Effects of different algal diets on growth and development of the larvae of the copepod Bestiolina amoyensis

doi:10.21203/rs.3.rs-4274273/v1

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Effects of different algal diets on growth and development of the larvae of the copepod Bestiolina amoyensis

https://doi.org/10.21203/rs.3.rs-4274273/v1

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Copepods are an important food source for many economically important fish larvae. Especially the larvae of copepod, compared to rotifers and artemia, they are a very promising live feed. Bestiolina amoyensis with small body size, nutrient-rich, excellent reproductive capacity and wide range of adaptability, making it being a promising biological feed for aquaculture. However, the effects of different algal diets on the growth and development of B. amoyensis larvae have not been studied. In this study, Isochrysis galbana (Iso), Pavlova viridis (Pav) and Chaetoceros miielleri (Cha) were selected to feed larvae in single- or mixed-species diets: Iso, Pav, Cha, Iso + Pav, Iso + Cha, Pav + Cha, Iso + Pav + Cha. The effects were evaluated by several growth and development indicators, including survival rate, ingestion, development time, and carbon content. The larvae fed Iso or Iso + Pav + Cha had the highest survival rates compared with other diet combinations. The development time of the larvae fed Cha was longer compared with all other algal diets. Ingestion by nauplii (1.72 × 10⁵ cells/ind) and copepodites (3.82 × 10⁵ cells/ind) was highest when fed Iso. The larvae fed a 3-species diet had the highest carbon content compared with other algal diets. Our findings demonstrate that a combination of the 3 species could maximize growth and development of B. amoyensis larvae.

Copepod

Algal diets

Growth and development

Larvae growth parameters

Copepods are one of the most important zooplankton in the ocean and are a key trophic link between primary producers and secondary consumers in marine ecosystems (Turner 2004). Copepods are the main food source for most planktivores at higher trophic levels, and they are ideal prey for different developmental stages of economically valuable fish and shrimp species (Frederiksen et al. 2006). Research has shown that copepods are suitable nutritional sources in the aquaculture industry (Buskey et al. 2007) since copepods have a higher abundance of eicosapentaenoic acid (EPA), docosahexaenoic acid (DHA), and other polyunsaturated fatty acids (PUFA) compared with rotifers and Artemia nauplii (Støttrup 2000; McKinnon et al. 2003). Copepods also stimulate strong feeding responses in fish larvae through their distinctive swimming patterns that differ from that of rotifers and Artemia nauplii (Støttrup et al. 1997; Doi et al. 1997; Buskey et al. 1993). The addition of copepods as a live feed could enhance the growth and survival rate of fish larvae compared with rotifers and Artemia nauplii (Shields et al. 1999; Payne et al. 2001).

The composition of the algal diet of copepods plays a key role in regulating their growth and reproduction. More importantly, algal diet composition can significantly affect population growth, egg production, and egg-hatching success (Milione et al. 2007; Gusmao et al. 2009). Lee et al. (2006) evaluated the effects of different microalgal diets on the reproductive and productive performance of the Cyclopoida copepod, Paracyclopina nana, demonstrating that female copepods fed with a mixed diet comprising 2 algal species had higher fecundity than females fed with a single-species algal diet. Mixed-species algal diets have been recommended for filter-feeders since single-species cultures may not meet their nutritional requirements (Brown 1989; Kleppel et al. 1995).

Copepod nauplii (~ 100 µm) are smaller than rotifers and Artemia nauplii, making them highly suitable as feed for the first larval feeding stage of various fish species with a small mouth gape size, such as groupers, snappers, and some ornamental fish and shrimps (Payne et al. 2001; Payne et al. 2001). Furthermore, copepods have 12 developmental stages from egg to adult, including stage 1 (N1) to stage 6 (N6) nauplii and stage 1 (C1) to stage 5 (C5) copepodites, which can meet the different nutritional needs of juvenile fish at different development stages (Raisuddin et al. 2007). Li et al.(2006) studied the effects of different diets on the development and survival rate of Acartia bifilosa nauplii, demonstrating that the particle size of microalgae is a key factor affecting feeding rates by copepod nauplii, accounting for the different developmental stages. Li et al.(2006) found that copepod nauplii and copepodites fed mixed-species algal diets had higher survival rates than those fed a single-species algal diet. The growth and development of copepods incur a high demand for nutrients and energy, and a single-species algal diet may be deficient in certain nutrients (Buttino et al. 2009).

B. amoyensis is widely distributed in the Pacific Ocean and has been reported to co-exist with B. similis in tropical coastal and estuary waters (McKinnon et al. 2003). However, little research has been conducted on B. amoyensis. Wang et al. (2021) studied the effects of concentration and photoperiod on egg production, female life expectancy, and population dynamics of B. amoyensis, demonstrating that the species was a potentially valuable feed in aquaculture. However, there has been no research on the growth and development of the larvae of B. amoyensis, and the effects of different diets on the larvae have not been evaluated. Therefore, the goal of the study was to compare the effects of different algal diets on the growth and development of the larvae of B. amoyensis, with the objective of identifying an optimal diet for high biomass production of B. amoyensis.

Microalgal culture

Three species of microalgae, Isochrysis galbana (Iso), Pavlova viridis (Pav) and Chaetoceros miielleri (Cha) were used in this experiment. Algae were obtained from the Collaborative Innovation Centre of Ornamental Marine Species and Public Service Platform of Industrialization. The algae were cultivated in 70 L cylindrical acrylic cylinders with 0.01 µm filtered, UV-irradiated, and chlorinated seawater (salinity 28 psu) in a temperature-controlled room. The 3 microalgae species were maintained at 25 ± 1 ºC with gentle aeration and f/2 medium was used for the cultures (Guillard and Ryther, 1962). The photoperiod was set as 24 h continuous light with a light intensity of approximately 4000–5000 lux.

Bestiolina amoyensis stock culture

Copepods were collected using a plankton net at Dragon Boat Pond, Jimei District, Xiamen, China, in July 2022 and brought to the laboratory. After separation (Wang et al. 2021), the cultivation of B. amoyensis was gradually scaled up to a 300 L tank filled with 0.01 µm filtered seawater and exposed to gentle aeration. Cultivation conditions were maintained at a salinity of 28 ± 1 psu, temperature of 26 ± 1°C, and a light regime of 12:12-h light:dark with a light intensity of 500 lux. Approximately 30% of the culture water was exchanged daily using a 5 cm diameter hollow cylindrical isolation device with the bottom covered with 48 µm mesh. Before the experiments began, B. amoyensis was fed daily with the microalga Iso.

Experimental design and setup

Seven diet treatments including three single-species diets (Iso, Pav and Cha), three 2-species diets (Iso + Pav, Iso + Cha, Pav + Cha,) and one 3-species diet (Iso + Pav + Cha) were set up. All microalgal diets were equal in biomass, which was calculated using carbon concentrations for each species according to Strathmann (1967). Algae were fed to copepod cultures at a concentration of 680 µg/mL with a 1:1 carbon ratio. The algae used in the experiments were all in the exponential growth stage. Four parameters, including the survival rate, the development time, growth indexes, and ingestion, were measured to assess the effects of different diets on the growth and development of B. amoyensis larvae.

Effect of diet on survival rate of larvae

The experiment was set up with 7 diet treatment groups and 5 replicates per diet treatment. Mature females with genital node protrusion were selected from the stock culture prepared in a 300 L tank and transferred to 6-well plates loaded with different diets. The plates were placed in an incubator and eggs were collected within 6 h. The eggs were incubated in the dark until hatching to obtain N1 nauplii. Fifty healthy and active N1 nauplii were randomly selected from each replicate, transferred to 30 mL Petri dishes, and placed in an incubator at a temperature of 26°C and with a photoperiod of 12:12-h light:dark, with the light source placed underneath. Live nauplii were transferred to a new dish daily using a light trap and a pipette, and the dead nauplii were collected and counted. Once all nauplii reached the copepodite stage, the survival rate was calculated using the following formula:

Nauplii survival rate (%) =(50-the number of dead nauplii)/50 × 100

Mature females were cultured in 2.5 L containers with a 75 µm strainer at the bottom. Each culture container was suspended in a 5 L clear PET box containing 4 L of culture water to collect the eggs produced. Each PET box was pre-filled with a different diet to prevent the effect of previous algae on the experiment and placed in an incubator for 5 h of dark incubation. The container holding the mature female was subsequently transferred to another 5 L PET box containing 4 L of culture water and the treatment diet, to obtain eggs for a 2nd replicate. This procedure was repeated until 5 replicate cultures of eggs were obtained for each diet treatment. The eggs in each 5 L culture box were incubated and cultured to obtain C1 copepodites. Fifty healthy and active C1 copepodites were randomly selected from each replicate, under a dissecting microscope, placed in 30 mL Petri dishes, and incubated under the same conditions as described above for nauplii. The survival rate of copepodites was calculated using the following formula:

Copepodite survival rate (%) =(50-the number of dead copepodites)/50 × 100

Effect of diet on the development time of larvae

The larval development time experiment was set up with 7 diet treatment groups and 3 replicates per diet treatment. The same procedure, as described above for the survival experiment, was carried out to obtain 5 replicate cultures of eggs per diet treatment. Approximately 30 individuals from each replicate were collected at 12-h intervals, and the proportion of the larvae at each developmental stage was counted. Stage-specific developmental times were calculated according to the method outlined by Landry (1975) and defined as the time at which 50% of individuals had reached that stage. Mid-development time (MDT) was calculated by fitting an s-shaped Hill function to the percentage of each developmental stage in the population since spawning, using the following equation:

y = Mx^p/(c^p+x^p)

where y is the percentage of each developmental stage in the population, x is the time in days since spawning, M is the highest value on the y-axis, and the coefficients p and c correspond to the gradient of the curve.

Effect of diet on carbon content of larvae

Following the same procedure described above for the larval development time experiment, 7 diet treatment groups and 5 replicates per diet treatment were set up for the carbon content experiment. Five larvae from each of the 12 larval development stages were selected from each replicate, and the pre-length and width of each larva were measured. The measurements were repeated 3 times and averaged. The wet weight (WW) of each larval stage was calculated from the body length and width using the following formula according to Svetlichny (1983):

WW = Kc × prosomal length × width²

where Kc is a constant (0.6 for calanoids and 0.705 for cyclopoids; McKinnon and Duggan, 2003). Subsequently, dry weight (DW) was calculated as 0.135 × WW (Postel et al., 2000), and carbon weight (W) was calculated as 0.42 × DW (Beers, 1966).

Effect of diet on ingestion by larvae

The ingestion experiment consisted of 5 control groups containing algae but no copepods and 5 experimental groups containing algae and copepods. It has been reported that the first 3 stages of copepod nauplii rely on yolk. Therefore, the main development stage IV nauplii and stage III copepodite were included in a 24-h feeding experiment. See above for the method of obtaining eggs. From egg hatching to the stage IV nauplii, observations were conducted at 6-h intervals. Five individuals at stage IV nauplii were selected and transferred to 30 mL Petri dishes with 20 mL water, which were pre-filled with different diets. The remaining larvae were hatched to stage III copepodite, and the copepodite ingestion experiment was conducted in the same way as the nauplius feeding experiment. The concentration of algae in each diet treatment was measured before and after the experiment and used to calculate ingestion. The formula for ingestion is as follows:

Ingestion = (Initial algal concentration – algal concentration after experiment)×V/n

where v is the volume of water in the experiment, n is number of experimental individuals.

Data analysis

All statistical analyses were conducted using SPSS version 26.0. Comparisons of the four developmental and growth parameters (survival rate, development time, ingestion, and carbon content) of copepods fed different diets were made using one-way analysis of variance followed by Duncan’s multiple range test. Data are presented as mean ± SE. Significant differences between experimental groups were determined as P ≤ 0.05.

The survival rates of nauplii and copepodite fed different algal diets are shown in Fig. 1. The survival of nauplii and copepodite was significantly influenced by the algal diet. Both nauplii (94.00 ± 1.25%) and copepodites (92.66 ± 0.67%) fed with Iso showed the highest survival rates. For nauplii, there were no significant differences in survival rate between nauplii fed the Iso, Pav, and Iso + Pav + Cha diets (P > 0.05). However, the latter 3 diets resulted in higher survival rates when compared with nauplii fed a 2-species mixed diet, including the Iso + Pav (82.67 ± 2.87%), Iso + Cha (81.33 ± 3.09%), and Pav + Cha (82.67 ± 3.56%) diets. Unexpectedly, nauplii fed with Pav showed the lowest survival rate (50.67 ± 3.56%), and this was significantly different to all other diet treatments. The survival rates of copepodites showed similar patterns to that of nauplii. Compared with other treatments, copepodites fed the Iso, Pav (86.67 ± 1.05%) and Iso + Pav + Cha (89.33 ± 4.00%) diets showed the highest survival rates (P < 0.05). The lowest copepodite survival rate (30.0 ± 2.9%) was recorded for the Cha diet, and the survival rates of copepodites fed a 2-species mixed diet were lower than 75%.

The results of the development time experiment are shown in Fig. 2 and Table I. Figure 1 shows the curve of development time from hatching to each larval stage fitted by the Hill function. Table I shows the MDT for each developmental stage defined as the time at which 50% of the population had developed to that stage. For N1 and N4–C5 stages, the groups fed with Iso + Pav + Cha showed the highest development rates compared with other treatments, but the highest development rates were recorded when B. amoyensis was fed Iso at N2 (0.68 ± 0.01 d) and N3 (1.17 ± 0.03 d). With the exception of the 3-species mixed diet, diet treatments including Cha resulted in long developmental times. The longest development times were observed for male (7.53 ± 0.03 d) and female (7.79 ± 0.01 d) C5 copepods fed Cha, while the shortest development times were observed for male (5.64 ± 0.02 d) and female (5.89 ± 0.01 d) C5 copepods fed Iso + Pav + Cha. The development time of females was longer than males in all algal diet treatment groups.

Table 2

Twenty-four-hour ingestion of stage 4 nauplii of *B. amoyensis* when fed one of 7 different algal diets.
Algal Diets	Ingestion by stage 4 nauplii (cells/ind)	Ingestion by stage 3 copepodites (cells/ind)
I. galbana	1.60^a*10⁵	3.61^A*10⁵
P. viridis	1.51^a*10⁵	3.26^A*10⁵
C. miielleri	1.14^a*10⁵	3.01^A*10⁵
I. galbana + P. viridis	1.72^a*10⁵	3.82^A*10⁵
I. galbana + C. miielleri	1.42^a*10⁵	3.23^A*10⁵
P. viridis + C. miielleri	1.32^a*10⁵	2.56^A*10⁵
I. galbana + P. viridis + C. miielleri	1.46^a*10⁵	3.50^A*10⁵

Ingestion by stage 4 nauplii of B. amoyensis was significantly influenced by microalgal diets (P < 0.05; Table II). The ingestion of all algae did not significantly different. Copepod fed Iso + Pav and Cha had the highest ingestion (1.72 × 10⁵ cells/ind) and the lowest ingestion (1.14 × 10⁵ cells/ind). Except for Iso + Pav, the ingestion of other mixed algae is below 1.5 × 10⁵ cells/ind. For stage 3 copepodites, there were no significant differences in ingestion among all algae. Copepods fed Pav + Cha (2.56 × 10⁵ cells/ind) had the lowest ingestion rates, and the ingestion was more than 3 × 10⁵ cells/ind in all other diet treatments.

Table Ⅲ shows the carbon content of larvae from stage 1 nauplii up to stage 5 copepodite. The larvae fed different algal diets had different carbon content. The carbon content of the first 4 nauplii stages was highest when fed Iso + Pav + Cha (N1: 11.64 ± 0.21 µg; N2: 15.04 ± 0.34 µg; N3: 27.30 ± 0.33 µg; N4: 38.42 ± 0.73 µg). The N5 and N6 nauplii stages had the highest carbon content when fed with Iso (N5: 56.50 ± 0.55 µg; N6: 62.82 ± 0.57 µg). For copepodite stages, the carbon content was highest when fed Iso + Pav + Cha (C1: 81.23 ± 2.29 µg; C2: 156.56 ± 2.31 µg; C3: 318.40 ± 5.02 µg; C4: 448.53 ± 5.49 µg; C5M: 612.17 ± 4.38 µg; C5F: 739.09 ± 5.22 µg), and the carbon content was lowest when fed Cha (C1: 61.57 ± 0.58 µg; C2: 119.52 ± 1.69 µg; C3: 214.26 ± 2.49 µg; C4: 354.45 ± 3.16 µg; C5M: 475.79 ± 2.37 µg; C5F: 579.40 ± 5.48 µg).

The composition of algal diets has previously been shown to strongly affect the growth of copepods (Murray et al. 2002; Yu et al. 2017). Our findings demonstrate that an optimal algal diet composition increased larval survival rate, accelerated larval development, and increased larval ingestion, while sub-optimal diets resulted in larval death or retarded larval development. A sub-optimal diet may provide inadequate nutrition (Jones et al. 2005), include food items of unsuitable size (Li et al. 2008), and/or contain biotoxins (Yu et al. 2016). The algal diet strongly influences survival rate of larvae, and studies suggest that a diatom diet can have negative effects on naupliar development (Carotenuto et al. 2002; Ianora et al. 2004; Koski et al., 2008). For example, larvae of the copepod Temora stylifera had high mortality rates when fed diatoms (Carotenuto et al.2002), and a closely related species, Temora longicornis, also had retarded development and high larval mortality when fed diatoms (Koski et al. 2008). However, some studies have shown that copepods favor diatoms, which sustain copepod development from hatching to adulthood (Vidal 1980). Luo et al. (2019) found that naupliar larvae fed the diatom Cyclotella meneghiniana had a low growth rate while copepodites fed C. meneghiniana had high growth rates, suggesting that C. meneghiniana was more suitable as food for copepodites rather than for nauplii.

Our results showed that both nauplii and copepodites fed with C. miielleri had the lowest survival rate, indicating that C. miielleri is not a suitable diet for B. amoyensis. This could be caused by aldehydes produced by diatoms that can impair copepod development. Another possible explanation for the low survival rates of copepod larvae fed a diatom diet is that diatoms have thick cell walls, which make them more difficult to digest compared with the other algal species examined in the present study (I. galbana and P. viridis) that have no cell walls. While not all diatom species per se are toxic, the nutritional composition of diatoms may be insufficient to support copepod recruitment and development in a single-species algal diet (Jones et al. 2005). However, a diatom diet does not affect all copepod species in the same way, suggesting that the effects of a diatom diet may be species-specific. Single-species and mixed-species algal diets that do not contain diatoms are also expected to affect larval survival rates. Generally, copepods fed with mixed-species algal diets—that are of higher nutritional value than a single-species diet—have a higher survival rate compared with single-species algal diets, which do not meet their nutritional requirements (Brown et al. 1989; Kleppel et al. 1995). For example, a 3-species algal diet containing Iso + Tet + Pav was found to be the best diet for B. similis (Camus et al. 2009). However, harpacticoid copepods fed with a mixed-species microalgal diet consisting of diatom, green algae, and flagellated algae did not exhibit the highest overall reproductive performance (Matias-Peralta et al. 2012). In the present study, the performance of copepods fed a 2-species algal diet, especially the diets containing C. miielleri, was worse than the performance of copepods fed a single-species algal diet, but the 3-species algal diet (Iso + Pav + Cha) produced the highest larval survival rates compared with the other algal diets. Therefore, not all mixed-species algal diets are suitable for the needs of B. amoyensis larvae. It is thus essential to select the appropriate algal diet according to the needs of individual copepod species.

While temperature is a key factor affecting copepod larval development time (Santhanam et al. 2021), nutritional composition of the algal diet also significantly influences larval development time. Dietary deficiencies in DHA and EPA may cause delayed growth, increased mortality, and reduced stress tolerance in fish. Most species of marine fish have a higher requirement for DPA, compared with EPA, since DPA has a higher physiological efficiency during larval development and is present at a higher concentration in fish larval tissue. The relative proportion of DHA to EPA in larval diets is considered to be crucial, and the optimal ratio of DHA to EPA was determined as 2:1 (Sargent et al. 1997). The ratio of DHA to EPA in the copepod A. royi varied when fed different microalgal diets, and all copepods had a DHA:EPA ratio exceeding 2:1, except copepods fed with Tet or Nan + Tet. Notably, a high DHA:EPA ratio was observed for copepods fed Iso (6:1) and Iso + Nan (4:1) diet treatments, which also supported high population sizes of copepods (Pan et al. 2018). Our results show that the larval development time of copepods fed a mixed-species algal diet was shorter than that of copepods fed a single-species algal diet except for those fed Iso. The 3-species algal diet (Iso + Pav + Cha) had a high content of DHA and EPA and resulted in the shortest development time from stage 1 nauplius to stage 5 copepodite. The algae P. viridis and C. miielleri have higher levels of EPA compared with DHA, while I. galbana has higher levels of DHA compared with EPA. Our results showed that the development time of copepods fed Iso was significantly shorter than that of copepods fed Pav or Cha. When larvae were fed mixed-species algal diets, in which DHA is higher than EPA, they developed quicker than larvae fed Cha, which is low in DHA and high in EPA. Therefore, the content of DHA and EPA should be balanced during the larval development time. The optimal ratio of DHA and EPA occurs when DHA is higher than EPA and can shorten copepod larval development time, while suboptimal DHA:EPA may not meet larval nutritional requirements, which may extend the development time and lead to high mortality.

Particle size is an important factor affecting ingestion of algae by copepods. Some studies have shown that algae with a size of < 10 µm or a volume of < 500–1,000 µm³ are not effectively grazed by copepods (Katechakis et al. 2004; Irigoien et al. 2002; Sommer et al. 2000). However, our results contradict these findings, which could be because our study used copepod larvae while previous studies concerned adult copepods. Although there were no significant differences in ingestion for all experiments, the ingestion of individuals fed with Cha were lower than the ingestion of other two single algae. The mouthparts of copepod larvae are smaller than those of the adults, and thus larvae may prefer algae of a smaller particle size. Since the particle size of C. miielleri is larger than that of I. galbana and P. viridis, larvae are likely to ingest less C. miielleri compared with I. galbana and P. viridis, consistent with our results. In addition to particle size, other characteristics of algae will also affect their ingestion by copepod larvae. For example, the accessibility of algae varies between species, and diatoms tend to sink to the container bottom within 1–2 h if not maintained in suspension (Brugnano et al. 2016). In our experiment, C. miielleri tended to sink to the bottom of cultures, which will have led to a decrease in the concentration of the diatom and the contact rate with larvae, leading to a decrease in ingestion. This could be another explanation for reduced ingestion of C. miielleri.

Carbon is the main source of nutrient composition in copepods. DHA, EPA, and lipids in copepods have a strong relationship with carbon. Therefore, understanding the amounts of carbon ingested in the diet and in the body can indicate the amount of carbon consumed and stored. However, there is little research on carbon content. Our results show that the carbon content ingested was significantly higher than the carbon content in the body of stage 4 nauplii and stage 3 copepodites. This is likely explained by some of the carbon ingested being stored in the body as lipids and used for life activities.

We confirm that different algae have different effects on the larvae development of B. amoyensis, and the same algae also has different effects on different larvae development. A single algae has a negative impact on the larvae development, especially P. viridis and C. miielleri. Our findings demonstrate that a combination of the 3 species, Iso + Pav + Cha, could maximize culture productivity of B. amoyensis larvae. This study further understand that Iso + Pav + Cha is suitable algal for the B. amoyensis larvae development. Future research will mainly focus on the effects of Iso + Pav + Cha on the adult of B. amoyensis.

Funding

This work was supported by Guiding project of Fujian Provincial Department of Science and Technology (2022N0014), Natural Science Foundation of Xiamen, China (3502Z202372021) and Research start-up funds of Jimei University (ZQ2021023).

Competing interests

The authors declare that they have no conflict of interest.

Author contributions

Zhouyang Ma, Shuhong Wang design research methods and experimental processes. Collecting, processing and analysis data. Write the first draft of the paper. Participate in research design and method selection. Assist in data collection, processing, and analysis. Provide economic and technical support.

Nan Chen, Yueping Zhang : Participate in paper writing and revision. Responsible for the planning, design and implementation of the entire research. Responsible for supervising and coordinating the overall research. Prepared figures 1-2 and Table1-3.

All authors reviewed the manuscript."

Ethics approval

No approval of research ethics committees was required to accomplish the goals of this study because experimental work was conducted with an unregulated invertebrate species.

Compliance with ethical standards

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.

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Tables 1 and 3 are available in the Supplementary Files section.

No competing interests reported.

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Effects of different algal diets on growth and development of the larvae of the copepod Bestiolina amoyensis

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Abstract

Figures

Introduction

Material and methods

Microalgal culture

Experimental design and setup

Effect of diet on survival rate of larvae

Effect of diet on the development time of larvae

Effect of diet on carbon content of larvae

Effect of diet on ingestion by larvae

Data analysis

Results

Discussion

Declarations

References

Tables

Additional Declarations

Supplementary Files

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