the developing foregut during larval and metamorphic stages to examine the development of the venom gland. Results support the hypothesis of homology between the venom gland and the mid-oesophageal gland of other gastropods. They also suggest that the mid-region of the gastropod foregut, like the anterior region, is divisible into dorsal and ventral developmental modules that have different morphological, functional and ontogenetic fates. In larvae of C. lividus, the ventral module of the middle foregut transformed into the anatomically novel venom gland of the post-metamorphic stage by rapidly pinching-off from the main dorsal channel of the mid-oesophagus, an epithelial remodelling process that may be similar to other cases where epithelial tubes and vesicles arise from a pre-existing epithelial sheet. The developmental remodelling mechanism could have facilitated an abrupt evolutionary transition to the derived morphology of this important gastropod feeding innovation.     

Test cell migration and tunic formation during posthatching development of the larva of the ascidian, Ciona intestinalis

Morphological changes in the tunic layers and migration of the test cells during swimming period in the larva of the ascidian, Ciona intestinalis , were observed by light and electron microscopy. The swimming period was divided into three stages. In stage 1, further formation of juvenile tunic layer started only in the larval trunk and neck region. In stage 2, the layer became swollen in the ventral and dorsal sides of the neck region and in stage 3, the swelling expanded backward. Concomitantly with these changes, the outermost larval tunic layer (outer cuticular layer), which had been formed before hatching, also swelled in the neck region in stage 2 and formed two humps in stage 3, although the layer did not change in the tail region during the swimming period. Test cells that were present over the entire larval tunic layer in stage 1 began to move from the surface of the fin toward that of the side of the body in stage 2, and finally gathered to form six bands running radially from the anterior end to the posterior end of the trunk region and aligned along the lateral sides of body in the tail region in stage 3. In electron microscopic observations, pseudopodia protruding from the test cells invaded the larval tunic, following which they extended proximate to the juvenile tunic in the trunk region. In the tail region, which had no juvenile tunic layer as that described, the pseudopodia invaded and remained adjacent to the surface of the epidermis or the sensory cilia protruded from the epidermis. Metamorphosis of the larvae, further tunic formation, degradation of adhesive papilla, attachment of larva to the substratum and tail resorption commenced after these morphological changes occurred. The possible role of the test cells in metamorphosis is discussed.     

Laboratory observations on the feeding behaviour, reproduction and morphology of Galeodea echinophora (Gastropoda: Gassidae)

Galeodea echinophora fed on Echinocardium cordatum in an aquarium. Every few days, each G. echinophora emerged from the sand and foraged for 1–3 h. On detecting an Echinocardium , the Galeodea stopped locomotion and attacked the buried prey from the surface of the sand. The proboscis was extended down to the prey and a small area of test was cleared of spines. A disc was cut out of the softened test, leaving a hole of about 2 mm in diameter. All flesh except the gut was removed from the prey, the entire procedure taking 50–180 min.
One Galeodea echinophora laid 120 egg capsules on the side of the aquarium. These were kept at 13^oC and hatched after 112–159 days. Within the capsule, veligers fed on the yolk cells of abortive embryos. Juveniles hatched at the crawling stage, and at first secreted strings of mucus acting as drogues, but after 1 day the juveniles crawled over the substratum. They readily attached themselves to adult Echinocardium cordatum , apparently feeding on the epithelium between the spines or tube feet. Dissection revealed entry of the acinar glands into the proboscis gland ducts, a widening of these ducts as they empty into the buccal cavity and a dorsal fold in the anterior oesophagus. Radular teeth and jaws of Galeodea differ little among species; a taxonomic review of the genus is needed.     

Mating behavior of the squid Loligo opalescens

In the laboratory, the squid Loligo opalescens exhibits dominance behavior during spawning. A single dominant male keeps other male squid from coming near the egg mass he is guarding. Females are allowed to approach the egg mass. The dominant squid uses postural and color displays directed toward challenging males. Similar dominance behavior and displays have not been observed in natural spawns in the ocean.     

Honeycomb structure in the lamina lucida of epidermal basement membrane during metamorphosis of Rana temporaria ornativentris

In this study we examine the structure of the lamina lucida during metamorphosis of Rana temporaria ornativentris. During the metamorphosis of anuran larvae, both the epidermal cells and the dermal connective tissues in the tail regenerate. The basal surface of the epidermis becomes irregular and the epidermal basement membrane detaches from the epidermal cells, showing a widened lamina lucida. In this widened lamina we observed a geometrical honeycomb structure and a ladder structure. Each side of the honeycomb structure was approximately 40 nm and the intervals of the ladder structure were approximately 50 nm. From our observations we believe that the honeycomb and ladder appearances are different aspects of the same structure. At the beginning of metamorphosis anchoring filaments were prominent in the lamina lucida and, when the lamina lucida was tangentially cut, the lamina lucida showed the honeycomb structure. These results suggest that both the honeycomb and the ladder structures observed in the widened lamina lucida originate from constituents of the lamina lucida and become morphologically evident during the epidermal-dermal separation.     

Influence of rearing and experimental temperatures on predator avoidance behaviour in a freshwater pulmonate snail

1. Predicted increases in the temperature of freshwaters is likely to affect how prey species respond to predators. We investigated how the predator avoidance behaviour of the freshwater pulmonate snail Lymnaea stagnalis is influenced by the temperature at which it was reared and that at which behavioural trials were carried out. 2. Crawl‐out behaviour of juvenile snails from two populations (high predation risk versus low predation risk) reared at either 15 or 20 °C was assessed in response to predation cues (predatory fish kairomones and conspecific alarm cues) in behavioural trials at both 15 and 20 °C. 3. Trial temperature had a significant effect on the time that snails spent in avoidance, regardless of their population of origin. Crawl‐out behaviour was greater during behavioural trials at 15 °C, but there was no effect of trial temperature on the speed with which animals showed avoidance behaviour. 4. There was no interactive effect of rearing temperature (RT) and trial temperature, but the effect of RT on avoidance behaviour did differ between populations. For an RT of 15 °C, snails from the South Drain (high risk) population showed a more rapid and longer avoidance response than those from the Chilton Moor (low risk) population. In contrast, for snails reared at 20 °C, there was no difference between populations for the duration of the avoidance response and snails from Chilton Moor crawled out faster than those from South Drain. 5. Hence, whilst (predictable) differences relative to natural predation threat in crawl‐out behaviour were apparent at 15 °C, raising the developmental temperature to 20 °C eliminated or, in the case of latency, reversed these differences. This suggests that L. stagnalis populations that cohabit with predatory fish and experience high developmental temperatures may have a reduced ability to respond to fish predation risk.     

Multifractal anisotropic swimming: the optimal foraging behaviour of grouper larvae

It was hypothesized that the Malabar grouper Ephinephelus malabaricus larvae have developed search patterns adapted to the distribution of their prey to maximise their net energy intake per unit time. Analysis of the swimming behaviour of E. malabaricus larvae in both the presence and absence of Artemia sp. nauplii is presented to test this hypothesis. A method derived from turbulence studies (the moment function of the displacements) was used to characterize the behaviour. The results revealed that larval swimming pattern was multifractal (intermittent and long‐range‐correlated) and isotropic (i.e. uniform in all directions) in the presence of prey, but multifractal and anisotropic (i.e. more frequent long displacement on the vertical axis) in the absence of prey. It is suggested that the search behaviour observed in the absence of prey is an adaptive response to prey distribution pattern, which is often characterised by multifractality and anisotropy (i.e. larger patches on the horizontal axes). In the presence of prey, E. malabaricus shifted to intensive search behaviour. Other possible contributors to the observed patterns are discussed. It is concluded that multifractality and anisotropy of swimming patterns observed in the experiment are mainly explained in an optimal foraging theory framework.