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Effects of nutrient limitations on three species of zooplankton
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Lei CHEN1, 2, Chaolun LI1, 2, 3, 4, *, Konglin ZHOU5, Yongqiang SHI6, Mengtan LIU7
Acta Oceanologica Sinica | 2018, 37(4) : 58 - 68
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Acta Oceanologica Sinica | 2018, 37(4): 58-68
• Marine Biology •
Effects of nutrient limitations on three species of zooplankton
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Lei CHEN1, 2, Chaolun LI1, 2, 3, 4, *, Konglin ZHOU5, Yongqiang SHI6, Mengtan LIU7
Affiliations
  • 1 Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
  • 2 University of Chinese Academy of Sciences, Beijing 100049, China
  • 3 Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China
  • 4 Center of Deep Sea Research, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
  • 5 Key Laboratory of Marine Ecosystem and Biogeochemistry, Second Institute of Oceanography, State Oceanic Administration, Hangzhou 310012, China
  • 6 Key Laboratory of Sustainable Development of Marine Fisheries of Ministry of Agriculture, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China
  • 7 Jiaozhou Bay Marine Ecosystem Research Station, Chinese Ecosystem Research Network, Qingdao 266071, China
Published: 2018-04-25 doi: 10.1007/s13131-017-1122-z
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Nutrient imbalance—a mismatch in nutrient ratios between the available food supply and the demands of consumers—has the potential to be transported up food chains, exposing zooplankton to nutrient limitations. In this study, the response of Calanus sinicus (copepod), Moina mongolica (cladocera), and Brachionus plicatilis (rotifer) to nutrient-limited (no-limited, P-limited, and N-limited) food were evaluated from the perspective of growth, reproduction, and stoichiometric homoeostasis. The results indicated that the growth of three species was suppressed under nutrient-limited (especially P-limited) conditions. However, the effect of nutrient limitations on their reproduction was species-specific. For C. sinicus, the dietary UFA (unsaturated fatty acid) as a major phospholipid component affected their egg production and total FA supporting energy promoted the hatchability of eggs. Furthermore, excess carbon in the diet promoted egg production but reduced hatching success. For M. mongolica, nutritional (P and UFA) and energy (total FA) support affected their fecundity. B. plicatilis fecundity exhibited the same pattern of growth (no-limited>N-limited>P-limited). In terms of stoichiometric homeostasis, B. plicatilis’s elemental compositions were less likely to be affected by nutrient limitations than M. mongolica. We suggest that the effects of nutrient imbalances could potentially become an evolutionary force affecting ecosystem structure and stability in eutrophic waters.

zooplankton  /  nutrient  /  growth  /  reproduction  /  stoichiometric homoeostasis
Lei CHEN, Chaolun LI, Konglin ZHOU, Yongqiang SHI, Mengtan LIU. Effects of nutrient limitations on three species of zooplankton[J]. Acta Oceanologica Sinica, 2018 , 37 (4) : 58 -68 . DOI: 10.1007/s13131-017-1122-z
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1 Introduction
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Eutrophication is a major pollution problem worldwide (Howarth, et al., 2002) that is associated with increased nutrient concentrations and altered nutrient ratios (based on the Redfield ratio) (Arai, 2001; Nixon, 1995; Purcell et al., 2007). Eutrophication probably changes the nutrient content of phytoplankton (an important food resource for zooplankton) (Rhee, 1978; Elser, 2002; Dickman et al., 2008). Nutrient imbalances between food resources and consumers can cause a mismatch between nutrient supply and demand in planktonic food webs. This mismatch has the potential to affect the growth and reproduction of consumers (Sterner and Elser, 2002). As organisms have different nutrient use strategies, this effect might vary among species. Species-specific changes are likely to become an evolutionary force affecting ecosystem structure, functioning and stability (Chapin et al., 1997; Knops et al., 2002; Sterner and Elser, 2002). However, the mechanisms and approaches involved with species-specific changes in growth and reproduction caused by altered nutrient ratios are not fully understood.
Ecological stoichiometry offers a new perspective in the study of eutrophication (Sterner and Elser, 2002). It is generally accepted that the stoichiometry of primary producers is highly affected by nutrient conditions (Goldman et al., 1979; Hall et al., 2005; Klausmeier et al., 2004; Rhee, 1978; Sterner and Elser, 2002). For example, the molar N:P ratio of Scenedesmus spp. closely tracks variations in N:P supply ratios (Rhee, 1978). Animals usually maintain relative homeostasis (Elser et al., 2000); however, herbivores that encounter low-quality food sources experience difficulty maintaining strict homeostasis when feeding on food that is limited in P or N because of the costs of homeostasis, leading to a mismatch between supply and demand (Elser et al., 2001; Malzahn et al., 2010; Van Nieuwerburgh et al., 2004).
Nutrient supplies from food influence life-history traits such as growth, reproduction and fitness (Sterner and Elser, 2002; Sterner and Schulz, 1998). Studies have shown that the growth conditions of some species of herbivores are affected by nutrient limitations. In Acartia tonsa, P-limited food reduced its growth rate (expressed as RNA:DNA) and no compensatory growth occurred (Malzahn and Boersma, 2012). In Cladocera galeata, P-limited algae was a poor food resource, as the somatic growth rate was lower than N+P-saturated and N-limited algae, which were of a comparable quality (Weers and Gulati, 1997). The somatic growth of Brachionus calyciflorus decreased under P- or N-limited conditions, and the growth rate correlated negatively with the food C:N ratio (Hessen et al., 2007; Jensen and Verschoor, 2004). Under nutrient-limited conditions, reproduction may also be affected. Augustin and Boersma (2006) found that A. tonsa fed with N-limited algae produced more eggs; however, the egg hatching was not significantly affected. B. calyciflorus reproduction decreased when fed with P- or N-limited algae (Jensen and Verschoor, 2004).
Zooplankton have various reproductive modes. Ventura and Catalan (2005) found that some species (Cladocera pulicaria, Cyclops abyssorum, and Diaptomus cyaneus) with different reproductive modes had different elemental variability. The stoichiometric changes (C:P and C:N) of females and their reproductive tissues during reproduction were species specific. Therefore, the effects of nutrient limitations on these species may differ, and the effects on species with different reproductive modes are not fully understood. Therefore, we investigated the effects of food quality (no-limited, P-limited, and N-limited) on the condition of planktonic crustaceans with different reproductive modes. Calanus sinicus (copepod), Moina mongolica (cladocera), and Brachionus plicatilis (rotifer) were chosen as experimental subjects because (1) C. sinicus performs gamogenetic reproduction and the eggs hatch externally from the females, (2) the parthenogenetic reproduction of M. mongolica involves unfertilized eggs that grow up in the brood pouch, and (3) the parthenogenetic reproduction of B. plicatilis is different from that of M. mongolica because the eggs incubate outside the females. In this study, the main objectives were (1) to compare the different responses of three species to nutrient limitations based on their growth, reproduction, and elemental homoeostasis (just for M. mongolica and B. plicatilis) and, (2) based on dietary nutrients (C, N, and P), fatty acids, and amino acids, to explore the potential limiting factors of the growth and reproduction of the three species.
2 Materials and methods
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2.1 Food preparation
Stock cultures of Phaeodactylum tricornutum (diatom) and Skeletonema costatum (diatom) were cultivated in an f/2 culture medium (Guillard and Ryther, 1962), and the Chlorella vulgaris (green algae) was cultivated in a Chlorella culture medium (625 μmol/L NH4NO3, 28.7 μmol/L K2HPO4 and ferric citrate). The seawater used in the experiment was collected from the Huiquan Bay in Qingdao, China. Prior to the experiment, the seawater was filtered through a sterile 0.2 μm filter, heated to a boil, cooled and stored until use. All algal treatments were maintained at (20±0.5)°C under a 12 L:12 D of photoperiod at 4 000 lx of light intensity. The salinity was 30 to 31.
The no-limited treatment consisted of culture-enriched seawater. The two limitation treatments were enriched according to the culture recipe but without the addition of the limiting nutrient (N-limited and P-limited) (Boersma et al., 2009; Malzahn et al., 2010; Schoo et al., 2014). The ionic strength was maintained by the addition of KCl. To ensure the quality and constant supply of algae, new cultures of the three treatments were inoculated every other day and harvested after 5 d. Preliminary tests indicated that the nutrient composition (percentage of dry weight, C%, N% and P%) and molar ratios (C:N, C:P and N:P) of P. tricornutum, C. vulgaris, and S. costatum changed significantly under experimental conditions after a growth period of 5 d (all P<0.05, Table 1). These conditions allowed the zooplankton to feed on algae with different nutritional contents.
2.2 Zooplankton preparation
The adult copepod C. sinicus used for the experiment was collected from R/V Beidou in the Yellow Sea of China during June 2014. The cladocera M. mongolica was obtained from the Ocean University of China. Dormant eggs of rotifer B. plicatilis were bought from a commercial hatchery. Before the experiment, M. mongolica was cultivated in seawater for about one year, and B. plicatilis was hatched in seawater.
Since the survival temperature and appropriate food concentration were different for these three species, they were cultivated at their appropriate temperature and fed with their appropriate food, respectively. The copepod C. sinicus was bred at 8°C, and others were at 20°C. In this study, C. vulgaris (6.5 μg/mL, calculated by carbon) was used as food for the rotifer B. plicatilis, since C. vulgaris was a common bait for B. plicatilis (Chen and Wu, 2005; Yang and Ye, 2000). The cladocera M. mongolica fed on P. tricornutum (5 μg/mL). Before the experiment, M. mongolica was cultivated for about three months feeding on P. tricornutum. S. costatum and P. tricornutum, which were mixed in the same concentration, were used as the food for the copepod C. sinicus (0.5 μg/mL for nauplii and 2 μg/mL for adults). This mixed food could support nauplii and adults with ideal particle size scale (Li et al., 2006). The salinity of seawater used in this experiment was 30 to 31.
2.3 Growth and reproduction experiments
C. sinicus—Groups of 12 adult females and 4 adult males were placed into spawn bottles and eggs harvested within 24 h were used for the experiment. They were placed into 24 glass beakers at 125 eggs per beaker. Three treatments (no-limited, N-limited and P-limited)×eight replicates were established. Algae were added and refreshed every other day. After the eggs hatched, growth conditions of nauplii (total length and developmental stage) were monitored.
Fifteen groups (three treatments×five replicates) of nine adult female copepods and four adult males were placed into spawn bottles. Algae were added and refreshed every other day. After cultivation for 48 h, the egg production of three treatments was monitored for 5 d. The egg production rate represents the number of eggs produced by one female during one day. Every day, the eggs produced were transferred into 6-well microtiter plates. The hatching success was calculated as the percentage of eggs hatched in 24 h of the total eggs.
M. mongolica—Newborns within 12 h after birth were collected. They were transferred to 6-well microtiter plates with three individuals per well. Three treatments (no-limited, N-limited and P-limited)×eighteen replicates were established. Algae were added separately to the three treatments and refreshed every other day. Since there were about 6 d before subitaneous eggs production, in this study, the growth condition was monitored every 2 d. Forty-five individuals were randomly selected from each treatment and their total lengths were measured using the ocular micrometer of a dissecting microscope (Olympus SZ61). After 6 d, the subitaneous eggs were counted for fecundity determination. The fecundity was assessed as the number of subitaneous eggs produced by one female during the experiment.
B. plicatilis—Resting eggs were incubated in shallow dishes containing sterile seawater. Neonate (<2 h) were transferred to 24-well microtiter plates at two individuals per well in a 2 mL food suspension. Three treatments (no-limited, N-limited and P-limited)×forty-eight replicates were established. C. vulgaris were added separately and refreshed every other day. As B. plicatilis produced eggs after the cultivation of about 40 h, in this study, the growth condition was observed every 12 h. Twenty individuals, which were randomly selected from each treatment, were fixed in ultrapure water. Then, their bodies were turned over to measure the maximum area (including the foot and egg) from the top view using an inverted microscope (Nikon AZ100) with the software of NIS-Elements D 3.0. After cultivation of 36 h, the fecundity was assessed as the number of eggs produced by one individual during the experiment.
Comparison of growth rate between species—The variation in the species’ growth rate based on their food’s stoichiometry (N:P, C:P, and C:N) was compared. The growth rate was calculated as G=(Lt-L0)/t, where G is the growth rate, Lt and L0 are the total length of C. sinicus and M. mongolica or the root square of the maximum area of B. plicatilis after t days and at the beginning of the experiments, and t is the experimental duration. The stoichiometry of each species’ food was used as the x-axis, and the corresponding growth rate was used as the y-axis.
2.4 Homoeostasis experiments
Newborns (within 12 h for M. mongolica, 2 h for B. plicatilis and 24 h for C. sinicus) were transferred to 2 L beakers at 10 ind./L for M. mongolica, 100 ind./L for B. plicatilis, and 5 ind./L for C. sinicus. Three treatments×three replicates were established. Since these three species had different life history traits (especially life span) (Lin and Li, 1984; Wang and He, 2001), their response time to nutrient conditions were different. In this study, M. mongolica were cultivated for 10 d, and B. plicatilis were cultivated for 5 d under different nutrient conditions. Then they were collected to analyze C, N, and P contents. For C. sinicus, samples collected after cultivation of 15 d were not enough to analyze C, N, and P contents.
To estimate the ability of M. mongolica and B. plicatilis to maintain homoeostasis, the homoeostatic regulation coefficient (H) was calculated according to the following equation (Sterner and Elser, 2002): y=c x 1 H . The H in this study was calculated to linearize the equation above using logarithms (Sterner and Elser, 2002): logy=logc+ logx H , where y is the stoichiometry (e.g., N:P and C:P) of M. mongolica or B. plicatilis and x is the stoichiometry of their food. Linear regressions were fitted, and the parameters of these regressions were used to assess the homoeostatic responses of these three species.
2.5 Analytical procedures
For analysis of the C and N contents, the samples were coated with tin boats and measured using an elemental analyzer (Elementar Company (EL), Germany). To analyze the P content, the samples were weighed and digested with 5 mL of nitric acid and 1 mL of perchloric acid; then, the temperature of the heating plate was increased from 175°C to 220°C to dry out the acid solution. Next, the solution was cooled to room temperature and 1:1 nitric acid was added to the sample. The sample was rinsed with Milli-Q deionized water and transferred to 25 mL specimen tubes. Then, all samples with a series of standard solution (0, 1, 5, 10, 20, 50 μg/L) and with a 20 μg/L Rh internal standard solution were analyzed using an ICP plasma emission spectrometer (Thermo Fisher Scientific, iCAP-Qc).
To analyze the amino acid content, approximately 20 mg of each of the samples was placed in an ampoule and 10 mL of 6 mol/L HCl and N2 were added; then, the ampoule was sealed and placed in a 110°C drying oven for 24 h of hydrolyzation. Subsequently, 0.02 mol/L of HCl was added to a volume of 10 mL. The amino acid content was evaluated using high-performance liquid chromatography (HPLC) with phenylisothiocyanate as the reagent. An Agilent 1100 liquid chromatograph was used with a Venusil-AA (4.6×250 mm, 5 μm) column at a temperature of 40°C, detection wavelength of 254 nm, mobile phase A of 0.1 mol/L sodium acetate (7% acetonitrile), mobile phase B of 80% acetonitrile, and gradient elution of 1 mL/min. The fatty acids were measured as fatty acid methyl esters (FAMEs) after the method described by Liu et al. (2011).
2.6 Statistical analysis
The nutrient composition and molar ratios of C. vulgaris, P. tricornutum, S. costatum, and a combination of P. tricornutum and S. costatum as well as their nutritional content (fatty acid, amino acid) were statistically analyzed using a one-way ANOVA with treatment as the variable. Tukey’s HSD test was used as the post hoc test. The Kruskal-Wallis test was used when the data did not approach homoscedasticity (Levene’s test) or normality (Kolmogorov-Smirnov test). All statistical tests were carried out with SPSS 19.0 and Origin 9.0.
3 Results
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3.1 Food nutrition
Figure 1 showed that, for P. tricornutum and the mixture of P. tricornutum and S. costatum, the lowest content of total fatty acids (FA), saturated FA (SFA), and unsaturated FA (UFA) and the highest value of SFA/UFA were detected in the no-limited treatment. However, the highest content of total FA, SFA, and UFA and the lowest value of ω3/ω6 FA were exhibited in the N-limited treatment. In terms of amino acids (AA), the no-limited treatment had the highest content and the N-limited treatment had the lowest content.
For C. vulgaris, the no-limited treatment had the lowest content of total FA, SFA, and UFA and the lowest value of SFA/UFA. In terms of AA, the no-limited treatment had the highest content. In contrast, the P-limited treatment had the highest content of total FA, SFA, and UFA; the highest value of SFA/UFA; the lowest value of ω3/ω6 FA; and the lowest content of AA.
3.2 Zooplankton growth
The total length of C. sinicus exhibited significant differences among the three treatments on the 11th day (Kruskal-Wallis test, P<0.01; Fig. 2). The no-limited treatment resulted in the highest value of total length, followed by the N-limited treatment and the P-limited treatment (no-limited: 692 μm, N-limited: 648 μm, and P-limited: 517 μm; Fig. 2). The no-limited treatment also had the highest percentage of individuals reached the stage of Copepodite 1. The P-limited treatment had the lowest percentage (no-limited: 60%, and P-limited: 20%; Fig. 2).
For M. mongolica, the highest value of total length was observed in the no-limited treatment and the lowest value was found in the P-limited treatment during the three days after the experiment started (Fig. 3a). However, during the three days before the experiment ended, the lowest value of the total length was observed in the N-limited treatment (Fig. 3a).
For B. plicatilis, during 36 h after the experiment started, the highest value of the maximum area was found in the no-limited treatment and the lowest value was found in the P-limited treatment (Fig. 3b). In contrast, during 12 h before the experiment ended, individuals in the N-limited treatment had the highest value of the maximum area, followed by those in the no-limited treatment and those in the P-limited treatment.
The highest growth rate of the three species (C. sinicus, M. mongolica, and B. plicatilis) was obtained when the dietary N:P value was 20 to 30 (Fig. 4a). This finding was in line with the Redfield ratio (N:P=16). When the N:P value deviated from 20 to 30, the growth rate of the three species declined. The extent of this decline was species specific. In general, compared with M. mongolica and C. sinicus, the growth rate of B. plicatilis declined more rapidly with the deviation of the N:P value (from 20 to 30) (Fig. 4a).
The highest growth rate was obtained when the C:P was 100–200, which was in line with the Redfield ratio (C:P=106). The growth rate of B. plicatilis exhibited a more substantial increase with the P sufficiency than that of M. mongolica and C. sinicus. With respect to the dietary C:N value, the growth rate of B. plicatilis decreased more slowly under N deficiency than under the other treatments.
3.3 Zooplankton reproduction
Both the egg production and hatching rate of C. sinicus were affected by nutrient conditions (no-limited, N-limited, and P-limited) (Figs 5a, b). During most of the experiment, the highest value of the egg production rate was found in the P-limited treatment and the lowest value was observed in the N-limited treatment (Fig. 5a). On the whole, the hatching success was negatively affected by P limitation. During most of the experiment, the hatching success in the P-limited treatment was lower than that in the no-limited treatment (Fig. 5b).
The fecundity (eggs per individual) of M. mongolica was significantly different among the three treatments (one-way ANOVA, P<0.01; Fig. 6a). Individuals in the N-limited treatment exhibited the highest fecundity, whereas those in the P-limited treatment had the lowest fecundity (N-limited: 0.49, no-limited: 0.16, and P-limited: 0.03; Fig. 6a).
The fecundity (eggs per individual) of B. plicatilis differed significantly among the three treatments (one-way ANOVA, P<0.01; Fig. 6b). The no-limited treatment exhibited the highest value of fecundity (0.88, Fig. 6b), followed by the N-limited treatment, with a value of 0.69, and the P-limited treatment, with the lowest value of 0.41 (Fig. 6b).
3.4 Zooplankton elemental homoeostasis
From the perspective of the homoeostatic regulation coefficient (H), for each stoichiometry (N:P, P%, etc.), the H value of B. plicatilis was higher than that of M. mongolica (Table 2). Furthermore, the absolute value of 1/H (slope) of B. plicatilis was closer to zero than that of M. mongolica (Table 2). For example, the 1/HC:P value of M. mongolica differed by 0.27 from zero, whereas the value of B. plicatilis differed by just 0.08; the absolute value of 1/HC% was 9.62 for M. mongolica and was only 0.57 for B. plicatilis (Table 2).
4 Discussion
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4.1 Growth
In our study, the growth of three species was suppressed by nutrient limitations (especially P limitation) (Figs 2 and 3). The P limitation was strongly coupled to the RNA synthesis (Elser et al., 1996; Sterner and Hessen, 1994), which has been detected in copepods (Malzahn and Boersma, 2012), cladocera (Vrede et al., 2002), and rotifers (Hessen et al., 2007). As ribosomes are the machinery of proteins synthesis, there was a close association between the P supply and protein synthesis. In P-limited treatment, protein synthesis of three species could be suppressed, and then, their growth may be negatively affected.
N-limitation also had effect on the growth of organisms and could be associated with AA content. In this study, under the N-limited condition, dietary essential AA (EAA) content was significantly lower than that in the no-limited treatment (Fig. 1 and Table 2). It was reported that non-essential AA synthesis could also be suppressed under the N-limited condition (Sterner and Elser, 2002). Lack of essential and unessential AA under N-limited condition could negatively affect protein synthesis. And then, the growth was potentially suppressed.
4.2 Reproduction
Under nutrient-limited conditions, three species exhibited different performance in terms of reproduction (Figs 5 and 6). And different mechanism how nutrient limitation affected the reproduction of three species was detected.
4.2.1 Dietary stoichiometry and reproduction
This study indicated that the main factor of dietary stoichiometry affecting the reproduction of three species was C:P ratio.
For copepods, eggs had a higher value of C:P than tissues (females without eggs) (Becker and Boersma, 2005). Females should balance the gain and loss of egg production from the perspective of nutrient output. In this study, the dietary C:P ratio in the P-limited treatment (449, Table 1) was far above the Redfield ratio (106), suggesting the carbon excess. For copepods, it was an effective strategy to produce more eggs to relieve the carbon surplus, since eggs had a higher C:P ratio than tissues (Becker and Boersma, 2005). Accordingly, the highest egg production rate (on the whole) was observed in the P-limited treatment (Fig. 5a). Inversely, the N-limited treatment, which was relatively carbon deficient (dietary C:P=58), exhibited the lowest egg production rate (Fig. 5a).
For cladocera, the P concentration in eggs was reported to be constant (Becker and Boersma, 2005; Færøvig and Hessen, 2003). Thus, the number of eggs would be suppressed if the dietary nutrient was limited. Under P-limited condition, females which were phosphorus deficient (dietary C:P, 750; TERC:P, 250) could not support high egg production (Fig. 6a). Inversely, in N-limited treatment, females with relative excess of phosphorus (dietary C:P=53.5) tended to produce more eggs (Fig. 6a).
In this study, newly born rotifers were cultured under nutrient-limited conditions until the fecundity was detected (36 h of cultivation). It can be speculated that these rotifers reached maturity later and had shorter reproductive period than those in the no-limited treatment. Meanwhile, it was reported that, under nutrient-limited conditions, reproduction of the rotifer Brachionus calyciflorus reduced (Jensen and Verschoor, 2004). Thus, shorter reproductive period and lower daily reproduction may be the reasons for the lower fecundity in nutrient-limited treatments (Fig. 6b).
4.2.2 Dietary biochemical composition and reproduction
For C. sinicus, dietary EAA content in the N-limited treatment was significantly lower than that of others (P<0.05, Fig. 1 and Table 2). Helland et al. (2003) reported that EAA content of Calanus finmarchicus eggs was quite constant irrespective of their maternal diet. In this study, dietary EAA in the N-limited treatment (Fig. 1 and Table 2) could meet the needs of fewest eggs, leading to the lower egg production rate (Fig. 5). Besides that, Phospholipids were known to be used to form gonads (Kattner et al., 2007; Lee et al., 2006) and cell constituents (e.g., membranes) in the process of gonadogenesis and oogenesis (Kattner et al., 2007; Lee et al., 2006). PUFA, as major components of phospholipids (Chen et al., 2012; Harrison, 1990), had effect on the egg production (Sargent and Falk-Petersen, 1988). In our study, the N-limited treatment had the lowest proportion (total FA content percentage) of UFA (Fig. 1 and Table 3), which may cause PUFA deficiency and restrained the egg production (Fig. 5).
Meanwhile, as fatty acids were used to provide energy for embryonic development (Kattner et al., 2007), the highest storage of total FA in the N-limited treatment (Fig. 1 and Table 3) could facilitate the higher hatching success (Fig. 5).
For M. mongolica, in the N-limited treatment, significantly higher concentration of total FA and UFA (Fig. 1 and Table 3) may promote higher fecundity (Fig. 6), since fatty acids are essential to egg development as major energy support and PUFA play an important role in the structural and complex physiological development of cladocera (Weers and Gulati, 1997).
For B. plicatilis, the lowest quality of dietary FA and AA in P-limited treatment (Fig. 1, Tables 2 and 3) could cause the worst growth and reproduction, since dietary FA and AA have been shown to be important for zooplankton growth and reproduction (e.g., Jensen and Verschoor, 2004; Müller-Navarra, 1995; Urabe et al., 2002).
4.3 Stoichiometric homoeostasis
B. plicatilis and M. mongolica had different values of H, implying different abilities in terms of maintaining constant chemical compositions. For each stoichiometry (N:P, P%, etc.), the 1/H (slope) of B. plicatilis was much closer to zero than that of M. mongolica (Table 2). As the slope (1/H) of zero represents the condition of homeostasis (Sterner and Elser, 2002), the above results implied that B. plicatilis exhibited a greater ability than M. mongolica to maintain constant elemental compositions. In other words, compared with M. mongolica, B. plicatilis’s elemental compositions were less likely to be affected by nutrient limitations.
4.4 Relationship with eutrophication
Exploring different response of species to nutrient limitations could provide valuable insights into the mechanism of population succession under the condition of eutrophication. Changes in N:P stoichiometry over time have been observed in coastal areas (Wang, 2006). It was reported that, in the Changjiang (Yangtze River) Estuary, China, the N:P ratio has increased sharply approximately from 50 to 125 in ten years (Wang, 2006). This changing nutrient stoichiometry could be transported up the food chain and caused a mismatch between nutrient supply and demand in planktonic food webs, leading to nutrient limitation (Sterner and Elser, 2002). Our study found that effect of this nutrient limitation on the growth, reproduction, and stoichiometric homoeostasis varied with species. In this study, three species with different reproductive modes exhibited different patterns of reproduction among three treatments and different mechanism how nutrient limitation affected their reproduction was detected. It could be speculated that populations with different reproductive modes might be affected by nutrient limitations differently. In the long run, this process could become an evolutionary driving force and likely change the process and direction of population succession in coastal areas.
5 Conclusions
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Our study indicated that the nutrient imbalance associated with eutrophication influenced zooplankton growth, reproduction and stoichiometric homeostasis. The growth of three species was suppressed under nutrient-limited (especially P-limited) conditions. However, the effect of nutrient limitations on their reproduction was species-specific. For example, the highest fecundity was detected in no-limited treatment for B. plicatilis, while in N-limited treatment for M. mongolica. Dietary C:P ratio, FA and AA content played important roles on this species-specific response. As for the stoichiometric homeostasis, B. plicatilis exhibited a greater ability to maintain a constant chemical composition in the bodies of M. mongolica. These effects of nutrient imbalance could potentially become an evolutionary force affecting ecosystem structure and stability in water bodies undergoing eutrophication. Further studies examining the physiological processes underlying these species-specific responses will deepen our understanding of the ecological consequences of eutrophication in marine ecosystems.
Acknowledgements
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The authors thank the crew on R/V Beidou for their assistance in the field. We are grateful to Jin Xin and Ji Peng for their invaluable help during shipboard research activities.
Funding
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  • The National Key R & D Program of China under contract No. 2017YFC1404401; the National Natural Science Foundation of China under contract No. 41476139; the National Basic Research Program of China under contract No. 2015CB452903.
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Appendix
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Year 2018 volume 37 Issue 4
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Article Info
doi: 10.1007/s13131-017-1122-z
  • Receive Date：2017-05-24
  • Online Date：2026-04-13
  • Published：2018-04-25
Article Data
Affiliations
History
  • Received：2017-05-24
  • Accepted：2017-09-18
Funding
The National Key R & D Program of China under contract No. 2017YFC1404401; the National Natural Science Foundation of China under contract No. 41476139; the National Basic Research Program of China under contract No. 2015CB452903.
Affiliations
    1 Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
    2 University of Chinese Academy of Sciences, Beijing 100049, China
    3 Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China
    4 Center of Deep Sea Research, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China
    5 Key Laboratory of Marine Ecosystem and Biogeochemistry, Second Institute of Oceanography, State Oceanic Administration, Hangzhou 310012, China
    6 Key Laboratory of Sustainable Development of Marine Fisheries of Ministry of Agriculture, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China
    7 Jiaozhou Bay Marine Ecosystem Research Station, Chinese Ecosystem Research Network, Qingdao 266071, China

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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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