Linking herbivore-induced defences to population dynamics

1. Theoretical studies have shown that inducible defences have the potential to affect population stability and persistence in bi‐ and tritrophic food chains. Experimental studies on such effects of prey defence strategies on the dynamics of predator–prey systems are still rare. We performed replicated population dynamics experiments using the herbivorous rotifer Brachionus calyciflorus and four strains of closely related algae that show different defence responses to this herbivore. 2. We observed herbivore populations to fluctuate at a higher frequency when feeding on small undefended algae. During these fluctuations minimum rotifer densities remained sufficiently high to ensure population persistence in all the replicates. The initial growth of rotifer populations in this treatment coincided with a sharp drop in algal density. Such a suppression of algae by herbivores was not observed in the other treatments, where algae were larger due to induced or permanent defences. In these treatments we observed rotifer population densities to first rise and then decline. The herbivore went extinct in all replicates with large permanently defended algae. The frequency of herbivore extinctions was intermediate when algae had inducible defences. 3. A variety of alternative mechanisms could explain differential herbivore persistence in the different defence treatments. Our analysis showed the density and fraction of highly edible algal particles to better explain herbivore persistence and extinctions than total algal density, the fraction of highly inedible food particles or the accumulation of herbivore waste products or autotoxins. 4. We argue that the rotifers require a minimum fraction and density of edible food particles for maintenance and reproduction. We conjecture that induced defences in algae may thus favour larger zooplankton species such as Daphnia spp. that are less sensitive to shifts in their food size spectrum, relative to smaller zooplankton species, such as rotifers and in this way contributes to the structuring of planktonic communities.     

盐酸四环素浓度和食物密度对萼花臂尾轮虫生活史特征的综合影响

近年来,抗生素的环境污染问题已引起人们的广泛关注,其在环境中的残留可对水生态系统的结构和功能产生重要影响。迄今,盐酸四环素浓度和食物密度对轮虫生活史特征的影响研究尚未见报道。以萼花臂尾轮虫(Brachionus calyciflorus)为受试动物,研究了在不同斜生栅藻(Scenedesmus obliquus)密度下,不同浓度的盐酸四环素(Tetracycline hydrochloride)对萼花臂尾轮虫生活史特征的影响。结果表明,食物密度和盐酸四环素浓度对轮虫的生命期望、净生殖率、世代时间、内禀增长率、平均寿命和后代混交率,以及食物密度和盐酸四环素浓度间交互作用对除了内禀增长率外的其他5个统计学参数均具有显著影响。在各食物密度下,轮虫的特定年龄繁殖率高峰值随着盐酸四环素浓度的增加呈现先增加后降低的趋势;盐酸四环素对轮虫生长和繁殖参数的影响呈现"低促高抑"的特点。3个食物密度下,高浓度的盐酸四环素显著提高了萼花臂尾轮虫的后代混交率,且在1.0×10~6个/mL藻密度下毒物浓度与轮虫后代混交率间具有显著的剂量-效应关系。食物密度的高低显著影响盐酸四环素对萼花臂尾轮虫的毒性效应。     

INDUCIBLE COLONY FORMATION WITHIN THE SCENEDESMACEAE: ADAPTIVE RESPONSES TO INFOCHEMICALS FROM TWO DIFFERENT HERBIVORE TAXA1

We studied the occurrence of colony formation within 40 different strains of Scenedesmaceae (Chlorococcales, Chlorophyta) in response to grazing‐released infochemicals from the herbivorous zooplankters Brachionus calyciflorus Pallas (Rotifera) and Daphnia magna Strauss (Cladocera). With the exception of two strains, all strains showed similar responses to both B. calyciflorus and D. magna infochemicals, either no response or inducible colony formation. Colony size was found to increase with B. calyciflorus infochemical concentration and could be described by a sigmoid function. The increase in colony size was more pronounced in the Scenedesmus species tested than in Desmodesmus species, which was probably due to higher threshold infochemical concentrations for colony induction in Desmodesmus. Therefore, the adaptivity of colony formation to the herbivory threat only holds above the threshold concentration for colony induction and as long as maximum colony size has not been attained. Taking this into account, our results suggest that inducible colony formation is a common adaptive response of many Scenedesmaceae to the threat of herbivory.     

Effect of two microalgae concentrations on body size and egg size of the rotifer <Emphasis Type="Italic">Brachionus calyciflorus</Emphasis>

The rotifer, Brachionus calyciflorus, was grown with two algae species (Chlorella sp. and Scenedesmus obliquus) at different concentrations (0.1, 1 and 10 × 10⁶ cells ml⁻¹). The body size (lorica biovolume) of individual rotifer and their egg size were measured when the populations were roughly in the exponential phase of population growth. The body size of the rotifers differed significantly (P < 0.05) among the two algae species used, however this effect was not observed for egg size. The body size of rotifers fed on higher densities of Chlorella sp. (10 × 10⁶ cells ml⁻¹) was significantly larger than for those fed on lower and medium densities (0.1 and 1 × 10⁶ cells ml⁻¹). Body size and egg size of rotifers fed with different amounts of Scenedesmus did not differ significantly. The egg size was significantly larger at higher food level of Chlorella. A significantly positive correlation was observed between the adult rotifer body size and their egg size.     

Algal defenses,population stability,and the risk of herbivore extinctions: a chemostat model and experiment

The effects of inducible defenses and constitutive defenses on population dynamics were investigated in a freshwater plankton system with rotifers as predators and different algal strains as prey. We made predictions for these systems using a chemostat predator–prey model and focused on population stability and predator persistence as a function of flow-through rate. The model exhibits three major types of behavior at a high nutrient concentration: (1) at high dilution rates, only algae exist; (2) at intermediate dilution rates, algae and rotifers show stable coexistence; (3) at low dilution rates, large population fluctuations occur, with low minimum densities entailing a risk of stochastic rotifer extinctions. The size and location of the corresponding areas in parameter space critically depend on the type of algal defense strategy. In an 83-day high-nutrient chemostat experiment we changed the dilution rate every 3 weeks, from 0.7 to 0.5 to 0.3 to 0.1 per day. Within this range of dilution rates, rotifers and algae coexisted, and population fluctuations of algae clearly increased as dilution rates decreased. The CV of herbivore densities was highest at the end of the experiment, when the dilution rate was low. On day 80, herbivorous rotifers had become undetectable in all three chemostats with permanently defended algae (where rotifer densities had already been low) and in two out of three chemostats where rotifers had been feeding on algae with inducible defenses (that represented more edible food). We interpret our results in relation to the paradox of enrichment.     

Larval rearing of burbot (Lota lota L.) using Brachionus calyciflorus rotifer as starter food

Burbot Lota lota L. is one of the endangered freshwater fish species in western Europe for which the development of controlled larval rearing procedures could produce enough material for stock enhancement. The suitability of the freshwater rotifer Brachionus calyciflorus as a start food for larviculture of burbot was investigated. After yolk‐absorption, the larvae were stocked in 40‐L tanks under different feeding conditions: clear water rearing conditions with rotifers (Brachionus calyciflorus) for 10 days (R), green water conditions (Chlorella sp.) with rotifers offered for 10 days (MALR), green water conditions (Chlorella sp.) for 3 days followed by clear water in combination with rotifer feeding for 7 days (AL3R), and clear water conditions with Artemia nauplii offered for 10 days (Art). After the 10‐day feeding, all groups received Artemia nauplii up to 35 days post‐hatching. Larval survival was counted at day 10 and at the end of the 35‐day rearing experiment. At day 35, a significant survival difference was noted between the groups where rotifers were supplemented with algae vs only Artemia. At the end of the experiment, the highest survival rate (69.20%) was obtained with larvae receiving only algae in the first 3 days of feeding. Lowest survival rate (24.90%) was obtained with larvae receiving only Artemia for 35 days. This indicates that smaller prey are essential for burbot at first feeding. Larval length and wet weight were measured at the time of mouth opening, at days 7, 10, and 21, and at the end of the experiment (day 35). On day 35, mean length of the larvae varied significantly between the treatments. However, the final wet weight of the larvae did not vary significantly between the treatments.     

Steady-state rotifer growth in a two-stage, computer-controlled turbidostat

Steady-state populations of rotifers (Brachionus calyciflorus)were maintained in twostage, continuous-flow turbidostatic cultureon the green alga Chlorella pyrenoidosa. In this system, themaximum specific growth rate,µ^max of the rotifers wasmaintained by using a computer to control the concentrationof algae, as rotifer food, in the rotifer culture. As rotifersconsumed algae, the turbidity decreased until a set-point wasreached. Then fresh algal suspension (supplied from a steady-statealgal chemostat) was metered into the rotifer culture, whichwas held in the dark. Rotifer and algal populations, as wellas rotifer µ^max entered steady states. These steady-stateresults were consistent with previous data from chemostat studies,but growth transients indicated that the of the µ^maxrotifersmay be subject to selection. The system is unique in providinga means to explore population dynamics of a metazoan maintainednear its µ^max.     

Effect of the cyclopoid copepod Mesocyclops thermocyclopoides on the interactions between the predatory rotifer Asplanchna intermedia and its prey Brachionus calyciflorus and B. angularis

In many shallow, eutrophic subtropical ponds, brachionid rotifers are common prey of the predatory copepod Mesocyclops thermocyclopoides. The predatory rotifer Asplanchna intermedia, which is itself a potential prey of the copepod, also feeds preferentially on brachionids. We studied in the laboratory the population dynamics of two mutually competing prey species, Brachionus angularis and B. calyciflorus, in the presence of the two predators A. intermedia and M. thermocyclopoides. The experimental design included separate population dynamics studies with one prey–one predator, two prey–one predator, one prey–two predator, and two prey–two predator systems. These combinations were compared with controls, in which both the prey species (B. angularis and B. calyciflorus) were grown separately and in combination with each other. In the absence of any predator, B. angularis generally eliminated the larger B. calyciflorus. Selective predation by the copepod allowed B. calyciflorus to persist longer in competition with B. angularis. Feeding by M. thermocyclopoides on A. intermedia reduced the predation pressure on B. calyciflorus. However, given enough time, the cyclopoid copepod was able to eliminate both the brachionids as well as the predatory Asplanchna.     

Effects of the blue-green alga Microcystis aeruginosa on zooplankton competitive relations

Summary Field distribution patterns and laboratory feeding experiments have suggested that blooms of colonial blue-green algae strongly inhibit relatively large-bodied daphnid cladocerans. We conducted laboratory experiments to test the hypothesis that blooms of the colonial blue-green alga Microcystis aeruginosa would shift competitive dominance away from large-bodied daphnid cladocerans toward smaller-bodied cladocerans, copepods, and rotifers. In laboratory competition experiments, increasing the proportion of M. aeruginosa in the algal food supply resulted in a shift from dominance by the relatively largebodied cladoceran Daphnia ambigua to dominace by the copepod Diaptomus reighardi. The small-bodied cladoceran Bosmina longirostris was always numerically heavily dominant over D. ambigua, but its estimated population biomasses were only slightly higher than those of D. ambigua. Daphnia ambigua consistently outcompeted the rotifer Brachionus calyciflorus. Our results demonstrate that blooms of M. aeruginosa can alter zooplankton competitive relations in laboratory experiments, favoring small-bodied cladocerans and copepods at the expense of large-bodied cladocerans. However, contrary to predictions, blooms of M. aeruginosa did not improve the competitive ability of rotifers.     

The efficacy of Scenedesmus morphology as a defense mechanism against grazing by selected species of rotifers and cladocerans

Phytoplankton often develop various defense mechanisms in response to zooplankton grazing, such as spines and colonies. While it is now known that increased spine length and cells in a colony of members of the genus Scenedesmus, when zooplankton grazing is intense, helps in reducing zooplankton filtering rates, the effect of these defense mechanisms at the population level has been observed in few studies. Here we present data on the growth rates of four zooplankton species, Brachionus calyciflorus, B. patulus, Ceriodaphnia dubia and Daphnia pulex at two food levels using two species of colony-forming Scenedesmus spp.: S. acutus (cell length = 18.2 ± 0.4 µm; width = 4.2 ± 0.1 µm; average colony length = 90 µm; width: 21 µm) and S. quadricauda (cell length: 21 ± 0.5 width 7.5 ± 0.3 µm; average colony length: 84 µm; width: 30 µm). Whereas S. acutus had no spines, S. quadricauda had spines of 6–10 µm. Population growth experiments of the test rotifers and cladocerans were conducted in 100 ml containers with 50 ml of the medium with test algae. Algae concentrations used were: 13 and 52 mg dw l^–1 of each of the two algal species offered in colonial forms. We used an initial inoculation zooplankter density of 1 ind. ml^–1 for either of the rotifer species and 0.2 ind. ml^–1 for either of the cladoceran species. In all, we had 64 test containers (4 test species of zooplankton × 2 test species of algae × 2 algal densities × 4 replicates). We found a significant effect of algal size on the growth rates of all the four tested species of zooplankton. The population growth rates of zooplankton ranged from –0.58 to 0.66 and were significantly higher on diet of S. acutus than of S. quadricauda. Thus, our study confirms that the larger colony size and the formation of spines in S. quadricauda were effective defenses against grazing by both rotifers and smaller sized cladoceran Ceriodaphnia dubia but that larger-bodied Daphnia pulex could exploit both the algal populations equally.     

Utilization of cyanobacteria by Brachionus calyciflorus: Anabaena flos-aquae (NRC-44-1) as a sole or complementary food source

The rotifer Brachionus calyciflorus can utilize the cyanobacterium Anabaena flos-aquae as either a sole or supplementary food source in laboratory culture. Positive population growth rates accompany food densities of 10 or 100 µg dry weight ml^–1, but slightly negative rates are found at a lower density (1.0 µg ml^–1). These results are consistent for rotifers feeding on two strains of A. flos-aquae, UTEX-1444 and NRC-44-1, with slightly enhanced survivorship and reproduction with the latter food. A 1:1 mixture (by dry weight) of Euglena gracilis and A. flos-aquae (NRC-44-1) produces survivorship comparable to that of control rotifer cohorts fed E. gracilis alone, but elicits significantly greater fecundity and population growth rates than found with the control food suspension at the same biomass density.     

Studies on Brachionus (Rotifera): an example of interaction between fundamental and applied research

The genus Brachionus has been the main subject of studies reported in about 1000 papers published since 1950. About three-fourths of these deal with Brachionus plicatilis and B. rotundiformis and are mainly related to their use as prey for aquatic organisms. Also abundant, but to a lesser extent, are studies on B. calyciflorus, many of which are concerned with aquatic ecotoxicology. These studies constitute an interesting interaction between fundamental and applied research. For example, advances in fundamental biology have been applied to improve the production of rotifer biomass. Alternatively, new perspectives in fundamental research on rotifers have emerged while solving technical and biological problems related to the rearing of aquatic animal larvae. This review describes some aspects that have shown a significant advance due to such interaction between fundamental and applied research on rotifers, e.g. growth conditions, biochemical composition and morphotypes.     

Transgenerational and within-generational induction of defensive morphology in Brachionus calyciflorus (Rotifera): importance of maternal effect

Maternal effects on the induction of defensive morphology are regarded as an adaptive strategy. For instance, a female can transmit environmental conditions related to predation risk to offspring of the same generation or succeeding generations. However, studies have presented limited information regarding such an adaptive maternal effect on monogonont rotifers. In the present study, the maternal effects on the spine development of rotifers were evaluated using Brachionus calyciflorus-Asplanchna models. Asplanchna can release soluble kairomones into the environments, thereby inducing B. calyciflorus to form defensive morphs (e.g., elongated posterolateral spines). Our empirical data supported the hypothesis that an amictic Brachionus-experienced Asplanchna kairomones could produce offspring with longer posterolateral spine in the current or succeeding generation than those of a non-experienced amictic female. On the basis of our data, we speculated that the maternal effect of B. calyciflorus may involve the transfer and dilution of inducers (e.g., hormone) within and between generations. On one hand, our results reinforced the within-generation maternal effects on induction of defensive morphology of rotifers; on the other hand, our results enhanced transgenerational inducible defense to other planktonic taxa that have been only observed in cladocera.     

Rotifer digestive enzymes: direct detection using the ELF technique

Hydrolytic enzymes involved in rotifer digestive processes were investigated directly at the sites of enzyme action using the ELF (Enzyme Labelled Fluorescence) technique. After enzymatic hydrolysis of an artificial ELF substrate, the fluorescent product ELF alcohol (ELFA) marked the sites of enzyme action. The time development of ELFA labelling was studied at different incubation times. Phosphatases, β-N-acetylhexosaminidases and lipases were examined in Brachionus angularis, B. calyciflorus, Keratella cochlearis and Lecane closterocerca from fed-batch cultures. We detected activities of all studied enzymes mostly in the stomach and intestine of rotifers. L. closterocerca was the only species showing enzyme activity at the mastax. Lipase activity was observed in the stomach and intestine of all species and in the mastax of L. closterocerca. Phosphatases were frequently located at the corona of B. calyciflorus. In other cases, both phosphatases and β-N-acetylhexosaminidases were rarely detected at the corona, and on the lorica and epidermis of some species. Guest editors: S. S. S. Sarma, R. D. Gulati, R. L. Wallace, S. Nandini, H. J. Dumont and R. Rico-Martínez Advances in Rotifer Research     

Rotifers as predators on small ciliates

Clearance rates of Synchaeta pectinata, Brachionus calyciflorus and Asplanchna girodi on Tetrahymena pyriformis (46 µm in length) at a density of 10 cells ml^–1, in the presence of algal food, were 2.5 to 6.1 ml rot.^–1 day^–1. Clearance rates of these rotifers were, respectively, about 2, 3, and 13 times lower on Strobilidium gyrans (58 µm in length) than on T. pyriformis, indicating that the saltations of S. gyrans are an effective escape response. Clearance rates of S. pectinata were considerably lower on Colpidium striatum (81 µm) than on S. gyrans, suggesting that S. pectinata may not be able to ingest ciliates of this size. S. pectinata had a clearance rate of 19 ml rot.^–1 day^–1 on S. gyrans at a density of 1.2 cells ml^–1, in the absence of edible algal food. Rotifers may prey extensively on ciliates in natural plankton communities, ingesting 25 to 50 individuals in the 45–60 µm size range day^–1.     

Reduced investment in sex as a cost of inducible defence in Brachionus calyciflorus (Rotifera)

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Neuropharmacology of rotifer feeding,oviposition, and anesthesia

Effect of acetylcholine and anticholinergic drugs on feeding, oviposition, and anesthesia in rotifers was investigated. Neurotransmitter as well as antagonist drugs inhibited feeding in Brachionus calyciflorus in a dose-dependent manner. Most antagonist drugs caused an oscillating tachyphylaxis (drug habituation): the drug effect wore off and returned several times within an hour. Acetylcholine inhibited oviposition in Philodina acuticornis, and this effect was antagonized by all groups of anticholinergic drugs. The strongest antagonism was caused by neuromuscular blockers, and thus the cause of oviposition inhibition may be a cloacal sphincter spasm. Acetylcholinesterase inhibitory insecticides also antagonize the acetylcholine effect. Acetylcholine potentiates the anesthetic activity of ionizing local anesthetics (procaine, lidocaine) as well as that of atropine and the beta-adrenergic blocker propranolol. Muscarinic antagonists (atropine, benactyzine) and propranolol caused foot paralysis in B. calyciflorus, which is also potentiated by acetycholine. Further details of these results are given by Nogrady and Keshmirian (1986a, b).     

Combined influences of particulate and dissolved factors in the toxicity of Microcystis aeruginosa (NRC-SS-17) to the rotifer Brachionus calyciflorus

The rotifer Brachionus calyciflorus is subject to the combined influence of particulate and dissolved factors derived from the toxic cyanobacterium Microcystis aeruginosa. Toxicity manifests itself through reduction of cohort survivorship and probably though reduction of cohort reproduction. Toxic effects are seen only when there is a particulate food material available in suspension, either M. aeruginosa itself or another food type which may act as a carrier for a dissolved toxic factor. Regardless of exact mechanism, the presence of a toxic strain of this blue-green may lead to diminution of population growth of co-occurring rotifer populations.     

In situ tests on inducible defenses in Dictyota kunthii and Macrocystis integrifolia (Phaeophyceae) from the Chilean coast

Numerous experimental studies have reported inducible defenses in macroalgae, but most of them have been conducted in laboratory environments where algae were maintained detached from the substratum and in artificial flow regimes. The results of those experiments might not reflect the natural situation, which can only be studied in situ. We examined whether the brown macroalgae Dictyota kunthii (C. Agardh) Greville and Macrocystis integrifolia (Bory) show inducible defenses following exposure to different grazing levels (direct, water-borne cues from nearby grazed conspecifics, presence of a non-grazing herbivore and natural grazing) in field experiments, striving to maintain natural conditions as much as possible. We measured palatability of algae after exposure to different grazing levels by using live algae and agar-based food containing non-polar extracts. M. integrifolia showed no induction of defenses (at least not of non-polar compounds), suggesting constitutive defenses, absence of defenses (tolerance) or use of another strategy to avoid herbivory. These results are similar to those from previous laboratory experiments. In D. kunthii, defense was induced after two weeks of direct grazing by amphipods under field conditions. Water-borne cues from nearby grazed conspecifics, presence of a non-grazing herbivore and natural grazing did not induce defenses. Induction of defense in response to direct grazing agrees with results from a previous laboratory study, but while indirect cues induced defenses in the laboratory, there was no measurable induced defense in the field. Probably chemical cues from grazers are diluted quickly in the field, not reaching concentrations that cause induction of defenses. This might be the reason why in some algae induction by direct grazing is a more important defensive strategy than induction by water-borne cues. The results from our study also suggest that laboratory experiments showing induced defenses in response to grazed neighbours or mere grazer presence need to be interpreted with caution.     

Foraging behaviour of Brachionus calyciflorus (Pallas): variations in the swimming path according to presence or absence of algal food (Chlorella)

Both swimming and attachment behaviour of immature female Brachionus calyciflorus (Pallas) from a young orthoclone were analyzed under four experimental conditions: with and without algae (Chlorella), and with fed and starved individuals. Eighteen hours before the recording, two random groups were formed. To the first group, Chlorella was added. The second was placed in pure water. Both were filmed in red light to avoid a phototactic effect. Video-recorded swimming behaviour of B. calyciflorus was analyzed by automatic tracking. Each B. calyciflorus was filmed alternately in the presence or absence of Chlorella for five periods of 15 min. Under indentical light and temperature conditions the number of animals attached to the culture dish was measured with both starved and fed females. We observed a significant difference in swimming paths depending on the presence or absence of food, and the physiological state of the individuals. In the presence of Chlorella the linear speed was lower and the angular speed was greater. This increase in angular speed was more pronounced when females were subjected to a period of starvation before the experimentation. The attachment behaviour increased in the algal environment. This modification of swimming behaviour enables females to increase the time spent in a favorable food environment.