Abstract
Predation is a well-known factor that structures rotifer communities. However, the role of protists as predators is relatively understudied. Here, we investigated predatory behavior of Actinosphaerium sp., a freshwater heliozoan, on seven rotifer species. Predators and prey were collected from a local playa; except for Brachionus calyciflorus that served as a naive prey control. Prey included large species (≥ 175 µm mean length: Asplanchna sieboldii, B. calyciflorus, Platyias quadricornis, and Lacinularia flosculosa) and small species (< 175 µm: Cephalodella gibba, Euchlanis dilatata, and Lepadella patella). Four experiments were conducted. (1) Single prey items of varying size and motility. Larger prey types were ~ 1.7 to 3.0 times more likely to be ingested than small prey. No L. flosculosa were ingested, contrary to field observations. No correlation was found between swimming speed and predation risk. (2) Preference tests. Asplanchna sieboldii and B. calyciflorus were favored prey. (3) Growth rate of Actinosphaerium on mixed diets, with and without Asplanchna. Highest population growth of Actinosphaerium was observed in presence of A. sieboldii. (4) Prey defenses. Susceptibility of spined versus unspined B. calyciflorus resulted in no significant difference in predation risk. Thus, size and being mobile (compared to sessility) are the primary risk factors influencing rotifer predation vulnerability.
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Introduction
Rotifers play an important role as primary consumers in freshwater systems (Wallace et al., 2006, 2015), so understanding how their communities are structured is key to interpreting ecological and evolutionary processes affecting them. Predation is a well-known factor that structures rotifer communities (Lynch, 1979; Williamson, 1983; Li et al., 2022). Rotifers are consumed by an array of freshwater predators including larval fishes (Stenson, 1982; Zhang et al., 2022), aquatic insects (Moore & Gilbert, 1987; Walsh, 1995; Hampton et al., 2000; Hampton & Gilbert, 2001), hydra (Walsh, 1995), cyclopoid copepods (Williamson, 1983), predatory rotifers (Gilbert, 1967, 2017, 2019), and some protists (Bell et al., 2006; Weithoff & Bell, 2022). However, they are not defenseless.
Defensive mechanisms exhibited by freshwater protists and invertebrates are varied and widespread across the phylogenetic spectrum [e.g., ciliates (Buonanno et al., 2013, 2017, 2020), cladocerans (Stenson, 1987; Herzog et al., 2016), copepods (Almeda et al., 2017; Buskey et al., 2017), insects and mites (Kerfoot et al., 1980; Kerfoot, 1982; Hershey & Dodson 1987), and gastrotrichs (Balsamo et al., 2020)]. In Rotifera (sensu stricto) defensive mechanisms include behavioral, morphological, and chemical strategies (Stemberger, 1985; Wallace et al., 2015). Behavioral defenses include diel vertical migration (DVM) (Williamson & Magnien, 1982), changes in swimming velocity (Williamson, 1987; Gilbert & Kirk, 1988; Parysek & Pietrzak, 2020) and turning angles (Obertegger et al., 2018), passive sinking (Stemberger & Gilbert, 1987a), and facultative sessility (Gilbert, 2019). But swimming behavior can be modified depending on whether the individual possesses another defense mechanism. For example, Parry et al. (2022) found that Brachionus calyciflorus Pallas, 1766, which lack defensive spines increased their swimming speed in presence of the rotiferan predator Asplanchna brightwellii Gosse, 1850, but spined (defended) individuals did not. Behavioral defenses also can be associated with specific structures. For example, Polyarthra species make rapid saltatory movements by rapidly moving their paddles, flexing them anteriorly from the resting position alongside the body. In Polyarthra vulgaris Carlin, 1943 these jumps can move the animal 15 body lengths within ~ 60 ms−1. Saltation movements also are produced by the movement of arms in Hexarthra. In Scaridium an elongated foot and toes appear to enable similar escape movements (H. Segers, pers. commun.). In contrast, Filinia terminalis (Plate, 1886) possesses long spines that flex, but these function act as foils to deter predation by the predatory copepod Skistodiaptomus (Diaptomus) pallidus (Herrick, 1879). On the other hand, Yin et al., (2017) showed that lorica thickness increased in the offspring of amictic females of two species of Brachionus (Brachionus angularis Gosse, 1851 and B. calyciflorus) when the adult females were exposed to a kairomone produced by A. brightwellii (Gosse, 1850).
Another method of avoiding predation is by increasing size. In the colonial rotifer, Conochilus hippocrepis (Schrank, 1803), overall colony size is important in deterring predation by the copepod Parabroteas sarsi (Daday, 1901), which can consume entire small colonies (Diéguez & Balseiro, 1998). Larger colonies of the sessile rotifer Sinantherina socialis (Linnaeus, 1758) are also better at avoiding the predatory snail Physa sp. and the amphipod Hyallela azteca (Saussure, 1858) than are solitary animals (Garcia, 2004). On the other hand, the larger size achieved by coloniality should increase the risk of predation (Wallace et al., 2015). Species in the genus Sinantherina may be avoiding this size pitfall in two ways: (1) Sinantherina spinosa (Thorpe, 1893) possess short spines on their anteroventral surface that may irritate the buccal cavity of small-mouthed fishes (Wallace et al., 2015); (2) Sinantherina socialis has been shown to be unpalatable to certain small mouthed fishes and the nymphs of dragonflies and damselflies (Felix et al., 1995; Walsh et al., 2006). Rotifers also may have better survival by avoiding sympatric predators spatially or temporally: spatially by DVM (noted above); temporally by differences in seasonal growth (Feike & Heerkloss, 2009) or by initiating mixis (diapause) at low population levels (Gilbert & Diéguez, 2010).
Other mechanisms that aid in evading predation include spines located at the anterior and/or posterior end of the animal; these interfere with a predator’s ability to manipulate the prey. Permanent spines are found in species of Kellicottia (Havens, 1990), Keratella (Stemberger, 1985; Williamson, 1987; Green, 2007; Gilbert, 2009; Zhang et al., 2017), and Plationus (Sarma et al., 2011). Some genera possess species with spines that are induced embryologically when a specific predator’s kairomone is present at sufficient levels. This phenomenon is seen in certain species of Brachionus (Gilbert, 2017, 2018), Keratella (Garza-Mouriño et al., 2005; Gilbert, 2011), Lecane (Soto & Sarma, 2009), and perhaps Notommata (Koste 1981). In a similar fashion male Asplanchna sieboldii (Leydig, 1854) are protected from cannibalistic females by development of lateral, body wall outgrowths induced by their diet (Gilbert, 1977).
While much is known about consumption of rotifers by predaceous zooplankters and other aquatic invertebrates and how they can reduce predation risk (Table 1), comparatively little is known about the role of protists as predators on rotifers or the factors that influence their prey selectivity. Actinophryid heliozoans are common passive predators of microorganisms, including rotifers, in freshwater systems (Mikrjukov & Patterson, 2001; Weithoff & Bell, 2022). Previous studies indicate that heliozoans can feed on varied prey having a wide range of sizes and that the consumption of their prey varies among species (Bell et al., 2006; Weithoff & Bell, 2022). For instance, Bell et al. (2006) found that although Actinophrys sol (Müller, 1773) ingested a variety of prey, they showed positive population growth only under certain diets, including those with rotifers present. Weithoff and Bell (2022) noted higher consumption of Elosa worrallii Lord, 1891 than Cephalodella sp., although the mechanism leading to increased predation risk was not clear.
Here we investigated predatory behavior of Actinosphaerium sp. on seven rotifer species to test the hypothesis that motility and prey size influence predator selection behavior. Observations of Actinosphaerium sp. (hereafter Actinosphaerium) consuming a variety of prey in field samples led to four types of laboratory experiments: (1) Feeding trials: Single prey type trials were conducted to see which of six naturally co-occurring rotifer species and one naïve species can be consumed by Actinosphaerium; (2) Preference tests: Ingestion of combinations of six prey types were compared; (3) Population growth: Actinosphaerium fed with mixed prey diets with and without A. sieboldii were monitored to determine whether presence of a predatory rotifer influenced their population growth; and (4) Prey defenses: B. calyciflorus with and without were tested to determine whether spines altered predation susceptibility.
Methods
Collection
Brachionus calyciflorus was obtained from Florida Aquafarms (http://floridaaquafarms.com/), the remaining rotifer species and the predator were collected from two sites at Hueco Tanks State Park & Historic Site, El Paso, TX, USA. The predator, Actinosphaerium, and the prey species—Asplanchna sieboldii, Platyias quadricornis (Ehrenberg, 1832), and Lacinularia flosculosa (Müller, 1773)—were collected from Laguna Prieta (GPS coordinates: 31.9247, − 106.0471), while Cephalodella gibba (Ehrenberg, 1830), Euchlanis dilatata Ehrenberg, 1830 and Lepadella patella (Müller, 1773) were isolated from Behind Ranch House playa (GPS coordinates: 31.9241, − 106.0417).
Laboratory observations
Field collected samples were placed in large Petri dishes within the first 12 h after collection and observed under a dissecting microscope every 1–2 days for approximately 2 weeks. Predatory events were documented by taking photomicrographs.
Culture techniques
Cultures of all species were maintained at room temperature, except for B. calyciflorus which was cultured at 25°C, in modified MBL media (Stemberger 1981) under a 16:8 L:D cycle. Asplanchna sieboldii was fed with B. calyciflorus and Chlamydomonas reinhardtii Dangeard, 1888 (UTEX Culture Collection for Algae at UT-Austin strain 90); while the remainder of the rotifers were fed a mixture of Chlorella vulgaris (UTEX strain 30) and C. reinhardtii. Actinosphaerium were fed with ciliates found in the original field sample and a mixture of the rotifers used as prey in this study. All Actinosphaerium sp. used in the experiments were isolated without food for 48 h prior to experimentation and ranged in maximum length from 513 to 976 μm.
Swimming speed and size
Swimming speeds were obtained from the literature (Table 2). Sizes of rotifer species used in this study (Table 2) were determined by using a SPOT© digital camera and Spot 5.6 software©, attached to a Zeiss Axioscope©. To determine the influence of swimming speed on predation risk, rotifer species were placed into three groups: sessile (~ 0 mm/s), slow (< 400 mm/s) and fast (≥ 400 mm/s). To see effect of prey size on the number of captures by Actinosphaerium, prey items were grouped into two sizes categories based on their maximum length (excluding foot, toes, and spines): small (< 175 µm) and large (≥ 175 µm). Shapiro–Wilk test, ANOVA, and a Tukey post-hoc test were conducted for both swimming speed and size.
Feeding trials
Except for L. flosculosa, experimental treatments consisted of 20 prey items of a single species offered to an Actinosphaerium for 40 min. Experiments were conducted in ambient light at 25°C in 1 ml of MBL using 24-well plates with 4 replicates per treatment. Due to the difficulty of separating the colonies without harming the individual animals, treatments for L. flosculosa consisted of single colonies comprised of 10–21 animals (n = 10). ANOVA and a Tukey post-hoc test were done to compare captures by the predator.
Preference tests
All prey rotifer species were used in the choice trials except for L. flosculosa since it was not consumed in the single species feeding trials. Five rotifers of each species were simultaneously offered to a single predator under the same conditions as the feeding trials and observed for 40 min. Each treatment was replicated four times. Ivlev’s electivity index (1) was calculated to determine predator preferences among the prey items (Jacobs, 1974).
where E is the electivity index, r is the fraction food type eaten, and p is the fraction of the food type available in the experiment. Additionally, a Chi-Squared and Fisher’s exact test were conducted to analyze capture frequencies of the prey in preference trials.
Population growth
Following the preference test, treatments were incubated at 25°C with 16:8 L:D cycle. Actinosphaerium were counted at 24, 48 and 72 h. Treatments consisted of two mixed diets offered to a single Actinosphaerium at a single time: (1) 5 rotifers of each species except L. flosculosa and A. sieboldii and (2) 5 rotifers of each species including A. sieboldii. Treatments were incubated at 25°C under a 16:8 L:D cycle in modified MBL. Actinosphaerium were counted at 24, 48, and 72 h. Means of the diet treatments were compared using an unpaired T-test.
Prey defenses
Diapausing eggs from the commercial stock of B. calyciflorus were hatched and incubated in MBL at 25°C under a 16:8 L:D cycle following the manufacture’s protocol. After 72 h, cultures were separated into two containers of 1 l and place at room temperature (~ 20°C). After 2 days, approximately 200 ml of A. sieboldii culture media filtrate along with 20 A. sieboldii were added to one of the cultures to induce spine formation in B. calyciflorus. Later, a single species feeding trial was carried out as described above for the prey consisting of B. calyciflorus with and without spines. Finally, a preference test was conducted as described above except that prey consisted of 10 spined and 10 un-spined B. calyciflorus per treatment (n = 4). Means of the two prey groups were compared using an unpaired T-test.
Analyses
All statistical analyses were done using RStudio version 4.1.3 (R_Core_Team, 2022).
Results
Observations
In field samples that were transferred into large Petri dishes to facilitate observation, Actinosphaerium were observed to consume diverse prey such as midge larvae, sessile colonial ciliates, and several rotifer species including the sessile colonial species L. flosculosa (Fig. 1).
Swimming speed and size
In single-prey trials, predation risk varied among the three motility categories (ANOVA, F = 5.9, P = 0.007) with increased risk for motile prey (fast and slow) as compared to sessile prey (Tukey’s multiple comparison, P < 0.05). However, there was no significant difference in risk between the two motile categories (slow and fast) (Fig. 2). No L. flosculosa (sessile) were consume even after 72 h of exposure to Actinosphaerium. These results show that although the ability to move is a risk factor for rotifers, speed is not. Additionally, in single-prey trials, larger prey were captured twice as often as small prey (ANOVA, F = 11.4, P = 0.002) (Fig. 3).
Feeding trials
The naïve prey B. calyciflorus was the most consumed prey (ANOVA, F = 24.7, P < 0.001, Tukey, P < 0.05), while Lacinularia flosculosa was not consumed at all (Fig. 4). In fact, 95% of Actinosphaerium produced cysts (#/individual, mean ± SD: 9.6 ± 3.5) in the Lacinularia treatment, which is a known response to starvation in heliozoans (Smith, 1903; Bell et al., 2006). For the rest of the prey, although the consumption rate was variable, it was not statistically significant. Of prey consumed, B. calyciflorus was ingested from 15.2 to 56.5% more frequently than the other prey species. Under our experimental conditions, naïve preys are more susceptible to predation by Actinosphaerium than naturally co-occurring prey species.
Preference tests
Statistical analysis was done by the size-grouping categories previously described. Large and small prey were captured at significantly different frequencies (χ2 = 8.4, P = 0.004); larger prey species were captured 13 times more frequently than small species (Fisher’s Exact test, Odds Ratio = 13.0, P = 0.004). Consistent with the feeding trials, these preference test results show that size influences Actinosphaerium prey selection. Ivlev’s electivity index showed A. sieboldii (0.33) and B. calyciflorus (0.33) as favored prey items. Low or negative values were found for C. gibba (0.20), P. quadricornis (− 0.33), E. dilatata (− 1.00), and L. patella (− 1.00) (Fig. 5). Values in brackets are approximate mean lengths (µm).
Population growth
The population growth of Actinosphaerium on mixed prey diets with and without A. sieboldii showed that highest population growth occurred in the presence of A. sieboldii. Population growth was higher when the protist was fed with A. sieboldii than without at each time point (T-test, t = 6.1 (24 h), 6.6 (48 h), and 6.8 (72 h), all P ≤ 0.05) (Fig. 6). After 3 days, no rotifers remained in any of the treatments.
Prey defenses
There was no significance difference in the frequency of capture of B. calyciflorus individuals with and without spines (χ2 = 0.48, P = 0.488), that is, although the capture of spined specimens was 1.5 times higher than that of specimens without spines, the differences were not statistically significant (Fisher’s Exact Test, Odds Ratio = 1.5, P = 0.488). This indicates that the spines are not efficient defenses for this predator.
Discussion
Our research demonstrates that the freshwater heliozoan Actinosphaerium is an effective predator on many rotifer species with which it co-occurs in temporary desert playas. In field observations, Actinosphaerium with partially ingested and digested rotifers were observed frequently during the summer growing season. In samples from field collections, we observed large numbers of the sessile rotifer L. flosculosa being consumed by the heliozoan and we saw the resting eggs of this species within the heliozoans. However, in laboratory feeding trials, no L. flosculosa were ingested; this may be an artifact of our experimental protocol. In the field, heliozoans may come into contact with sessile colonies due to wind, animal, or other natural disturbances that mix the water column producing currents. However, in laboratory conditions we found that predation risk was greater for motile prey. As noted above, with sessile prey the predator often produced cysts as a survival strategy. Although swimming speed was not correlated with increased predation (see next), this result was likely due to increased probably of predator–prey interactions.
Swimming speed and size
Two factors that determine prey vulnerability are their motility and size. Examples illustrating the importance of these factors include the following. Jara and Perotti (2010) reported a reduction of activity in three species of anuran tadpoles in response to presence of aquatic insect predators; they also noted a relationship between prey size and predation susceptibility. In their study of oyster-eating snails, Pusack et al. (2018) reported that predatory drills prefer to eat medium-sized oysters (50–75 mm). Sarma and Nandini (2007) found that rotifer size affects vulnerability to predation in rotifer-rotifer interactions, while (Parry et al., 2022) observed swimming speed changes of spineless B. calyciflorus in the presence of A. brightwellii. Similarly, Santos-Medrano et al. (2017) found that rotifer and non-rotifer prey selection by A. brightwellii is influenced by the size, biomass, and swimming speed of their prey. These predators are all active in seeking their prey. Heliozoans are passive predators so we assumed that increased prey swimming speeds and/or specific swimming behaviors would lead to increased encounters between heliozoans and their prey. However, in our study we found no significant differences in consumption rate for rotifers with swimming speed ranging from 0.98 to 0.17 mm s−1.
Predation trials and preference tests
In single prey exposure trials, we expected a higher consumption of small prey since they comprise lower biomasses than larger prey. However, we found that larger prey items were captured more often in both single and multiple-prey exposure trials. It is possible that Actinosphaerium did not reached its feeding saturation point, even with a prey density of 20 individuals ml−1, and that large prey were easier to capture due to the larger surface area that can come into contact with the axopods. Aside from the B. calyciflorus population used in this study, which rarely co-occurs with the predator in our collection site, Asplanchna sieboldii was the preferred prey. That preference could be important because predation on Asplanchna may potentially have an indirect control of herbivores in an ecosystem (Snyder & Wise, 2001). That is, predilection of Actinosphaerium for A. sieboldii might cause a trophic cascade: reduction in the population of Asplanchna would release its control of herbivorous rotifers, which would then lead to a reduction in the algae population. On the other hand, given that sexuality and cannibalism induction in Asplanchna can be affected by diet and population density (Gilbert & Thompson, 1968; Gilbert & Litton, 1978; Gilbert, 2017), another possibility is that this type of intraguild predation has the opposite effect: it could keep the Asplanchna population stable and thereby controlling the population levels of grazing rotifers. This has been seen in other studies where intraguild predation allows Asplanchna populations to persist (Gilbert & Confer, 1986; Gilbert, 2017). In either case, predation on Asplanchna would influence algae populations, which would then have implications for community structure, as well as water clarity and oxygenation (Järvenpää & Lindström, 2004; Morgan et al., 2006). For instance, Weithoff and Bell (2022) showed that interactions between heliozoan predators and rotifer/ciliate prey had different outcomes on community structure as algal concentrations varied.
Population growth
We also found that heliozoan growth was greatest when the predatory rotifer Asplanchna was present. These results show that the predation strategy of Actinosphaerium follows the principles of Optimal Foraging Theory, which states: (1) that the energetic profitability of the prey determines the selectivity of the predator and (2) the contribution of an individual to the next generation depends on its foraging strategy (MacArthur & Pianka, 1966; Pyke, 1984; Kumar et al., 2022). This is consistent for two reasons. (1) Assuming a larger prey size tends to a higher biomass, the passive predation of Actinosphaerium selecting large and mobile prey implies a higher biomass consumption with minimum energy expenditure. (2) Results of the population growth experiment showed that heliozoans fed Asplanchna produced more offspring.
The greater population growth of the heliozoan in the presence of Asplanchna may be explained by a greater amount of biomass in the treatment. However, a reduction in the growth of Actinosphaerium would also have been expected due to competition exerted by Asplanchna. Given that the prey species used in this experiment have different biomasses, equitable distribution among the treatments represented a challenge; however, future research could control the number of rotifers per treatment, for example, by adding one extra individual per species in the treatment without Asplanchna to equalize the total number of rotifers. In this study we maintained the same number of individuals per species (except A. sieboldii) in both treatments, thus the biomass of the prey species remains controlled, making the Asplanchna effect easier to visualize, but certainly the model is not exempt from improvements.
Prey defenses
Coloniality and morphological adaptations seem to be inefficient methods used by rotifers to evade predation by heliozoans. Brachionus calyciflorus spines were not an effective defensive strategy against predation by Actinosphaerium. Likewise, previous reports (Kulmer et al., 2020) and our field observations provided evidence of the consumption of colonial protozoans and rotifers. In addition, Chin et al. (2022) found that Amoeba proteus (Pallas, 1766) was able to consume colonial choanoflagellates more efficiently than single individuals by changing its behavior. On the other hand, the method by which heliozoans capture prey seems to be largely mediated by chemicals (Sakaguchi et al., 2001). Thus, defense strategies could be chemical rather than morphological. Actynophrids possess at least two types of extrusomes (Mikrjukov & Patterson, 2001) that secrete glycoprotein-binding substances involved in chemical prey recognition (Sakaguchi et al., 2001; Bhadra et al., 2017) and immobilization (Esteban & Fenchel, 2020). Furthermore, glycoprotein classes of pheromones on the surface of rotifers varies among species (Snell & Morris, 1993; Snell et al., 1995; Snell & Rico-Martinez, 1996; Jezkova et al., 2022), which could modify predation susceptibility as has been reported in other predator–prey interactions (White et al., 2022). For these reasons, chemical defense mechanisms should be a topic for future research.
Predation pressure favors the appearance of defensive strategies (Gilbert, 1980a; Riessen & Gilbert, 2018; Alvarado-Flores et al., 2022). Both intraguild and generalist predation can dampen trophic cascades (Snyder & Wise, 2001). The top-down regulation of the predator to its prey is stronger in specialist predators than in generalists (Lou & Nie, 2022), although the effect of generalists is more marked when they inhabit a low-diversity community (Strong, 1992; Snyder & Wise, 2001). Therefore, although the susceptibility of rotifer prey was different in this study, given that Actinosphaerium sp. is a generalist predator, perhaps the predation pressure exerted is not strong enough to induce the evolution of defense mechanisms in its prey.
Conclusions
Rotifers fall prey to a variety of predators, and because of their small size they are components in both the classic food web and the microbial loop (Wallace et al., 2015). Yet they are not without their defenses, which include (1) small size, (2) escape movements, both slow (small increases in swimming speed), swift ones (jumps), and diel migrations, (3) physical foils, and (4) unpalatability (Wallace et al., 2006, 2015). However, many rotifers appear to have no defense against being engulfed whole by (1) protists (Wallace et al., 2015), (2) Cnidaria (Hydra) (Walsh, 1995), (3) micrometazoans (i.e., rotifers (Gilbert, 1980b) and copepods (Green & Shiel, 1992)), (4) insects (Walsh, 1995; Hampton & Gilbert, 2001), and (5) vertebrates (Lair et al., 1996; Snell et al., 2018). Of these predators, we know relatively little about the dynamics of interactions with protists. Here we have shown that there are two important risk factors for predation by Actinosphaerium: (1) prey size and (2) prey movement in relationship to the predator. Movement could be either by the prey’s own movement or that initiated by water currents. Another factor that might influence prey susceptibility include habitat complexity such as that found in the littoral zone (Walsh, 1995; Meksuwan et al., 2014). Most studies to date have focused on planktonic predator–prey interactions or laboratory studies in the absence of vegetation. Actinosphaerium fed efficiently on colonies in glass dishes containing plants with abundant L. flosculosa colonies.
Our observations indicate that Actinosphaerium can consume a varied diet, with its prey including insect larvae, ciliates, and rotifers, but prefer larger, mobile prey (> 175 µm). These results are consistent with Optimal Foraging Theory, which makes heliozoan/rotifer predator–prey interactions a suitable model for future research on intraguild predation and Optimal Foraging Theory. However, some limitations of this research should be considered. For example, the volume of the experimental vessel and the static experimental conditions are very different from natural settings. Both factors may have contributed to the discrepancy between predation on L. flosculosa in field samples and in our experiments. Finally, if we are to understand the importance of actynophryds within the microbial loop in aquatic systems and their influence of community structure, additional research is needed on a wider variety of prey types.
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
Code availability
Not applicable.
References
Almeda, R., H. van Someren Gréve & T. Kiørboe, 2017. Behavior is a major determinant of predation risk in zooplankton. Ecosphere 8(2): e01668. https://doi.org/10.1002/ecs2.1668.
Alvarado-Flores, J., M. A. Arzate-Cárdenas, D. Pérez-Yañez & E. Cejudo, 2022. Environmental stressor induces morphological alterations in zooplankton. Latin American Journal of Aquatic Research 50(1): 1–12. https://doi.org/10.3856/vol50-issue1-fulltext-2774.
Balsamo, M., T. Artois, J. P. Smith, M. A. Todaro, L. Guidi, B. S. Leander & N. W. Van Steenkiste, 2020. The curious and neglected soft-bodied meiofauna: Rouphozoa (Gastrotricha and Platyhelminthes). Hydrobiologia 847(12): 2613–2644. https://doi.org/10.1007/s10750-020-04287-x.
Bell, E. M., G. Weithoff & U. Gaedke, 2006. Temporal dynamics and growth of Actinophrys sol (Sarcodina: Heliozoa), the top predator in an extremely acidic lake. Freshwater Biology 51: 1149–1161. https://doi.org/10.1111/j.1365-2427.2006.01561.x.
Bhadra, M., M. Kobayashi, R. Higuchi, L. Chen & T. Suzaki, 2017. Major vault protein of the protozoan Raphidiophrys contractilis has a binding property to β-1,3-glucan and is involved in food capturing. International Journal of New Technology and Research 3(7): 1–7.
Buonanno, F., T. Harumoto & C. Ortenzi, 2013. The defensive function of trichocysts in Paramecium tetraurelia against metazoan predators compared with the chemical defense of two species of toxin-containing ciliates. Zoological Science 30(4): 255–261. https://doi.org/10.2108/zsj.30.255.
Buonanno, F., A. Anesi, G. Di Giuseppe, G. Guella & C. Ortenzi, 2017. Chemical defense by erythrolactones in the euryhaline ciliated protist, Pseudokeronopsis erythrina. Zoological Science 34(1): 42–51. https://doi.org/10.2108/zs160123.
Buonanno, F., E. Catalani, D. Cervia, C. Cimarelli, E. Marcantoni & C. Ortenzi, 2020. Natural function and structural modification of climacostol, a ciliate secondary metabolite. Microorganisms 8(6): 809. https://doi.org/10.3390/microorganisms8060809.
Buskey, E. J., J. R. Strickler, C. J. Bradley, D. K. Hartline & P. H. Lenz, 2017. Escapes in copepods: comparison between myelinate and amyelinate species. Journal of Experimental Biology 220(5): 754–758. https://doi.org/10.1242/jeb.148304.
Chin, N. E., T. C. Wu, J. M. O’Toole, K. Xu, T. Hata & M. A. R. Koehl, 2022. Formation of multicellular colonies by choanoflagellates increases susceptibility to capture by amoeboid predators. Journal of Eukaryotic Microbiology. https://doi.org/10.1111/jeu.1296.
Diéguez, M. & E. Balseiro, 1998. Colony size in Conochilus hippocrepis: defensive adaptation to predator size. Hydrobiologia 387(388): 421–425. https://doi.org/10.1023/A:1017042610913.
Esteban, G. F. & T. M. Fenchel, 2020. Feeding. In Esteban, G. F. & T. M. Fenchel (eds), Ecology of Protozoa. Springer, Cham, Switzerland: 33–54.
Feike, M. & R. Heerkloss, 2009. Does Eurytemora affinis (Copepoda) control the population growth of Keratella cochlearis (Rotifera) in the brackish water Darß-Zingst Lagoon (southern Baltic Sea)? Journal of Plankton Research 31(5): 571–576. https://doi.org/10.1093/plankt/fbp004.
Felix, A., M. E. Stevens & R. L. Wallace, 1995. Unpalatability of a colonial rotifer, Sinantherina socialis, to small zooplanktivorous fishes. Invertebrate Biology 114: 139–144. https://doi.org/10.2307/3226885.
Garcia, M. A., 2004. The asexual life history of the colonial rotifer, Sinantherina socialis (Linnaeus). Department of Biology and Evolutionary Biology. Doctoral Dissertation, Yale University, New Haven: 129.
Garza-Mouriño, G., M. Silva-Briano, S. Nandini, S. S. S. Sarma & M. E. Castellanos-Páez, 2005. Morphological and morphometric variations of selected rotifer species in response to predation: a seasonal study of selected brachionid species ftom Lake Xochimilco (Mexico). Hydrobiologia 546: 169–179. https://doi.org/10.1007/s10750-005-4114-5.
Gilbert, J. J., 1966. Rotifer ecology and embryological induction. Science 151: 1234–1237. https://doi.org/10.1126/science.151.3715.123.
Gilbert, J. J., 1967. Asplanchna and postero-lateral spine production in Brachionus calyciflorus. Archiv Für Hydrobiologie 64(1): 1–62.
Gilbert, J. J., 1977. Defenses of males against cannibalism in the rotifer Asplanchna: size, shape, and failure to elicit tactile feeding response. Ecology 58(5): 1128–1135. https://doi.org/10.2307/1936933.
Gilbert, J. J., 1980a. Further observations on developmental polymorphism and its evolution in the rotifer Brachionus calyciflorus. Freshwater Biology 10(3): 281–294. https://doi.org/10.1111/j.1365-2427.1980.tb01202.x.
Gilbert, J. J., 1980b. Observations on the susceptibility of some protists and rotifers to predation by Asplanchna girodi. Hydrobiologia 73: 87–91. https://doi.org/10.1007/978-94-009-9209-2_17.
Gilbert, J. J., 1985. Escape response of the rotifer Polyarthra: a high-speed cinematographic analysis. Oecologia 66: 322–331. https://doi.org/10.1007/BF00378293.
Gilbert, J. J., 2009. Predator-specific inducible defenses in the rotifer Keratella tropica. Freshwater Biology 54: 1933–1946. https://doi.org/10.1111/j.1365-2427.2009.02246.x.
Gilbert, J. J., 2011. Induction of different defences by two enemies in the rotifer Keratella tropica: response priority and sensitivity to enemy density. Freshwater Biology 56(5): 926–938. https://doi.org/10.1111/j.1365-2427.2010.02538.x.
Gilbert, J. J., 2017. Spine development in two taxa of Brachionus calyciflorus from Lake Littra, Australia: constitutive and induced defenses against Asplanchna. Journal of Plankton Research 39(6): 962–971. https://doi.org/10.1093/plankt/fbx048.
Gilbert, J. J., 2018. Morphological variation and its significance in a polymorphic rotifer: environmental, endogenous, and genetic controls. BioScience 68(3): 169–181. https://doi.org/10.1093/biosci/bix162.
Gilbert, J. J., 2019. Attachment behavior in the rotifer Brachionus rubens: induction by Asplanchna and effect on sexual reproduction. Hydrobiologia 844: 9–20. https://doi.org/10.1007/s10750-018-3805-7.
Gilbert, J. J. & C. W. Burns, 2000. Day and night vertical distributions of Conochilus and other zooplankton in a New Zealand reservior. Verhandlungen Internationale Vereinigung Limnologie 27: 1909–1914.
Gilbert, J. J. & J. L. Confer, 1986. Gigantism and the potential for interference competition in the rotifer genus Asplanchna. Oecologia 70(4): 549–554. https://doi.org/10.1007/BF00379902.
Gilbert, J. J. & M. C. Diéguez, 2010. Low crowding threshold for induction of sexual reproduction and diapause in a Patagonian rotifer. Freshwater Biology 55: 1705–1718. https://doi.org/10.1111/j.1365-2427.2010.02405.x.
Gilbert, J. J. & K. L. Kirk, 1988. Escape response of the rotifer Keratella: description, stimulation, fluid dynamics, and ecological significance. Limnology and Oceanography 33(6): 1440–1450. https://doi.org/10.4319/lo.1988.33.6part2.1440.
Gilbert, J. J. & J. R. Litton, 1978. Sexual reproduction in the rotifer Asplanchna girodi: effects of tocopherol and population density. Journal of Experimental Zoology 204(1): 113–121. https://doi.org/10.1002/jez.1402040110.
Gilbert, J. J. & R. W. Stemberger, 1984. Asplanchna-induced polymorphism in the rotifer Keratella slacki. Limnology and Oceanography 29(6): 1309–1316. https://doi.org/10.4319/lo.1984.29.6.1309.
Gilbert, J. J. & G. A. Thompson Jr., 1968. Alpha tocopherol control of sexuality and polymorphism in the rotifer Asplanchna. Science 159: 734–736. https://doi.org/10.1126/science.159.3816.734.
Green, J., 2007. Morphological variation of Keratella cochlearis (Gosse) in Myanmar (Burma) in relation to zooplankton community structure. Hydrobiologia 593(1): 5–12. https://doi.org/10.1007/s10750-007-9072-7.
Green, J. D. & R. J. Shiel, 1992. A dissection method for determining the gut contents of calanoid copepods. Transactions of the Royal Society of South Australia 116(4): 129–132.
Gunter, D. D. & L. A. Knight Jr., 1978. Observations of the rotifer Sinantherina semibullata (Thorpe) from Ross Barnett reservoir. Mississippi. Egyptian Journal of Microbiology 13(12): 99–106.
Hampton, S. E. & J. J. Gilbert, 2001. Observations of insect predation on rotifers. Hydrobiologia 446(447): 115–121. https://doi.org/10.1023/A:1017543121353.
Hampton, S. E., J. J. Gilbert & C. W. Burns, 2000. Direct and indirect effects of juvenile Buenoa macrotibialis (Hemiptera: Notonectidae) on the zooplankton of a shallow pond. Limnology and Oceanography 45(4): 1006–1012. https://doi.org/10.4319/lo.2000.45.4.1006.
Havens, K. E., 1990. Chaoborus predation and zooplankton community structure in a rotifer-dominated lake. Hydrobiologia 198(1): 215–226. https://doi.org/10.1007/BF00048636.
Hershey, A. E. & S. I. Dodson, 1987. Predator avoidance by Cricotopus: cyclomorphosis and the importance of being big and hairy. Ecology 68(4): 913–920. https://doi.org/10.2307/1938362.
Herzog, Q., C. Tittgen & C. Laforsch, 2016. Predator-specific reversibility of morphological defenses in Daphnia barbata. Journal of Plankton Research 38(4): 771–780. https://doi.org/10.1093/plankt/fbw045.
Hochberg, R. & A. Ablak Gurbuz, 2007. Functional morphology of somatic muscles and anterolateral setae in Filinia novaezealandiae Shiel and Sanoamuang, 1993 (Rotifera). Zoologischer Anzeiger 246: 11–22. https://doi.org/10.1016/j.jcz.2006.10.002.
Hochberg, R., A. Hochberg & C. Chan, 2015. Ultrastructure of the rotifer integument: peculiarities of Sinantherina socialis (Monogononta: Gnesiotrocha). Invertebrate Biology 134(3): 181–188. https://doi.org/10.1111/ivb.12085.
Jacobs, J., 1974. Quantitative measurement of food selection. Oecologia 14(4): 413–417. https://doi.org/10.1007/BF00384581.
Jara, F. G. & M. G. Perotti, 2010. Risk of predation and behavioural response in three anuran species: influence of tadpole size and predator type. Hydrobiologia 644(1): 313–324. https://doi.org/10.1007/s10750-010-0196-9.
Järvenpää, M. & K. Lindström, 2004. Water turbidity by algal blooms causes mating system breakdown in a shallow-water fish, the sand goby Pomatoschistus minutus. Proceedings of the Royal Society of London Series b: Biological Sciences 271: 2361–2365. https://doi.org/10.1098/rspb.2004.2870.
Jezkova, I., R. Ortells, J. Montero-Pau & M. Serra, 2022. Insight into incipient reproductive isolation in diverging populations of Brachionus plicatilis rotifer. Hydrobiologia 849(15): 3299–3311. https://doi.org/10.1007/s10750-022-04927-4.
Kerfoot, W. C., 1982. A question of taste: crypsis and warning coloration in freshwater zooplankton communities. Ecology 63(2): 538–554. https://doi.org/10.2307/1938969.
Kerfoot, W. C., D. L. J. Kellogg & J. R. Strickler, 1980. Visual observations of live zooplankters: evasion, escape, and chemical defenses. In Kerfoot, W. C. (ed.), Evolution and Ecology of Zooplankton Communities. The University Press of New England, Hanover: 10–27.
Kossova, A. A., 1979. Contraction of Sinantherina semibullata (Monimotrochida, Flosculariidae) as a defense reaction against eating out. Zoologichekii Zhurnal 58(11): 1728–1729 (in Russian, with English summary).
Koste, W., 1981. Zur Morphologie, Systematik und Ökologie von neuen monogononten Rädertieren (Rotatoria) aus dem Überschwemmungsgebiet des Magela Creek in der Alligator-River-Region Australiens, N.T. Teil 1. Osnabrücker Naturwissenschaftliche Mitteilungen 8: 97–126.
Kulmer, W. E., J. Jorge, P. M. Kim, N. Iftekhar & M. A. R. Koehl, 2020. Does formation of multicellular colonies by choanoflagellates affect their susceptibility to capture by passive protozoan predators? Journal of Eukaryotic Microbiology 67(5): 555–565. https://doi.org/10.1111/jeu.12808.
Kumar, R., S. Kumari, A. Malika, A. P. Sharma & H. U. Dahms, 2022. Protistan epibionts affect prey selectivity patterns and vulnerability to predation in a cyclopoid copepod. Scientific Reports 12(1): 22631. https://doi.org/10.1038/s41598-022-26004-5.
Lair, N., H. Taleb & P. Reyes-Marchant, 1996. Horizontal distribution of the rotifer plankton of Lake Aydat (France). Aquatic Sciences 58(3): 253–268. https://doi.org/10.1007/BF00877512.
Li, Y., R. Wang, H. Su, J. Wang, P. Xie & F. Chen, 2022. Eutrophication and predation mediate zooplankton diversity and network structure. Limnology and Oceanography 67: S133–S145. https://doi.org/10.1002/lno.11957.
Lou, Y. & H. Nie, 2022. Global dynamics of a generalist predator–prey model in open advective environments. Journal of Mathematical Biology 84(6): 46. https://doi.org/10.1007/s00285-022-01756-w.
Lynch, M., 1979. Predation, competition, and zooplankton community structure: an experimental study. Limnology and Oceanography 24(2): 253–272. https://doi.org/10.4319/lo.1979.24.2.0253.
MacArthur, R. H. & E. R. Pianka, 1966. On optimal use of a patchy environment. The American Naturalist 100(916): 603–609. https://doi.org/10.1086/282454.
Meksuwan, P., P. Pholpunthin, E. J. Walsh, H. Segers & R. L. Wallace, 2014. Nestedness in sessile and periphytic rotifer communities: a meta-analysis. International Review of Hydrobiology 99(1–2): 48–57. https://doi.org/10.1002/iroh.201301703.
Mikrjukov, K. A. & D. J. Patterson, 2001. Taxonomy and phylogeny of Heliozoa. III. Actinophryids. Acta Protozoologica 40: 3–25.
Moore, M. V. & J. J. Gilbert, 1987. Age-specific Chaoborus predation on rotifer prey. Freshwater Biology 17(2): 223–236. https://doi.org/10.1111/j.1365-2427.1987.tb01044.x.
Morgan, A. M., T. V. Royer, M. B. David & L. E. Gentry, 2006. Relationships among nutrients, chlorophyll- a, and dissolved oxygen in agricultural streams in Illinois. Journal of Environmental Quality 35(4): 1110–1117. https://doi.org/10.2134/jeq2005.0433.
Obertegger, U., A. Cieplinski, M. Raatz & P. Colangeli, 2018. Switching between swimming states in rotifers—case study Keratella cochlearis. Marine and Freshwater Behaviour and Physiology 51(3): 159–173. https://doi.org/10.1080/10236244.2018.1503541.
Parry, V., U. E. Schlägel, R. Tiedemann & G. Weithoff, 2022. Behavioural responses of defended and undefended prey to their predator—A case study of Rotifera. Biology 11(8): 1217. https://doi.org/10.3390/biology11081217.
Parysek, M. & B. Pietrzak, 2020. Weak swimming response of a bdelloid rotifer to chemical cues of a native copepod predator. Journal of Ethology 39(1): 135–139. https://doi.org/10.1007/s10164-020-00676-w.
Pourriot, R., 1974. Relations prédature-poie chex les rotifères: influence du prédature (Asplanchna brightwelli) sur la morphologie de la proie (Brachionus bidentata). Annales D’hydrobiologie 5(1): 43–55.
Pusack, T. J., J. W. White, H. G. Tillotson, D. L. Kimbro & C. D. Stallings, 2018. Size-dependent predation and intraspecific inhibition of an estuarine snail feeding on oysters. Journal of Experimental Marine Biology and Ecology 501: 74–82. https://doi.org/10.1016/j.jembe.2018.01.005.
Pyke, G. H., 1984. Optimal Foraging Theory: a critical review. Annual Review of Ecology and Systematics 15: 523–575. https://doi.org/10.1146/annurev.es.15.110184.002515.
R_Core_Team, 2022. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
Rico-Martinez, R. & T. W. Snell, 1997. Mating behavior in eight rotifer species: using cross-mating tests to study species boundaries. Hydrobiologia 356: 165–173. https://doi.org/10.1023/A:1003194216467.
Riessen, H. P. & J. J. Gilbert, 2018. Divergent developmental patterns of induced morphological defenses in rotifers and Daphnia: ecological and evolutionary context. Limnology and Oceanography. https://doi.org/10.1002/lno.11058.
Sakaguchi, M., H. Murakami & T. Suzaki, 2001. Involvement of a 40-kDa glycoprotein in food recognition, prey capture, and induction of phagocytosis in the protozoan Actinophrys sol. Protist 152(1): 33–41. https://doi.org/10.1078/1434-4610-00041.
Salt, G. W., 1987. The components of feeding behavior in rotifers. Hydrobiologia 147(1): 271–281. https://doi.org/10.1007/BF00025754.
Santos-Medrano, G. E., R. Rico-Martinez & C. A. Velásquez-Rojas, 2001. Swimming speed and Reynolds numbers of eleven freshwater rotifer species. Hydrobiologia 446(447): 35–38. https://doi.org/10.1023/A:1017512820019.
Santos-Medrano, G. E., D. Robles-Vargas, S. Hernández-Flores & R. Rico-Martínez, 2017. Life table demography of Asplanchna brightwellii Gosse, 1850 fed with five different prey items. Hydrobiologia 796(1): 169–179. https://doi.org/10.1007/s10750-016-3069-z.
Sarma, S. S. S. & S. Nandini, 2007. Small prey size offers immunity to predation: a case study on two species of Asplanchna and three brachionid prey (Rotifera). Hydrobiologia 593: 67–76. https://doi.org/10.1007/s10750-007-9069-2.
Sarma, S. S. S., R. A. Lara Resendiz & S. Nandini, 2011. Morphometric and demographic responses of brachionid prey (Brachionus calyciflorus Pallas and Plationus macracanthus (Daday) in the presence of different densities of the predator Asplanchna brightwellii (Rotifera: Asplanchnidae). Hydrobiologia 622: 179–187. https://doi.org/10.1007/s10750-010-0494-2.
Smith, G., 1903. Actinosphaerium eichorni: a biometrical study in the mass relations of nucleus and cytoplasm. Biometrika 2(3): 241–254. https://doi.org/10.2307/2331600.
Snell, T. W. & P. D. Morris, 1993. Sexual communication in copepods and rotifers. Hydrobiologia 255(256): 109–116. https://doi.org/10.1007/BF00025828.
Snell, T. W. & R. Rico-Martinez, 1996. Characteristics of the mate-recognition pheromone in Brachionus plicatilis (Rotifera). Marine and Freshwater Behaviour and Physiology 27(2–3): 143–151. https://doi.org/10.1080/10236249609378960.
Snell, T. W., R. Rico-Martinez, L. N. Kelly & T. E. Battle, 1995. Identification of a sex pheromone from a rotifer. Marine Biology 123: 347–353. https://doi.org/10.1007/BF00353626.
Snell, T. W., R. K. Johnston & A. B. Matthews, 2018. Utilizing Brachionus biodiversity in marine finfish larviculture. Hydrobiologia 844(1): 149–162. https://doi.org/10.1007/s10750-018-3776-8.
Snyder, W. E. & D. H. Wise, 2001. Contrasting trophic cascades generated by a community of generalist predators. Ecology 82(6): 1571–1583. https://doi.org/10.1890/0012-9658(2001)082[1571:CTCGBA]2.0.CO;2.
Soto, C. S. & S. S. S. Sarma, 2009. Morphological changes in Lecane stokesii (Pell, 1890) (Rotifera: Lecanidae) induced by allelochemicals from the predator Asplanchopus multiceps (Schrank, 1793). Allelopthy Journal 23(2): 215–222.
Stemberger, R. S., 1981. A general approach to the culture of planktonic rotifers. Canadian Journal of Fisheries and Aquatic Sciences 38: 721–724. https://doi.org/10.1139/cjfas-2015-0076.
Stemberger, R. S., 1985. Prey selection by the copepod Diacyclops thomasi. Oecologia 65(4): 492–497. https://doi.org/10.1007/BF00379662.
Stemberger, R. S. & J. J. Gilbert, 1984. Spine development in the rotifer Keratella cochlearis: induction by cyclopoid copepods and Asplanchna. Freshwater Biology 14: 639–647. https://doi.org/10.1111/j.1365-2427.1984.tb00183.x.
Stemberger, R. S. & J. J. Gilbert, 1987a. Multiple-species induction of morphological defenses in the rotifer Keratella testudo. Ecology 68: 370–378. https://doi.org/10.2307/1939268.
Stemberger, R. S. & J. J. Gilbert, 1987b. Defenses of planktonic rotifers against predators. In Kerfoot, W. C. & A. Sih (eds), Predation: Direct and Indirect Impacts on Aquatic Communities. University Press of New England, Hanover: 227–239.
Stenson, J. A. E., 1982. Fish impact on rotifer community structure. Hydrobiologia 87(1): 57–64. https://doi.org/10.1007/BF00016662.
Stenson, J. A. E., 1987. Variation in capsule size of Holopedium gibberum (Zaddach): a response to invertebrate predation. Ecology 68(4): 928–934. https://doi.org/10.2307/1938364.
Strong, D. R., 1992. Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 73(3): 747–754. https://doi.org/10.2307/1940154.
Wallace, R. L., 1980. Ecology of sessile rotifers. Hydrobiologia 73: 181–193. https://doi.org/10.1007/978-94-009-9209-2_31.
Wallace, R. L., 1987. Coloniality in the phylum Rotifera. Hydrobiologia 147: 141–155. https://doi.org/10.1007/978-94-009-4059-8_20.
Wallace, R. L. & H. A. Smith, 2009. Rotifera. In Likens, G. E. (ed.), Encyclopedia of Inland Waters, Vol. 3. Elsevier, Oxford: 689–703.
Wallace, R. L., T. W. Snell, C. Ricci & T. Nogrady, 2006. Rotifera: Biology, Ecology and Systematics, 2 ed., Vol. 1. Backhuys Publishers, Leiden.
Wallace, R. L., T. W. Snell & H. A. Smith, 2015. Phylum Rotifera. In Thorp, J. H. & D. C. Rogers (eds), Thorp and Covich’s Freshwater Invertebrates, Ecology and General Biology. Vol. I. Elsevier, Waltham: 225–271.
Walsh, E. J., 1995. Habitat-specific predation susceptibilities of a littoral rotifer to two invertebrate predators. Hydrobiologia 313(314): 205–211. https://doi.org/10.1007/BF00025952.
Walsh, E. J., M. Salazar, J. Remirez, O. Moldes & R. L. Wallace, 2006. Predation by invertebrate predators on the colonial rotifer Sinantherina socialis. Invertebrate Biology 125: 325–335. https://doi.org/10.1111/j.1744-7410.2006.00064.x.
Weithoff, G. & E. M. Bell, 2022. Complex trophic Interactions in an acidophilic microbial community. Microorganisms 10(7): 1340. https://doi.org/10.3390/microorganisms10071340.
White, T. E., T. Latty & K. D. L. Umbers, 2022. The exploitation of sexual signals by predators: a meta-analysis. Proceedings of the Royal Society B: Biological Sciences 289: 20220444. https://doi.org/10.1098/rspb.2022.0444.
Williamson, C. E., 1983. Invertebrate predation on planktonic rotifers. Hydrobiologia 104: 385–396. https://doi.org/10.1007/BF00045996.
Williamson, C. E., 1987. Predator–prey interactions between omnivorous diaptomid copepods and rotifers: the role of prey morphology and behavior. Limnology and Oceanography 32(1): 167–177. https://doi.org/10.4319/lo.1987.32.1.0167.
Williamson, C. E. & R. E. Magnien, 1982. Diel vertical migration in Mesocyclops edax: implications for predation rate estimates. Journal of Plankton Research 4(2): 329–339. https://doi.org/10.1093/plankt/4.2.329.
Yin, X., W. Jin, Y. Zhou, P. Wang & W. Zhao, 2017. Hidden defensive morphology in rotifers: benefits, costs, and fitness consequences. Scientific Reports 7(1): 4488. https://doi.org/10.1038/s41598-017-04809-z.
Zhang, H., C. Brönmark & L.-A. Hansson, 2017. Predator ontogeny affects expression of inducible defense morphology in rotifers. Ecology 98(10): 2499–2505. https://doi.org/10.1002/ecy.1957.
Zhang, H., Y. He, L. He, K. Zhao, J. García Molinos, L. A. Hansson & J. Xu, 2022. Plasticity in rotifer morphology induced by conflicting threats from multiple predators. Freshwater Biology 67(3): 498–507. https://doi.org/10.1111/fwb.13857.
Acknowledgements
We thank Patrick D. Brown and the students in the Walsh laboratory for field assistance. This project was funded in part by CONACYT 2021-000021-01EXTF-00067 (ASSA) and the National Science Foundation (DEB 2051704 (EJW) and DEB 2051710 (RLW)).
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This project was funded in part by several agencies including the National Science Foundation: DEB 2051704 (EJW); DEB 2051710 (RLW), the Ripon College SOAR program (RLW), and CONACYT 2021-000021-01EXTF-00067 (ASSA).
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Sanchez-Avila, A.S., Wallace, R.L. & Walsh, E.J. Motility and size of rotifers as risk factors for being consumed by the passive protistan predator Actinosphaerium sp.. Hydrobiologia 851, 3109–3123 (2024). https://doi.org/10.1007/s10750-023-05260-0
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DOI: https://doi.org/10.1007/s10750-023-05260-0