Effects of temperature and phytoplankton community composition on subitaneous and resting egg production rates of Acartia omorii in Tokyo Bay

Population dynamics

The abundance of A. omorii peaked in April 2016, March 2017, and April–May 2018, ranging from 2.99 × 10⁴ to 6.73 × 10⁴ individuals m⁻³ (Fig. 3, Table 1). Anakubo and Murano²⁸ reported that the abundance of A. omorii, including individuals from the nauplius to adult stage, peaked at 5.34 × 10⁴ m⁻³ in April 1981 in Tokyo Bay. Itoh and Aoki¹⁸ surveyed A. omorii in Tokyo Bay from March 1990 to November 1992 and found that abundance peaked at 2.13 × 10⁴ individuals m⁻³ in March. Tachibana et al.⁴⁰ reported that abundance peaked at 2.60 × 10⁴ individuals m⁻³ in April in 2007. The peak abundance in Tokyo Bay apparently occurs between March and May; this pattern was also observed in the Seto Inland Sea (Table 1). According to Kasahara et al.¹⁵, the peak period of abundance of adults and later-stage copepodites in the Seto Inland Sea occurred in mid-May at > 3.5 × 10⁴ individuals m⁻³. The abundance of adults and later-stage copepodites significantly decreased in July. The planktonic population disappeared from the water column in mid-August and recovered in November, when the water temperature was < 20 °C. Similarly, Liang and Uye¹⁷ reported that the abundance of A. omorii, including nauplii, in the Seto Inland Sea increased in February 1987 to 5.8 × 10⁴ individuals m⁻³; a second peak was observed in June at 6.9 × 10⁴ individuals m⁻³. The planktonic population disappeared in late July and appeared again in late October. Therefore, the peak of the abundance of this species (copepodites and adults) in Tokyo Bay was close to that in the Seto Inland Sea. Additionally, the period of disappearance of the planktonic population (late July or August–October) was almost the same in the Seto Inland Sea and Tokyo Bay^16,18,28,40. The water temperature in both Tokyo Bay and the Seto Inland Sea ranged from 8 °C to 28 °C. The seasonal dynamics of A. omorii populations are probably common in warm inner bays where summer water temperatures exceed 25 °C.

In contrast, the abundance of A. omorii in Onagawa Bay peaked at 4 × 10³ individuals m⁻³ in September and decreased to < 5 × 10² individuals m⁻³ in December^14,38. The water temperature in Onagawa Bay ranged from 4.5 °C to 23.2 °C, which was 3–5 °C lower than that in Tokyo Bay and the Seto Inland Sea (Table 1). The peak population abundance period is likely to depend on the temperature range. However, this is not the case for Okirai Bay and Otsuchi Bay, where water temperature range was lower than that in Onagawa Bay, and the planktonic populations disappeared in autumn, as in Tokyo Bay and the Seto Inland Sea (Table 1). In these two bays, A. omorii abundance was low even at the peak, with 2.9 × 10² and 3 × 10³ individuals m⁻³ in Okirai Bay and Otsuchi Bay, respectively. In Otsuchi Bay, A. hudsonica was present throughout the study and showed remarkable abundance peaks (> 1.5 × 10⁴ individuals m⁻³) in May⁴¹. Furthermore, in Okirai Bay, A. steueri appeared from July to March and peaked in September, with the maximum value exceeding 1.5 × 10³ individuals m⁻³⁴². In these bays, copepods are more diverse, and A. omorii abundance may be controlled by competition among these Acartia species. A. omorii was predominant in Tokyo Bay, the Seto Inland Sea, and Onagawa Bay^{14,15,16,18,28,40,43}. These results suggest that the population dynamics of A. omorii are probably affected by competition with other copepods. When competition is at a negligible level, population dynamics may be primarily affected by water temperature via resting egg production.

It should be noted that the population dynamics is also affected by their grazers such as jellyfish. In Tokyo Bay, abundance of Auriela aurita s.l. was high until August with the highest abundance of 1.6 ind. M⁻³⁴⁴. Itoh et al.⁴⁵ found that vertical distribution of A. omorii was affected by Auriela sp. in the bay. A. omorii had a sharp peak at 9 m depth in the vertical profile, however the abundance was very low at 10- and 11 m depth where Aruriela sp. was abundant (> 50 g wet weight m⁻³). Hence summer jellyfish bloom probably has a strong negative impact on the abundance of A. omorii. Unfortunately, we do not have enough information on jellyfish abundance in Onagawa Bay, effect of jellyfish should be considered for the better understanding of A. omorii dynamics in future.

A. omorii abundance became zero only from September to November 2016 in the 3 years of the present study. However, in other years, A. omorii appeared at low abundance in summer, as reported in previous studies conducted in Tokyo Bay ^16,18,28,40. The period of complete disappearance was short, and low densities were recorded throughout the year in most studies (Table 1), indicating that the population is maintained in the planktonic stages even under unfavorable conditions in Tokyo Bay.

EPR and egg type dynamics

SEPR peaked in winter (January or February) and May in both years at both stations (Fig. 8a). The second peaks were caused by increase in unhatched egg production, except for station CB in 2017 (Figs. 7b,c and 8b,c). Increase in unhatched egg production occurred when the surface water temperature exceeded 18 °C (Fig. 2a) and day length increased to > 14 h, similar to that reported by Uye⁵. From January to May 1982, 80% of eggs that were newly spawned by A. omorii females collected in Fukuyama Harbor of the Seto Inland Sea were subitaneous; resting eggs appeared in June when the surface water temperature exceeded 17.5 °C. In the present study, on June 9, 32% of the total eggs produced were resting and did not hatch within 14 days but hatched after being reincubated at 15 °C for 2 weeks. Uye⁵ also demonstrated the effect of photoperiod on egg production by A. omorii via laboratory experiments under two temperature conditions (15 °C and 20 °C ± 1 °C). Approximately half were resting eggs under l4L–10D photoperiodic conditions at both water temperatures, indicating that photoperiod is important for shift to resting eggs. Many copepods have dormancy strategies at the thermal limits of species distribution⁴⁶. In Tokyo Bay, the photoperiod exceeds 14 h in mid-May, when the water temperature usually exceeds 18 °C (Fig. 2a). Therefore, higher water temperatures and increased day length periods are synchronized in early summer in Tokyo Bay and may serve as cues for diapause egg production.

Unhatched PEPR exceeded subitaneous PEPR from May to June (Fig. 9), when abundance drastically decreased to < 1 × 10⁴ individuals m⁻³ (Fig. 4). Itoh and Aoki¹⁸ reported that resting eggs of A. omorii were abundant in the bottom sediment of Tokyo Bay in June, when the water temperature increased to approximately 20 °C. In the present study, in May 2018, 37% (station F3) and 47% (station CB) of unhatched eggs were quiescent and hatched immediately when the water temperature decreased (Fig. 10). Therefore, this unhatched PEPR probably avoided an unsuitable temperature for hatching and development. Similar results were reported for A. steueri; the PEPR for diapause eggs accounted for up to 98% of total PEPR from May to June¹⁰. Subsequently, adult abundance became low until September or October. The production rate of resting eggs reaches its highest level in common with these species just before the warm period when the population abundance becomes low. These Acartia species may have a strategy to avoid high temperatures by sensing increase in water temperature and producing diapause eggs with a long dormant period just before summer.

The egg types produced by A. omorii differed among females (Fig. 11). Even on the same day, many females produced only subitaneous eggs or only resting eggs (quiescent and diapause eggs). This difference may be related to the age. Walton⁴⁷ reported that Onychodiaptomus birgei females initially produced subitaneous eggs and then switched to producing resting eggs during their lifetimes. The difference may also be related to the history of environmental conditions each individual experiences in the field according to their age. In contrast, few females simultaneously produced all egg types: subitaneous, quiescent, and diapause eggs (Fig. 11). Other Acartia species also simultaneously produce subitaneous and resting eggs^4,37,48. For example, Drillet et al.³⁷ found that during 2 days of incubation, half of the females of A. tonsa simultaneously produced subitaneous and delayed-hatching eggs. Takayama and Toda⁴ also reported that several females of A. japonica simultaneously produced subitaneous, diapause, and delayed-hatching eggs. The simultaneous production of different eggs types by an individual is probably related to environmental factors in a complex way and therefore should be investigated using molecular and endocrine approaches.

In the present study, most females produced only subitaneous eggs in the early period of A. omorii appearance from November to April (Fig. 9); the proportion of females producing both diapause and quiescent eggs was high (> 45%) (Fig. 6) in the late period of A. omorii appearance (in May at station CB and in early June at station F3). However, in early June at station CB and late June at station F3, when the abundance sharply decreased, the proportion of females producing subitaneous eggs increased, whereas those producing quiescent eggs decreased from the previous month (Fig. 11). Uye⁵ reported a similar result; the proportion of diapause eggs to total eggs produced by A. omorii in the Seto Inland Sea peaked on June 9 and then reduced by half by June 30. Quiescent eggs have been defined as subitaneous eggs with arrested development that remain in a quiescent stage in unsuitable environmental conditions⁴⁹. Uye⁵ defined diapause eggs as eggs that did not hatch during 2 weeks at in situ water temperatures but hatched within 2 weeks when the incubation temperature decreased to 15 °C. These eggs may be classified as quiescent eggs in the present study. The results of Uye⁵ and the present study suggest that not all produced eggs of this species shift from subitaneous to quiescent eggs at higher water temperatures.

As mentioned in the previous subsection, a planktonic population of A. omorii has been found in mid-summer at low abundance in Tokyo Bay^16,18,28,40 (Fig. 3). Similar results were reported in Maizuru Bay⁵⁰. Itoh et al.⁴⁵ investigated the vertical distribution of copepods at 1-m depth intervals at station F3 in Tokyo Bay in mid-summer, when hypoxia develops near the bottom, and showed that A. omorii population had a sharp peak, with densities exceeding 1.5 × 10³ individuals m⁻³, at 8 m at a water temperature of 18 °C and just above the hypoxic zone⁴⁵. This suggests that A. omorii maintains a planktonic stage even at low density in mid-summer, whereas most of the population estivates by forming resting eggs in bottom sediments. These mid-summer populations are presumably hatched from subitaneous eggs spawned in mid-July (Figs. 7, 10). Uye⁵ also reported that more than half of the eggs were still subitaneous in late July in the Seto Inland Sea. Therefore, we tentatively think that this phenomenon is a bet-hedging strategy of A. omorii in an unfavorable and uncertain environment. In contrast, Ueda⁵⁰ stated that the increase in subitaneous EPR in summer was due to immature development of this species. Thus, these remaining populations may not contribute to the autumnal development of the population. To understand how A. omorii survive in mid-summer, more detailed field investigations are warranted, including egg and nauplii dynamics in the water column, egg hatching process from sediments, and differences in endogenous factors in individual females producing subitaneous and diapause eggs in summer.

Information on A. omorii’s delayed-hatching eggs is strictly limited. Delayed-hatching eggs are eggs hatching over a wide time span regardless of environmental conditions^4,11. Takayama and Toda⁴ defined the unhatched eggs of A. japonica hatching during 72 h–50 days as “delayed-hatching eggs.” Thus, delayed-hatching eggs may have been included in the quiescent and diapause eggs defined in this study. Our results showed that no eggs hatched between 48–96 h and 7 days in the experiment at in situ water temperature; many quiescent eggs hatched within a few days after reincubation at lower water temperatures (Figs. 10, 11). Therefore, delayed-hatching eggs may not have been produced in the present study.

Effects of water temperature on the production of subitaneous and diapause eggs

Multiple regression analysis revealed that subitaneous SEPR negatively correlated with bottom water temperature, inconsistent with the results of Uye³. EPR and copepod growth generally increase with increased water temperature⁵¹. Uye³ reported that EPR of A. omorii also increased with water temperature; they developed a simple model equation describing the fecundity of A. omorii in Onagawa Bay via a laboratory experiment:

where F is daily fecundity (eggs female⁻¹ day⁻¹), T is water temperature (°C), S is chlorophyll a concentration (µg L⁻¹), and W_f is female carbon content (µg). The fecundity predicted by the above described model was similar to the observed EPR of this species in Onagawa Bay³.

Many studies have used Uye’s equation to estimate A. omorii egg production. Kang et al.⁵² reported A. omorii’s EPR in Ilkwang Bay to be 22–57 eggs female⁻¹ day⁻¹, which was higher than that in the present study (1.6–18.7 eggs female⁻¹ day⁻¹) (Fig. 7a). Liang and Uye¹⁷ estimated A. omorii’s EPR in the Seto Inland Sea by two methods: the above described model (estimated incubation fecundity)³ and based on the number of eggs remaining in the water column and the adult female population (egg-ratio fecundity)⁵³. In the Seto Inland Sea, the estimated incubation fecundity was 26–60 eggs female⁻¹ day⁻¹ and the egg-ratio fecundity was 0.5–25 eggs female⁻¹ day⁻¹; the estimated incubation fecundity was always greater than the egg-ratio fecundity¹⁷.

Suspension-feeding copepods may ingest their own eggs and nauplii. In the Seto Inland Sea, possible egg predators were the dominant copepods Centropages abdominalis and A. omorii⁵⁴. Based on their abundance (0.2–39 predators L⁻¹) and assuming a predator clearance rate of 50 mL d⁻¹, C. abdominalis and A. omorii could remove 1–86% of eggs in the water column per day. Liang and Uye¹⁷ noted that their predators were abundant when the abundance of surviving eggs in the water column was low; therefore, they tentatively concluded that the difference between the two estimates was due to egg loss by predation, including cannibalism. However, it is unlikely that fecundity reached its highest value (> 50 eggs female⁻¹ day⁻¹) in mid-July when the population disappeared from the water column¹⁷. At that time, the water temperature was 25 °C, which also does not support the increase in fecundity observed by Liang and Uye¹⁷.

The model equation of Uye³ was derived from Onagawa Bay, where the average water temperature is 7.7–21.9°C⁵⁵. In laboratory experiments using A. omorii from Onagawa Bay, EPR decreased when the water temperature exceeded 22.5°C³. In Uye’s equation³, the decrease in egg production above 22.5 °C was not foreseen, whereas water temperature exceeded 22.5 °C in the Seto Inland Sea¹⁷, Ikkwang Bay⁵², and Tokyo Bay (Fig. 2). Thus, Uye’s model equation³ is not applicable to these warm environments.

Based on the temperature regime, seasonal population dynamics and egg types produced are divided into two types: no resting egg production in the colder Onagawa Bay and resting egg production in the warmer Tokyo Bay and Seto Inland Sea. As mentioned above, A. omorii in Onagawa Bay exists throughout the year, even in summer¹⁴ and hardly produces diapause eggs^5,7. However, the population almost disappears in late summer in Tokyo Bay^16,18,28,40 and the Seto Inland Sea^15,17. Furthermore, in these warm coastal waters, A. omorii produced diapause eggs just before copepodite disappearance from the water column. Therefore, a separate equation for estimating egg production should be developed, depending on the temperature regime of the habitat.

Recent climate change, particularly global warming, may affect A. omorii’s egg production. In Tokyo Bay, between 1955 and 2015, the water temperature increased by 1.0 °C and 0.94 °C at the surface and bottom layers, respectively, in winter and autumn^56,57. In summer, the water temperature at both the surface and bottom layers decreased, probably due to strengthened estuary circulation^56,57. Considering the response of A. omorii to water temperature, the increase in winter temperature might reduce subitaneous egg production, resulting in delayed population increase. In contrast, the decrease in summer temperature might lead to reduced diapause egg production per amount of body carbon. The long-term trends of water temperature might have different effects on each egg type production and alter the dynamics of A. omorii egg production.

Effects of phytoplankton composition on the production of subitaneous and diapause eggs

The EPR of A. omorii may be saturated at low (1–2 µg L⁻¹) chlorophyll a concentrations^3,19. However, multiple regression analysis revealed that small diatoms stimulate subitaneous SEPR (Figs. 8, 12). The EPR at station CB was quite high (> 14 eggs female⁻¹ day⁻¹) in January and February 2018, when the diatoms comprised Skeletonema and Chaetoceros. In contrast, at station F3, EPR drastically decreased from 18.7 ± 6.3 eggs female⁻¹ day⁻¹ in January to 8.4 ± 4.6 eggs female⁻¹ day⁻¹ in February 2018. The EPR at station F3 in February was significantly lower than that at station CB (Tukey’s post hoc test, p < 0.01). In this month, small-sized nanoflagellates accounted for 99% of total phytoplankton carbon biomass. Studies have reported that diatoms have a positive effect on copepod EPRs in both laboratory experiments^58,59 and field investigations^60,61,62,63. In the present study, hatching success was also high (> 95%) at station CB in January and February 2018, suggesting that small diatoms ingestion enhances A. omorii’s egg production.

It is also likely that small nanoflagellates have an adverse effect on egg production. At station F3, the proportion of nanoflagellates to total phytoplankton carbon biomass was high (> 93%) in February and March (Fig. 12), when EPR was quite low (< 8.4 eggs female⁻¹ day⁻¹) (Fig. 7a). The EPR of Temora longicormis was reduced from 20 eggs female⁻¹ day⁻¹ when they were feeding on Thalassiosira weissflogii to 10 eggs female⁻¹ day⁻¹ when they were feeding on Tetraselmis suecica and to < 5 eggs female⁻¹ day⁻¹ when Dunaliella tetriolecta was used as prey⁶⁴. Sopanen et al.⁶⁵ reported that the haptophyte Prymnesium had a strong negative effect on the EPR of A. clausi, even when it was fed in a mixture with Rhodomonas, which is known to support reproduction in Acartia⁶⁶. The bloom of some nanoflagellate species may reduce copepod egg production.

Unhatched SEPR positively correlated with the proportion of large diatoms to total phytoplankton carbon biomass and proportion of dinoflagellates to total phytoplankton carbon biomass (Figs. 8, 12). Large diatom biomass was mostly accounted for by the genus Pleurosigma (cell size 160 µm), and the most common large dinoflagellates were Ceratium furca (cell size 145 µm) and C. fusus (cell size 350 µm). These sizes are probably above or close to the maximum size of the edible prey for A. omorii³⁶. Therefore, both large diatoms and dinoflagellates cannot be consumed by A. omorii. Furthermore, in early June 2017 and May 2018, when unhatched eggs accounted for the highest proportion of total eggs produced during each year (Fig. 10), the proportion of small diatoms was quite low (< 4%), while that of large phytoplankton carbon biomass was high (> 60% and > 35% in early June 2017 and May 2018, respectively) (Fig. 12). Food availability may be involved in egg type switching³⁷. The fraction of delayed-hatching eggs of A. tonsa was greater at low-food concentrations (Rhodomonas salina, 2000 cells mL⁻¹) than at high-food concentrations (40,000 cells mL⁻¹)³⁷. The primary cues for switching from subitaneous eggs to diapause eggs in Tokyo Bay seem to be water temperature and photoperiod. However, low-food availability, such as during the temporary disappearance of small diatoms and the bloom of inedible species, might stimulate diapause egg production by A. omorii.

Finally, the possible effect of prey availability on the small-scale horizontal distribution of A. omorii in Tokyo Bay should be noted. Itoh and Nishida⁶⁷ reported that the abundance of A. omorii was higher on the east side of Tokyo Bay than on the west side. Chlorophyll a concentration was generally higher on the west side of Tokyo Bay in summer; however, on the east side of Tokyo Bay, it was higher in winter⁶⁸. Even in the present study, diatom blooms were observed every winter in the vicinity of station CB, whereas diatom biomass was relatively low in the vicinity of station F3 every year (Fig. 12). Therefore, the horizontal distribution of phytoplankton may also influence A. omorii abundance through egg production, which is positively affected by small diatoms.

Our preliminary results show that edible diatoms may stimulate subitaneous EPR; however, the effects of individual diatom species are currently unknown. The production of cytotoxic compounds, including polyunsaturated aldehydes, by diatoms may vary at the genus, species or clonal level^69,70. Toxicity tolerance also varies with copepod species^71,72. Therefore, to clarify the effect of diatom species on A. omorii egg production, in situ monitoring of cytotoxic compounds and chemical and molecular analysis of the toxicity tolerance of A. omorii is warranted.

Source: Ecology - nature.com