Seasonal adaptations and the role of lipids in oceanic zooplankton

Oceanic zooplankton species exhibit quite diverse life history traits. A major driving force determining their life strategies is the seasonal variability in food supply, which is most pronounced in polar oceans where fluctuations in primary production are extreme. Seasonal adaptations are closely related to the trophic level of zooplankters, with strongest pressures occurring on herbivorous organisms. The dominant grazers, calanoid copepods and krill (Euphausiacea), have developed fascinating solutions for successful overwintering at higher latitudes. They usually exhibit a very efficient storage and utilization of energy reserves to reduce the effect of a highly seasonal primary production. The predominant larger Calanus species from the Arctic and Calanoides acutus from the Antarctic biosynthesize large amounts of high-energy wax esters with long-chain monounsaturated fatty acids and alcohols (20:1 and 22:1 isomers) as major components. They survive the dark season at depth in a stage of dormancy called diapause. In contrast, the Antarctic Calanus propinquus, a winter-active species, synthesizes primarily triacylglycerols, which are dominated by long-chain monounsaturated fatty acids with 22 carbon atoms (2 isomers) and yield even higher calorific contents. The omnivorous and carnivorous species, which are less subjected to seasonal food shortage, usually do not exhibit such an elaborate lipid biosynthesis. Herbivores usually do not utilize much of their enormous lipid reserves for overwintering, but channel this energy towards reproductive processes in late winter/early spring. Timing of reproduction is critical especially at high latitudes due to the short production period, and lipid reserves ensure early spawning independent of external resources. These energetic adaptations (dormancy, lipid storage) are supplemented by other life strategies such as extensive vertical migrations, change in the mode of life, and trophic flexibility.     

Evolution of the Arctic Calanus complex: an Arctic marine avocado?

Before man hunted the large baleen whales to near extinction by the end of the nineteenth century, Arctic ecosystems were strongly influenced by these large predators. Their main prey were zooplankton, among which the calanoid copepod species of the genus Calanus, long considered key elements of polar marine ecosystems, are particularly abundant. These herbivorous zooplankters display a range of adaptations to the highly seasonal environments of the polar oceans, most notably extensive energy reserves and seasonal migrations to deep waters where the non-feeding season is spent in diapause. Classical work in marine ecology has suggested that slow growth, long lifespan and large body size in zooplankton are specific adaptations to life in cold waters with short and unpredictable feeding seasons. Here, we challenge this understanding and, by using an analogy from the evolutionary and contemporary history of the avocado, argue that predation pressure by the now nearly extinct baleen whales was an important driving force in the evolution of life history diversity in the Arctic Calanus complex.     

Early is better: seasonal egg fitness and timing of reproduction in a zooplankton life-history model

Timing of reproduction influences future prospects of offspring and therefore the reproductive value of parents. Early offspring are often more valuable than later ones when food availability and predation risk fluctuate seasonally. Marine zooplankton have evolved a diversity of life history strategies in response to seasonality. We present a state-dependent life history model for the annual and herbivorous high-latitude copepod Calanoides acutus . Individuals are characterised by four states; developmental stage, structural size, energy reserves and vertical location. There are two habitats, a surface habitat with seasonal predation risk and food availability, and a safer deep habitat with no food and low metabolism (diapause). Optimal life histories (diapause and energy allocation strategies) are found by dynamic programming. Seasonal egg fitness (reproductive value) emerges from the model and peak values are typically before the feeding season. Disentangling the fitness components, we conclude that seasonality in egg fitness is caused both by environmental seasonality in food and predation risk and by time-constraints on development and diapause preparation. Realised egg production, as predicted from population simulations, does not match the seasonal peak in offspring fitness but is delayed relative to peak egg fitness. We term this an 'internal life history mismatch' as constraints and tradeoffs cause sub-optimal birth dates for most eggs whereas mothers maximise their reproductive value by high number of eggs rather than few and optimally timed eggs. The earliest eggs have a disproportionately high contribution to population recruitment, emphasising the importance of early eggs and the need to understand seasonal patterns in offspring fitness.     

The adaptive value of energy storage and capital breeding in seasonal environments

Timing of reproduction in a seasonal cycle is a life history trait with important fitness consequences. Capital breeders produce offspring from stored resources and, by decoupling feeding and reproduction, may bend the constraints caused by seasonality in food or predation. Income breeders, on the other hand, produce offspring from concurrent food intake, with the disadvantage of less flexibility, but with high efficiency and no inventory costs of carrying stores. Here, we assess relative profitability of capital and income breeding in herbivorous zooplankton inhabiting seasonal, high-latitude environments. We apply a state-dependent life history model where reproductive values are used to optimise energy allocation and diapause strategies over the year. Three environmental scenarios were modelled: an early, an intermediate, and a late feeding season. We found that capital breeding was most important in the early season. Capital breeding ranged from 7–9% of the eggs produced but, because of the high reproductive value of early eggs, capital breeding ranged from 9–30% when measured in terms of reproductive value. The main benefit of capital breeding was reproduction prior to the feeding season – when the reproductive value of an egg peaked. In addition, capital breeding was also used to increase egg production rates at times of income breeding. For individuals born late in the season the model predicted a two-year cycle instead of the typical annual life cycle. These individuals could then reap the benefits of early reproduction and capital breeding in their second year instead of income breeding late in the first year. We emphasize the importance of evaluating reproductive strategies such as capital and income breeding from a complete life cycle perspective. In particular, knowing the seasonality in offspring fitness is essential to appreciate evolutionary and population-level consequences of capital breeding.     

A review of reproductive strategies in cephalopods

Cephalopod reproductive strategies are reviewed in order to clarify their current, confusing status. Based on the type of ovulation, spawning pattern and growth between egg batches or spawning periods, five comprehensive and flexible cephalopod reproductive strategies are defined. Accordingly, with these three factors the following classification is proposed. (a) Spawning once (formerly semelparity) consisting of simultaneous terminal spawning, with synchronous ovulation, monocyclic spawning and absence of growth between egg batches. (b) Spawning more than once (formerly iteroparity) including: (i) polycyclic spawning with egg-laying occurring in separate batches during the spawning season and growth occurring between production of egg batches and spawning seasons; (ii) multiple spawning, with group-synchronous ovulation, monocyclic spawning and growth between egg batches; (iii) intermittent terminal spawning, with group-synchronous ovulation, monocyclic spawning and no growth between egg batches; (iv) continuous spawning, with asynchronous ovulation, monocyclic spawning and growth between egg batches. Examples of species exhibiting each of these reproductive strategies are given. The large amount of inter-species variation in several life-history traits related to reproductive events is discussed.     

Female investment in offspring size and number shifts seasonally in a lizard with single-egg clutches

The timing of reproduction strongly influences reproductive success in many organisms. For species with extended reproductive seasons, the quality of the environment may change throughout the season in ways that impact offspring survival, and, accordingly, aspects of reproductive strategies may shift to maximize fitness. Life-history theory predicts that if offspring environments deteriorate through the season, females should shift from producing more, smaller offspring early in the season to fewer, higher quality offspring later in the season. We leverage multiple iterations of anole breeding colonies, which control for temperature, moisture, and food availability, to identify seasonal changes in reproduction. These breeding colonies varied only by the capture date of the adult animals from the field. We show that seasonal cohorts exhibit variation in key reproductive traits such as inter-clutch interval, egg size and hatchling size consistent with seasonal shifts in reproductive effort. Overall, reproductive effort was highest early in the season due to a relatively high rate of egg production. Later season cohorts produced fewer, but larger offspring. We infer that these results indicate a strategy for differential allocation of resources through the season. Females maximize offspring quantity when environments are favorable, and maximize offspring quality when environments are poor for those offspring. Our study also highlights that subtle differences in methodology (such as capture date of study animals) may influence the interpretation of results. Researchers interested in reproduction must be conscious of how their organism’s reproductive patterns may shift through the season when designing experiments or comparing results across studies.     

Seasonal variations in the total lipid content of Chorismus antarcticus (Pfeffer) (Crustacea: Decapoda) at South Georgia

The Antarctic benthic prawn Chorismus antarcticus (Pfeffer) was sampled regularly for a year and its total lipid content measured. Immature and transitional prawns had very variable lipid contents but similar mean values (2.92 and 2.91 % fresh wt, respectively); the variation was, in part, due to fluctuations in lipid reserves associated with ecdysis. Maturation of the testes involved the synthesis of ≈ 1.8 mg lipid, and female prawns synthesized an average of 50 % of their own lipid content for the gonad. Fecundity did not appear to be limited by the demand for egg lipid and synchrony in the breeding cycle was probably related to the planktonic feeding of the newly-hatched larvae. Eggs showed an unusual increase in total lipid content during the early stages of embryonic development, followed by the more normal decrease; larvae probably hatch with some reserve lipid.Available data on lipid contents of Antarctic crustaceans are briefly reviewed. The high lipid contents observed in herbivorous Antarctic planktonic crustaceans are due to the patterns of feeding imposed by the strongly seasonal nature of primary production in Antarctic waters, rather than low temperature per se. There is no evidence from the benthos of any systematic elevation of lipid content in polar species, although there is an indication of an increased lipid content in the muscle of polar crustaceans.     

Spawning of bluefin tuna in the black sea: historical evidence, environmental constraints and population plasticity

The lucrative and highly migratory Atlantic bluefin tuna, Thunnus thynnus (Linnaeus 1758; Scombridae), used to be distributed widely throughout the north Atlantic Ocean, Mediterranean Sea and Black Sea. Its migrations have supported sustainable fisheries and impacted local cultures since antiquity, but its biogeographic range has contracted since the 1950s. Most recently, the species disappeared from the Black Sea in the late 1980s and has not yet recovered. Reasons for the Black Sea disappearance, and the species-wide range contraction, are unclear. However bluefin tuna formerly foraged and possibly spawned in the Black Sea. Loss of a locally-reproducing population would represent a decline in population richness, and an increase in species vulnerability to perturbations such as exploitation and environmental change. Here we identify the main genetic and phenotypic adaptations that the population must have (had) in order to reproduce successfully in the specific hydrographic (estuarine) conditions of the Black Sea. By comparing hydrographic conditions in spawning areas of the three species of bluefin tunas, and applying a mechanistic model of egg buoyancy and sinking rate, we show that reproduction in the Black Sea must have required specific adaptations of egg buoyancy, fertilisation and development for reproductive success. Such adaptations by local populations of marine fish species spawning in estuarine areas are common as is evident from a meta-analysis of egg buoyancy data from 16 species of fish. We conclude that these adaptations would have been necessary for successful local reproduction by bluefin tuna in the Black Sea, and that a locally-adapted reproducing population may have disappeared. Recovery of bluefin tuna in the Black Sea, either for spawning or foraging, will occur fastest if any remaining locally adapted individuals are allowed to survive, and by conservation and recovery of depleted Mediterranean populations which could through time re-establish local Black Sea spawning and foraging.     

The biology, life cycle and ecophysiology of the Antarctic mite Alaskozetes antarcticus

This paper is dedicated to the late Nigel Bonner, who as Head of the Life Sciences Division at British Antarctic Survey, encouraged and supported this research with his characteristic enthusiasm.
The cryptostigmatid mite Alaskozetes antarcticus (Michael) is a dominant member of many terrestrial communities in the maritime Antarctic, where it survives extreme temperatures, short cold summers, numerous freeze-thaw cycles, desiccating conditions and a limited season for growth and reproduction. However, examination of features of its biology, from morphology, through life-history strategy to physiology, indicate very little specialization to the Antarctic environment. Alaskozetes antarcticus is a herbivore/detritivore, typical of the Cryptostigmata in general, with low feeding and growth rates, long life span and low reproductive output. Physiological specializations exist in the form of low enzyme activation energies and elevated metabolic rates at low temperatures when compared with temperate species, and associated low optimum temperatures for activity, feeding and growth. Growth rates comparable with temperate species are achieved in the field, with an extended life cycle of five years or more as a result of the short growing season, and the ability of all life stages to overwinter equally successfully. Overwintering survival, involving supercooling enhanced by the use of antifreezes such as glycerol, although initially described in Antarctic species, is now known to be characteristic of many temperate relatives, so it is not a specific adaptation to the polar environment. The obvious success of A. antarcticus in maritime Antarctic terrestrial environments must be attributed to a combination of several features characteristic of the Cryptostigmata in general, rather than to specific polar adaptations.     

Life strategy, ecophysiology and ecology of seaweeds in polar waters

Polar seaweeds are strongly adapted to the low temperatures of their environment, Antarctic species more strongly than Arctic species due to the longer cold water history of the Antarctic region. By reason of the strong isolation of the Southern Ocean the Antarctic marine flora is characterized by a high degree of endemism, whereas in the Arctic only few endemic species have been found so far. All polar species are strongly shade adapted and their phenology is finely tuned to the strong seasonal changes of the light conditions. The paper summarises the present knowledge of seaweeds from both polar regions with regard to the following topics: the history of seaweed research in polar regions; the environment of seaweeds in polar waters; biodiversity, biogeographical relationships and vertical distribution of Arctic and Antarctic seaweeds; life histories and physiological thallus anatomy; temperature demands and geographical distribution; light demands and depth zonation; the effect of salinity, temperature and desiccation on supra-and eulittoral seaweeds; seasonality of reproduction and the physiological characteristics of microscopic developmental stages; seasonal growth and photosynthesis; elemental and nutritional contents and chemical and physical defences against herbivory. We present evidence to show that specific characteristics and adaptations in polar seaweeds help to explain their ecological success under environmentally extreme conditions. In conclusion, as a perspective and guide for future research we draw attention to many remaining gaps in knowledge. Dedicated to Prof. Dr. Gunter O. Kirst and to Prof. Dr. Klaus Lüning on occasion of their retirement 28. Februar 2006 and 31. March 2006, respectively.     

Maturity and spawning pattern of Sardinella aurita in relation to water temperature and zooplankton abundance off Ghana, West Africa

Studies on the maturity and spawning pattern of Sardinella aurita Valenciennes in relation to sea surface temperature (SST) and zooplankton abundance were carried out during the period 1986–91 in Ghanaian waters (West Africa). Both sexes exhibited synchronous seasonal maturation patterns. The mean length at first maturity occurred at approximately16.7 cm for males and 17.1 cm for females. The mean length at first maturity (L₅₀) increased in comparison with that observed in the 1970s. Three spawning seasons were identified: a major season which extends from July to October, and two minor seasons which occur in March and December. Significant correlations were found between the female gonadosomatic index and SST, between egg abundance and SST, and between egg abundance and zooplankton abundance. The SST seems to be an important factor in species maturation. There is a time lag between attainment of peak gonad maturation and onset of spawning. Spawning appears to commence in response to the start of the coastal upwelling which is characterised by a sharp decrease in SST and an increase in zooplankton abundance.     

Population dynamics of the ubiquitous Antarctic benthic amphipod Orchomenella franklini and its vulnerability to environmental change

Comprehensive ecological research is still lacking for many of the species that dominate the Antarctic benthos, preventing an adequate understanding of their potential response to environmental change. Here, population dynamics were explored in one of the most ubiquitous nearshore Antarctic benthic amphipods, Orchomenella franklini. Sex, reproductive status and body length were recorded for over 6,000 individuals, sampled from a variety of locations and times at Casey station in East Antarctica. Several life history traits were revealed for O. franklini that exemplify adaptations predicted for a polar environment. These include delayed reproduction, extended brood incubation, low fecundity, longevity and seasonal breeding linked to the summer phytoplankton bloom. There was also preliminary evidence of inter-annual and spatial fluctuations in population structure, potentially reflecting local environmental heterogeneity such as sea-ice duration. The influence of both large scale and local environmental conditions on the ecology of O. franklini provides insight into the vulnerability of this species to environmental change.     

The reproductive biology of some serolid isopods from the Antarctic

Summary Several species of serolid isopod from Signy Island, South Orkney Islands and also from South Georgia were studied, and aspects of their reproductive behaviour and associated morphology are discussed. InSerolis polita Pfeffer egg-laying took place at a mean age of 28 months, and the eggs were then incubated in a ventral marsupium for a period of 20 months before the release of juveniles in the spring. The mean egg dry weight at spawning was 0.68 mg forS. polita and 3.35 mg forSerolis cornuta Studer. The egg weight increased during marsupial development due to the uptake of minerals, but the total calorific content fell. Within each species brood size was linearly related to female size and the mean number of eggs varied from 40 forS. polita to 232 forSerolis pagenstecheri Pfeffer. There was no detectable marsupial mortality.S. polita appeared to breed repeatedly at two-year intervals, butS. cornuta probably only breeds once. The reproductive biology of Antarctic serolids is compared with that of temperate isopods, and it is shown that they produce larger young which is related to their larger adult size. The extremely protracted period of marsupial incubation is associated with the need to synchronize reproduction with the seasonal nature of Antarctic primary production.     

Variations in clutch and egg sizes in the amphidromous goby <Emphasis Type="Italic">Rhinogobius</Emphasis> sp. CB along a river course and within a spawning season

Rhinogobius sp. CB is a common amphidromous goby in Japan. I investigated egg and clutch sizes along a river course and within a spawning season in the Aizu River, Kii Peninsula, Japan. Clutch size within the same female size did not differ along the course of the river, but decreased from early to later in the spawning season. Egg size within the same female size decreased from early to later in the spawning season and from the upper to the lower reaches. These results mean energy resources allocated to the ovary decreased seasonally and locally. Several factors are presented to explain these variations, such as female somatic conditions, a tradeoff between reproduction and growth, food availability, water temperature, and presence of competitive species. Some factors explaining the seasonal and local variations in egg size, such as water temperature and food availability for offspring, are also presented. Egg size correlated well with female size. The trend in egg size variation with female size seems to be an adaptation for their migrating pattern, as larvae from larger female, which tended to inhabit the upper reaches, would have a greater endurance against starvation during their migration to the sea.     

The effect of food limitation on gonad development and egg production of the planktonic copepod Calanus finmarchicus

Calanus finmarchicus, one of the dominant copepods species of the North Atlantic, often encounters low food concentration or quality during the reproductive period; however, our knowledge on the effect of these conditions on reproduction processes is scarce. The present study combines experiments with histological observations to describe the response of C. finmarchicus to limited food focussing on (1) oocyte maturation processes, (2) gonad morphology, (3) egg production rates as a function of spawning frequency and clutch size, and (4) the fuelling of egg production by measuring carbon and nitrogen content of the females. In the laboratory, C. finmarchicus females were exposed to 0, 10, 50, 150 or >300 μg C l⁻¹ for several days. To account for food quality and season, reproductive activity was compared in April and July 1999 between females feeding on diatoms or dinoflagellates. The effect of feeding history was studied in February with females fed and starving prior to the experiment. Feeding conditions had severe effects on oocyte maturation process. Hence, egg production varied significantly with food concentration and quality, season and feeding history due to variation in both clutch size and spawning frequency. Clutch size differed by a factor of 2-4 between food limited and well fed females, and is thus an important parameter for modelling egg production. Changes in clutch size were related to changes of the number of maturing oocytes in the females gonads indicating that the latter can be used to precise the prediction of egg production from preserved samples. The proportion of females carrying at least some mature oocytes was relatively high at low food availability. Apparently, these females used internal body reserves as the carbon and nitrogen content decreased significantly under these conditions. These results indicate that C. finmarchicus embarks on the strategy to enable reproduction in all or many females of a population at low rates when feeding conditions are unfavourable.     

Seasonal and spatial variations in the zooplankton community of an Eastern Antarctic coastal location

Summary The zooplankton community of a shallow coastal area in Eastern Antarctica was found to be one of low species diversity dominated by Copepoda. It was comprised of the more common Antarctic oceanic copepod species, medusae, molluscs, euphausiids, several copepod species associated with the ice-water interface and, in summer, benthic fauna larvae. Most species of copepods displayed a marked seasonality in abundance with peak numbers between March and May. It is proposed that several factors, including phytoplankton seasonality contribute to the zooplankton species composition, zooplankton seasonality, and to the temporal differences in the period of maximum abundance between copepod species. Annual vertical migratory behaviour in conjunction with the circulation of Prydz Bay are important determining factors for those species which can be considered as oceanic; Calanoides acutus, Calanus propinquus, Ctenocalanus citer, Metridia gerlachei, Oithona similis and Oncaea curvata. However, for copepod species which can be classified as inshore residents, such as Stephos longipes, Paralabidocera antarctica and Drepanopus bispinosus, it is their association with the ice water interface that determines their seasonal appearance and abundance. Some differences were established between the zooplankton community of the Vestfold Hills and that of other Antarctic coastal regions. This may be attributed, in part, to the extensive shallow areas of the Vestfold Hills coastal region. Spatial distribution of the zooplankton with depth and between sites was investigated and found to be essentially homogenous. When differences were established, in the majority of cases all species present, all age classes and both sexes contributed to the differences.     

Seasonal effects on egg production and level of paternity in a natural population of a simultaneous hermaphrodite snail

In a seasonal environment, the suitable time window for females to reproduce is restricted by both environmental conditions and the availability of males. In simultaneous hermaphrodites, which are female and male at the same time, selection on a trait that is solely beneficial for one sexual function cannot occur independently. Therefore, it is assumed that the optimal time window for reproduction is a compromise between the two sexual functions in simultaneous hermaphrodites, mediated by environmental conditions. We examined seasonal patterns of reproduction and the resulting paternity in a natural population of the simultaneously hermaphroditic land snail Arianta arbustorum. Adult and premature individuals (snails in a short protandric phase) were collected on four occasions over the entire active season. The snails were allowed to deposit eggs after which we assessed the level of paternity in their hatched offspring. Individuals mated throughout the reproductive season, whereas egg production – the major task of the female function – was restricted to the first half of the season. Snails collected in autumn were allowed to hibernate under laboratory conditions. As a result, we found that premature individuals began to mate late in the reproductive season, but did not start to produce eggs before emerging from hibernation. Our results demonstrate a temporal shift of reproductive activities; the egg production and oviposition occur mainly in the first half of the season, while sperm production and mating occur over the entire season. In subadult and adult snails, sperm obtained from several partners in the second part of the reproductive season are stored during hibernation for the fertilization of eggs in the successive years. These results extend our understanding of the influence of both natural and sexual selection on reproductive strategies in hermaphrodites.     

Reproduction mode of European Bitterling (Rhodeus amarus,Bloch, 1782) determined through rapid oocyte counts and size determination using digital imaging

This study focuses on assessing the reproduction mode of an important model species for evolutionary and behavioural ecology by using digital image analysis: the European bitterling Rhodeus amarus (Bloch, 1782). Specifications of mode of reproduction were determined using oocyte size distribution, seasonal dynamics in mean oocyte diameter and total number of oocytes in ovary samples gained from April to July 2007. The rapid oocyte count was enabled by using lucia image analysis software, which also provided measurement and colour estimations of oocytes. Bitterling ovaries showed features typical for indeterminate spawners, i.e. a continuous distribution of oocyte size over the reproductive season and recruitment of new pre‐vitelogenic oocytes in the second half of the reproductive season. These results are consistent with the view that the European bitterling is a batch spawning fish with indeterminate fecundity.     

Observations on the seasonal breeding biology and fine structure of the egg surface in the white piranha Serrasalmus brandtii from the São Francisco River basin,Brazil

In the Juramento Reservoir, south‐eastern Brazil, the white piranha Serrasalmus brandtii showed a prolonged reproductive season, with evidence for multiple spawning and a reproductive peak associated with seasonal rains. The egg surface exhibited a honeycomb‐like pore canal arrangement and an adhesive apparatus surrounding the micropyle. Electron microscopic analysis suggests a role for the micropylar cell and neighbouring follicular cells in secretion of substances for egg attachment.     

The Behaviour of the Mediterranean Tripterygion Species (Pisces,Blennioidei)

The behaviour of the three mediterranean benthic fish Tripterygion tripteronotus, T. xanthosoma, and T. melanurus is described from observations in the field and observations on captive animals. The ♂♂ defend a territory only during the reproductive season; ♀♀ do not defend a territory. At the height of the breeding season, a male T. tripteronotus on average spawns with four ♀♀ Per day. The ♂ defends the territory against egg predators and cleans the eggs. ♀♀ spawn repeatedly during a spawning season. A spawning pair of T. tripteronotus frequently attracts conspecifics. The majority of these “satellites” are small, sexually mature ♂♂, which do not own a territory themselves. The reproductive strategies of the two types of ♂♂ (territorial ♂♂ and satellite ♂♂) and of the ♀♀ are discussed. On the basis of ethological, morphological, and palaegeographic data the evolution of the eastern-atlantic and mediterranean Tripterygiidae is reconstructed. A bibliography of the literature on eastern-atlantic and mediterranean Tripterygiidae is given. As in their morphology and anatomy, benthic fish show convergent adaptations in their behaviour. Some of these are pointed out and discussed.