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Article

Effects of Temperature and Food Concentration on the Population Recruitment of Acartia bifilosa (Copepoda, Calanoida): Implications for the Over-Summering Life History Strategy in Jiaozhou Bay

by
Zhan Zhang
1,2,3,4,†,
Zhencheng Tao
1,2,4,5,*,†,
Xiaotong Gao
6,
Lei Wang
6 and
Song Sun
1,2,4,5,*
1
Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
2
Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China
3
Library of Ocean University of China, Qingdao 266100, China
4
University of Chinese Academy of Sciences, Beijing 100049, China
5
Center for Ocean Mega-Science, Chinese Academy of Sciences, 7 Nanhai Road, Qingdao 266071, China
6
Jihongtan Reservoir Management Station, Shandong Water Diversion Project Operation and Maintenance Center, Qingdao 266111, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Water 2022, 14(21), 3541; https://doi.org/10.3390/w14213541
Submission received: 26 September 2022 / Revised: 29 October 2022 / Accepted: 1 November 2022 / Published: 4 November 2022
(This article belongs to the Special Issue Conserving Biodiversity in Aquatic Ecosystems: Challenges and Solutions)
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Abstract

:
To obtain a clear understanding of the over-summering life history strategy of the dominant species A. bifilosa in the Jiaozhou Bay, the effects of high temperature and food concentration (represented by chlorophyll a, Chl a) simulating in situ summer conditions on the reproduction and post-embryonic development of A. bifilosa were studied. We found that the A. bifilosa population did not disappear from the seawater column in summer, and its abundance increased from June to July, and then sharply declined in August. Both temperature and food concentration had a significant influence on the reproduction of A. bifilosa. The results showed that 20 °C could not trigger the decline in population abundance and the resting egg strategy, and 28 °C was the upper threshold of A. bifilosa in the Jiaozhou Bay. Higher food concentration was essential for A. bifilosa to maintain population recruitment at a higher temperature. Nauplii could develop to adults in the higher-food-level treatments (10 and 15 μg/L Chl a). However, nauplii could not develop to copepodite at 28 °C with 5 μg/L Chl a. Neither temperature nor food concentration could induce resting eggs, and no resting eggs were detected in our study. A principal components analysis showed that temperature plays a more vital role than food concentration in determining the population recruitment of A. bifilosa. We suggest that A. bifilosa populations could sustain the high-temperature season independent of producing resting eggs in the Jiaozhou Bay, and implications for the over-summering life history strategy of A. bifilosa in the Jiaozhou Bay should be further discussed.

1. Introduction

It is important to know the life history traits of copepods in their habitats because they play very important roles in marine systems as a major link in food webs [1] and a potential influencer of nutrient recycling [2]. In the natural marine ecosystem, many copepods encounter adverse environmental conditions. To sustain their population through the inhospitable period, both physiological and behavioral adaptations are required [3]. When the environment becomes too severe to be inhabited, life history strategies such as production of resting eggs or suspension development during various developmental stages are necessitated [4,5]. According to the life history theory, strategies that maximize fitness will be favored [6]. Thus, a copepod species needs to resort to a life history strategy, and the kind of strategy strongly depends on the degree of its adaptation to the main in situ environmental factors, such as temperature and food [7].
From Europe to Asia, Acartia bifilosa (Giesbrecht, 1881) was found to dominate in many temperate coastal and estuarine waters [8,9,10,11]. As one of the main prey species for herring and Mysids, it constitutes a large fraction of zooplankton biomass and production [12,13,14]. Furthermore, it has a great adaptability to different brackish-water environments [15,16]. Thus, it has been selected as a keystone species for zooplankton production and ecosystem dynamics in many regions [9,13,15,16,17]. High temperature is harsh to A. bifilosa despite the temperature tolerance limits and the life history strategies that may be different in different geographical areas [15,18,19,20]. In Southampton Water, it totally disappears from the seawater column when the seawater temperature exceeds 20 °C in late summer and autumn, relying on diapause eggs for recruitment [18], whereas, in some other regions, such as the northern Baltic Sea, Biscay Bay, and Bohai Sea, A. bifilosa is a perennial copepod in the seawater column [9,15,21], despite the summer temperature sometimes approaching 24 °C [15]. These results indicate that the recruitment of A. bifilosa in those areas may not totally depend on the benthic resting eggs, and that some autochthonous populations adapt to high temperatures in warm seasons.
As some studies have reported, the resting eggs of A. bifilosa are commonly spiny and crinkled [18,22]. It was reported that the smooth eggs and “spiny resting eggs” were found in the Jiaozhou Bay [23]. Acartia bifilosa has long been recognized to produce the resting eggs in June for the over-summering. However, this old assumption is not convincing because of a lack of evidence from both mass field investigation and laboratory experiments. During the study of a fixed site in the Jiaozhou Bay, A. bifilosa was the dominant copepod species in spring in the Jiaozhou Bay and then disappeared completely from the seawater column within a couple of months in summer when the seawater temperature exceeded 20 °C (from June) [24]. The resting eggs presumably produced in June are regarded as the only strategy to over-summer [23]. Over the past several decades, no further information about the life history strategy of this species in this bay has been reported. This has led to a longstanding view that A. bifilosa is not present in this bay from late summer onward, and only relies on the hatching of mud-buried resting eggs in the following cold seasons to repopulate. However, such a single fixed-site survey may not be representative because the Jiaozhou Bay is a semi-closed bay with an area of about 374 km2, and an average depth of less than 10 m. The seawater exchange rate of the Jiaozhou Bay between the bay and the open sea is high (7%), with a half exchange period of only 5 days [25]; therefore, copepods in this bay may experience continuously changing environmental factors in a relatively short period which may result in the wide range of life history parameters. This bay is particularly far from homogeneous in terms of both temperature profile and trophic distribution. The seawater temperature in the summer months ranges from 20 °C to 28 °C (June to August), and the difference in surface temperatures across the whole bay can vary significantly with a difference of up to 3–6 °C [26,27]. In terms of trophic distribution, the Chl a horizontal distribution patterns showed that the concentration decreased from north to south perennially [28,29]; particularly in summer, the phytoplankton community composition was diverse whilst the fluctuation of phytoplankton density was greater [28]. The genus Acartia is generally not adapted to low food concentration [30] and is often found to be food limited in natural conditions [19,31,32]; hence, since the food quantity availability for A. bifilosa in summer may be uneven, this might result in variable life history parameters. If A. bifilosa has the potential to adapt to high-temperature summer environments, i.e., females have the opportunity to reproduce normally and newly hatched nauplii have the opportunity to develop into the adult stage, they might not have to solely depend on resting eggs, which is considered a costly strategy [33].
Although the environmental variations in the Jiaozhou Bay are well known [14,27], (1) the distribution and abundance patterns of A. bifilosa in the whole bay are not available, and (2) its reproductive and developmental responses to high temperature and food concentration in summer in this bay have never been studied. As a dominant species, the presence, abundance, and life history strategy of A. bifilosa are apparently very important to the Jiaozhou Bay ecosystem. In the present study, we aimed to investigate the presence and abundance of A. bifilosa in summer and the effects of temperature and food concentration on some main life history parameters, and its over-summering life history strategy in the Jiaozhou Bay.

2. Materials and Methods

2.1. Field Investigation

Broad-scale survey cruises were conducted at 13 stations on 17 to 21 June, 13 to 14 July, and 9 to 11 August 2004 by the Jiaozhou Bay Marine Ecosystem Research Station (JMERS) (Figure 1). The environmental parameters were also routinely measured by JMERS in addition to the biological investigation. Zooplankton were collected using a midi-zooplankton net (mesh size: 160 µm, mouth opening: 0.08 m2). Zooplankton nets were towed vertically from near the bottom (maximum depth: 35 m, station D5) up to the surface at a rate of about 0.8 m/s. Zooplankton samples were preserved in 5% buffered formalin seawater solution immediately upon collection. After being transported to the laboratory, A. bifilosa was identified and counted using a stereoscopic microscope. Zooplankton abundance data are presented in ind/m3.

2.2. Laboratory Experiments

From June onward, A. bifilosa began to gradually encounter higher temperatures (>20 °C), approaching the presumed period to produce resting eggs. Two separate laboratory experiments were simultaneously conducted on female reproduction and post-embryonic development in June.
Live zooplankton were collected using a midi-zooplankton net towed from 2 m above the seafloor to the surface in July, with the average seawater temperature about 24 °C. The contents of the net cod end were stored in a 30 L isotherm tank filled with surface seawater and transported to the laboratory within 1 h of sampling. Within 3 h of capture, healthy adult A. bifilosa females with active swimming, complete body, and appendages were sorted and rinsed twice in filtered seawater, which was filtered with a 20 µm mesh to remove zooplankton and retain phytoplankton. The reproduction experiments were performed under four different temperatures (20 °C, 22 °C, 25 °C, and 28 °C). Furthermore, 20 °C, 22 °C, and 25 °C represent the average seawater temperature in June, July, and August in the Jiaozhou Bay. On the other hand, 28 °C is the highest annual seawater temperature recorded, typically occurring in August. At the beginning of the culture experiments, the incubated temperature of A. bifilosa was set to 24 °C. In addition, the culture temperature of the constant temperature incubator was increased or lowered by one degree per hour until it reached the designed temperature.
Acartia bifilosa in the laboratory was reared on a mixed algal diet consisting of four kinds of algae isolated from the Jiaozhou Bay (Skeletonema costatum, Platymonas subordiformis, Isochrysis galbana, and Nannochloris oculata) at the ratio 1:1:1:1 in terms of carbon concentrations. Four treatments (20 °C, 22 °C, 25 °C, and 28 °C) were designed in the egg production experiment. In each treatment, five females were placed in Petri dishes (diameter 10 cm) containing 30 mL seawater with a final diet concentration of 1.0 μg C/mL, which can satisfy the needs of A. bifilosa [34]. Six replicates were conducted in each treatment. Females were daily recorded and carefully transferred to new dishes containing the same food level. Eggs were counted and placed in hatching dishes containing 10 mL 20 µm-filtered-seawater under the experimental temperatures. The hatching rate was defined as hatched nauplii developed into naupliar stage N2. All copepod incubations were carried out in an incubator for 24 h (light/dark = 12/12 h) at a constant temperature (±0.5 °C). Four levels of food concentration, measured as concentrations of Chl a (0, 5, 10, 15 μg/L), covered the average concentrations of Chl a in the Jiaozhou Bay in summer. Reproduction experiments were conducted for 6 days and designed to measure three life history parameters: female survival rate (FSR), egg production rate (EPR), and hatching rate (HR). The EPR data are presented as eggs/(female·day). Cannibalism on eggs by adults was not observed in the reproduction experiments, consistent with other reports [15,16,19].
Post-embryonic development experiments were conducted for 2 weeks to focus on whether the nauplii under the tested conditions could complete development from hatching to adulthood. Acartia bifilosa females were incubated in the egg production equipment, which is a patented device developed by our laboratory [35]. Eggs were collected and hatched in the respective treatment conditions for 24 h to obtain N1 nauplii for post-embryonic development investigation. In each treatment, a 500 mL beaker containing 90–100 newly hatched N1 nauplii was placed in an incubator. The post-embryonic development time (PDT) of each developmental stage was monitored. All individuals of each treatment were gently counted and checked daily using a 10 mL glass bowl under a dissecting microscope at each developmental stage in the air-conditioned room. Stage durations were calculated using the median development time of stage frequencies defined as the time for 50% of the cohort to molt to the next stage. For the three food-level treatments, about three-quarters of the food suspension was replaced with a new prepared medium at the experimental temperature every 2 days using a pipette covered with a 38 μm mesh to minimize operation damage. From egg to adult, A. bifilosa can develop to six nauplius stages (N1, N2, N3, N4, N5, and N6) and five copepodite stages (C1, C2, C3, C4, and C5) [36].

2.3. Data Analysis

The contour figures of Acartia bifilosa abundance were based on Kriging interpolation and generated with Golden Software Surfer V14.0 (Golden Software LLC, Golden, CO, USA). The differences among the treatments under different temperatures and food concentrations were examined using a one-way ANOVA. Pearson correlation analyses of A. bifilosa population recruitment (EPR, HR, and PDT) and environmental factors (temperature and food level) were statistically evaluated using IBM SPSS Statistics V20 (IBM Corp., Armonk, NY, USA). To assess the similarity of the incubation treatments, a cluster analysis was conducted using PRIMER V6.0 software (PREMIER Biosoft, Palo Alto, CA, USA). A principal components analysis (PCA) was carried out using IBM SPSS Statistics V20 to analyze the impact of the environmental factors on the A. bifilosa population recruitment.

3. Results

3.1. Environmental Conditions and Distribution of Acartia bifilosa Abundance

The seawater temperature, salinity, and Chl a concentration from June to August in the Jiaozhou Bay were 20–28 °C, 29–31 psu, and 2–8 μg/L, respectively.
The distributions of A. bifilosa in the Jiaozhou Bay from June to August are shown in Figure 2. The field investigation not only validated the presence of the A. bifilosa population in the seawater column of the Jiaozhou Bay during summer but also showed an increased abundance in July. In June (average seawater temperature 20 °C), the population of A. bifilosa was mainly distributed in the northeast and south parts of the bay, with abundance ranging from 2000 to 3000 ind/m3. In July (average seawater temperature 22 °C), a dense population appeared in the west part of the bay with an increased abundance of 3000–7000 ind/m3. In August, although the average seawater temperature was over 25 °C, the A. bifilosa population was mainly distributed in the inner bay, and the abundance of A. bifilosa sharply decreased to 500–1000 ind/m3.

3.2. Female Survival

Temperature and food concentration had different effects on the female survival of A. bifilosa. With two higher food concentrations (10 μg/L and 15 μg/L Chl a), the FSRs of A. bifilosa were maintained over 73% during the incubation, and the differences between the two higher food concentrations were not significant at each experimental temperature (one-way ANOVA, p > 0.05), which indicated a food satiety level of 10 μg/L Chl a in maintaining female survival. Under a higher experimental temperature (22 °C, 25 °C, and 28 °C), there was no significant difference between the A. bifilosa FSRs incubated with four food concentrations (one-way ANOVA, p > 0.05). However, the FSRs of A. bifilosa at the two lower food concentrations (0 and 5 μg/L Chl a) significantly decreased with the increase in temperature, especially at higher temperatures of 25 °C and 28 °C (Figure 3). At 25 °C, with the food concentration of 5 μg/L Chl a, 90% of females survived for 4 days, and the FSRs decreased quickly to 57% on the fifth day. On the other hand, with 0 μg/L Chl a, 90% of females survived for 3 days, and the FSRs decreased quickly to 50% on the fourth day. At 28 °C, with 5 μg/L Chl a, the FSRs decreased for the first 2 days, and then remained stable at 53% on the subsequent experimental days, whereas females with 0 μg/L Chl a died completely on the fourth day (Figure 3). These results showed that temperature had a significant effect on female survival in food-limited conditions.

3.3. Egg Production

At all four experimental temperatures, A. bifilosa in the 0 μg/L Chl a treatment could not produce eggs throughout the experimental period. Thus, the corresponding hatching success and post-embryonic development experiments were not conducted. The differences of between the EPRs of A. bifilosa with four food concentrations were significant at each experimental temperature (one-way ANOVA, p > 0.05). Similarly, at each food concentration, there were significant differences between the EPRs of A. bifilosa at the four experimental temperatures.
Egg production of A. bifilosa was affected by both temperature and food concentration (Table 1). A. bifilosa in the 0 μg/L Chl a treatment at all four experimental temperatures did not produce eggs. The highest EPRs in the three food concentration treatments (5, 10, and 15 μg/L Chl a) were always achieved at the two lower temperatures (20 °C and 22 °C) (Figure 4). The EPRs significantly decreased over 22 °C in all three food levels, indicating that 22 °C represented a milestone temperature for A. bifilosa to decrease egg production. EPRs in the 5 μg/L Chl a treatment were significantly lower than those in the 10 μg/L and 15 μg/L Chl a treatments. There was no significant difference in average EPR between 10 μg/L Chl a and 15 μg/L Chl a at 20 °C and 22 °C, respectively, indicating a food satiety level of 10 μg/L Chl a in the egg production of A. bifilosa. Only the highest food concentration (15 μg/L Chl a) could sustain egg production throughout the experimental period at the highest temperature of 28 °C, although the average EPR was only 0.73 eggs/(female·day). At the food concentration of 10 μg/L Chl a, females maintained egg production for 5 days at 25 °C and only produced eggs on the first day at 28 °C. At the food concentration 5 μg/L Chl a, females produced eggs for only 2 days at 25 °C and could not produce any eggs at 28 °C (Figure 4). The lower food concentration could not support continuous egg production at 25 °C and 28 °C or enough eggs for the hatching rate estimation.

3.4. Hatching Success

The average HRs of A. bifilosa eggs produced under different seawater temperatures and Chl a concentrations were mostly higher than 60% (Table 1). The resting eggs of A. bifilosa were generally spiny or crinkled. All eggs produced in our experiments were smooth. Therefore, neither the four temperatures nor the food concentrations in the present work could induce the resting eggs of A. bifilosa. The remaining eggs in each experimental treatment were continuously hatched for 3 more days, but no more hatching occurred, and the eggs were considered nonviable, eventually decomposing probably due to microbes.
The EPRs of A. bifilosa with 5 μg/L Chl a under 28 °C were 0 during the whole experiment period. Under the conditions of 10 μg/L Chl a under 28 °C and 5 μg/L Chl a under 28 °C, the spawning behaviors of A. bifilosa only lasted for 1 day and 2 days, respectively. So, the HR data of A. bifilosa in the above three treatments are not continuous (Figure 5). The average HR was always the highest at 22 °C in each of the three food concentration treatments and significantly decreased with increasing temperature from 22 °C to 28 °C (one-way ANOVA, p < 0.01). Different ranges of food concentration had different effects on the HRs in different temperature ranges. Increasing food concentration from 5 μg/L to 10 μg/L Chl a could obviously increase the HRs at all tested temperatures (Figure 5). However, the HRs decreased with the food concentration increasing from 10 μg/L to 15 μg/L Chl a at 20 °C and 22 °C. At 25 °C and 28 °C, there was no significant difference between hatching rates with 10 μg/L and 15 μg/L Chl a.

3.5. Post-Embryonic Development

The developmental stage of A. bifilosa succession at four different temperatures and three food concentrations is shown in Figure 6. Acartia bifilosa was able to develop from egg to adult at all tested temperatures from 20 °C to 28 °C at the two highest food concentrations (10 μg/L to 15 μg/L Chl a). At the lower food concentration (5 μg/L Chl a), N1 could not develop to the adult stage at higher temperatures (25 °C and 28 °C), only developing to the C4 and N6 stages, respectively. At a food concentration of 10 μg/L Chl a, the developmental times at 28, 25, 22, and 20 °C from N1 to adult were 11, 10, 11.5, and 12 days, respectively. To develop from N1 to adult at 28, 25, 22, and 20 °C with 15 μg/L Chl a, the required time was 10, 9, 11, and 12 days, respectively (Table 1). Developmental times were always the shortest at 25 °C with a food concentration of 10 μg/L to 15 μg/L Chl a (Figure 6).

3.6. Relationship between Acartia bifilosa Population Recruitment and Environmental Factors

The correlations between A. bifilosa population recruitment and environmental factors are shown in Table 2. The EPR, HR, and PDT were all negatively correlated with temperature (p < 0.05). The three population recruitment parameters were not significantly correlated with food condition. The cluster analysis of the A. bifilosa population recruitment parameters under different temperatures and food levels in the Jiaozhou Bay is shown in Figure 7. All treatments of A. bifilosa incubation experiments were clustered into two groups. The similarity between the two groups was less than 50%. The first group included two treatments. The first group included the treatments with the lowest food level (5 μg/L Chl a) and higher temperatures (25 °C and 28 °C), with a similarity of over 70%. In the second group, the similarity of the remaining 10 treatments exceeded 85%. The population recruitment parameters of A. bifilosa and the environmental parameters in the Jiaozhou Bay were analyzed using a PCA (Figure 8). The cumulative percentage of variance for the initial eigenvalues of the two principal components was 80.25% of the total variance explained by the five components (temperature, food level, EPR, HR, and PDT). The total variance of principal component 1 was 59.89%. In the principal component 1 matrix, the PCA loading value (absolute value) of temperature (−0.794) was higher, and that of food level (0.519). The effect of the temperature on population supplementation was greater than that of food. The temperature showed significant negative correlations with the population recruitment parameters of A. bifilosa. The effect of food on the population recruitment was positive, but the correlation was not significant.

4. Discussion

4.1. Combination Effect of Temperature and Food Concentration

It is well known that higher temperatures increase the energy cost of both females and larvae regarding copepod metabolism [20,37,38]. Several studies have shown that the upper temperature tolerance limits of A. bifilosa are different in different habitats in the world, while the combined effects of ocean acidification and global warming predicted for the year 2100 on A. bifilosa, showed that higher temperatures could decrease the egg viability and nauplii development of A. bifilosa [39]. Acartia bifilosa distributed in the small temperate estuary of Mundaka began to produce fewer eggs beyond 20 °C and could maintain its population in situ with the lowest egg production rate under 24 °C [15]. The fatal temperature for the female survival and egg production of A. bifilosa in the northern Baltic Sea was 24 °C [19]. In the Jiaozhou Bay, A. bifilosa in situ still maintained its population in August which is the warmest month of the year (average temperature 25 °C), but the wild A. bifilosa collected in mid-summer (June) was able to adapt to temperatures as high as 28 °C but only with the highest food concentration (15 μg/L Chl a). Therefore, A. bifilosa in the Jiaozhou Bay can be considered more tolerant to high temperatures compared to the estuary of Mundaka, the northern Baltic Sea, and Southampton Water. Furthermore, 28 °C may be approaching the upper threshold for A. bifilosa in the Jiaozhou Bay. The most optimal temperature for both egg production and hatching success was 22 °C in the laboratory incubation experiments. Both the EPR and the HRs declined drastically at 25 °C. However, with higher food concentrations, the development of nauplii to adult was faster at 25 °C than at 22 °C, which suggested that this efficient biological response may contribute to maintaining the low abundance in August.
If the food is not enough to afford the energy cost of females or larvae over time, the A. bifilosa population loses its chance to stay in the seawater. The effect of food availability on the life history parameters of copepods is relatively much more difficult to evaluate than physical factors such as temperature, partly because it is related to several factors in both field and laboratory conditions such as maternal feeding history, food quality, and algal exudates [34,40,41]. In the northern Baltic Sea, A. bifilosa could be well adapted to fluctuating food conditions, and the females could not survive over 50 h with a food concentration of 5–9 μg/L Chl a at 24 °C [19]. In the present study, more than 50% of females could survive over 6 days without a food supply, and they could not produce any eggs during this period. N1 larvae reared under food-limited conditions could not develop to the adult stage at 25 °C and 28 °C, whereas the two higher food concentrations (10 and 15 μg μg/L Chl a) could sustain the complete N1–adult development. Therefore, A. bifilosa has few chances to reproduce normally with a food concentration of 5 μg/L Chl a in August.
Comparing the effects of temperature and food concentration on the development of copepods, food is generally considered to be as important a factor as temperature in controlling the development succession [42]. However, although both temperature and food concentration have important effects on the reproduction and post-embryonic development of A. bifilosa, according to the results of the PCA, temperature plays a more vital role than food concentration in determining the population recruitment of A. bifilosa. We suggest that temperature is a more influential factor than food concentration for the population recruitment of A. bifilosa in the Jiaozhou Bay.

4.2. Implications for the Over-Summering Life History Strategy in the Jiaozhou Bay

The sole resting egg over-summering strategy of A. bifilosa has been long recognized [43,44]. Resting eggs generally include three types: diapause, quiescence, and subitaneous [22]. Resting eggs of A. bifilosa were found in sediment off the southern coast of Finland, representing the first observations of resting calanoid eggs in the Baltic Sea [13]. Both the production of diapause eggs and arrest of development in the subitaneous eggs of A. bifilosa at low temperatures occurred in the English Channel [18]. Acartia bifilosa could not produce diapause eggs in summer and autumn in the northern Baltic Sea [21]. The subitaneous eggs buried in low-oxygen sediment may be used as a survival strategy on seasonal time scales, which could free A. bifilosa from the pressure to produce diapause eggs [45]. The population of A. bifilosa was completely disappeared in late summer in the Jiaozhou Bay, where temperature was regarded as the only main environmental factor to determining the population presence of A. bifilosa [24]. The eggs of A. bifilosa collected from the benthic mud could be hatched in the laboratory [23]. However, the types of the eggs (diapause, quiescence, or subitaneous) collected from the mud were not determined, and a single-fixed-site survey may not be representative of such a semi-closed bay. Furthermore, as the predominant species, A. bifilosa occurs continuously in the Jiaozhou Bay throughout the year, with large abundance peaks from late spring to early summer showing a more definite trend of size variation with temperature than other dominant species [10,46].
According to the seawater exchange period and the peak biomass of Chl a occurring in summer in the Jiaozhou Bay [25,29], A. bifilosa populations drifting with turbulence could encounter sufficient food in summer for normal reproduction and development. Thus, A. bifilosa in the Jiaozhou Bay would not be strongly negatively affected by food shortage during the summer. Our field investigation results showed that A. bifilosa could be found throughout the summer in the Jiaozhou Bay. The resting eggs were prevented from developing and hatching by external unfavorable conditions such as high temperature and oxygen depletion. As a genetically controlled state of arrested development, females always produce resting eggs in response to an unsuitable living environment [21,45,47,48,49]. We did not find resting eggs in our experiments, strongly suggesting that the A. bifilosa population in the Jiaozhou Bay can sustain the high-temperature seasons independent of producing resting eggs. Considering the post-embryonic development time from N1 nauplii to adult at 20 °C and 22 °C (11 to 12 days) under different food levels, the number of generations occurring after mid-June can be estimated, completing one generation of A. bifilosa by late June. The high survival rates of females at 20 °C and 22 °C would also ensure successful recruitment by reproducing normally in the seawater rather than producing resting eggs in June. Therefore, we suggest that there seem to be multiple life history strategies of A. bifilosa for over-summering in the Jiaozhou Bay, e.g., normal reproduction at high temperature, subitaneous eggs in low-oxygen sediment, and diapause eggs, all of which may contribute to the population recruitment of A. bifilosa in the Jiaozhou Bay.

Author Contributions

Z.Z. and Z.T. designed the experiments and drafted the manuscript; X.G. and L.W. designed field collection; Z.Z. and Z.T. performed the statistical analyses and wrote the main manuscript text; S.S. supervised all processes. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Natural Science Foundation of P. R. China (Nos. 42090044 and 42130411) and the National Key R&D Program of China (2017YFC1404402).

Data Availability Statement

Datasets for this research are included in this paper.

Acknowledgments

We thank the JMERS for their assistance of zooplankton sampling in this study.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Kleppel, G.S. On the diets of calanoid copepods. Mar. Ecol. Prog. Ser. 1993, 99, 183–195. [Google Scholar] [CrossRef]
  2. Dubischar, C.D.; Lopes, R.M.; Bathmann, U.V. High summer abundances of small pelagic copepods at the Antarctic Polar Front-implications for ecosystem dynamics. Deep-Sea Res. Part II Top. Stud. Oceanogr. 2002, 49, 3871–3887. [Google Scholar] [CrossRef] [Green Version]
  3. Fiksen, O.; Giske, J. Vertical distribution and population dynamics of copepods by dynamic optimization. ICES J. Mar. Sci. 1995, 52, 483–503. [Google Scholar] [CrossRef]
  4. Grice, G.D.; Marcus, N.H. Dormant eggs of marine copepods. Oceanol. Mar. Biol. Annu. Rev. 1981, 19, 125–140. [Google Scholar]
  5. Dahms, H.U. Dormancy in the Copepoda—An Overview. Hydrobiologia 1995, 306, 199–211. [Google Scholar] [CrossRef]
  6. Roff, D.A. The Evolution of Life Histories: Theory and Analysis; Chapman and Hall: New York, NY, USA, 1992; p. 535. [Google Scholar]
  7. Halsband-Lenk, C.; Hirche, H.J.; Carlotti, F. Temperature impact on reproduction and development of congener copepod populations. J. Exp. Mar. Biol. Ecol. 2002, 271, 121–153. [Google Scholar] [CrossRef] [Green Version]
  8. Collins, N.R.; Williams, R. Zooplankton Communities in the Bristol Channel and Severn Estuary. Mar. Ecol. Prog. Ser. 1982, 9, 1–11. [Google Scholar] [CrossRef]
  9. Wang, R.; Zhang, H.Y.; Wang, K.; Zuo, T. Function performed by small copepods in marine ecosystem. Oceanol. Limnol. Sin. 2002, 33, 453–460. [Google Scholar]
  10. Sun, X.H.; Sun, S.; Li, C.L.; Zhang, G.T. Seasonal and spatial variability in egg production, abundance and production of small copepods in and near Jiaozhou Bay, China. J. Plankton Res. 2011, 33, 741–750. [Google Scholar] [CrossRef]
  11. Ge, R.P.; Chen, H.J.; Liu, G.X.; Zhu, Y.Z.; Jiang, Q. Diel vertical migration of mesozooplankton in the northern Yellow Sea. J. Oceanol. Limnol. 2021, 39, 1373–1386. [Google Scholar] [CrossRef]
  12. Hansson, S.; Larsson, U.; Johansson, S. Selective Predation by Herring and Mysids, and Zooplankton Community Structure in a Baltic Sea Coastal Area. J. Plankton Res. 1990, 12, 1099–1116. [Google Scholar] [CrossRef]
  13. Viitasalo, M. Calanoid Resting Eggs in the Baltic Sea—Implications for the Population-Dynamics of Acartia Bifilosa (Copepoda). Mar. Biol. 1992, 114, 397–405. [Google Scholar] [CrossRef]
  14. Sun, S.; Li, C.L.; Zhang, G.T.; Sun, X.X.; Yang, B. Long-term changes in the zooplankton community in the Jiaozhou bay. Oceanol. Limnol. Sin. 2011, 42, 625–631. [Google Scholar]
  15. Uriate, I.; Cotano, U.; Villate, F. Egg production of Acartia bifilosa in the small temperate estuary of Mundaka, Spain, in relation to environmental variables and population development. Mar. Ecol. Prog. Ser. 1998, 166, 197–205. [Google Scholar] [CrossRef]
  16. Burdloff, D.; Gasparini, S.; Villate, F.; Uriarte, I.; Cotano, U.; Sautour, B.; Etcheber, H. Egg production of copepod Acartia bifilosa in two contrasting European estuaries in relation to seston composition. J. Exp. Mar. Biol. Ecol. 2002, 274, 1–17. [Google Scholar] [CrossRef]
  17. Gorokhova, E. Relationships between nucleic acid levels and egg production rates in Acartia bifilosa: Implications for growth assessment of copepods in situ. Mar. Ecol. Prog. Ser. 2003, 262, 163–172. [Google Scholar] [CrossRef] [Green Version]
  18. Castro-Longoria, E.; Williams, J.A. The production of subitaneous and diapause eggs: A reproductive strategy for Acartia bifilosa (Copepoda: Calanoida) in Southampton Water, UK. J. Plankton. Res. 1999, 21, 65–84. [Google Scholar] [CrossRef]
  19. Koski, M.; Kuosa, H. The effect of temperature, food concentration and female size on the egg production of the planktonic copepod Acartia bifilosa. J. Plankton Res. 1999, 21, 1779–1789. [Google Scholar] [CrossRef]
  20. Chinnery, F.E.; Williams, J.A. Photoperiod and temperature regulation of diapause egg production in Acartia bifilosa from Southampton Water. Mar. Ecol. Prog. Ser. 2003, 263, 149–157. [Google Scholar] [CrossRef] [Green Version]
  21. Katajisto, T. Development of Acartia bifilosa (Copepoda: Calanoida) eggs in the northern Baltic Sea with special reference to dormancy. J. Plankton Res. 2003, 25, 357–364. [Google Scholar] [CrossRef]
  22. Choi, S.Y.; Jang, M.C.; Youn, S.H.; Seo, M.H.; Soh, H.Y. Egg production and hatching patterns of Acartia erythraea (Copepoda, Calanoida), with a note on its two egg types, in a eutrophic bay in Korea. J. Plankton Res. 2021, 43, 428–441. [Google Scholar] [CrossRef]
  23. Zhong, X.F.; Xiao, Y.C. Resting eggs of Acartia bifilosa Giesbrecht and A. pacifica Steuer in the Jiaozhou Bay. Mar. Sci. 1992, 5, 55–59. [Google Scholar]
  24. Zhong, X.F.; Xiao, Y.C. Seasonal cycles of abundance of three copepod species population in the Jiaozhou Bay. Mar. Sci. 1992, 1, 44–48. [Google Scholar]
  25. Liu, R.Y. Characteristics of Physical Environmental of the Jiaozhou Bay; Science Press: Beijing, China, 1992; pp. 2–3. [Google Scholar]
  26. Shen, Z.L.; Liu, Q.; Wu, Y.L.; Yao, Y. Nutrient structure of seawater and ecological responses in the Jiaozhou Bay, China. Estuar. Coast. Shelf Sci. 2006, 69, 299–307. [Google Scholar]
  27. Sun, S.; Sun, X.X.; Zhang, G.T.; Tang, H.B.; Liu, Q.; Li, G.M. Long-term changes in major meteorological and hydrological factors in the Jiaozhou bay. Oceanol. Limnol. Sin. 2011, 42, 632–638. [Google Scholar]
  28. Li, C.L.; Zhang, F.; Shen, X.; Yang, B.; Shen, Z.L.; Sun, S. Concentration, distribution and annual fluctuation of chlorophyll-a in the Jiaozhou Bay. Oceanol. Limnol. Sin. 2005, 36, 499–506. [Google Scholar]
  29. Sun, X.X.; Sun, S.; Zhang, Y.S.; Zhang, F. Long-term changes of chlorophyll-a concentration and primary productivity in the Jiaozhou bay. Oceanol. Limnol. Sin. 2011, 42, 654–661. [Google Scholar]
  30. Paffenhöfer, G.A.; Stearns, D.E. Why is Acartia tonsa (Copepoda: Calanoida) restricted to nearshore environments? Mar. Ecol. Prog. Ser. 1988, 42, 33–38. [Google Scholar] [CrossRef]
  31. Durbin, E.G.; Durbin, A.G.; Smayda, T.J.; Verity, P.G. Food Limitation of Production by Adult Acartia tonsa in Narragansett Bay, Rhode-Island. Limnol. Oceanogr. 1983, 28, 1199–1213. [Google Scholar] [CrossRef]
  32. Irigoien, X.; Castel, J. Feeding rates and production of the copepod Acartia bifilosa in a highly turbid estuary; the Gironde (SW France). Hydrobiologia 1996, 311, 115–125. [Google Scholar] [CrossRef]
  33. Hairston, N.G.; Caceres, C.E. Distribution of crustacean diapause: Micro- and macroevolutionary pattern and process. Hydrobiologia 1996, 320, 27–44. [Google Scholar] [CrossRef]
  34. Li, J.; Sun, S.; Li, C.L.; Zhang, Z.; Pu, X.M. Effects of different diets on the reproduction and naupliar development of the copepod Acartia bifilosa. J. Exp. Mar. Biol. Ecol. 2008, 355, 95–102. [Google Scholar] [CrossRef]
  35. Tao, Z.C.; Wang, Y.Q.; Wang, J.J.; Liu, M.T.; Zhang, W.C. Photobehaviors of the calanoid copepod Calanus sinicus from the Yellow Sea to visible and UV-B radiation as a function of wavelength and intensity. J. Oceanol. Limnol. 2019, 37, 1289–1300. [Google Scholar] [CrossRef]
  36. Yoon, W.D.; Shim, M.B.; Choi, J.K. Description of the developmental stages in Acartia bifilosa Giesbrecht (Copepoda: Calanoida). J. Plankton Res. 1998, 20, 923–942. [Google Scholar] [CrossRef] [Green Version]
  37. Chinnery, F.E.; Williams, J.A. The influence of temperature and salinity on Acartia (Copepoda: Calanoida) nauplii survival. Mar. Biol. 2004, 145, 733–738. [Google Scholar] [CrossRef]
  38. Pu, X.M.; Sun, S.; Yang, B.; Ji, P.; Zhang, Y.S.; Zhang, F. The combined effects of temperature and food supply on Calanus sinicus in the southern Yellow Sea in summer. J. Plankton Res. 2004, 26, 1049–1057. [Google Scholar] [CrossRef] [Green Version]
  39. Vehmaa, A.; Hogfors, H.; Gorokhova, E.; Brutemark, A.; Holmborn, T.; Engstrom-Ost, J. Projected marine climate change: Effects on copepod oxidative status and reproduction. Ecol. Evol. 2013, 3, 4548–4557. [Google Scholar] [CrossRef] [Green Version]
  40. David, D.; Souissi, S.; Seuront, L. Effects of Chlorophyll concentration and temperature variation on the reproduction and survival of Temora longicornis (Copepoda, Calanoida) in the Eastern English Channel. J. Exp. Mar. Biol. Ecol. 2005, 318, 145–162. [Google Scholar]
  41. Ianora, A.; Miralto, A.; Halsband-Lenk, C. Reproduction, hatching success, and early naupliar survival in Centropages typicus. Prog. Oceanogr. 2007, 72, 195–213. [Google Scholar] [CrossRef]
  42. Souissi, S.; Carlotti, F.; Nival, P. Food and temperature dependent function of moulting rate in copepods: An example of parameterization for population dynamics models. J. Plankton Res. 1997, 19, 1331–1346. [Google Scholar] [CrossRef]
  43. Uye, S. Resting egg production as a life history strategy of marine planktonic copepods. Bull. Mar. Sci. 1985, 37, 440–449. [Google Scholar]
  44. Marcus, N.H. Ecological and evolutionary significance of resting eggs in marine copepods: Past, present, and future studies. Hydrobiologia 1996, 320, 141–152. [Google Scholar] [CrossRef]
  45. Katajisto, T. Effects of anoxia and hypoxia on the dormancy and survival of subitaneous eggs of Acartia bifilosa (Copepda: Calanoida). Mar. Biol. 2004, 145, 751–757. [Google Scholar]
  46. Sun, X.H.; Sun, S.; Li, C.L.; Wang, M.X. Seasonal change in body length of important small copepods and relationship with environmental factors in Jiaozhou Bay, China. Chin. J. Oceanol. Limn. 2012, 30, 404–409. [Google Scholar] [CrossRef]
  47. Drillet, G.; Hansen, B.W.; Kiorboe, T. Resting egg production induced by food limitation in the calanoid copepod Acartia tonsa. Limnol. Oceanogr. 2011, 56, 2064–2070. [Google Scholar]
  48. Engstrom-Ost, J.; Holmborn, T.; Brutemark, A.; Hogfors, H.; Vehmaa, A.; Gorokhova, E. The effects of short-term pH decrease on the reproductive output of the copepod Acartia bifilosa—A laboratory study. Mar. Freshw. Behav. Phy. 2014, 47, 173–183. [Google Scholar] [CrossRef]
  49. Broman, E.; Brusinm, M.; Dopsonm, M.; Hylanderm, S. Oxygenation of anoxic sediments triggers hatching of zooplankton eggs. Proc. R. Soc. B Biol. Sci. 2015, 282, 20152025. [Google Scholar] [CrossRef]
Water 14 03541 g001 550
Figure 1. The location of the Jiaozhou Bay and sampling stations in the Jiaozhou Bay.
Figure 1. The location of the Jiaozhou Bay and sampling stations in the Jiaozhou Bay.
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Figure 2. Horizontal distribution of Acartia bifilosa abundance (ind/m3) in the Jiaozhou Bay from June to August.
Figure 2. Horizontal distribution of Acartia bifilosa abundance (ind/m3) in the Jiaozhou Bay from June to August.
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Figure 3. Female survival rates of Acartia bifilosa under different seawater temperatures (20, 22, 25, and 28 °C) and Chl a concentrations (a): 15 μg/L, (b): 10 μg/L, (c): 5 μg/L, (d): 0 μg/L.
Figure 3. Female survival rates of Acartia bifilosa under different seawater temperatures (20, 22, 25, and 28 °C) and Chl a concentrations (a): 15 μg/L, (b): 10 μg/L, (c): 5 μg/L, (d): 0 μg/L.
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Figure 4. Egg production rates of Acartia bifilosa under different seawater temperatures (20, 22, 25, and 28 °C) and Chl a concentrations (a): 15 μg/L, (b): 10 μg/L, (c): 5 μg/L).
Figure 4. Egg production rates of Acartia bifilosa under different seawater temperatures (20, 22, 25, and 28 °C) and Chl a concentrations (a): 15 μg/L, (b): 10 μg/L, (c): 5 μg/L).
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Figure 5. Hatching rates of Acartia bifilosa eggs which were produced under different seawater temperatures (20, 22, 25, and 28 °C) and Chl a concentrations (a): 15 μg/L, (b): 10 μg/L, (c): 5 μg/L).
Figure 5. Hatching rates of Acartia bifilosa eggs which were produced under different seawater temperatures (20, 22, 25, and 28 °C) and Chl a concentrations (a): 15 μg/L, (b): 10 μg/L, (c): 5 μg/L).
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Figure 6. Post-embryonic development of Acartia bifilosa under different seawater temperatures (20, 22, 25, and 28 °C) and Chl a concentrations (a): 15 μg/L, (b): 10 μg/L, (c): 5 μg/L).
Figure 6. Post-embryonic development of Acartia bifilosa under different seawater temperatures (20, 22, 25, and 28 °C) and Chl a concentrations (a): 15 μg/L, (b): 10 μg/L, (c): 5 μg/L).
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Figure 7. Cluster analysis of Acartia bifilosa population recruitment under different temperatures and food levels in the Jiaozhou Bay.
Figure 7. Cluster analysis of Acartia bifilosa population recruitment under different temperatures and food levels in the Jiaozhou Bay.
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Figure 8. PCA scatter diagrams of Acartia bifilosa population recruitment parameters (EPR, HR, PDT) and the environmental parameters (temperature and food level) in the Jiaozhou Bay. (EPR: egg production rate; HR: hatching rate; PDT: post-embryonic development time).
Figure 8. PCA scatter diagrams of Acartia bifilosa population recruitment parameters (EPR, HR, PDT) and the environmental parameters (temperature and food level) in the Jiaozhou Bay. (EPR: egg production rate; HR: hatching rate; PDT: post-embryonic development time).
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Table
Table 1. The average egg production rate [avEPR, eggs/(female·day)], average hatching rate (avHR), and the post-embryonic development time (PDT, day) from N1 stage to adult of Acartia bifilosa under different seawater temperatures and Chl a concentrations.
Table 1. The average egg production rate [avEPR, eggs/(female·day)], average hatching rate (avHR), and the post-embryonic development time (PDT, day) from N1 stage to adult of Acartia bifilosa under different seawater temperatures and Chl a concentrations.
Food Level (μg/L)Temperature (°C)avEPRavHR (%)PDT
15280.736810
252.39789
2210.358511
2011.947412
10280.026711
250.747610
2210.219111.5
2010.418812
5280***
250.1171**
221.897712
203.857512
0280**
250**
220**
200**
Note: * data absent because of no egg production; ** data absent because N1 could not develop to adult.
Table
Table 2. Pearson correlations between Acartia bifilosa population recruitment (avEPR, HR, and PDT) and environmental factors (temperature and food level) in the Jiaozhou Bay.
Table 2. Pearson correlations between Acartia bifilosa population recruitment (avEPR, HR, and PDT) and environmental factors (temperature and food level) in the Jiaozhou Bay.
avEPRavHRPDT
Temperature (°C)−0.775 **−0.629 *−0.722 *
Food level (μg/L)0.4320.073−0.542
Note: * negative correlation (p < 0.05); ** negative correlation (p < 0.01).
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Zhang, Z.; Tao, Z.; Gao, X.; Wang, L.; Sun, S. Effects of Temperature and Food Concentration on the Population Recruitment of Acartia bifilosa (Copepoda, Calanoida): Implications for the Over-Summering Life History Strategy in Jiaozhou Bay. Water 2022, 14, 3541. https://doi.org/10.3390/w14213541

AMA Style

Zhang Z, Tao Z, Gao X, Wang L, Sun S. Effects of Temperature and Food Concentration on the Population Recruitment of Acartia bifilosa (Copepoda, Calanoida): Implications for the Over-Summering Life History Strategy in Jiaozhou Bay. Water. 2022; 14(21):3541. https://doi.org/10.3390/w14213541

Chicago/Turabian Style

Zhang, Zhan, Zhencheng Tao, Xiaotong Gao, Lei Wang, and Song Sun. 2022. "Effects of Temperature and Food Concentration on the Population Recruitment of Acartia bifilosa (Copepoda, Calanoida): Implications for the Over-Summering Life History Strategy in Jiaozhou Bay" Water 14, no. 21: 3541. https://doi.org/10.3390/w14213541

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