The effects of climate change on the reproduction of coastal invertebrates

Environmental cues control or synchronize the reproductive cycle of many marine invertebrates. Of these environmental cues, photoperiod and temperature have been shown to moderate reproduction either individually or in combination. In addition, they may act directly or, in the case of photoperiod, set circannual clock mechanisms. These environmental cues may affect a number of reproductive parameters, including sex determination, gametogenesis and spawning. Gonadotrophic and spawning hormones appear to act as the transducers between the environment and the gamete, and limited evidence indicates that temperature and photoperiod can alter levels of these. Such processes occur in a range of estuarine invertebrates that constitute important components of the diets of overwintering birds. Global warming is likely to uncouple and alter the phase relationship between temperature and photoperiod and this is likely to have significant consequences for animals that develop gametes during the winter and spawn in the spring in temperate northern latitudes. Species that cue reproduction to photoperiod are likely to be particularly vulnerable. Although this is unlikely to lead to extinctions, it may cause local extirpations. However, this will depend on speed of adaptation to changing climate in relation to speed of climate change and the degree of mixing between populations across the range of the species. More likely will be significant impacts on fecundity, spawning success and recruitment, and this may have significant implications for overwintering birds of national and international importance, and, ultimately, on the conservation status of estuaries such as the Humber in the UK.     

Cellular and functional adaptation to thermal stress in ovarian granulosa cells in mammals

Climate change represents a significant environmental challenge to human welfare. One of many negative impacts may be on animal reproduction. Elevated ambient temperature unfavourably influences reproductive processes in mammals. High temperature can affect reproductive processes such as follicle development and may alter follicular fluid concentrations of amino acids, fatty acids, minerals, enzymes, antioxidants defence and growth factors. These impacts may lead to inferior oocyte competence and abnormal granulosa cell (GCs) function. Mammalian oocytes are enclosed by GCs that secret hormones and signalling molecules to promote oocyte competence. GCs are essential for proper follicular development, oocyte maturation, ovulation, and luteinization. Many environmental stressors, including thermal stress, affect GC function and alter oocyte development and growth. Several studies documented a link between elevated ambient temperature and increased generation of cellular reactive oxygen species (ROS). ROS can damage DNA, reduce cell proliferation, and induce apoptosis in GCs, thus altering oocyte development. Additionally, thermal stress induces upregulation of thermal shock proteins, such as HSP70 and HSP90. This review provides an update on the influence of thermal stress on GCs of mammals. Discussions include impacts to steroidogenesis (estradiol and progesterone), proliferation and cell cycle transition, apoptosis, oxidative stress (ROS), antioxidants related genes, heat shock proteins (HSPs) and endoplasmic reticulum responses.     

A neotropical forest bird can measure the slight changes in tropical photoperiod

Many tropical birds breed seasonally, but it is largely unknown which environmental cues they use to time reproduction. Changes in tropical photoperiod have been regarded as too small to be used as a proximate environmental cue. This hypothesis, however, has never been rigorously tested. Here, we report on experimental evidence that photoperiodic changes characteristic of tropical latitudes stimulate reproductive activity in a neotropical bird from the forest understory. In the central Republic of Panam (9 degrees N), photoperiod varies annually between 12 hours (December) and 13 hours (June). Free-living spotted antbirds (Hylophylax n. naevioides) had regressed gonads in December, but increased gonads ahead of the rainy (the breeding) season in May. Captive spotted antbirds exposed to a ''long'' photoperiod of 13 hours increased gonadal size eight-fold and song activity six-fold over that of control birds remaining on a simulated ''short'' photoperiod of 12 hours of daylight. Moreover, even a photoperiod of 12 hours 17 minutes was sufficient to stimulate gonadal growth in photostimulated birds over that of controls. The dramatic changes in gonadal development were not accompanied by similar changes in hormone titres such as luteinizing hormone and testosterone as expected from temperate zone birds. We propose a more general role of the tropical photoperiod in the regulation of seasonal events in tropical organisms, or in temperate zone species migrating to the tropics.     

Interactions of environmental temperature with photoperiod in determining age at maturity in a semelparous polychaete Nereis (neanthes) virens sars

1. 1. Larger members of the Polychacta exhibit two contrasting life cycles: semelparous in the Nereidae, iteroparous in most others.

2. 2. In semelparous forms environmental interaction determines age at reproduction and fecundity in the single spawning event whereas in iteroparous forms such interaction influences the variable age specific reproductive effort.

3. 3. Development of aquaculture has created conditions where organisms are grown under conditions of optimum temperature for growth and unlimited food.

4. 4. We present data on the life history responses (reaction norms) of the semelparous Nereis virens in which age at death in natural populations varies between 3 to 8+ years.

5. 5. In Nereis virens minimum life span (= generation time) in culture is one year but the lifespan remains modular 12 months without manipulation of photoperiod.

6. 6. Environmental temperature plays two roles: i) in conjunction with energy availability to determine “age at first/only reproduction” and secondly as an element (with photoperiod) in the control of gametogenic processes imposing seasonality on the life cycle.

7. 7. The observations suggest that long generation time in natural populations of N. virens is associated with reduced growth rate and that low growth rate is associated with reproduction at a larger size.

     

Significance of haemolymph juvenile hormone titer changes in timing of migration and reproduction in adult Oncopeltus fasciatus

Previous studies had shown that both migratory flight and ovarian maturation in Oncopeltus fasciatus were stimulated by juvenile hormone (JH), yet the two behaviors were mutually exclusive. To understand the relationship of this hormone to these behaviors, haemolymph juvenile hormone titers were determined in both sexes of Oncopeltus throughout the adult stage by the Manduca pigmentation bioassay. Animals reared under long day conditions (17L:7D, 24°C) showed an immediate rise in haemolymph titers of JH after adult emergence whereas those reared in a short day photoperiod (12L:12D, 24°C) had a more gradual increase in hormone titers. Migratory flight behavior occurred during periods of intermediate hormone titers while oviposition did not begin until JH titers had reached their peak. It was concluded that lower JH titers normally stimulate flight in the prereproductive adult whereas higher titers are required for complete ovarian development. The corpus allatum in Oncopeltus thus coordinates migration and reproduction in response to the environmental cues of photoperiod, temperature, and food quality.     

动物季节性繁殖分子调控机理研究进展

动物季节性发情繁殖涉及下丘脑-垂体-性腺轴系统复杂的神经内分泌过程,并受光照周期等环境因素的影响。褪黑激素则作为光周期信号分子调控动物季节性繁殖活动。近年来研究发现,对GnRH分泌有重要影响的Kiss1/GPR54系统既受褪黑激素的调控又受到性腺类固醇激素反馈调节,Kiss1/GPR54系统很可能是调控动物季节性繁殖的关键因子;同时动物季节性繁殖很可能还存在一条涉及TSH-DIO2/DIO3系统的逆向调控通路,该系统同样显著影响GnRH合成释放并受褪黑激素调控。文章就褪黑激素中心信号,特别是Kiss1/GPR54和TSH-DIO2/DIO3系统对繁殖季节性调控的最新研究进展进行综述。     

Endocrine and reproductive differences and genetic divergence in two populations of the cockroach Diploptera punctata

The viviparous cockroach, Diploptera punctata, has been a valuable model organism for studies of the regulation of reproduction by juvenile hormone (JH) in insects. As a result of its truly viviparous mode of reproduction, precise regulation of JH biosynthesis and reproduction is required for production of offspring, providing a model system for the study of the relationship between JH production and oocyte growth and maturation. Most studies to date have focused on individuals isolated from a Hawaiian population of this species. A new population of this cockroach was found in Nakorn Pathom, Thailand, which demonstrated striking differences in cuticle pigmentation and mating behaviours, suggesting possible physiological differences between the two populations. To better characterize these differences, rates of JH release and oocyte growth were measured during the first gonadotrophic cycle. The Thai population was found to show significantly earlier increases in the rate of JH release, and oocyte development as compared with the Hawaiian population. Breeding experiments to determine the degree of interfertility between the two populations demonstrated greatly reduced fertility in crosses between the two populations. Additionally, levels of genetic divergence between the two populations estimated by sequencing a fragment of the mitochondrial 16S rRNA gene were surprisingly high. The significant differences in physiology and mating behaviours, combined with the reduced interfertility and high levels of sequence divergence, suggest that these two populations of D. punctata are quite distinct, and may even be in the process of speciation. Moreover, these studies have important implications for the study of JH function in the reproductive cycle of insects, as differences in timing of rates of JH biosynthesis may suggest a process of heterochrony in reproduction between the two populations.     

Reproductive ecology of female Oligocottus snyderi Greeley: a North American intertidal sculpin

The reproductive condition of female Oligocottus snyderi Greeley during 18+ months at Dillon Beach, California was examined. Seasonal differences in reproductive condition were identified by diameter measurements of ovarian follicles in pre-vitellogenic, cortical alveoli and vitellogenic stages of development which showed that female O. snyderi appeared capable of reproduction during 6 to 8 months of the year. Reproduction occurred from late autumn to early spring and it is likely that females reproduce more than once a year. Follicular development within the population was asynchronous; development within individual females was group synchronous. The percentage of females with vitellogenic follicles in each collection was negatively correlated with photoperiod and productivity and positively correlated with wave action. Conversely, the percentage of newly recruited individuals in each sample was positively correlated with photoperiod and productivity. It appears that reproduction and recruitment in O. snyderi are significantly influenced by annual productivity cycles; daylength changes may provide an anticipatory cue for the productivity cycle.     

Dancing to the rhythms of geological time: the biorhythm capabilities of Polychaeta in a geological context

Summary

Errant polychaete worms in the Orders Eunicida (family Eunicidae) and Phyllodocida (families Nereidae and Polynoidae) exhibit a highly developed biorhythmic capability. The Pacific palolo worms are well known for a precisely timed annual breeding event in which mass spawning occurs at a particular time of day, on one day per year, that day having a fixed relationship to the lunar period. Nereidae and Polynoidae exhibit photoperiodic responses that determine the breeding season by regulation of oocyte growth. Nereis virens shows short-term cycles of foraging activity; automated recording of these patterns has revealed four distinct behaviour rhythm phenotypes: circadian, tidal, lunidian and arrhythmic, the last phenotype being expressed during the photoperiod induced growth diapause. The Eunicids and Phyllodocids are represented in the fossil record by scolecodonts, their fossilised jaws. There was a major radiation of these polychaetes during the Ordovician and the earliest suggested polychaete fossils are from the Cambrian. The simultaneous expression of tidal and circadian rhythmicity is characteristic of intertidal animals and it is likely that this complex behavioural repertoire was found in the ancestors of modern terrestrial forms, such as tetrapods and arthropods, prior to their emergence onto land during the Carboniferous and Silurian periods at least 400 Ma. The period of the earth's rotation, and hence day length and tidal period, has long been known to be increasing, and additionally the moon to be retreating from the earth, due to the phenomenon of tidal friction caused by the gravitational interactions between the moon and the earth. These changes are significant over a geological time scale. Consequently, the length of day was substantially less (and the number of days in a year more) than at present in the Cambrian and Ordovician periods. Recent theoretical analysis of the period of the earth's rotation suggests that the day length prior to a critical period (t _crit ) around 1800 Ma may have been stable, with a length of only 4 h. At that time a period of more rapid change in the dynamics of the rotation was initiated. The implications of this theory for the evolution of the biological clock are discussed.     

Seasonal changes in brain melatonin concentration in the three-spined stickleback (Gasterosteus aculeatus): towards an endocrine calendar

Pineal organ and its hormone melatonin (N-acetyl-5-methoxytryptamine) is likely involved in timing and synchronisation of many internal processes, such as reproduction, with annual changes in environmental cues, i.e., photoperiod and water temperature. The seasonal changes in melatonin profile in stickleback brains related to the following reproductive phases were examined, and the link between melatonin concentrations and the stages of spawning cycle was analysed. Two wild populations of sticklebacks were exposed to annual environmental changes in their natural habitats. Brains, gonads, kidneys and livers were collected over 2 years. Melatonin was measured using RIA and the indices, gonadosomatic (GSI), nephrosomatic (NSI) and hepatosomatic (HSI), were calculated. The role of melatonin, as a component of internal calendar engaged in the control of seasonal breeding in this species, is discussed. The extremely high melatonin levels observed in early spring (March) and autumn (October) seem to mark out a time frame for spawning in sticklebacks. The seasonal pattern of melatonin production and identified development stages of gonads suggests the potential inhibitory effect of the hormone on stickleback reproduction in shortening photoperiod and stimulatory effect in lengthening photoperiod.     

Climate change and seasonal reproduction in mammals

Seasonal reproduction is common among mammals at all latitudes, even in the deep tropics. This paper (i) discusses the neuroendocrine pathways via which foraging conditions and predictive cues such as photoperiod enforce seasonality, (ii) considers the kinds of seasonal challenges mammals actually face in natural habitats, and (iii) uses the information thus generated to suggest how seasonal reproduction might be influenced by global climate change. Food availability and ambient temperature determine energy balance, and variation in energy balance is the ultimate cause of seasonal breeding in all mammals and the proximate cause in many. Photoperiodic cueing is common among long-lived mammals from the highest latitudes down to the mid-tropics. It is much less common in shorter lived mammals at all latitudes. An unknown predictive cue triggers reproduction in some desert and dry grassland species when it rains. The available information suggests that as our climate changes the small rodents of the world may adapt rather easily but the longer lived mammals whose reproduction is regulated by photoperiod may not do so well. A major gap in our knowledge concerns the tropics; that is where most species live and where we have the least understanding of how reproduction is regulated by environmental factors.     

Effects of temperature on reproductive output, egg provisioning, juvenile hormone and vitellogenin titres in the butterfly Bicyclus anynana

Environmentally induced phenotypic plasticity is common in nature. Hormones, affecting multiple traits and signaling to a variety of distant target tissues, provide a mechanistic link between environments, genes and trait expression, and may therefore well be involved in the regulation phenotypic plasticity. Here, we investigate whether in the tropical butterfly Bicyclus anynana temperature-mediated plasticity in egg size and number, with fewer but larger eggs produced at lower temperatures and vice versa, is under control of juvenile hormone, and whether different temperatures cause differences in egg composition. Female B. anynana butterflies showed the expected response to temperature, however, we found no evidence for an involvement of juvenile hormone. Neither haemolymph JH II and JH III titres nor vitellogenin levels differed across temperatures. The smaller eggs produced at the higher temperature contained relatively higher amounts of water, free carbohydrates and proteins, but relatively lower amounts of lipids. While these smaller eggs had a lower absolute energy content, total reproductive investment was higher at the higher temperature (due to a higher fecundity). Overall, our study indicates that temperature-mediated plasticity in reproduction in B. anynana is mechanistically related to a biophysical model, with oocyte production (differentiation) and oocyte growth (vitellogenesis) having differential temperature sensitivities.     

Female reproductive responses to photoperiod and male odours in the subterranean rodentCtenomys talarum

The tuco-tucoCtenomys talarum Thomas, 1898 is a solitary subterranean rodent that breeds seasonally in coastal sand-dune grasslands from Argentina. We assessed whether short-day photoperiod determines the onset of reproduction by an increase in female’s receptivity and whether male odour interacts with photoperiod as a cue by producing a greater response in receptivity. Receptivity was measured by an increase in the percentage of vaginal epithelial cells, particularly cornified cells. Females were trapped during their non-reproductive season (summer-long days) and randomly assigned to different day-length experimental groups: constant summer (CS), early winter (EW), and natural (NA) photoperiod. We examined the vaginal epithelium using vaginal smears during the first experimental phase (120 days) to test the effect of photoperiod. In the second experimental phase (15 days), we presented the females with male-soiled shavings to test the effect of photoperiod and male odor.Ctenomys talarum females showed some evidence of reproductive responsiveness to photoperiodic cuing. The proportion of epithelial cells peaked earlier in females when winter day-length was advanced than in females under natural photoperiod. Contrary to that expected, male odours did not stimulate female receptivity. These results suggest that, while photoperiod may participate in regulating reproduction, the integration of other environmental and social factors, as well as the identification of bodily conditions that lead to differences in individual response needs further consideration.     

Manipulation of photoperiod perception advances gonadal growth but not laying date in the great tit

In seasonal environments, organisms use biotic and abiotic cues to time various biological processes that are crucial for growth, survival and reproductive success. Photoperiod is the best‐known cue used to regulate gonadal development, migration and moult of many animal species. In birds, the relationship between photoperiod and gonadal development is clearly established, but we have little understanding on whether photoperiod also regulates actual timing of egg laying under natural conditions. Elucidating the link between photoperiod and timing of breeding is however key to understand whether an evolutionary change in sensitivity to photoperiod is a possible mechanism through which organisms could adjust their seasonal timing in response to climate warming. Here, we investigated the causal relationship between photoperiod, gonadal growth and laying date in wild female great tits. We experimentally increased the photoperiod perceived by the birds in spring by clipping head feathers, and we subsequently monitored gonadal development in the lab and egg laying dates in the wild. We show that our manipulation increased the photoperiod perceived by the birds to a level that approximately corresponds to an advancement of ten calendar days. This increase in perceived photoperiod led to an acceleration of gonadal development, but not to an advancement of egg laying dates. Our results indicate that photoperiod sensitivity is not constraining the advancement of laying date under current environmental conditions and suggest that evolution of sensitivity to other supplementary cues is necessary to advance reproduction under global warming.     

Photoperiod regulation of neuron death in the adult canary

The avian brain undergoes naturally occurring cell death and neuronal replacement in adulthood. Little is known about how neuron survival in adult birds is regulated. However, previous work suggests that this process is open to environmental control. We now report that a reduction in day length from springlike to fall-like conditions can dramatically increase cell death in adult male canaries. Many of the dying cells are projection neurons in the motor pathway controlling song learning and production. Circulating levels of gonadal steroids were not correlated with photoperiod-induced changes in the magnitude of cell death. Our results suggest that neuronal death in adult male canaries is regulated by seasonal changes in photoperiod, and that this occurs independent of chronic changes in gonadal steroid hormone levels. Day length may serve as a predictive environmental cue to time cell death in accordance with seasonal reproduction. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 223–231, 1997

1 This is a US Government work and, as such, is in the public domain in the United States of America.

     

Fruit abundance may fine-tune timing of reproduction of the Chilean Elaenia (Elaenia chilensis), a long-distance migratory bird in South America

Timing of reproduction has a great impact on the breeding success of birds because a mismatch with the moment when environmental conditions are warm or when food is most plentiful can reduce nestling survival and increase the energetic cost of parental care. Consequently, birds synchronize gonadal maturation with the most favourable environmental conditions, using photoperiod changes throughout the year as an initial proximal cue. Additionally, non-photic cues, such as temperature and food abundance, may be necessary to fine-tune reproductive timing. However, the influence of non-photic cues on finely tuning reproductive timing is not yet fully understood for migratory birds. Here, we evaluate how much non-photic cues influence the reproductive timing of the Chilean Elaenia Elaenia chilensis, a long-distance migrant that reproduces in the Andean–Patagonian Forest. We assessed associations of mean temperature, ripe fruit and arthropod abundances with the number of nests in the laying period, and also with the number of nests with hatchlings. In both analyses we used cross-correlations and partial least squares path modelling. Mean temperature was not consistently associated with the breeding phenology of Chilean Elaenias. The increase in number of nests in the laying period was preceded by the increase in caterpillar abundance and coincided with the increase in ripe fruit abundance. The timing of nests with hatchlings matched with the timing of highest ripe fruit abundance. Both types of food could contribute to the beginning of reproduction of birds and be used as proximal cues by Chilean Elaenias. Ripe fruits would also be beneficial for nestling growth because parents feed them with fruits, and might potentially play an ultimate role in reproduction. Because ripe fruit abundance was related to the egg-laying and hatching stages, it may be the main cue used by Chilean Elaenias to fine-tune reproductive timing. These findings allow advances in our understanding of the importance of non-photic cues in the reproductive phenology of migratory birds and also generalize our knowledge among regions and taxa, as most studies on this topic focus on the Northern Hemisphere.     

Juvenile Hormone Stimulation of Oocyte Development and Embryogenesis in the Parthenogenetic Ovaries of an Aphid,Aphis fabae

Summary

The parthenogenetic ovaries of the black bean aphid, Aphis fabae, contain developing embryos. When reared at 15°C in long days (LD 16:8) oocyte development begins within the ovaries of the largest embryos of a fourth instar mother 24–48 hr after her ecdysis from the third instar. Starvation, decapitation and precocene III treatment inhibit embryonic oocyte development; juvenile hormone treatment reverses this inhibition. A method for the in vitro culture of embryos is described and under these conditions juvenile hormone again stimulates oogenesis. Embryogénie growth in vivo, as measured by the increase in length of the oldest daughter embryos, is also stimulated by juvenile hormone treatment. The results are discussed in relation to other roles proposed for juvenile hormone in aphid development.     

Photoperiod regulates growth of male accessory glands through juvenile hormone signaling in the linden bug,Pyrrhocoris apterus

Adult reproductive diapause is characterized by lower behavioral activity, ceased reproduction and absence of juvenile hormone (JH). The role of JH receptor Methoprene-tolerant (Met) in female reproduction is well established; however, its function in male reproductive development and behavior is unclear. In the bean bug, Riptortus pedestris, circadian genes are essential for mediating photoperiodically-dependent growth of the male accessory glands (MAGs). The present study explores the role of circadian genes and JH receptor in male diapause in the linden bug, Pyrrhocoris apterus. These data indicate that circadian factors Clock, Cycle and Cry2 are responsible for photoperiod measurement, whereas Met and its partner protein Taiman participate in JH reception. Surprisingly, knockdown of the JH receptor neither lowered locomotor activity nor reduced mating behavior of males. These data suggest existence of a parallel, JH-independent or JH-upstream photoperiodic regulation of reproductive behavior.     

Effects of Juvenile Hormone and Precocene on the Reproduction of Brachionus calyciflorus

We studied the effects of juvenile hormone and precocene on reproduction of the rotifer Brachionus calyciflorus. Amictic females of B. calyciflorus that were 2‐4 hours old were exposed to different concentrations of juvenile hormone (0.004, 0.02, 0.1, 0.5, 2.5, 12.5 mg/L) and/or precocene (0.05, 0.25, 0.75, 3.75, 7.5 mg/L) for 24 h. They were then transferred to a new medium without hormone and checked every 2 h during the next 48 h, and thereafter monitored daily until the individual died. Precocene had no effects on the length of the rotifer juvenile period, hatching time of the first neonate, lifetime reproduction, or the mixis ratio. In contrast, juvenile hormone at 0.5, 2.5, and 12.5 mg/L significantly prolonged the juvenile period by 6.1, 9.2, and 8.6%, respectively. When 26‐28‐h‐old amictic females were exposed to the same concentration series of juvenile hormone or precocene, precocene at 3.75 mg/L resulted in an increase in lifetime reproduction of 30.39%. However, at 0.75 and 3.75 mg/L precocene, a significantly lower percentage of mictic females was found, whereas juvenile hormone had no effect on the lifetime reproduction or mixis ratio. The population growth test showed that juvenile hormone had significant effects on the population growth rate and mixis ratio, but no effect on resting egg production. In comparison, precocene had no effect on any of these parameters. (© 2012 WILEY‐VCH Verlag GmbH & Co. KGaA, Weinheim)     

Photoperiodicity and increasing salinity as environmental cues for reproduction in desert adapted rodents

Understanding the ways environmental signals, regulate reproduction and reproductive behavior of desert adapted rodents is a major gap in our knowledge. In this study, we assessed the roles of photoperiod and diet salinity, as signals for reproduction. We challenged desert adapted common spiny mice, Acomys cahirinus, males and females with osmotic stress, by gradually increasing salinity in their water source - from 0.9% to 5% NaCl under short and long days (SD and LD, respectively). Photoperiodicity affected testosterone levels, as under LD-acclimation, levels were significantly (p<0.05) higher than under SD-acclimation. Salinity treatment (ST) significantly reduced SD-acclimated male body mass (W(b)) and testis mass (p<0.005; normalized to W(b)). ST-LD-females significantly (p<0.005) decreased progesterone levels and the numbers of estrous cycles. A reduction in white adipose tissue (WAT) to an undetectable level was noted in ST-mice of both sexes under both photoperiod regimes. Receptors for vasopressin (VP) and aldosterone were revealed on testes of all male groups and on WAT in control groups. Our results suggest that photoperiod serves as an initial signal while water availability, expressed by increased salinity in the water source, is an ultimate cue for regulation of reproduction, in both sexes of desert-adapted A. cahirinus. We assume that environmental changes also affect behavior, as water seeking behavior by selecting food items, or locomotor activity may change in extreme environment, and thus indirectly affect reproduction and reproductive behavior. The existence of VP and aldosterone receptors in the gonads and WAT suggests the involvement of osmoregulatory hormones in reproductive control of desert adapted rodents.