Non-consumptive effects of predator presence on copepod reproduction: insights from a mesocosm experiment

Reproduction in planktonic animals depends on numerous biotic and abiotic factors. One of them is predation pressure, which can have both direct consumptive effects on population density and sex ratio, and non-consumptive effects, for example on mating and migration behaviour. In copepods, predator vulnerability depends on their sex, motility pattern and mating behaviour. Therefore, copepods can be affected at multiple stages during the mating process. We investigated the reproductive dynamics of the estuarine copepod Eurytemora affinis in the presence and absence of its predator the mysid Neomysis integer in a mesocosm experiment. We found that the proportion of ovigerous females decreased in the presence of predators. This shift was not caused by differential predation as the absolute number of females was unaffected by mysid presence. Presence of predators reduced the ratio of males to non-ovigerous females, but not by predation of males. Our combined results suggest that the shift from ovigerous to non-ovigerous females under the presence of predators was caused by either actively delayed egg production or by shedding of egg sacs. Nauplii production was initially suppressed in the predation treatment, but increased towards the end of the experiment. The proportion of fertilized females was similar in both treatments, but constantly fell behind model predictions using a random mating model. Our results highlight the importance of non-consumptive effects of predators on copepod reproduction and hence on population dynamics.     

Adjusting the timing of hatching to changing environmental conditions has fitness costs in blue tits

After laying the first egg, a bird can, to a certain extent, adjust the hatching date of the brood to environmental conditions. However, costs of this adjustment have remained largely unexplored. We studied potential costs of hatching delay in a population of blue tits in southern Finland. We explored the factors underlying hatching delay and investigated the association between hatching delay, clutch hatchability and female body condition. Finally, we reciprocally cross-fostered a large number of broods irrespective of their experienced hatching delay to address possible downstream effects of hatching delay on developmental parameters in offspring. We found that hatching delay was associated with early laying dates and low mean temperatures during the egg-laying phase. Furthermore, we found evidence that delayed hatching negatively affected the breeding performance. Hatchability of the clutch was lowered and the breeding female was energetically impaired, resulting in smaller clutch sizes, lower female body mass at hatching and lowered survival of nestlings reared in nests that had experienced a long hatching delay. In addition, delayed hatching had a significant negative effect on the body mass of nestlings prior to fledging. However, ultimately we did not find evidence that delayed hatching affected survival of the breeding female nor recruitment of fledglings in the local breeding population. Our study demonstrates that environmental conditions during egg laying can have lasting effects throughout the breeding and nestling phase. Furthermore, our results emphasize the importance of energetic tradeoffs by breeding females during the early breeding phase to manage reproductive costs.     

The diatom Thalassiosira rotula affects reproductive success in the copepod Acartia clausi

Fecundity, egg viability and fecal pellet production are reported for Acartia clausi females collected in the Bay of Naples, Italy, from April to October 1992 and fed either with a diatom (Thalassiosira rotula) or dinoflagellate (Prorocentrum minimum) diet, at food saturated conditions. The diatom diet significantly reduced both egg and fecal pellet production as well as hatching success. Blockage of egg development occurred with both axenic and non-axenic cultures of T. rotula, suggesting that inhibitors were provided by the diatoms and not by the bacteria associated with diatom cultures. Low hatching success was also artificially induced by exposing newly spawned A. clausi eggs to high concentrations of diatom extracts, indicating the presence of deleterious, inhibitory compounds blocking copepod embryogenesis. Fecundity and hatching success diminished significantly with female age. In contrast, female longevity was not significantly modified by food type. The presence of males did not significantly alter fecundity or egg viability. Females continued to produce viable eggs throughout the period of incubation, with and without males, in both food conditions, indicating that remating is infrequent and not necessary to sustain viable egg production in this species. The succession in low and high population densities may therefore be the outcome of variations in survival rates of eggs, rather than reproductive protential perse; such variations may strongly depend on the adult copepod diet.     

Long-term experiments on lifespan, reproductive activity and timing of reproduction in the Arctic copepod Calanus hyperboreus

Several experiments were conducted with starved and fed females of the Arctic copepod Calanus hyperboreus (1) to investigate their lifespan, reproductive period, egg production and egg viability; (2) to study the effect of origin, i.e., Atlantic and Arctic Waters in the Greenland Sea, on the timing of reproduction; and (3) to study the effect of time of collection on the onset of reproductive activity as a first approach to study control mechanisms of the reproductive cycle. Females collected in October produced up to 1,000 eggs and had a maximum lifespan of 164 days without feeding, whereas fed females produced up to ca. 6,000 eggs and survived up to 806 days. These observations support earlier assumptions that females were multiannual-iteroparous, i.e., capable to spawn in successive years, which would be unique for calanoid copepods. In starved females, clutch size decreased significantly with each spawning event. Viable eggs were produced during most of the life time. There was no difference in the timing of reproductive activity between females from the West Spitsbergen Current and the Greenland Sea Gyre. Fed and starved females collected in May and June began to spawn circa 2 and 4 months after collection, respectively, whereas females collected in August and October started spawning at the same time, in the middle of October. This indicates initiation of reproductive activity in the field in August, coincident with the descent into deep waters. Potential cues for the untimely spawning of females collected in spring and ‘unnatural’ feeding in fall experiments are discussed. Their large size, robustness and combination of different types of diapause in their life cycle make C. hyperboreus a good model organism to study diapause control mechanisms.     

Environmental cues and constraints affecting the seasonality of dominant calanoid copepods in brackish, coastal waters: a case study of Acartia, Temora and Eurytemora species in the south-west Baltic

Information on physiological rates and tolerances helps one gain a cause-and-effect understanding of the role that some environmental (bottom–up) factors play in regulating the seasonality and productivity of key species. We combined the results of laboratory experiments on reproductive success and field time series data on adult abundance to explore factors controlling the seasonality of Acartia spp., Eurytemora affinis and Temora longicornis, key copepods of brackish, coastal and temperate environments. Patterns in laboratory and field data were discussed using a metabolic framework that included the effects of ‘controlling’, ‘masking’ and ‘directive’ environmental factors. Over a 5-year period, changes in adult abundance within two south-west Baltic field sites (Kiel Fjord Pier, 54°19′89N, 10°09′06E, 12–21 psu, and North/Baltic Sea Canal NOK, 54°20′45N, 9°57′02E, 4–10 psu) were evaluated with respect to changes in temperature, salinity, day length and chlorophyll a concentration. Acartia spp. dominated the copepod assemblage at both sites (up to 16,764 and 21,771 females m^?3 at NOK and Pier) and was 4 to 10 times more abundant than E. affinis (to 2,939?m^?3 at NOK) and T. longicornis (to 1,959?m^?3 at Pier), respectively. Species-specific salinity tolerance explains differences in adult abundance between sampling sites whereas phenological differences among species are best explained by the influence of species-specific thermal windows and prey requirements supporting survival and egg production. Multiple intrinsic and extrinsic (environmental) factors influence the production of different egg types (normal and resting), regulate life-history strategies and influence match–mismatch dynamics.     

Phytoplankton food quality determines time windows for successful zooplankton reproductive pulses

Recruitment success at the early life stages is a critical process for zooplankton demography. Copepods often dominate the zooplankton in marine coastal zones and are prey of the majority of fish larvae. Hypotheses interpreting variations of copepod recruitment are based on the concepts of "naupliar predation," "nutritional deficiency," and "toxic effect" of diatom diets. Contradictory laboratory and field studies have reached opposite conclusions on the effects of diatoms on copepod reproductive success, blurring our view of marine food-web energy flow from diatoms to higher consumers by means of copepods. Here we report estimates of copepod feeding selectivity and reproduction in response to seasonally changing phytoplankton characteristics measured in a highly productive coastal upwelling area off the coast of central Chile. The variable phytoplankton diversity and changing food quality had a strong and highly significant impact on the feeding selectivity, reproduction, and larval survival of three indigenous copepod species. Seasonal changes in copepod feeding behavior were related to the alternating protozoan-diatom diets, mostly based on dinoflagellates and ciliates during winter and autumn (low highly unsaturated fatty acids [HUFA]/polyunsaturated fatty acids [PUFA] availability), but switched to a diet of centric and chain-forming diatoms (high HUFA/PUFA availability) during the spring/summer upwelling period. Ingestion of diatom cells induced a positive effect on egg production. However, a negative relationship was found between egg hatching success, naupliar survival, and diatom ingestion. Depending on the phytoplankton species, diets had different effects on copepod reproduction and recruitment. In consequence, it seems that the classical marine food web model does not apply to some coastal upwelling systems.     

Effects of dissolved cyanobacterial toxins on the survival and egg hatching of estuarine calanoid copepods

Toxic cyanobacteria occur in fresh, brackish, and marine waters worldwide. Harmful effects of intact cyanobacterial cells on zooplankton are well known, but only a few studies have focused on the effects of dissolved toxins. We investigated experimentally how the cyanobacterial toxins anatoxin-a, microcystin-LR, and nodularin affect estuarine calanoid copepods, by monitoring effects on egg hatching and survival in Eurytemora affinis. We also investigated effects of nodularin on the survival of Acartia bifilosa. All exposures were carried out using purified dissolved toxins. We found that the egg hatching was unaffected by these toxins, whereas survival was marginally affected by high concentrations of anatoxin-a and nodularin. For microcystin-LR, we found reduced survival at concentrations that were lower than those known to affect other meso-zooplankton.     

Fate of domoic acid ingested by the copepod <Emphasis Type="Italic">Acartia clausi</Emphasis>

Two important issues in the studies of harmful algae include ecological role of the toxic compounds and their fate through the food web. The aims of this study were to determine whether the production of domoic acid is a strategy evolved to avoid predation and the role of copepods in the fate of this toxic compound through the food web. The copepod Acartia clausi was fed with single and mixed cultures of the toxic diatom Pseudo-nitzschia multiseries and the non-toxic diatom Pseudo-nitzschia delicatissima. Ingestion rate as a function of diatom abundance was the same for the toxic and non-toxic Pseudo-nitzschia species, indicating no selective feeding behaviour against P. multiseries. The toxins ingested by the copepods did not affect mortality, feeding behaviour, egg production and egg hatching of the copepods. Copepods assimilated the 4.8% of the total domoic acid ingested. Although the amount of toxins daily detoxificated by the copepods was 63.6%, the copepods accumulated domoic acid in their tissues. We conclude that domoic acid is not toxic for copepods and, probably for this reason, this toxin does not act as feeding deterrent for copepods. However, even though the production of domoic acid has apparently not evolved to deter predation, copepods may play an important role on the fate of this toxic compound through the marine food web.     

Temperature effects on fecundity,development and survival of the benthopelagic calanoid copepod, <Emphasis Type="Italic">Pseudocyclops xiphophorus</Emphasis>

The shallow-living, benthopelagic copepod species Pseudocyclops xiphophorus Wells (R Soc Edimburg 67:1967), collected over a yearly cycle from the fouling material in the brackish water Lake Faro (North-eastern Sicily), showed marked seasonal fluctuations in population abundances, with maximum numbers recorded in autumn. Highest in situ egg production rates coincided with periods of low adult and juvenile densities and vice versa, except in autumn when peaks in egg production and adult population densities were coincident. In this period, mean daily egg production rates reached a maximum of 4–5 eggs per female, when surface water temperature was 17–18°C. Egg production rates declined drastically in winter and were completely arrested when surface temperatures dropped to 10–12°C. In March, daily egg production rates began to increase again with an increase in ambient temperatures, reaching a maximum at the end of August. In the laboratory, as in the field, mean daily egg production rates were positively correlated with temperature, with values ranging from 2.2 ± 0.3 (16°C) to 8.9 ± 2.6 (30°C) (mean ± S.D.) eggs per female per day. At 32°C, P. xiphophorus females survived but did not reproduce. At 34°C, all specimens died after a few days. In terms of total egg production for the entire female lifespan, maximum values occurred at 16°C and minimum at 24°C. Temperature also dramatically affected female life span, which was shorter at higher temperatures. Development time of eggs decreased with increasing temperature, as also development time from egg to adulthood. Remating was necessary for the continued production of fertile eggs at 16°C because female life span was longer. The unique egg-laying behaviour in this species may ensure higher survival rates of egg stages compared to free-spawning and egg-carrying calanoid species. After releasing the egg pair, the female swims over the eggs with a rotatory motion, secreting a substance which facilitates the adhesion of the eggs to the bottom; she then continues to swim over the eggs until they are attached. Although egg production rates in this species are low compared to other pelagic copepods, they are within the range of values reported for egg-carrying species. The greater fecundity at higher temperatures compared to other subtemperate species indicates that the species is well adapted to the higher temperatures of coastal lagoons and brackish water lakes where it contributes to the biofouling community.     

Reproductive biology of the planktonic copepod Temora stylifera

Laboratory studies on the reproductive cycle of the planktonic copepod Temora stylifera, collected from the Gulf of Naples between October 1987 and March 1988, showed that females oscillated between a light and dark gonadal condition. Histological preparations indicated that the dark condition corresponded to a ripe stage of oogenesis as compared to the light or unripe maturation state of primary oocytes. The number of eggs released within 24 h was strongly dependent on the reproductive status of the female at the time of incubation. Light unfed females rarely reverted to a dark or ripe condition and egg deposition in such cases was almost always zero. Dark females produced eggs within 24 h under all experimental food conditions, reverting from dark to light soon after egg deposition. Successively, the length of the interclutch period was strongly dependent on the type of food present. A high percentage of infertile eggs was almost always present. We suggest that short-term studies, not taking into consideration the condition of gonads at the time of incubation, will underestimate potential egg production rates. Females maintained for longer than three or four days produced mainly infertile eggs. After remating, females reinitiated the production of fertile eggs but egg viabilities never reached 100% hatching success, indicating poor efficiency in the fertilization of mature oocytes. We hypothesize a possible cause and effect relationship between egg viabilities and seasonal fluctuations in population densities.Died tragically at sea during a cruise     

Strain-related physiological and behavioral effects of <Emphasis Type="Italic">Skeletonema marinoi</Emphasis> on three common planktonic copepods

Three strains of the chain-forming diatom Skeletonema marinoi, differing in their production of polyunsaturated aldehydes (PUA) and nutritional food components, were used in experiments on feeding, egg production, hatching success, pellet production, and behavior of three common planktonic copepods: Acartia tonsa, Pseudocalanus elongatus, and Temora longicornis. The three different diatom strains (9B, 1G, and 7J) induced widely different effects on Acartia tonsa physiology, and the 9B strain induced different effects for the three copepods. In contrast, different strains induced no or small alterations in the distribution, swimming behavior, and turning frequency of the copepods. 22:6(n-3) fatty acid (DHA) and sterol content of the diet typically showed a positive effect on either egg production (A. tonsa) or hatching success (P. elongatus), while other measured compounds (PUA, other long-chain polyunsaturated fatty acids) of the algae had no obvious effects. Our results demonstrate that differences between strains of a given diatom species can generate effects on copepod physiology, which are as large as those induced by different algae species or groups. This emphasizes the need to identify the specific characteristics of local diatoms together with the interacting effects of different mineral, biochemical, and toxic compounds and their potential implications on different copepod species.     

Copepod recruitment and food composition: do diatoms affect hatching success?

Laboratory experiments were conducted to differentiate between factors controlling the hatching success of copepod eggs. Factors that could affect viability of eggs; viz food quality, female condition and external factors were investigated. In a series of experiments the copepod Acartia tonsa Dana was fed several different diets while egg production and hatching success were monitored. The diet was analysed for fatty acid content as an indicator of food quality. Both egg production and hatching were found to be affected by the nutritional quality of the food. Hatching was also highly dependent on female fertility. External effects were tested by exposing eggs to diatom extracts. Negative effects were only evident at high extract concentrations, but disappeared when aeration was supplied to the solution. Oxygen measurements showed that failure to hatch was due to hypoxia in the extracts. No inhibitory or toxic effects of diatom cell components on hatching could be found.     

Seasonal and long-term variations in the body size of planktonic copepods in the northern Baltic Sea

Seasonal and long-term variations in the body size of planktonic copepods were studied in the northern Baltic Sea. The influence of temperature, salinity and phytoplankton concentration to the body size of Eurytemora affinis, Acartia bifilosa and Limnocalanus macrurus (Calanoida) was examined at three sea areas, differing in their hydrographical and trophic conditions (an archipelago area and an enclosed bay on the SW coast of Finland in 1992 and at an open sea station in the Gulf of Bothnia in 1991). There was an inverse relationship between copepod body length and temperature, while there was a direct effect of phytoplankton concentration. According to multiple regression analysis, the relative importance of these factors varied according to species, developmental stage and study area. In the archipelago area, copepod body size was mainly determined by temperature, while in the open Gulf of Bothnia, phytoplankton concentration was usually more important. Interannual variation in the summer body length of E. affinis and A. bifilosa was examined using samples collected over 18 years (1967 to 1984) in the archipelago area. In this analysis, the inverse relationship between water temperature and copepod body size disappeared; in E. affinis the average female length correlated positively with summer temperature. We suggest that the length and timing of the study period greatly influence the investigator's view of the factors regulating copepod body size.     

Carbon requirements of a population of the estuarine copepod Eurytemora affinis

The production of algae in the Patuxent River estuary (Maryland, USA) was much less than the carbon requirements of a population of the calanoid copepod Eurytemora affinis. Detrital carbon was present in quantities that suggest turnover times of 8 to 83 days for this pool, assuming that all algal production was consumed by E. affinis. We hypothesize that E. affinis must consume detritus to meet a part of its requirements for energy.     

Food supplementation affects egg albumen content and body size asymmetry among yellow-legged gull siblings

Parental decisions can determine offspring experience of environmental conditions. Such ‘maternal’ effects act both before and after hatching via, e.g., egg quality or the social milieu predisposed by parents. Resource availability may constrain the expression of adaptive maternal effects, and the specific pattern of allocation of these effects among offspring depending on their sex or birth order can result in different fitness payoffs to parents. Declining egg mass with laying order observed in several bird species may constitute an adaptive strategy of parental favouritism towards early hatching offspring with larger reproductive value but may also result from nutritional constraints on laying effort. A previous study has shown that the small size of the third, last laid (c-)egg in yellow-legged gull (Larus michahellis) clutches depends on food availability and that food-supplemented mothers increase the size of their female but not male c-eggs. Here, we show that increased mass of c-eggs laid by females supplemented with food after clutch initiation depends on increased albumen mass, which, in turn, enhances the size of daughters at hatching. Because asynchronous hatching results in a competitive disadvantage of c-chicks, present results suggest that mothers relieved from nutritional constraints enhance the size of daughters to compensate for their larger susceptibility to hatching last. The study also confirms the role of egg albumen content in determining hatchling size, previously experimentally detected only in one species in the wild. The effect of increased egg mass on offspring size persisted at least until day 8 after hatching, when, however, it did not vary with sex, suggesting intense negative selection on small female c-chicks in control broods. Hence, maternal effects mediated by egg albumen content had persistent effects on offspring size.     

Rapana venosa as an indicator species for TBT exposure over decadal and seasonal scales

Imposex and decline in reproductive output in marine gastropods have been linked to tributyltin (TBT) exposure. This study describes Chesapeake Bay, USA, veined rapa whelk Rapana venosa imposex incidence and sex ratios from 1998 to 2009. Tissue TBT concentrations (ng g^?1) were examined with respect to whelk sex, size, and water temperature at the time of collection, and also to egg case size, hatching success, and veliger diameter. Imposex incidence declined and population sex ratios moved closer to parity from 1998 to 2009. Observed TBT concentrations (ng g^?1) were higher in James River than in Ocean View whelks with higher TBT concentrations observed in males than in females. Exponential declines in TBT concentrations from female-specific first to last clutches within a reproductive season were observed, indicating that whelks depurate TBT through egg case deposition. Egg capsule hatching success and veliger size were similar for female and imposex whelks. The R. venosa imposex levels observed in Chesapeake Bay apparently do not affect the production, release, or viability of larvae.     

A comparative study of the inhibitory effect of diatoms on the reproductive biology of the copepod Temora stylifera

Egg production and viability in the copepod Temora stylifera (collected in the Bay of Naples, Italy in 1992) were strongly dependent on food type. A flagellate (Isochrysis galbana) diet induced the production of good quality eggs that developed to hatching. By contrast, two diatoms (Chaetoceros curvisetum, Phaeodactylum tricornutum) resulted in poor egg quality, with hatching success as low as 20% of total egg production. With the third diatom tested, Skeletonema costatum, females produced eggs for only 3 to 4 d, after which time they either became sterile or died. These results are discussed in relation to previous findings regarding the impact of the dinoflagellate Prorocentrum minimum and the diatom Thalassiosira rotula on the hatching success of T. stylifera eggs. Low egg viability was possibly not due to an absence of remating or a deficiency of some specific essential nutrient required for egg development but to the presence of inhibitory compounds blocking cell division during early copepod embryogenesis. This questions the traditional view that diatoms are an important food item regulating copepod secondary production.     

Reproductive biology of deep-water calanoid copepods from the Arctic Ocean

Reproductive modes and egg production were studied in 15 species of meso- and bathypelagic copepods from nine Calanoida families in the Arctic Ocean. During shipboard incubation, females of seven species released eggs freely into the water and females of three species produced membrane-bound egg sacs. One species, Aetideopsis rostrata, produced a mass of eggs looking like an egg sac, but the “sac” lacked a membrane and disintegrated within 2 h. Females of four additional species were encountered with membrane-bound egg sacs in the preserved samples. In most families, only one reproductive mode, either egg-carrying (the Euchaetidae, Augaptilidae), or broadcast spawning (the Heterorhabdidae, Spinocalanidae, Scolecitrichidae, Tharybidae, Bathypontiidae) was observed. In contrast, different genera of the Aetideidae family demonstrated different reproductive modes, with broadcast spawning predominant in the benthopelagic species, and both broadcast spawning and egg-brooding in the planktonic species. Clutch size and egg diameter varied widely between species in both broadcast spawners and egg-brooders. In broadcast spawners, the clutch size varied from 1 to 95 eggs female⁻¹, while the average egg diameter ranged from 152 to 440 μm. The clutch size for egg brooders varied between 3 and 82, while average egg diameter varied from 258 to 732 μm. Deep-water broadcast spawners produced much larger eggs compared to surface-dwelling broadcast spawning species. This larger egg size may result in a reduction, or elimination, of feeding during naupliar stages, thereby improving the survival potential of deep-water species.     

Zooplankton population model coupled to a biogeochemical model of the North Western Mediterranean Sea ecosystem

A stage structured population (SSP) model based on Fennel's [Fennel, W., 2001. Modelling copepods with links to circulation models. Journal of Plankton Research, 23, 1217–1232] equations is applied to Centropages typicus (Kröyer), a dominant copepod species of the North Western Mediterranean Sea (NWMS) and a prey of small pelagic fish. The model considers five groups of stages and development rates are represented by a mechanistic formulation depending on individual specific growth in each stage. Individual growth is calculated from the individual energy budget depending on food availability and temperature.     

Early development and estimated life cycle of the mesopelagic copepod Pareuchaeta elongata in the southern Japan Sea

Life cycle of the mesopelagic copepod Pareuchaeta elongata was investigated combining laboratory rearing data on the eggs, nauplii, and early copepodites with field growth data on the late copepodites. Examination and incubation at near the in situ temperature (0.5°C) of egg sacs collected from the field indicated that the clutch size was 13 to 24 eggs (mean: 20), hatching time was 39.4d (mean), and hatchability was low (mean: 28.5%). The development time at 0.5°C was 2.4 d for Nauplius Stage 1 (N1), 4.6 d for N2, 6.2 d for N3. 7.4 d for N4, 7.1 d for N5, 20.8 d for N6, 36.7 d for Copepodite Stage 1 (C1) and 65.3 d for C2. From the numerical analysis of seasonal samples collected from the field, the development time was estimated as 1 mo for C3, 2 mo for C4 and 2.5 mo for C5. Thus, the egg hatching time plus the integrated development time by stage was 355 d or nearly 1 yr (i.e. span of one life cycle). Duration of the C6 (adult) was estimated as>2.5 mo. Combining the present data on development times of each stage with published data on the major spawning season (August to October) and ontogenetic migration, a schematic representation of the life cycle of this copepod was developed. Between-stage comparison of wet, dry, and ash-free dry weights of all developmental stages of preserved wild specimens revealed that there is almost no gain in weight during naupliar stages, and the greatest weight increment over the life cycle was during the C4 stage. The present results are compared with those for the same and related species living in other regions.