Free Access
Issue
Ann. Limnol. - Int. J. Lim.
Volume 55, 2019
Article Number 14
Number of page(s) 13
DOI https://doi.org/10.1051/limn/2019013
Published online 21 June 2019

© EDP Sciences, 2019

1 Introduction

Competition is a major biotic interaction regulating zooplankton population dynamics and community structure (e.g., Rothhaupt, 1990; Chase et al., 2002; Huang et al., 2014). Rotifers and cladocerans are two common constituents and dominant groups of freshwater zooplankton communities (Dumont and Negrea, 2002; Wallace et al., 2015). They overlap in their feeding niche (Dodson, 1974) and often compete for limited food resources. Cladocerans generally outcompete rotifers, due to a stronger exploitative and/or mechanical interference. They can also damage vulnerable rotifers to the extent of eliminating them from their natural ecosystem or culture medium in the laboratory (Gilbert, 1988). Natural planktonic structure is influenced by secondary metabolites from other aquatic organisms, which often act as allelochemicals (Sarma and Nandini, 2018). Many studies have focused on understanding the allelopathic effects of rotifer predators on their prey (e.g., Pavón-Meza et al., 2008; Peña-Aguado et al., 2008; Guo et al., 2011; Sarma et al., 2011; Nandini et al., 2014; Pan et al., 2017, 2018), between cladocerans and algal foods (e.g., Lampert et al., 1994; Lürling and Van Donk, 1996; Ha et al., 2001; Lürling, 2003; Yang et al., 2007), and between rotifers and algal foods (e.g., Yang et al., 2005, 2008; Verschoor et al., 2007; Ma et al., 2018). Prey mainly adapts to and alleviates allelopathic stress through changes in behavior, morphology or life-history strategies (Lass and Spaak, 2003). These allelochemicals are generally species-specific secondary metabolites, whose effect may differ among zooplankton. Hence, these allelochemicals are potentially important in controlling the population dynamics of competing species and structuring the plankton community (Vet, 1999; Mitchell and Carvalho, 2002).

Zooplankton release their chemicals, not only into the water column, but also on the surface of their algal food and other animals (Guo et al., 2011), resulting in phytoplanktivorous rotifers and cladocerans absorbing allelochemicals from both the water and their food (algae). The allelopathic interactions (e.g., amount released) of rotifers and cladocerans are regulated by environmental factors, such as food density and temperature (Verschoor et al., 2007; Pavón-Meza et al., 2008). Different conditions influence the amount of allelopathic substances produced, and temperature increases can result in possible degradation of the allelopathic substances.

In subtropical and tropical water bodies, small cladocerans (e.g., the genera Moina) can coexist with some rotifer species (e.g., the genera Brachionus) (Nogrady et al., 1993; Dumont et al., 1994; Lampert and Sommer, 1997; Wen et al., 2017). Their allelopathic interactions contribute to their coexistence, which may be regulated by allelopathic substances released by other small zooplankton. Hence, experiments assessing allelopathic interactions occurring within populations of one rotifer species and one cladoceran species will further the general understanding of the relationship among multiple rotifer and cladoceran species. Allelopathic effects of cladocerans on rotifers have been previously quantified (Conde-Porcuna, 1998; Guo et al., 2011; Gama-Flores et al., 2018). Conde-Porcuna (1998) found that allelochemicals from a cladoceran, Daphnia longispina, inhibit the reproduction and population growth of a rotifer, Keratella cochlearis. Conversely, allelochemicals secreted by a cladoceran, D. similis, stimulate the reproduction and population growth of a rotifer, B. calyciflorus (Guo et al., 2011). Gama-Flores et al. (2018) focused on the effects of a cladoceran-conditioned medium on the demography of brachionid rotifers. This study found that among the three rotifer species, B. havanaensis was the most sensitive in regard to the life history variable response to allelopathic substances from cladocerans, especially M. macrocopa. Conversely, B. calyciflorus hardly responded to the cladoceran allelochemicals. Moreover, the effects (i.e., stimulatory, inhibitory, or no response) of allelochemicals from the three cladoceran species on the population growth rates of the three rotifer species were not identical. These findings suggest that the effects of cladoceran allelochemicals on rotifers are inconclusive and depend on the rotifer species, rotifer life history variable, and origin of the allelochemical. Moreover, it remains unknown how rotifer-mediated allelochemicals affect the survivorship- or reproductive variables of cladocerans.

Our previous study focused on the outcomes of competition between B. calyciflorus and M. macrocopa, under different temperatures and food densities. We found that under each temperature condition, M. macrocopa outcompeted B. calyciflorus under low algal density conditions (0.5 × 106 cells/mL). The population growth rates of B. calyciflorus cultured with M. macrocopa were lower than the control growth rates. Meanwhile, the population growth rates of M. macrocopa cultured with B. calyciflorus were higher in the control growth rates, except under the highest temperature condition (Huang et al., 2014). These results suggest that B. calyciflorus allelochemicals stimulated the population growth of M. macrocopa. Conversely, B. calyciflorus outcompeted M. macrocopa under higher algal density conditions (1.0 and 3.0 × 106 cells/mL). The population growth rates of B. calyciflorus cultured with M. macrocopa were lower than the control growth rates. However, the growth rates were higher under the combination of the two higher temperature conditions and the highest algal density (Huang et al., 2014). This suggests that the M. macrocopa allelochemicals stimulated the population growth of B. calyciflorus. Based on these results, we speculated that allelopathic stimulation might exist in the competitive process of M. macrocopa and B. calyciflorus, which depends on the origin of allelochemicals, stage of the competitive process (i.e., the relative density of M. macrocopa and B. calyciflorus equal with the relative concentration of allelochemicals from M. macrocopa and B. calyciflorus), temperature, and algal density.

Allelopathic substances released by zooplankton are poorly understood and their extraction, purification, composition, chemical structure, and function remain unclear (Kalacheva et al., 2000; Ferland-Raymond et al., 2010; Guo et al., 2011; Sarma et al., 2018). Therefore, many scholars rely on zooplankton-conditioned mediums to replace the naturally secreted allelochemicals to conduct relative studies (e.g., Conde-Porcuna, 1998; Yang et al., 2005, 2007, 2008; Verschoor et al., 2007; Rodríguez et al., 2010; Guo et al., 2011; Gama-Flores et al., 2018; Sarma et al., 2018). Therefore, we also used plankton-conditioned mediums to replace the allelochemicals in our study.

We performed life table experiments to examine the interspecific effects of different concentrations of allelochemicals in M. macrocopa- and B. calyciflorus-conditioned medium on the main life history variables under different temperature and S. obliquus (algal) densities. These experiments tested the following hypotheses: (1) allelopathic stimulation exists in the competitive process between M. macrocopa and B. calyciflorus; (2) the allelopathy is stimulatory, inhibitory, or nearly invalid, depending on the origin and concentration of allelochemicals, life history variable, temperature, and algal density.

2 Materials and methods

2.1 Experimental organisms

B. calyciflorus was isolated from Lake Jiuliantang (31°33' N, 118° × 37' E, Wuhu city, China), and M. macrocopa was supplied by the Laboratory of Aquaculture Biology, Nagasaki University of Japan. Both species were clonally cultured from one amictic female for more than 1 year at 25 ± 1 °C under natural illumination via an incubator, using EPA medium (pH 7.4–7.8; prepared by dissolving 96 mg NaHCO3, 60 mg CaSO4, 60 mg MgSO4 and 4 mg KCl in 1 L distilled water; USEPA, 1985) and S. obliquus (1.0−2.0 × 106 cells/mL) as the exclusive food. Prior to experimentation, the two zooplanktons were fed on 0.5, 1.0, and 3.0 × 106 cells/mL S. obliquus at 20 ± 1, 25 ± 1, and 30 ± 1 °C for at least one week, respectively. During the period, the two zooplankton populations were kept in log-phase growth. S. obliquus were grown in a semicontinuous culture using HB-4 medium (Li et al., 1959) refreshed daily at 40%. Algae in exponential growth were centrifuged at 3000 rpm for 5 min, resuspended in the EPA medium, then stored at 4 °C. Stock algae density was determined using a hemocytometer, and subsequently diluted to the desired experimental density.

2.2 Conditioned medium (CM)

Zooplankton- (e.g., rotifer and cladoceran) conditioned medium usually contains the allelochemicals released by zooplankton in the culture process as well as the allelochemicals secreted by algae, providing food for the zooplankton. Verschoor et al. (2007) showed that the chemicals from S. obliquus have a strong stimulating effect on the feeding rate of B. calyciflorus. The findings suggested that the algae's allelochemicals may influence the feeding and reproduction rates of M. macrocopa. In this study, like the method of Conde-Porcuna (1998), we also used S. obliquus-conditioned mediums as controls under corresponding temperature and algae density to exclude any possible influence of S. obliquus allelochemicals on the reproduction and population growth of M. macrocopa and B. calyciflorus.

The S. obliquus-conditioned medium, M. macrocopa-conditioned medium (MCM), and B. calyciflorus-conditioned medium (CCM) were obtained separately with equivalent biomasses (Mitchell and Carvalho, 2002) every day. S. obliquus, M. macrocopa (< 24 h old), and B. calyciflorus (random age) were respectively placed in 200 mL of EPA medium in 250 mL glass beakers. After 24 h, the planktons were separated using a plankton mesh (pore size 20 µm). CMs were filtered using Millipore 0.22 µm filters (GSTF04700) to ensure that most of the present allelochemicals in the CM would not be degraded by microbial action (Loose et al., 1993).

2.3 Life-table experiments

We conducted cohort life table tests for B. calyciflorus exposed separately to MCM at 0.5 and 1.0 ind./mL of M. macrocopa (MCM-1 and MCM-2, respectively) and individual life table tests for M. macrocopa exposed separately to CCM at 5.0 and 10.0 ind./mL of B. calyciflorus (CCM-1 and CCM-2, respectively) to test the allelopathic interactions between B. calyciflorus and M. macrocopa relative to the concentration of allelochemical, temperature, and algal density. The S. obliquus- (stored in EPA medium for 24 h) conditioned medium was the control to avoid the likely effects of S. obliquus' allelochemicals in MCM or CCM on B. calyciflorus or M. macrocopa (Conde-Porcuna, 1998; Verschoor et al., 2007).

Tests were conducted in 5 mL mediums with algal densities of 0.5, 1.0, and 3.0 × 106 cells/mL S. obliquus in 8 mL transparent jars in a dark incubator at 20 ± 1, 25 ± 1, and 30 ± 1 °C, respectively. For the B. calyciflorus life table experiments, we used 81 test jars (3 temperatures × 3 algal densities × 3 treatments (MCM-1, MCM-2 plus 1 control) × 3 replicates) and each jar received 5 neonates (< 4 h old). For the M. macrocopa life table experiments, we used 405–540 test jars (3 temperatures × 3 algal densities × 3 treatments (CCM-1, CCM-2 plus 1 control) × 15–20 replicates) and each jar received 1 neonate (< 12 h old) of the third generation produced by parthenogenetic reproduction of M. macrocopa. Following inoculation, the surviving test individuals were counted every 12 h and transferred to a new jar containing corresponding algal densities (0.5, 1.0, and 3.0 × 106 cells/mL S. obliquus) and MCM or CCM under different temperatures (20 ± 1, 25 ± 1, and 30 ± 1 °C). Dead individuals and neonates, if any, were enumerated and removed. Both experiments were continued until the last adult individual in each replicate died.

The main life history variables including life expectancy at birth (e 0), net reproductive rate (R 0), generation time (T), intrinsic rate of population growth (rm ), average lifespan (LS), total number of offspring (NO) of B. calyciflorus and M. macrocopa were calculated using the following formulas (Pianka, 1988):

Life expectancy at birth (start of age x = 0) 

where Tx is the cumulative number of individuals from age x to maximum age, nx  = number of living individuals at the beginning of age x.

where l x (age-specific survival rate) is proportion of living individuals at the beginning of age x, mx (age-specific fecundity) is number of offspring produced per female at age x.

Intrinsic rate of population growth (rm ) was firstly estimated as r-rough

For final calculation, we solved the equation: 

where n is the age at maturity.

Total number of offspring (NO) is number of offspring produced per M. macrocopa or B. calyciflorus female during whole lifetime.

2.4 Statistical analysis

Analysis-of-variance (ANOVA) and multiple comparison tests were performed with SPSS 16.0 to quantify significant differences in the life expectancy at birth (e 0), net reproductive rate (R 0), generation time (T), intrinsic rate of population growth (rm ), average lifespan (LS), and total number of offspring (NO) of B. calyciflorus and M. macrocopa between the zooplankton-conditioned medium and control under different temperatures and algal densities. Data were first tested for homoscedasticity (Levene's test for ANOVA) and normality (Kolmogorov-Smirnoff test). Data that were non-normal or heteroscedastic were then analyzed using the Kruskal-Wallis tests.

3 Results

3.1 Effect of MCM concentration on B. calyciflorus

The three-way ANOVA results on the effects of temperature, algal density, and MCM concentration and their interactions on the main life history variables (i.e., e 0, R 0, T, rm , LS, and NO) of B. calyciflorus are presented in Table 1. Temperature, algal density and interactions of temperature × algal density, algal density × MCM and temperature × algal density × MCM had significant effects on the R 0 of B. calyciflorus (P < 0.05, Tab. 1). Temperature, algal density, and their interaction also had significant effects on the rm of B. calyciflorus (P < 0.01, Tab. 1). Compared to the controls, both the R 0 and rm of B. calyciflorus in MCM were significantly reduced under the combination of 20 °C and 0.5 × 106 cells/mL algal density (P < 0.05, Figs. 1 and 2 ). However, the R 0 and rm of B. calyciflorus in MCM were significantly elevated in MCM-2 under the combination of 25 °C and 3.0 × 106 cells/mL algal density (P < 0.05, Figs. 1 and 2). The both variables had no significant difference under the other combinations of temperature and algal density (P > 0.05, Figs. 1 and 2).

Temperature, algal density and interactions of temperature × algal density and algal density × MCM also had significant effects on the NO of B. calyciflorus (P < 0.05, Tab. 1). Compared to the controls, the NO of B. calyciflorus in MCM were significantly decreased under the combination of 20 °C and 0.5 × 106 cells/mL algal density (P < 0.05, Fig. 3). The variable had no significant difference under the other combinations of temperature and algal density (P > 0.05, Fig. 3).

Temperature, algal density, and the temperature × algal density and algal density × MCM interactions had significant effects on the e 0 and LS of B. calyciflorus (P < 0.05, Tab. 1). Compared to the controls, neither the e 0 or LS of B. calyciflorus in MCM had significant changes (P > 0.05, Figs. 4 and 5 ), except that they were significantly prolonged under the combination of 25 °C and 1.0 × 106 cells/mL algal density (P < 0.05, Figs. 4 and 5). Regardless of temperature and algal density, compared to the controls, MCM had no significant effects on the T of B. calyciflorus (P > 0.05, Fig. 6).

Table 1

Results of the three-way ANOVA testing the effects of temperature, algal density, competitor-conditioned medium concentration and their interactions on the selected life history variables of B. calyciflorus and M. macrocopa.

thumbnail Fig. 1

Effects of two concentrations of competitor-conditioned medium on the net reproductive rate (R 0) of B. calyciflorus and M. macrocopa under different temperatures and algal densities (mean ± SE). Control, MCM-1, MCM-2, CCM-1, CCM-2 and * are same with Figure 4.

thumbnail Fig. 2

Effects of two concentrations of competitor-conditioned medium on the intrinsic rate of population growth (rm ) of B. calyciflorus and M. macrocopa under different temperatures and algal densities (mean ± SE). Control, MCM-1, MCM-2, CCM-1, CCM-2 and * are same with Figure 4.

thumbnail Fig. 3

Effects of two concentrations of competitor-conditioned medium on the total number of offspring (NO) of B. calyciflorus and M. macrocopa under different temperatures and algal densities (mean ± SE). Control, MCM-1, MCM-2, CCM-1, CCM-2 and * are same with Figure 4.

thumbnail Fig. 4

Effects of two concentrations of competitor-conditioned medium on the life expectancy at birth (e 0) of B. calyciflorus and M. macrocopa under different temperatures and algal densities (mean ± SE). Control: S. obliquus-conditioned medium; MCM-1 and MCM-2: conditioned medium at 0.5 and 1.0 ind./mL−1 of M. macrocopa respectively; CCM-1 and CCM-2: conditioned medium at 5.0 and 10.0 ind./mL−1 of B. calyciflorus respectively; * P < 0.05.

thumbnail Fig. 5

Effects of two concentrations of competitor-conditioned medium on the average lifespan (LS) of B. calyciflorus and M. macrocopa under different temperatures and algal densities (mean ± SE). Control, MCM-1, MCM-2, CCM-1, CCM-2 and * are same with Figure 4.

thumbnail Fig. 6

Effects of two concentrations of competitor-conditioned medium on the generation time (T) of B. calyciflorus and M. macrocopa under different temperatures and algal densities (mean ± SE). Control, MCM-1, MCM-2, CCM-1, CCM-2 and * are same with Figure 4.

3.2 Effect of CCM concentration on M. macrocopa

The three-way ANOVA results on the effects of temperature, algal density, CCM concentration, and their interactions on the main life history variables (i.e., e 0, R 0, T, rm , LS, and NO) of M. macrocopa are presented in Table 1. Temperature, algal density, CCM, and their interactions all had significant effects on the R 0, rm and NO of M. macrocopa (P < 0.001, Tab. 1). The R 0, rm and NO of M. macrocopa cultured in CCM were significantly higher than in controls at all temperatures and algal densities (P < 0.05, Figs. 13), expect under a few conditions. Compared to the controls, R 0, rm and NO were significantly lower under the combination of 30 °C, 3.0 × 106 cells/mL algal density and CCM-2. The T was also prolonged under the combination of 20 °C and 3.0 × 106 cells/mL algal density (P < 0.05, Figs. 13 and 6). The rm of M. macrocopa was not significantly affected under the combination of 20 °C and 0.5 and 1.0 × 106 cells/mL algal density (P > 0.05, Fig. 2).

Temperature, algal density, and the temperature × algal density and temperature × CCM interactions had significant effects on the e 0 and LS of M. macrocopa (P < 0.05, Tab. 1). Both the e 0 and LS of M. macrocopa cultured in CCM-1 were significantly shorter than in the controls under the combination of 20 °C and 3.0 × 106 cells/mL algal density (P < 0.05, Figs. 4 and 5). The e 0 and LS of M. macrocopa cultured in CCM-1 were, however, significantly longer than in the controls under the combination of 25 °C and 3.0 × 106 cells/mL algal density (P < 0.05, Figs. 4 and 5). The both variables were not significantly affected under the other combinations of temperature and algal density compared to the controls (P > 0.05, Figs. 4 and 5). Regardless of temperature and algal density, compared to the controls, CCM had no significant effects on the T of M. macrocopa (P > 0.05, Fig. 6), except in CCM-2 under the combination of 20 °C and 3.0 × 106 cells/mL algal density (P > 0.05, Fig. 6).

4 Discussion

Many field observations and laboratory studies have shown that cladocerans inhibit the population growth of rotifers through exploitative competition and mechanical interference competition (Gilbert, 1985, 1988; Burns and Gilbert, 1986a, b). The relative importance of the two competitive mechanisms is debatable (Gilbert, 1985; Fussmann, 1996). Chemical interference through allelopathy has been documented for some zooplankton species and many respond to this stress (Tollrian and Harvell, 1999; Brönmark and Hansson, 2012). Only three cases of the allelopathic effects of cladocerans on rotifers have been reported to date (Conde-Porcuna, 1998; Guo et al., 2011; Gama-Flores et al., 2018). D. longispina allelochemicals inhibit the population growth rate of K. cochlearis (Conde-Porcuna, 1998). Contrarily, D. similis allelochemicals stimulate the population growth rate of B. calyciflorus (Guo et al., 2011). Gama-Flores et al. (2018) found that, compared to B. calyciflorus and Plationus patulus, B. havanaensis is more sensitive to the allelochemicals from Ceriodaphnia dubia and D. pulex, and especially to M. macrocopa. Inconsistent effects of allelochemicals from the three cladocerans on the population growth rates of the three rotifers were also detected. The effects of allelochemicals from cladoceran species on different rotifer species were either inconclusive, stimulating or inhibiting, or almost invalid, suggesting that the interaction depends on the origin of the allelochemical as well as the rotifer type. In fact, allelochemical concentrations in cladoceran-conditioned mediums accompanied with algae are higher than that in the controls without algae in the pre-culture experiments (Guo et al., 2011; Gama-Flores et al., 2018). Together, with the results that S. obliquus chemicals have a strong stimulating effect on the feeding rate of B. calyciflorus (Verschoor et al., 2007), allelochemicals from algae (i.e., food sources) may be responsible for the stimulatory effects of allelochemicals in cladoceran-conditioned medium on the population growth rates of the rotifers. The allelochemicals released by various algae that universally stimulated the feeding rates of different rotifers deserves further investigation.

Using the Conde-Porcuna (1998) method, S. obliquus-conditioned medium served as the control to exclude the effects of allelochemicals secreted by S. obliquus on the feeding rate of B. calyciflorus. Both R 0 and rm of B. calyciflorus in MCM were inhibited under the combination of 20 °C and 0.5 × 106 cells/mL algal density, as consistent with the findings of Conde-Porcuna (1998). Our previous study found that under the same temperature and density of S. obliquus, competition of M. macrocopa inhibited the population growth rates of B. calyciflorus, which resulted in the elimination of B. calyciflorus (Huang et al., 2014). These results indicated that the allelopathic inhibition of M. macrocopa on B. calyciflorus likely played a positive role in the competitive rejection of B. calyciflorus.

In the present study, both R 0 and rm of B. calyciflorus were stimulated in MCM-2 under the combination of 25 °C and 3.0 × 106 cells/mL S. obliquus, which supported our first hypothesis and Guo et al.'s (2011) conclusions. Under the same temperature and S. obliquus density conditions, the results of Huang et al. (2014) found that M. macrocopa's competition pressure stimulated the B. calyciflorus' population growth rate, and finally eliminated M. macrocopa. The allelopathic promotion of M. macrocopa on B. calyciflorus also likely aided the competitive rejection of M. macrocopa. Additionally, in our present study, the B. calyciflorus' NO in MCM was higher than that in controls under the combination of 20 °C and 0.5 × 106 cells/mL S. obliquus, while under the other combinations of temperature and algal density did not differ from the controls.

The present study found that the chemically-mediated effects of M. macrocopa on the R 0, rm and NO of B. calyciflorus were non-significant in many cases. The impacts were stimulatory or even inhibitory in a few cases that were dependent on temperature, food density, concentration of M. macrocopa allelochemical, and type of life history variables of B. calyciflorus. These results support our two hypotheses: (1) allelopathic stimulation exists in the competitive process between M. macrocopa and B. calyciflorus; (2) the allelopathy is stimulatory, inhibitory, or nearly invalid, depending on the origin and concentration of allelochemicals, life history variable, temperature, and algal density. However, more research should be performed to distinguish the relative importance of chemical interference, exploitative, and mechanical interference competitions in interspecific interactions of M. macrocopa and B. calyciflorus.

Allelopathic effects of rotifers on cladocerans have not been reported until now. Our previous study (Huang et al., 2014) found that, regardless of temperature, M. macrocopa outcompeted B. calyciflorus at 0.5 × 106 cells/mL S. obliquus, but the competition pressure of B. calyciflorus promoted the population growth rate of M. macrocopa. This implies that the chemical interference competitive stimulatory effects of B. calyciflorus on M. macrocopa are responsible for the increase in M. Macrocopa's population growth rate. In the present study, regardless of temperature, the R 0, rm and NO of M. macrocopa cultured in CCM were significantly higher than those in the controls at 0.5 × 106 cells/mL S. obliquus, with a few exceptions. These results support our previous study's implied results and our first hypothesis. These results also prove that allelopathic promotion of B. calyciflorus on M. macrocopa aids the competitive rejection of B. calyciflorus.

The M. macrocopa's rm cultured in CCM did not significantly differ from that in the controls under the combination of 20 °C and 0.5 × 106 cells/mL S. obliquus. This indicates that the allelopathic promotion of B. calyciflorus on M. macrocopa decreased under the lower temperature. Thus, the allelopathic stimulatory effects of B. calyciflorus on M. macrocopa were dependent on temperature. Regardless of temperature, Huang et al. (2014) proved that the population growth rates of M. macrocopa cultured with B. calyciflorus were higher than that in the controls (except under the highest temperature). Furthermore, the population densities increased after an initial decrease compared to that in the controls with higher densities of S. obliquus (1.0 and 3.0 × 106 cells/mL). Huang et al. (2014) also implied that the chemical interference competitive stimulatory effects of B. calyciflorus on M. macrocopa were responsible for the higher population growth rates and population densities of M. macrocopa cultured with B. calyciflorus. In the present study, regardless of temperature, the R 0, rm and NO of the M. macrocopa cultured in CCM were almost all significantly higher than in the controls with higher densities of S. obliquus (1.0 and 3.0 × 106 cells/mL). These findings support our 2014 (Huang et al.) implied findings and further supports our first hypothesis.

However, B. calyciflorus excluded M. macrocopa under the same temperatures and densities of S. obliquus (Huang et al., 2014), which indicated that the allelopathic promotion was lower than the exploitative inhibition of B. calyciflorus on M. macrocopa, and that the exploitative interference was more important. Meanwhile, compared to the controls, the R 0, rm , and NO of M. macrocopa cultured in CCM were significantly lower under the combination of 30 °C, 3.0 × 106 cells/mL algal density and CCM-2. The rm was significantly lower, likely due to the prolongation of the T under the combination of 20 °C and 3.0 × 106 cells/mL algal density. This indicates that the allelopathic inhibition of B. calyciflorus on M. macrocopa aided the competitive rejection of M. macrocopa. Additionally, the rm of M. macrocopa cultured in CCM was not significantly affected under the combination of 20 °C and 1.0 × 106 cells/mL algal density. Based on these results, we found that the allelopathic effects of B. calyciflorus on the R 0, rm , and NO of M. macrocopa were stimulatory in many cases, were inhibitory in a few cases, or were non-significant. The effects were dependent on temperature, food density, M. macrocopa life history variable, and the concentration of B. calyciflorus allelochemicals.

Our study found that the e 0, T, and LS of B. calyciflorus were significantly affected in only few cases due to MCM at all temperatures and algal densities. These findings are similar to the effects of CCM on the three life history variables of M. macrocopa. Similar results were observed in Gama-Flores et al. (2018). Based on the e 0, T, and LS, the interspecific effects of B. calyciflorus- and M. macrocopa-mediated allelochemicals are almost all invalid, indicating that the allelopathic effects between B. calyciflorus and M. macrocopa were dependent on the life history variable.

Our results found that the allelopathic substances from M. macrocopa and B. calyciflorus affected their life history variables in varying degrees. The allelopathic substances are, however, likely different in composition, amount, and activity. Prior to the present study, the information on the chemical nature of substances secreted by crustaceans and rotifers was almost completely lacking (Zadereev and Lopatina, 2015). The main difficulties in isolating and identifying these substances are related to their low concentrations in the medium, potential synergistic effects, and absence of easy and effective methods for determining the target components (Pohnert et al., 2007). Extraction, isolation, structure identification, and function studies of rotifer and cladoceran allelochemicals should be addressed in future work. These findings would be of crucial importance for understanding the interspecific competitive mechanism of zooplankton, especially rotifers and cladocerans, and their co-evolution under competitive pressure.

5 Conclusions

Compared to the allelopathic effects of M. macrocopa on B. calyciflorus, M. macrocopa had higher sensitivity to the B. calyciflorus allelochemicals. The chemically mediated effects of M. macrocopa on the main life history variables of B. calyciflorus are non-significant in many cases and stimulatory or inhibitory in a few cases. However, the allelopathic effects of B. calyciflorus on the main life history variables of M. macrocopa are stimulatory in many cases, but inhibitory and non-significant in a few cases. The underlying mechanisms for both chemically mediated effects should be further investigated. Overall, the interspecific allelopathic effects of B. calyciflorus and M. macrocopa were dependent on the origin and concentration of allelochemical, life history variable, temperature, and algal (food) density.

Acknowledgements

This work was supported by Natural Science Foundation of the Education Department of Anhui Province (KJ2015A228) and the Natural Science Foundation of China (31470015, 41877417).

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Cite this article as: Huang L, Xi Y, Wen X. 2019. Interspecific effects of the cladoceran- (Moina macrocopa) and the rotifer- (Brachionus calyciflorus) conditioned medium on main life history variables in relation to temperature and algal density. Ann. Limnol. - Int. J. Lim. 55: 14

All Tables

Table 1

Results of the three-way ANOVA testing the effects of temperature, algal density, competitor-conditioned medium concentration and their interactions on the selected life history variables of B. calyciflorus and M. macrocopa.

All Figures

thumbnail Fig. 1

Effects of two concentrations of competitor-conditioned medium on the net reproductive rate (R 0) of B. calyciflorus and M. macrocopa under different temperatures and algal densities (mean ± SE). Control, MCM-1, MCM-2, CCM-1, CCM-2 and * are same with Figure 4.

In the text
thumbnail Fig. 2

Effects of two concentrations of competitor-conditioned medium on the intrinsic rate of population growth (rm ) of B. calyciflorus and M. macrocopa under different temperatures and algal densities (mean ± SE). Control, MCM-1, MCM-2, CCM-1, CCM-2 and * are same with Figure 4.

In the text
thumbnail Fig. 3

Effects of two concentrations of competitor-conditioned medium on the total number of offspring (NO) of B. calyciflorus and M. macrocopa under different temperatures and algal densities (mean ± SE). Control, MCM-1, MCM-2, CCM-1, CCM-2 and * are same with Figure 4.

In the text
thumbnail Fig. 4

Effects of two concentrations of competitor-conditioned medium on the life expectancy at birth (e 0) of B. calyciflorus and M. macrocopa under different temperatures and algal densities (mean ± SE). Control: S. obliquus-conditioned medium; MCM-1 and MCM-2: conditioned medium at 0.5 and 1.0 ind./mL−1 of M. macrocopa respectively; CCM-1 and CCM-2: conditioned medium at 5.0 and 10.0 ind./mL−1 of B. calyciflorus respectively; * P < 0.05.

In the text
thumbnail Fig. 5

Effects of two concentrations of competitor-conditioned medium on the average lifespan (LS) of B. calyciflorus and M. macrocopa under different temperatures and algal densities (mean ± SE). Control, MCM-1, MCM-2, CCM-1, CCM-2 and * are same with Figure 4.

In the text
thumbnail Fig. 6

Effects of two concentrations of competitor-conditioned medium on the generation time (T) of B. calyciflorus and M. macrocopa under different temperatures and algal densities (mean ± SE). Control, MCM-1, MCM-2, CCM-1, CCM-2 and * are same with Figure 4.

In the text

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