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Grazing and performance of the copepod Pseudodiaptomus poplesia on a Chinese strain of Aureococcus anophagefferens
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Xuejia HE1, 2, Didi HAN1, 2, Liuyu HAN1, 2, 3, Songhui LU1, 2, *
Acta Oceanologica Sinica | 2018, 37(4) : 69 - 76
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Acta Oceanologica Sinica | 2018, 37(4): 69-76
• Marine Biology •
Grazing and performance of the copepod Pseudodiaptomus poplesia on a Chinese strain of Aureococcus anophagefferens
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Xuejia HE1, 2, Didi HAN1, 2, Liuyu HAN1, 2, 3, Songhui LU1, 2, *
Affiliations
  • 1 Research Center of Harmful Algae and Marine Biology, Jinan University, Guangzhou 510632, China
  • 2 Key Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, Jinan University, Guangzhou 510632, China
  • 3 South China Sea Institute of Planning and Environmental Research, State Oceanic Administration, Guangzhou 510300, China
Published: 2018-04-25 doi: 10.1007/s13131-018-1168-6
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Brown tides have recurred in estuary areas globally, but trophic interactions between the causative species Aureococcus anophagefferens and planktonic copepods remain poorly understood. In this study, we investigated performance (ingestion, growth, development and reproduction) of the planktonic copepod, Pseudodiaptomus poplesia, offered either mono-algal or mixed-algal diets containing a Chinese strain of A. anophagefferens. A typical Michaelis-Menten pattern existed between ingestion rate and food level when copepod fed on the mono-algal diet of this species. Nauplii exhibited the highest maximum ingestion rate (Imax) than copepodids and adult females. In addition, Imax value was higher in nauplii feeding on A. anophagefferens than on Skeletonema costatum. When fed mixtures of A. anophagefferens and S. costatum, P. poplesia selected against A. anophagefferens cells, but less strongly at the naupliar stage. Nauplii did not undergo metamorphosis and died at late naupliar stages feeding on A. anophagefferens alone, similar to those under starvation. Furthermore, the presence of A. anophagefferens greatly reduced the reproduction rate of females in mixtures but did not influence the growth rate of copepodids. These results suggest that P. poplesia nauplii may exert grazing pressure on A. anophagefferens population during a brown tide, which, however, may not be persistent because of copepod population decline.

A. anophagefferens  /  copepod  /  grazing  /  growth  /  development  /  reproduction
Xuejia HE, Didi HAN, Liuyu HAN, Songhui LU. Grazing and performance of the copepod Pseudodiaptomus poplesia on a Chinese strain of Aureococcus anophagefferens[J]. Acta Oceanologica Sinica, 2018 , 37 (4) : 69 -76 . DOI: 10.1007/s13131-018-1168-6
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1 Introduction
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Blooms of the eukaryotic microalga Aureococcus anophagefferens have recurred in estuary areas in USA and South Africa (Bricelj and Lonsdale, 1997; Probyn et al., 2001; Gobler et al., 2005). Recently, this species was also reported to be responsible for brown tides in estuaries of the Bohai Sea area in eastern China every year since 2009 (Zhang et al., 2012). Trophic interaction with zooplankton is the most direct and widespread biological factor to control phytoplankton population. It has been shown in previous studies that grazing of microzooplankton including protozoans and the nauplii of copepods can potentially regulate Aureococcus spp. population during brown tides (Deonarine et al., 2006; Smith et al., 2008).
Size of prey determines efficiency of grazing of copepod and the minimum size spectrum is generally 1–3 µm for copepod. It is expected theoretically that A. anophagefferens, with a size of 2–4 µm (Uye et al., 1983; Berggreen et al., 1988), may not be readily grazed by copepods. However, nauplii of Acartia tonsa exhibited a high ingestion rate feeding on A. anophagefferens alone in the study by Smith et al. (2008). Moreover, copepod at elder stages showed significant consumption on bacterioplankton or phytoplankton species less than 5 µm in early studies (Boak and Goulder, 1983; Nejstgaard et al., 1997; Broglio et al., 2004). Calbet et al. (2000) reported high consumption of 100%–260% body/d (calculated by carbon) on 2–5 µm nanoplankton by four species of small copepod in a subtropical bay. It appeared that these species flexibly shifted feeding preference according to the size spectrum of the phytoplankton assemblage, indicating opportunistic feeding (Poulet, 1977; Brucet et al., 2008). Thus copepodids or adult copepods may also graze on A. anophagefferens, which, however, has been ignored in previous studies.
Field and laboratory evidences have accumulated to show that brown tides bring about detrimental effects on their grazers, which will doubtlessly mitigate the grazing pressure from zooplankton. Bivalve mortality, the retarded growth of planktonic grazers, and the decreased egg production of copepods usually occurred during brown tides (Buskey and Stockwell, 1993; Bricelj and Lonsdale, 1997). Some hypothetical mechanisms may contribute to detrimental effects of A. anophagefferens. Some toxic excreta of this species may be involved. Dimethylsulfoniopropionate (DMSP) was found in the culture of A. anophagefferens (Keller et al., 1989), and was later proven to be able to inhibit the grazing of some tintinnids (Carlsson et al., 1990; Buskey and Hyatt, 1995). A dopamine analogue in the outer polysaccharide layer may also account for the inhibition of feeding ability of some bivalves (Gainey and Shumway, 1991). In addition, stickiness of the outer polysaccharide layer might cause feeding cessation in shellfish and feeding reduction in ciliates (Smith et al., 2008). However, the exact mechanism remains obscure so far. It was recently pointed out that the negative effect of this species on copepods could be associated with its nutritional inadequacy because the presence of alternative algal species in the diet mitigated adverse effects (Lonsdale et al., 1996). In most early studies, only survival and reproduction were used as endpoints for estimation of the impact of brown tides on copepods (Buskey and Stockwell, 1993; Lonsdale et al., 1996; Bricelj and Lonsdale, 1997). Recently, the impact of this species also manifested itself as suppression in ingestion and development of nauplii of A. tonsa even on mixed diets (Smith et al., 2008). Apperantly, the effect of A. anophagefferens on copepods is far from being well understood, and the copedite stages have been neglected in previous studies. Moreover, it is still unknown how these negative effects related to grazing behavior of elder stages of copepod. Finally, the negative effect of A. anophagefferens, derived from the morphological and toxicity traits, is probably strain-specific. In the study by Smith et al. (2008), even the different isolates exhibited different toxicities and led to different feeding responses in nauplii. This doubtlessly will complicate evaluation of the impact of A. anophagefferens on grazers.
The brackish-water calanoid copepod Pseudodiaptomus poplesia distributes in many temperate and subtropical estuaries in East Asia and is also the common species in the area with occurrence of brown tides in China. The objective of this work was to explore grazer-prey interaction between all developmental stages of P. poplesia and A. anophagefferens. A Chinese strain of A. anophagefferens and a common species Skeletonema costatum in Chinese coastal waters were chosen as main preys. We firstly examined feeding behavior of P. poplesia on A. anophagefferens in mono-algal or mixed-algal diets at juvenile and adult stages. Then, somatic growth, the development of juveniles, survival, and reproduction were investigated with and without the presence of alternative food particles to understand the effect of A. anophagefferens on the performance of P. poplesia.
2 Materials and methods
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2.1 Zooplankton and algae
The copepod P. poplesia were originally collected in the Daya Bay, the South China Sea (21°C, salinity of 25) and then maintained in our laboratory for half a year. They were fed a mixture of Isochrysis galbana and Thalassiosira weissflogii in 0.22-µm filtered seawater (salinity of 25). The Chinese strain of A. anophagefferens was firstly isolated from the Bohai Sea, China. The alga I. galbana originated from the Key Laboratory of Tropical Marine Bio-resources and Ecology, Chinese Academy of Sciences. These two species had been maintained in our laboratory for one and a half years, whereas T. weissflogii and S. costatum more than five years. The f/2 medium for culture of I. galbana and S. costatum was made from MBL artificial sea water (ASW; Cavanaugh, 1956) according to Guillard and Ryther (1962). Aureococcus anophagefferens was grown in L1 medium made also from ASW (Guillard and Hargraves, 1993). Algal cells were harvested at the exponential phase with centrifugation (3 000 r/min, 5 000 g) for 10 min at 4°C. The algal cells were re-suspended with ASW to prepare for the following feeding and performance experiments. All organisms were grown at 20°C under a 12 h:12 h light: dark cycle. Aureococcus anophagefferens was grown at an irradiance of 200 μE/(m2∙s), whereas T. weissflogii, I. galbana, and S. costatum at an irradiance of 100 μE/(m2∙s).
2.2 Grazing experiments
Grazing experiments were performed with nauplii, copepodids and adult females of P. poplesia on a mono-specific diet of A. anophagefferens or S. costatum. Food concentrations were 0.1, 0.25, 0.5, 0.75, 1.0, and 2 mg/L, equal to 6.9×104, 1.7×105, 3.4×105, 5.2×105, 6.9×105, and 1.4×106 cells/mL for A. anophagefferens and 6.7×103, 1.6×104, 3.3×104, 5.0×104, 6.6×104, and 1.3×105 cells/mL for S. costatum, respectively (Table 1). One hundred and eighty nauplii at Stage III (NIII), 180 copepodids at Stage IV (CIV) or 90 adult females from the same cohort were distributed equally into six 200-mL beakers holding 150 mL ASW and fed at corresponding food levels for acclimation for 1 d. Then 30 nauplii, 30 copepodids or 15 adult females of each beaker were further randomly distributed into three 50-mL tubes containing 50 mL medium at the corresponding food level using open-mouth pipettes. Each treatment had three control tubes containing only medium and algal cells. The tubes were capped and then placed in a Ferris wheel, which rotated at 0.8 r/min for 12 h in darkness at 20°C. At the beginning and end of the incubation, 3 mL of aliquots were sampled from each tube and fixed with Lugol’s iodine for determination of the initial and final cell densities. When the experiment ended, animals were counted for mortality estimation. During the experiment, the mortality was less than 5%. The cell densities were counted under inverted microscopy (Olympus IMT-2) using a Neubauer hemocytometer and plankton-counting chamber. Ingestion rate (IR, μg/(ind.∙d)) was calculated using the following equation (Frost, 1972):
$IR = \frac{{V{\rm{(}}\ln {C_{\rm{t}}} - \ln {C_{{\rm{tf}}}}{\rm{)(}}{C_{{\rm{tf}}}} - {C_0}{\rm{)}}}}{{N{\rm{(}}\ln {C_{{\rm{tf}}}} - \ln {C_0}{\rm{)}}t}},$
where V is the volume of seawater in the experimental beakers, N is the number of copepods, C0 and Ctf are the concentration of algal cells before and after feeding, respectively, Ct is the final algal concentration in each control tube, and t is the feeding time.
Ingestion rate data for P. poplesia were fitted to the Michaelis-Menten equation:
$IR = \frac{{{I_{\max }}(C - {C_0})}}{{{K_{IR}} + (C - {C_0})}},$
where Imax is the maximum ingestion rate (µg/(ind.∙d), calculated by carbon) or represented as the percentage of copepod body carbon ingested with unit of %/d, C is the prey concentration (mg/L), C0 is the concentration at which ingestion ceases, and KIR is the prey concentration sustaining 1/2 Imax.
2.3 Feeding selectivity
Feeding selectivity of P. poplesia was studied using a similar approach described for grazing experiments except for that mixed diets were used. Three mixed diets comprised 20:80, 50:50, or 80:20 A. anophagefferens:S. costatum (in carbon content) at a food level of 1 mg/L (Table 1). The experiment was conducted in triplicate in a Ferris wheel at 0.8 r/min for 12 h. Each replicate tube containing 50 mL medium had 10 nauplii at Stage III, 10 copepodids at Stage IV, or 5 adult females with the mixed algae. Each treatment had three control tubes containing only food particles. Based on IRs calculated following grazing experiments, three electivity indices were calculated and compared to determine whether P. poplesia displayed feeding preference for algal species in mixtures of algal cells: (1) Ivlev’s original index, (2) forage ratio, and (3) Jacob’s Index (a variation of Ivlev’s), which accounts for the relative abundance of the prey items (Ivlev, 1961; Jacobs, 1974). Ivlev and Jacob indices range from –1 (selective avoidance) to 1 (preference), and a value of zero indicates no selective behavior. FR index ranges from 0 to 1 (negative selection) and 1 to +∞ (positive selection), whereas a value of 1 indicates no selective behavior.
2.4 Development of juveniles
Copepods were fed 100% A. anophagefferens (Aa), 100% I. galbana (ISO), 100% S. costatum (SKE), 50:50 Aa:SKE, or 50:50 SKE:ISO or starved from naupliar stage to investigate the effect of A. anophagefferens on the growth and development of juveniles. Nauplii were cultured individually in Petri dishes each containing 10 mL medium with an initial food level of 1 mg/L except for the starved group. Food was added daily, and the medium was renewed every other day. There were 60 Petri dishes for each food regime. Every day, animals were inspected under a microscope, and development and survival were recorded. Body length was measured at the beginning of the incubation, at copedite Stage I, and Stage VI for each alive individual. The body length of copepodids and adults was measured immediately from the beginning of the cephalothorax to the end of the caudal rami without accounting for the caudal setae. For nauplii the total body length was measured. Specific growth rates (SGR) were calculated using the following equation:
$\mu = \frac{{\ln {l_t} - \ln {l_0}}}{t},$
where l0 and lt are the mean body length of P. poplesia at the beginning and end of a time interval t (d). The experiment lasted 20 d.
2.5 Reproduction experiment
Reproduction of matured adults in the development experiment was studied. One female without eggs and one male were transferred into a Petri dish containing 20 mL medium to produce eggs. There were 10 to 18 replicates for each treatment. During the four days of incubation, animals were fed with the same food regime as in the development experiment as medium was changed daily. Every day, the adults were gently transferred to new medium using open mouth pipettes, and the nauplii were counted under a stereo microscope. At the end of incubation, eggs in egg sacs were also counted. Reproduction rate was then calculated as the sum of nauplii and eggs divided by the number of female and the duration of incubation (4 d). Because the nauplii died in the treatments of starvation and A. anophagefferens alone, no reproduction was recorded for these two treatments.
2.6 Chemical measurement and data analysis
One hundred juveniles (Stages NIII or CIV) or 40 adult females were filtered gently on pre-combusted (480°C, 2 h) Whatman GF/C filters and then rinsed with 1 mL 2.5% ammonium formate solution for desalination. The samples were dried at 60°C for 48 h and weighed with a Sartorius microbalance to the nearest μg. Then, the particulate carbon and nitrogen were measured with a CHN analyzer (Series II CHNS/O Analyzer, PerkinElmer Instruments).
Differences in grazing, growth, reproduction, or survival rate of animals among treatments were compared by One-way ANOVA, and Turkey post-hoc tests were used to analyze differences between two treatments. The contribution of life stage and the interaction between algal species and life stage to Imax were analyzed by Two-way ANOVA. The Wilcoxin signed-rank test was applied to determine the significance of grazing preference. All statistical analyses were performed using SPSS 19.0 statistical software. The level of significance for all critical ranges was set at P<0.05.
3 Results
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3.1 Ingestion rate
Generally, IR of P. poplesia increased with food level up to a feeding plateau. Ingestion rate as a function of food level was closely fitted to Michaelis-Menten kinetics in all cases (P<0.05, Fig. 1 and Table 2). Copepodids and adults feeding on A. anophagefferens had comparable Imax values, which were 40%–48% higher than that of nauplii (P<0.01, One-way ANOVA and Tukey post-hoc tests). Accordingly, mass-specific Imax dropped remarkably from (89.5±7.2) to (43.0±3.4)%/d with increasing age, showing a typical allometric trend (P<0.000 1, One-way ANOVA; P<0.013, Tukey post-hoc tests). With S. costatum as the prey, Imax value increased continuously from (1.03±0.12) to (2.95±0.15) µg/(ind.∙d) with developmental stage (Table 2; P<0.01, One-way ANOVA and Tukey post-hoc tests), but no ontogenic variation in mass-specific Imax was present (all P>0.05, One-way ANOVA and Tukey post-hoc tests). The interaction between prey species and life stage on IR was analyzed. Both Imax and KIR values were strongly influenced by life stage (P<0.005) but only moderately by algal species (0.01<P<0.05). Furthermore, a strong interaction existed between the two factors (P<0.05, Two-way ANOVA). In detail, nauplii had a higher Imax value on A. anophagefferens than on S. costatum and the opposite trend occurred in female adults.
3.2 Grazing selectivity
Ivlev, Jacob and FR indices all indicated that P. poplesia selected against A. anophagefferens at Stages NIII, CIV and CVI regardless of proportion of A. anophagefferens and S. costatum in mixed diets (P<0.05, Wilcoxin signed-rank test) (Table 3). However, it seemed that nauplii were less selective than copepodids and adults because most of selectivity indices were close to the neutral values in nauplii (zero for Ivlev’s and Jacob’s indices and 1 for the FR index). Ingestion rate ratio (IRAa: IRSKE) was correlated significantly with Aa:SKE ratio in mixed-algal diets (Fig. 2). Slopes of regression were in the range of 0.17±0.04 to 0.36± 0.05 and nauplii had the highest value, demonstrating a tendency of opportunistic feeding.
Total ingestion rates (TIRs) of copepodids and adult females P. poplesia feeding on 20:80 (Aa:SKE) mixture was (0.27±0.06) and (0.47±0.05) μg/(ind. ∙d), higher than on 50:50 and 80:20 mixtures ((0.29±0.08) to (0.40±0.07) μg/(ind.∙d), Fig. 3). Differently, nauplii had comparable TIRs on all mixed-algal diets (Fig. 3). Generally, TIRs on mixed-algal diets were lower than on mono-algal diets in the study (P<0.05, One-way ANOVA and Tukey post-hoc tests).
3.3 Growth and development
The naupliar stage lasted (5.6±0.9) and (5.3±0.5) d in 100% ISO and 50:50 SKE: ISO treatments (P>0.05) but a significantly longer period of (6.6±0.9) and (7.1±0.6) d in 100% SKE and 50:50 Aa:ISO treatments (P≤0.001, One-way ANOVA and Tukey post-hoc tests; Table 4). In the contrast, the nauplii under starvation or feeding on 100% Aa diet died at Stage V on Day 9 or Day 11 (Fig. 4). On the other hand, copepodite duration was (9.8±1.3) and (10.1±0.9) d in 100% SKE and 50:50 SKE: ISO treatments (P>0.05), significantly shorter than that in 100% ISO and 50:50 Aa: ISO treatments ((11.6±0.9) and (12.7±0.5) d; P<0.05, One-way ANOVA and Tukey post-hoc tests; Table 4). Nevertheless, no obvious difference was shown with regard to body length at Stages CI and CVI among treatments ((500±0) and (522±34) µm vs. (1 236±20) and (1 289±87) µm; both P>0.05, One-way ANOVA and Tukey post-hoc tests). When growth rate was concerned, nauplii exhibited comparable growth rates in 100% Aa or 100% SKE or starvation treatments, significantly slower than those in the treatments with ISO. Moreover, among three treatments with ISO, nauplii had the slowest growth rate with the presence of Aa (Table 4; both P<0.05, one-way ANOVA and Tukey post-hoc tests). Differently, the copepodids had the highest and lowest growth rates in 100% SKE and 50:50 Aa:ISO treatments (P<0.05), whereas those feeding on 50:50 SKE:ISO diet had medium (P>0.05, One-way ANOVA and Tukey post-hoc tests; Table 4).
3.4 Eggs production and survival
The females feeding on 100% SKE, 100% ISO, and 50:50 SKE: ISO diets showed comparable egg production rates ((5.10±0.36) and (6.31±0.50) eggs/(ind. ∙d); all P>0.05, one-way ANOVA and Tukey post-hoc tests), higher than those feeding on 50:50 Aa: ISO diets (3.10±0.84 eggs/(ind.∙d); P<0.01, One-way ANOVA; Table 4).
None of the nauplii under starvation or feeding on 100% Aa diet lived longer than 9 d or 12 d (Fig. 4). At the end of incubation, the animals feeding on 100% ISO and 50:50 SKE: ISO diets had higher survival rate (80.0%±5.77% and 83.3%±8.82%), whereas lower survival rates appeared in 100% SKE and 50:50 Aa: ISO treatments (76.7%±8.82% and 72.2%±1.92%, Fig. 4; all P<0.01, One-way ANOVA and Tukey post-hoc tests).
4 Discussion
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4.1 Grazing behavior of copepods on A. anophagefferens
Significant grazing of A. anophagefferens by P. poplesia at Stages NIII, CIV and CIV was clearly shown in our study. Pseudodiaptomus poplesia exhibited Type II functional ingestion response to the mono-specific diet of A. anophagefferens because IR as a function of food level conformed to the Michaelis-Menten model regardless of developmental stage. The mass specific Imax showed a typical allometric trend and ranged from 43%/d to 90%/d. In previous studies dealing with the size spectrum of copepods, the lowest size limit was proposed to be located in the range of 1–3 µm for copepods, which suggests that negligible consumption was expected near the size limit (Uye et al., 1983; Berggreen et al., 1988). Following this assertion, A. anophagefferens individuals with a size of 2–4 µm, appeared to be unsuitable for grazing by copepods. However, several previous studies revealed that some species of copepod including Oithona simplex, O. Nana, Acrocalanus inermis, Parvocalanus crassirostris, Calanipeda aquaedulcis can exploit significantly small particles with cell size equal to or even smaller than 2 µm (Boak and Goulder, 1983; Calbet et al., 2000; Brucet et al., 2008), in agreement with this present study. For example, nauplii or adults of Eurytemora sp. grazed on free-living bacteria (Boak and Goulder, 1983). Thus, these species of copepod including P. poplesia behave as opportunistic feeders and can flexibly consume particles near the lower end of the size spectrum under the circumstance with a dominance of small particles. It was speculated that behavioral adaptation might be involved in feeding flexibility on small particles during the short-term feeding in this study, but this still needs to be verified in future studies.
Copepod exhibited ontogenic difference in grazing A. anophagefferens and this alga was readily grazed by nauplii in our study. Nauplii at Stage III had lower KIR value of the Michaelis-Menten function than copepodids and adults, indicating the weakening tendency of grazing for A. anophagefferens with developmental stage. In addition, nauplii had a 30% higher value of Imax feeding on A. anophagefferens than on S. costatum. Likewise, nauplii of A. tonsa showed a two-fold higher IR on A. anophagefferens than on I. galbana (Smith et al., 2008). There was disagreement on capability of different stages feeding on smaller-sized prey in literatures. Berggreen et al. (1988) found that nauplii of A. tonsa capture small prey more efficiently than adults. There was an obvious ontogenic trend in preference of prey size spectrum in Calanipeda aqueadulcis and nauplii consumed preferentially picoplankton (Brucet et al., 2008). In contrast, it was argued that nauplii of Eucalanus sp. were not able to capture small prey as efficiently as later stages because of immature feeding apendages (Paffenhöfer and Lewis, 1989). It remains unclear whether inter-specific difference exists in these findings.
On mixtures of A. anophagefferens and S. costatum, P. poplesia exhibited selective grazing against A. anophagefferens, as indicated by Ivlev’s, Jacob’s and FR indices. Our study demonstrated that the degree of selectivity against A. anophagefferens differed in different ontogenic stages. Elective indices values were high in most cases for copepodids and adults but close to neutral values in nauplii, pointing to less avoidance of A. anophagefferens in nauplii. It was speculated that copepod discriminated food particles in mixtures based on prey size rather than on other traits in this study since copepods did not show a clear rejection of A. anophagefferens in mono-algal diet. Aureococcus anophagefferens is smaller than S. costatum (2–4 µm vs. 5–8 µm), and this should be avoided by copepodids and adults in the mixture of both.
The edibility of A. anophagefferens appears to differ with strains and culture conditions when we compared the feeding behavior of copepod on different strains of A. anophagefferens in limited literatures. In the study by Smith et al. (2008), one strain, of which toxicity decreased after a long period (five years) of acclimation in the laboratory, was consumed by nauplii of A. tonsa but the other with a shorter period (two years) of laboratory maintenance was not. On the contrary, no inhibition of grazing was found when P. poplesia was fed the Chinese strain, which had been isolated less than two years. Therefore, it was speculated that the Chinese strain may not be as toxic as the American strain. It remains unclear whether any morphological or physiological difference exists between two strains.
4.2 Development, somatic growth and reproduction in copepod
Effects of A. anophagefferens on the performance of P. poplesia were examined continuously along different life stages in this present study. Nauplii did not complete metamorphosis or even survive on A. anophagefferens alone while the reproduction rate of females declined severely by 39%–50% with the presence of alternative algal species. Most of earlier studies usually used survival and reproduction rates to assess impacts of A. anophagefferens on copepod populations in field investigations (Buskey and Stockwell, 1993; Lonsdale et al., 1996; Bricelj and Lonsdale, 1997). These studies revealed that reproduction rates decreased greatly during brown tides, consistent to our laboratory work. Recently, Smith et al. (2008) for the first time reported retarded development of A. tonsa nauplii feeding on A. anophagefferens. The presence of alternative food particles mitigated the negative effect of A. anophagefferens on naupliar development of P. poplesia but not fully, which also occurred in the study by Smith et al. (2008) for A. tonsa. Nevertheless, it seems that development of copepodid was not affected in the presence of A. anophagefferens, probably since I. galbana itself is not good food for copepodids and masked the effect of A. anophagefferens.
Negative effects of the Chinese strain of A. anophagefferens on P. poplesia could be potentially caused by cellular toxicity or inadequate nutrition. As the correlation between IR and food level complied to Michaelis-Menten function with mono-specific diet of A. anophagefferens, possibility of cellular toxicity can be ruled out. Therefore, nutritional inadequacy may account for its detrimental effects, in agreement with the American strain (Bricelj and Lonsdale, 1997; Smith et al., 2008). Eicosapentaenoic acid (EPA) and docosapentaenoic acid (DHA) are regarded as the most important components of food particles for zooplankton and accounted for 4.8% and 14.6% of total fatty acids in the Chinese strain cells (personal communication), comparable to 3.5%–5.1% and 11.8%–14.0% in the American strain determined by Bricelj and Fisher (1989) and also close to those of a broad spectrum of algae. In recent years, researchers have become increasingly interested in nutritional sterol requirement of copepod. Giner and Boyer (1998) quantified the sterol composition of A. anophagefferens and found this species is rich in Δ5 components, which are suitable for copepod to utilize (Martin-Creuzburg and Von Elert, 2009). Therefore, it seems that lipid composition may not explain the detrimental effects of A. anophagefferens to copepod and other mechanisms should be involved for detrimental effects of the Chinese strain. Alternatively, P. poplesia always exhibited lower ingestion rates when feeding on mixed-algal diets of A. anophagefferens than on the mono-algal diet at the same food level, and actually, Smith et al. (2008) reported a similar phenomenon in A. tonsa. It appeared that copepods may suffer low food consumption. Yet, this should be verified in future quantitative studies.
In the Bohai Sea, S. costatum usually co-occurs with A. anophagefferens in the phytoplankton assemblage. It was inferred from our findings on grazing behavior that age class distribution of P. poplesia population determines grazing pressure on A. anophagefferens. Nauplii may contribute to control the A. anophagefferens population while copepodids and adults may contribute to development of the bloom by removing the alternative algal cells. Nutritional inadequacy of A. anophagefferens as food means that its negative effect is density-dependant. When a brown tide develops and reachs the climax, the detrimental effect of A. anophagefferens will appear gradually because copepods at elder stages than NII may consume a large amount of Aureococcus cells. Combining effects of A. anophagefferens on somatic growth in juveniles and reproduction in female adults, P. poplesia population will not maintain its development over a long term, which will constrain grazing pressure on A. anophagefferens population.
5 Conclusions
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Ingestion rates of P. poplesia at Stages NIII, CIV, and CVI complied with the Michaelis-Menten function on a mono-algal diet of Chinese strain of A. anophagefferens. There existed an ontogenic trend in preference to A. anophagefferens. In mixtures with S. costatum, A. anophagefferens was avoided strongly by copepodids and adult females, but weakly by nauplii, which suggested that naupliar P. poplesia may potentially exert grazing pressure on A. Anophagefferens population during a brown tide. Nevertheless, the somatic growth and metamorphosis of nauplii were greatly suppressed by the presence of A. anophagefferens, as was the reproduction of adult females. It is suggested that the overall robust development of the copepod population may not occur during a brown tide, which will constrain the role of copepods in the control of brown tides over the long term.
Funding
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  • The National Natural Science Foundation of China under contract No. 41276153; the Joint Project of National Nature Science Foundation of China-Guangdong under contract No. U1301235; the Public Science and Technology Research Funds Projects of Ocean under contract Nos 201305003-2 and 201305010-4; the Fundamental Research Funds for the Central Universities.
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Year 2018 volume 37 Issue 4
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Article Info
doi: 10.1007/s13131-018-1168-6
  • Receive Date：2016-11-24
  • Online Date：2026-04-13
  • Published：2018-04-25
Article Data
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History
  • Received：2016-11-24
  • Accepted：2017-05-16
Funding
The National Natural Science Foundation of China under contract No. 41276153; the Joint Project of National Nature Science Foundation of China-Guangdong under contract No. U1301235; the Public Science and Technology Research Funds Projects of Ocean under contract Nos 201305003-2 and 201305010-4; the Fundamental Research Funds for the Central Universities.
Affiliations
    1 Research Center of Harmful Algae and Marine Biology, Jinan University, Guangzhou 510632, China
    2 Key Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, Jinan University, Guangzhou 510632, China
    3 South China Sea Institute of Planning and Environmental Research, State Oceanic Administration, Guangzhou 510300, 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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