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Effects of photoperiod on oviposition of Lymnaea stagnalis. a Cumulative proportions of egg-laying snails 13–31 weeks after hatching. Different letters 25 and 31 weeks after hatching indicate significant differences (Tukey-type multiple comparisons for proportions, P < 0.05, sTable 1). The total number of egg masses (b) and the total number of eggs (c) per snail 31 weeks after hatching under five different photoperiods. Box plots indicate median, interquartile ranges, and maximum and minimum values inside 1.5 times the interquartile range. Open circles are outliers: values outside of 1.5 × the interquartile range. N = 31 (12L:12D), 28 (13L:11D), 25 (14L:10D), 31 (15L:9D), and 34 (16L:8D) for a–c. d Numbers of eggs per egg mass (average and SE). N = 9 (12L:12D), 18 (13L:11D), 18 (14L:10D), 19 (15L:9D), and 20 (16L:8D). Different letters in each graph of b–d indicate significant differences (Steel–Dwass test, P < 0.05, sTable 2)
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Photoperiod is a reliable cue to regulate growth and reproduction for seasonal adaptation. Although photoperiodism has been well studied in Chordata and Arthropoda, less is known about Mollusca. We examined photoperiodic effects on egg laying, body size, gonad-somatic index, oocyte size and relative amounts of caudodorsal cell hormone mRNA in indiv...
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The pond snail Lymnaea stagnalis exhibits clear photoperiodism in egg laying; it lays more eggs in long-day conditions than in medium-day conditions. A key regulator of egg laying is neurosecretory caudo-dorsal cells (CDCs) producing an ovulation hormone in the cerebral ganglia. Paired small budding structures of the cerebral ganglia (viz. the late...
Citations
... The abundance of light in such habitats determines the development of macrophytes, which serve as a primary food source for the lymnaeids and other phytophilous gastropods. The influence of photoperiod on physiological processes, growth, and reproduction of aquatic pulmonates (lymnaeids included) has been studied in many works (i.e., Kunigelis and Saleuddin 1978;Numata and Udaka 2009;Ter Maat et al. 2012;Kitai et al. 2021). The pond snails inhabiting mountain lakes at depths exceeding 250 m (see above) must spend their whole life in almost complete darkness, however, their physiological response to the lack of abundant light is virtually not studied. ...
The ecology of the lymnaeid snails, including their habitat preferences, resistance to abiotic factors, and interactions with other species of freshwater organisms, is briefly reviewed and accompanied by numerous illustrations. A special section deals with the patterns of life cycles, reproduction, and fecundity of the pond snails.
... Artificial light can also alter hormonal levels and thereby influence seasonal reproductive activities (Buchanan and Partecke 2012). For instance, increased perceived length of the day stimulates the production of an egg laying hormone in the pond snail Lymnaea stagnalis (Kitai et al. 2021). ...
Artificial light at night (ALAN) is a growing global problem altering the behavior of organisms and thereby community composition and ecosystem processes. Research has mostly focused on terrestrial ecosystems, but a growing number of studies show that aquatic ecosystems are increasingly affected. Here, we provide a conceptual framework that describes how ALAN can influence aquatic ecosystems through effects on the behavior of ecologically important invertebrates. These organisms provide a range of critical ecological functions, from serving as food for other organisms to nutrient cycling and the translocation of energy and matter within and between ecosystems. In addition, we systematically searched the literature to assess the current state of the field and identify knowledge gaps. The literature search reveals that an increasing number of studies find light pollution to alter the behavior of aquatic invertebrates, such as their movements, habitat choice, and foraging behavior, but that the fitness consequences of these behavioral changes are largely unknown, as are their impacts on populations, communities, and ecosystems. Yet, assessing the consequences of behavioral changes for higher ecological levels is of vital importance given the central role of these invertebrates in ecosystems. Thus, more research needs to be directed to the ecological consequences of behavioral responses of aquatic invertebrates to light pollution. Overall, more effort should be made to assess the ecological consequences of behavioral responses to ALAN, and, importantly, how negative effects of light pollution could be mitigated.
Significance statement
Light pollution is of growing ecological concern and influencing ecosystems through effects on the behavior of organisms. Aquatic ecosystems are increasingly exposed and an ecologically important group of organisms in these systems are invertebrates. Here, we discuss how artificial light at night alters the behavior of aquatic invertebrates and how this in turn influences ecosystem structure and function. Such an understanding of the mechanisms and pathways that underlie the effect of light pollution on aquatic ecosystems is needed if we are to develop efficient strategies to reduce negative effects of human-made lighting systems on ecosystems.
... In insects, crucial transplantation and organ culture experiments using the moths Antheraea pernyi and Manduca sexta have demonstrated that the photoperiodic mechanism involving the photoperiodic clock and counter resides in the brain (Williams and Adkisson 1964;Bowen et al. 1984b;Takeda and Suzuki 2022). Although this scheme has been proposed and is widely accepted in insects, we consider that it could also be applicable to the molluscan photoperiodic responses in which similar characteristics, such as critical day length and requirement of number of weeks for seasonal responses, are evident (Kitai et al. 2021). ...
... Importantly, a follow-up study explicitly demonstrated that egg laying in pond snails is photoperiodically controlled at the individual level. The cumulative proportion of egg-laying snails was higher in long-day conditions than in medium-day conditions of 12 h light and 12 h darkness with a critical day length between 12 and 13 h at 20 °C, although the gonad-somatic index did not change with photoperiod (Kitai et al. 2021). ...
... The expression levels of cdch mRNA in the cerebral ganglia were also higher under long-than under mediumday conditions (Kitai et al. 2021). These results suggest that cdch-expressing CDCs receive photoperiodic inputs that increase cdch expression and the excitability to release more CDCHs in response to long days. ...
The photoperiodic mechanism distinguishes between long and short days, and the circadian clock system is involved in this process. Although the necessity of circadian clock genes for photoperiodic responses has been demonstrated in many species, how the clock system contributes to photoperiodic mechanisms remains unclear. A comprehensive study, including the functional analysis of relevant genes and physiology of their expressing cells, is necessary to understand the molecular and cellular mechanisms. Since Drosophila melanogaster exhibits a shallow photoperiodism, photoperiodic mechanisms have been studied in non-model species, starting with brain microsurgery and neuroanatomy, followed by genetic manipulation in some insects. Here, we review and discuss the involvement of the circadian clock in photoperiodic mechanisms in terms of neural networks in insects. We also review recent advances in the neural mechanisms underlying photoperiodic responses in insects and snails, and additionally circadian clock systems in snails, whose involvement in photoperiodism has hardly been addressed yet. Brain neurosecretory cells, insulin-like peptide/diuretic hormone44-expressing pars intercerebralis neurones in the bean bug Riptortus pedestris and caudo-dorsal cell hormone-expressing caudo-dorsal cells in the snail Lymnaea stagnalis, both promote egg laying under long days, and their electrical excitability is attenuated under short and medium days, which reduces oviposition. The photoperiodic responses of the pars intercerebralis neurones are mediated by glutamate under the control of the clock gene period. Thus, we are now able to assess the photoperiodic response by neurosecretory cell activity to investigate the upstream mechanisms, that is, the photoperiodic clock and counter.
... Snails were kept under a natural light cycle in our experiments; therefore, it is not surprising that this difference was observed. The light-cycle-dependent seasonal differences in reproduction and in the expression of ovulation prohormone was previously confirmed in L. stagnalis [39]. Interestingly, seasonal differences in reproduction and in monoamine metabolism were observed even under artificial uniform light cycle during the year [40]. ...
Intense species-specific locomotion changes the behavioural and cognitive states of various vertebrates and invertebrates. However, whether and how reproductive behaviour is affected by previous increased motor activity remains largely unknown. We addressed this question using a model organism, the pond snail Lymnaea stagnalis. Intense crawling in shallow water for two hours had previously been shown to affect orienting behaviour in a new environment as well as the state of the serotonergic system in L. stagnalis. We found that the same behaviour resulted in an increased number of egg clutches and the total number of eggs laid in the following 24 h. However, the number of eggs per clutch was not affected. This effect was significantly stronger from January to May, in contrast to the September-December period. Transcripts of the egg-laying prohormone gene and the tryptophan hydroxylase gene, which codes for the rate-limiting enzyme in serotonin synthesis, were significantly higher in the central nervous system of snails that rested in clean water for two hours after intense crawling. Additionally, the neurons of the left (but not the right) caudo-dorsal cluster (CDC), which produce the ovulation hormone and play a key role in oviposition, responded to stimulation with a higher number of spikes, although there were no differences in their resting membrane potentials. We speculate that the left-right asymmetry of the response was due to the asymmetric (right) location of the male reproductive neurons having an antagonistic influence on the female hormonal system in the hermaphrodite mollusc. Serotonin, which is known to enhance oviposition in L. stagnalis, had no direct effect on the membrane potential or electrical activity of CDC neurons. Our data suggest that (i) two-hour crawling in shallow water enhances oviposition in L. stagnalis, (ii) the effect depends on the season, and (iii) the underlying mechanisms may include increased excitability of the CDC neurons and increased expression of the egg-laying prohormone gene.
... Previous studies have demonstrated that photoperiods have a clear effect on the reproduction, food intake, growth, temperature tolerance, locomotion, and learning ability of mollusks, including L. stagnalis (Bohlken and Joosse, 1981;Hemminga et al., 1985;Hommay et al., 2001;Hussein et al., 2020a;Kitai et al., 2021;Numata and Udaka, 2010;Ter Maat et al., 2012Wang et al., 2013). In addition, it has been shown that snails and slugs exposed to a longer day length (16 h light: 8 h dark) lay significantly more eggs (Limax valentianus: Numata and Udaka, 2010;L. ...
... A very recent study showed that individuals of L. stagnalis exposed to a normal day length (12 h light: 12 h dark) began egg-laying later than those exposed to a long day length. This latter finding provides solid evidence for egg-laying being influenced by day length and was further explained by the increased quantity of CDCH mRNA in the cerebral ganglia and commissure of the snails exposed to longer photoperiods (Kitai et al., 2021). ...
... Previous research did not look at light pollution, but did reveal a clear influence of different photoperiods on egg-laying (Benbellil-Tafoughalt et al., 2009;Ter Maat et al., 2012). Moreover, it has been shown that the total number of eggs under 12 h light/12 h dark were significantly lower than those exposed to longer days (Kitai et al., 2021). While these earlier findings highlight the importance of day length, different light intensities during the dark phase of the light/dark cycle have been largely overlooked. ...
Light is an important zeitgeber that regulates many behavioral and physiological processes in animals. These processes may become disturbed due to the changes in natural patterns of light and dark via the introduction of artificial light at night (ALAN). The present study was designed to determine the effect of possible consequences of ALAN on reproduction, hatching success, developmental success, growth rate, feeding rate, mortality rate, and locomotor activity of the simultaneous hermaphrodite pond snail Lymnaea stagnalis. Snails were exposed to different light intensities at night that simulate actual ALAN measurements from the snail's night environment. The data revealed that exposure to ALAN at a low level significantly affected the cumulative number of laid eggs. At the same time, snails exposed to ALAN laid smaller eggs than those laid under normal light-dark cycles. Additionally, high light-intensity of ALAN delayed development and hatching of eggs of L. stagnalis while it showed no effect on hatching percentage. Furthermore, ALAN increased both the feeding and growth rates but did not lead to mortality. The results also show that snails exposed to dark conditions at night travel longer distances and do so faster than those exposed to ALAN. In light of these findings, it is clear that ALAN may have an influence on snails and their abundance in an environment, possibly disturbing ecological stability.
The pond snail Lymnaea stagnalis exhibits clear photoperiodism in egg laying; it lays more eggs in long-day conditions than in medium-day conditions. A key regulator of egg laying is neurosecretory caudo-dorsal cells (CDCs) producing an ovulation hormone in the cerebral ganglia. Paired small budding structures of the cerebral ganglia (viz. the lateral lobe) also promote egg laying in addition to spermatogenesis and maturation of female accessory sex organs. However, it remains unknown which cells in the lateral lobe are responsible for these. Previous anatomical and physiological studies prompted us to hypothesize that canopy cells in the lateral lobe modulate activity of CDCs. However, double labeling of the canopy cell and CDCs revealed no sign of direct neural connections, suggesting that activity of CDCs is regulated either humorally or through a neural pathway independent of canopy cells. In addition, our detailed anatomical re-evaluation confirmed previous observations that the canopy cell bears fine neurites along the ipsilateral axon and extensions from the plasma membrane of the cell body, although the function of these extensions remains unexplored. Furthermore, comparison of electrophysiological properties between long-day and medium-day conditions indicated that the canopy cell’s activity is moderately under photoperiodic regulation: resting membrane potentials of long-day snails are shallower than those of medium-day snails, and spontaneously spiking neurons are only observed in long-day conditions. Thus, canopy cells appear to receive photoperiodic information and regulate photoperiod-dependent phenomena, but not provide direct neural inputs to CDCs.
