The annual pyloric cycle of Asterias rubens L. (echinodermata: Asteroidea)

doi:10.1016/0022-0981(77)90010-7

Journal of Experimental Marine Biology and Ecology

Volume 30, Issue 2, 1977, Pages 165-184

https://doi.org/10.1016/0022-0981(77)90010-7 Get rights and content

Abstract

Observations of biochemical changes in the pyloric caeca of Asterias rubens L. in different nutritional states and at different stages of the reproductive cycle show the existence of an annual cycle in the pyloric caeca. This pyloric cycle is closely related to that of the gonads. During the gonadal rest (May to September, when the gonads are barely visible) the pyloric caeca grow and store glycogen. During gonadal activity (October to April), they progressively autolyse and first accumulate, then liberate, lipid reserves. This winter pyloric autolysis provides the gonads with the structural material necessary for their annual growth. The summer pyloric growth must be interpreted as the accumulation of the structural material. Under normal conditions, during gonadal rest, the pyloric glycogen reserves ensure the survival of the animal. Pyloric lipid reserves appear only at the beginning of gonadal activity. Their synthesis is intimately related to the start of the gonadal activity of which they are the principal energy source. We believe that the pyloric cycle is under control of hormones that could be transported through the haemal system.

The pyloric caeca are the only reserve organs of starfish. Neither the other digestive organs nor the body wall accumulate energy reserves. During starvation of medium duration (2 to 4 weeks) the pyloric caeca suffice to ensure the survival of the animal by liberating their reserve material and simultaneously starting to autolyse. During prolonged starvation, general autolysis occurs and the size of the starfish diminishes.

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Understanding interactive effects of body size and competition on predator-prey relationships is key to predicting shifts in marine communities, particularly under accelerating pace of introductions of non-native species on a global scale. The common sea star, Asterias rubens (Linneaus), is a dominant indigenous predator in rocky subtidal habitats in eastern Canada, affecting community structure through sustained consumption of bivalve prey, mainly blue mussel, Mytilus edulis (Linneaus). Yet, considerable spatial and dietary overlaps with the indigenous rock crab, Cancer irroratus (Say), and introduced green crab, Carcinus maeneas (Linneaus), together with comparatively lower mobility in A. rubens, suggest the latter is poorly fit to compete with both crabs for M. edulis. A laboratory mesocosm experiment was used to examine competitive interactions for variably-sized M. edulis between small and large, 3-week starved A. rubens, and large C. irroratus or C. maenas (in one-on-one sea star versus crab face-offs) from southeastern Newfoundland. Mussel consumption in starved A. rubens, as well as four components of its natural feeding behaviour, were quantified over 75-h trials in relatively cold (~4 to 5.5 °C) seawater representative of the current northern limit of C. maenas' distribution in the northwestern Atlantic. Results showed that starved A. rubens (1) prioritizes consumption, upon contacting mussel prey, over non-feeding activities such as responding to physical contacts initiated by crabs; (2) alters consumption and feeding behaviour under prolonged exposure to C. irroratus; and (3) increases movement in presence of green crab, more so in large than small sea stars. Overall, findings demonstrate that A. rubens' foraging decisions vary ontogenetically and with competitor's identity. Observed differences in consumption and feeding behaviour in A. rubens exposed to familiar (rock crab) or unfamiliar (green crab) competitors also suggest timing and frequency of encounters with competitors have the potential to alter feeding patterns throughout an organism's lifetime.
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During the trials, 50% of the seawater and water-accommodating fraction (WAF) of the used lubricating oil (ULO), when applicable, was replaced every 24-h. Individuals were not allowed to feed for one week prior to the trials, nor were they fed during the experimental period. It is common for cold-water echinoderms to undergo periods of decreased or null feeding during autumn/winter seasons (Franz, 1986; Hamel and Mercier, 1998; Singh et al., 1999) with short-term starvation not significantly affecting biochemical (lipid, protein, and carbohydrate) stores (Féral, 1985; Jangoux and van Impe, 1977). The lighting was ~140 lx and followed ambient photoperiod.
In spite of increasing naval activities and petroleum exploration in cold environments, there is currently a paucity of tools available to monitor oil contamination in boreal marine life, especially in sedentary (non-fish) species that dominate benthic communities. This research aimed to identify biotic sources of variation in biomarkers using subarctic echinoderms, and to identify suitable biomarkers of their exposure to hydrocarbons. The focal species included the sea star Asterias rubens, the brittle star Ophiopholis aculeata, the sea urchin Strongylocentrotus droebachiensis, and the sea cucumber Cucumaria frondosa, which are among the most abundant echinoderms in the North Atlantic and Arctic Oceans. The latter two species are also commercially exploited. A series of 96-h acute exposures of the water-accommodating fraction (WAF) of used lubricating oil (ULO) were performed in different seasons (i.e. distinct reproductive stages). Digestive and reproductive tissues were analyzed for baseline and response levels of glutathione peroxidase (GPx) and ethoxyresorufin-O-deethylase (EROD). GPx activity was detected in the pyloric caecum, stomach, and gonad of sea stars, the intestine and gonad of sea cucumbers, and the gonad of brittle stars and sea urchins. No seasonal variation in baseline GPx activity occurred. Upon exposure to the ULO WAF, sex-based differences were elicited in the GPx activity of sea star stomachs (lower in females than males). EROD activity was present in the pyloric caeca of sea stars, and the gonads of brittle stars and sea urchins. An interaction between season and sex on baseline EROD activity was measured in the gonads of sea urchins. Ovaries exhibited significant seasonal variation in EROD activity and had greater activity than testes during the spawning and post-spawning seasons. Seasonal variation in EROD activity also occurred in sea star pyloric caeca and brittle star gonads. Furthermore, testes of sea urchins exposed to the ULO WAF exhibited suppressed EROD activity compared to baseline levels. The nearly universal presence of GPx activity highlights its potential as a useful biomarker, while EROD activity was much more limited. Findings suggest a complex relationship between temporal and biotic factors on both the baseline and response levels of enzymatic activity, emphasizing the need to consider sex and sampling season in studies of biomarkers of hydrocarbon exposure in boreal indicator species that display annual reproductive cycles.
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On the contrary, at the start of vitellogenesis, lipid levels start to decrease in the pyloric sphincter and increase in the gonads (Oudejans and Sluis, 1979). The stored energy in the pyloric caeca is used for gonadal development (Jangoux and Van Impe, 1977). The observed monthly differences in fat levels may depend more on environmental factors than gonadal development.
To study the annual variation in the composition of nutrients relevant to pig and poultry feeding, monthly samples of starfish (Asterias Rubens) were taken in Denmark. The effect of different locations and starfish sizes was also assessed. Crude protein (CP) and phosphorus were high from February to May and lower thereafter. The AA profile remained constant and followed the same pattern as CP. An opposite pattern of CP was observed for both ash and calcium. Fat followed no clear annual pattern. Starfish within the smallest size group had the lowest fat and CP levels and the highest ash and calcium levels. The most profound differences between locations were observed in May. The seasonal pattern in chemical composition seemed related to spawning and gonadal developments. Large and medium sized starfish caught between February and May will be most suitable for pig and poultry feed.
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The Vtg of the asterinid P. exigua also contains such a cleavage motif, RKRR (Prowse and Byrne, 2012). Studies on vitellogenesis in asteroids have proposed that synthesis of a yolk protein precursor takes place in the pyloric caeca prior to its transfer to the ovary or the oocytes within (Byrne, 1992; Carvalho and Ventura, 2002; Crump, 1971; Jangoux and van Impe, 1977; Voogt et al., 1985). These reports were based on biochemical analyses and on the inverse relationship between relative pyloric caeca and gonad weights during gametogenesis.
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Wave action and starvation modulate intra-annual variation in displacement, microhabitat selection, and ability to contact prey in the common sea star, Asterias rubens Linnaeus
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The common sea star, Asterias rubens, is a major predator in the rocky subtidal zone in the northern Gulf of St. Lawrence and along the Atlantic coast of Newfoundland, Canada. Knowledge about the ecology of A. rubens in these highly seasonal systems is largely limited to studies of interspecific competition for prey. Two experiments in an oscillatory wave tank were used to test the hypothesis that wave action and starvation modulate displacement, microhabitat selection, and ability to contact mussel (Mytilus edulis) prey in A. rubens from southeastern Newfoundland. Both experiments were carried out in two seasons (winter and summer) to quantify intra-annual variation in the effects of wave action (three wave velocities: null [0.0 m s^− 1], low [0.1 m s^− 1], and high [0.2 m s^− 1]) and starvation (two levels: fed and starved three weeks). Experiment 1, in which two sea stars were allowed to displace and make contact with six microhabitats typifying natural seabed heterogeneity, showed that A. rubens displaced up to 50% less with increasing wave velocity. Displacement was 120% higher in summer than winter and lower in starved than fed individuals in summer only. The sea star predominantly stayed on flat horizontal surfaces, did so more frequently in the presence than absence of waves, and spent more time in the two most uneven microhabitats in winter than summer regardless of wave velocity. Experiment 2, in which one sea star in the centre of a depression was allowed to move to the top of surrounding mounds, showed that more sea stars that left the centre of the depression reached the top of the mounds in summer than winter, in the absence than presence of waves, and when starved than fed. Sea stars that reached the top of mounds spent more time there in the presence than absence of mussels in summer only, when starved than fed in summer only, and in the presence than absence of mussels at null and low wave velocities. Measurements of wave height, sea temperature, and A. rubens abundance over six months at one subtidal site indicated that the sea star was > 4 times more abundant at 8 m than at 2 m and 4 m. This difference was unrelated to temperature and likely mainly caused by the wave environment. Collectively, results demonstrate that wave action, and to a lesser extent starvation, are key modulators of the inclination and ability of A. rubens to explore its environment and localize prey. In southeastern Newfoundland, the response of A. rubens to wave action and starvation is adaptable, being generally stronger in summer than winter, when sea temperature is markedly lower.
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The annual pyloric cycle of Asterias rubens L. (echinodermata: Asteroidea)

Abstract

Comp. Biochem. Physiol.

Chem. Zool.

Comp. Biochem. Physiol.

Comp. Biochem. Physiol.

Int. Rev. Cytol.

J. exp. mar. Biol. Ecol.

J. biol. Chem.

J. Lipid Res.

Structure and function in the pyloric caeca of Asterias forbesi

Biol. Bull. mar. biol. Lab., Woods Hole

Sur la surcharge en glycogène des organes reproducteurs de quelques invertébrés au moment de la ponte

C. r. Séanc. Soc. Biol.

La sexualité des astérides

Cah. Biol. mar.

Sur l'excrétion azotée des astéries (Asterias rubens L.)

C.r. Séanc. Soc. Biol.

Colorimetric method for determination of sugars and related substances

Analyt. Chem.

Annual reproductive cycles in four species of west coast starfishes

J. exp. Zool.

Growth and predation by ochre sea star, Pisaster ochraceus (Brandt), in Monterey Bay, California

Ophelia

Effet d'un jeûne de courte durée sur les principaux constituants biochimiques de l'oursin Arbacia lixula. I. Stade de repos sexuel

Mar. Biol.

Lipids in the economy of marine invertebrates

Physiol. Rev.

On the biochemical constitution of some Echinoderms

General physiology of the echinoderm body wall with special reference to asteroids and echinoids

Antarct. J. U.S.

Cyclic biochemical changes in several Echinoderms

J. exp. Zool.

Inorganic phosphates and phosphate esters in tissue extracts

Analyt. Chem.

Notes on starfish on an Essex oyster bed

J. mar. biol. Ass. U.K.