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Asplanchna-induced spine development in Brachionus calyciflorus. (a)-B. calyciflorus, preserved juvenile of basic morph with short spines. (b)-B. calyciflorus, preserved juvenile with long, induced spines. (c)Asplanchna brightwellii, live adult. Rotifers at the same magnification, and from laboratory cultures of clones from Lake Littra, Australia. Photographs by J. J. Gilbert. [Color figure can be viewed at wileyonlinelibrary.com]

Asplanchna-induced spine development in Brachionus calyciflorus. (a)-B. calyciflorus, preserved juvenile of basic morph with short spines. (b)-B. calyciflorus, preserved juvenile with long, induced spines. (c)Asplanchna brightwellii, live adult. Rotifers at the same magnification, and from laboratory cultures of clones from Lake Littra, Australia. Photographs by J. J. Gilbert. [Color figure can be viewed at wileyonlinelibrary.com]

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Article
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Induced morphological defenses commonly develop in some loricate rotifers as greatly increased spine development and in many species of the cladoceran genus Daphnia as an alteration in the shape and size of its head, producing helmets, crests, and neck spines. This restructuring of the shape of these animals during development, which reduces their...

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Context 1
... rotifers: the large predatory rotifer Asplanchna, cladocerans, and copepods (Table 1; Gilbert 1999Gilbert , 2017. Spine development may involve the lengthening of existing spines (anterior and posterior), the formation of new posterior spines, or both. This phenomenon is best known in the very pronounced response of B. calyciflorus to Asplanchna (Fig. 1). After exposure to the Asplanchna kairomone, this species develops very long posterolateral spines (often de novo) that articulate and can extend laterally from the body after contact with the predator, longer anterior and posteromedian spines, and a slightly larger body size. These modifications can provide a very effective ...
Context 2
... helmets are typically present at birth in those Daphnia species that develop these defenses, including D. ambigua (Hebert and Grewe 1985;Hanazato 1990Hanazato , 1991aHanazato and Ooi 1992), D. cucullata (Laforsch and Tollrian 2004c), D. galeata (Hanazato 1991b), and D. retrocurva (Brooks 1946). Daphnia then normally retain the helmet through the entire period of postembryonic development. ...
Context 3
... studies have also found that the small pointed helmet of D. ambigua is limited to the first 3-4 juvenile instars (Dodson 1989;Hanazato 1990Hanazato , 1991aHanazato and Ooi 1992), however, sometimes it is present through- out adult development (Hebert and Grewe 1985). While helmets are typically retained in adult instars, species induced by preda- tor kairomones in laboratory experiments often exhibit a pro- gressive decrease in relative helmet size (ratio of head length to body length) as the Daphnia grows larger, a pattern that has been observed in D. cucullata (Tollrian 1990;Laforsch and Tollrian 2004c), D. galeata (Hanazato 1991b), D. lumholtzi (Tollrian 1994), and D. mendotae (Bungartz and Branstrator 2003;Tanner and Branstrator 2006). In natural lake populations, on the other hand, relative helmet size often increases with Daphnia body length through postembryonic development, resulting in hel- mets that are usually greater in size than is observed in labora- tory experiments (Brooks 1946(Brooks , 1965Jacobs 1961a;Sorensen and Sterner 1992;Yurista 2000). ...

Citations

... This seasonally variable predation risk favored the evolution of inducible defenses in some species of the Daphniidae. Inducible defenses are a form of phenotypic plasticity that decreases an organism's vulnerability to specific predators (for reviews, see [4][5][6][7]). These defenses range from alterations in morphology or life-history parameters to behavior. ...
Article
Every ecosystem shows multiple levels of species interactions, which are often difficult to isolate and to classify regarding their specific nature. For most of the observed interactions, it comes down to either competition or consumption. The modes of consumption are various and defined by the nature of the consumed organism, e.g., carnivory, herbivory, as well as the extent of the consumption , e.g., grazing, parasitism. While the majority of consumers are animals, carnivorous plants can also pose a threat to arthropods. Water fleas of the family Daphniidae are keystone species in many lentic ecosystems. As most abundant filter feeders, they link the primary production to higher trophic levels. As a response to the high predatory pressures, water fleas have evolved various inducible defenses against animal predators. Here we show the first example, to our knowledge, in Ceriodaphnia dubia of such inducible defenses of an animal against a coexisting plant predator, i.e., the carnivorous bladderwort (Utricularia x neglecta Lehm, Lentibulariaceae). When the bladderwort is present, C. dubia shows changes in morphology, life history and behavior. While the morphological and behavioral adaptations improve C. dubia's survival rate in the presence of this predator, the life-history parameters likely reflect trade-offs for the defense.
... The freshwater crustacean genus Daphnia provides many well-studied examples of inducible defenses against vertebrate and/or invertebrate aquatic predators, reviewed by Riessen and Gilbert (2019) and Diel et al. (2020). For these model organisms, mechanical and chemical cues can trigger the expression of inducible defenses (Laforsch et al., 2006;Laforsch & Tollrian, 2004a). ...
Article
Full-text available
Phenotypic plasticity in defensive traits is a common response of prey organisms to variable and unpredictable predation regimes and risks. Cladocerans of the genus Daphnia are keystone species in the food web of lentic freshwater bodies and are well known for their ability to express a large variety of inducible morphological defenses in response to invertebrate and vertebrate predator kairomones. The developed defenses render the daphnids less susceptible to predation. So far, primarily large‐scale morphological defenses, like helmets, crests, and tail‐spines, have been documented. However, less is known on whether the tiny spinules, rather inconspicuous traits which cover many Daphnia’s dorsal and ventral carapace margins, respond to predator kairomones, as well. For this reason, we investigated two Daphnia species (D. magna and D. longicephala) concerning their predator kairomone‐induced changes in dorsal and ventral spinules. Since these small, inconspicuous traits may only act as a defense against predatory invertebrates, with fine‐structured catching apparatuses, and not against vertebrate predators, we exposed them to both, an invertebrate (Triops cancriformis or Notontecta maculata) and a vertebrate predator (Leucaspius delineatus). Our results show that the length of these spinules as well as spinules‐covered areas vary, likely depending on the predator the prey is exposed to. We further present first indications of a Daphnia species‐specific elongation of the spinules and an increase of the spinules‐bearing areas. Although we cannot exclude that spinescence is altered because it is developmentally connected to changes in body shape in general, our results suggest that the inducible alterations to the spinule length and spinules‐covered areas disclose another level of predator‐induced changes in two common Daphnia species. The predator‐induced changes on this level together with the large‐scale and ultrastructural defensive traits may act as the overall morphological defense, adjusted to specific predator regimes in nature. We investigated two Daphnia species (D. magna and D. longicephala) concerning their predator kairomone‐induced changes of the dorsal and ventral spinules. Since these small, inconspicuous traits may only act as a defense against predatory invertebrates, with fine‐structured catching apparatuses, and not against vertebrate predators, we exposed them to both, an invertebrate (Triops cancriformis or Notontecta maculata) and a vertebrate predator (Leucaspius delineatus). Our study discovers indications of predator‐dependent, alongside Daphnia clone‐specific, defensive increases in spinescence.
... At the same time, horn expression makes C. cornuta less vulnerable toChaoborus larvae predation (Gu et al., 2021). While, the co-expression of unique inducible defenses is influenced by development, indicating that there is a trade-off underlying the adaption to multiple predation risks (Riessen & Gilbert, 2019). Therefore, further studies are still needed to reveal how prey responses to multiple predators, especially in a complex biological and abiotic environment. ...
Preprint
Inducible defenses of prey are evolved under diverse and variable predation risks. In the co-evolution of prey and multiple predators with antagonistic selection pressures, whether inducible defense responses of prey will fall into a dilemma and its underlying mechanism are still unclear. Based on the antagonistic predation pressure from invertebrate predator Chaoborus larvae and vertebrate predator fish, we studied multi-traits and transcriptome of the freshwater crustacean Ceriodaphnia cornuta under multiple predation risks. Our results showed that Chaoborus larvae predation risks altered the expression of genes encoding cuticle protein and changed the biosynthesis of steroid hormone, cutin, suberine, and wax, promoting Ceriodaphnia to express horns and grow larger at a late development stage, whereas fish predation risks mainly triggered responses in genes encoding ribosome and pathways of unsaturated fatty acids biosynthesis, cysteine and methionine metabolism, resulting in a smaller individual size and earlier reproduction. The inducible responses on transcription and individual traits both revealed that predator unique responses are dominant and the antagonistic responses are the least. Besides, Pearson correlations between different predator unique responses are extremely weak. Furthermore, the unique individual traits triggered by different predators can be expressed simultaneously. These results indicated that Ceriodaphnia can avoid the dilemma by performing predator unique responses and diverse inducible responses are favored in the co-evolution of zooplankton and multiple predators.
... Rapid adaptation of a biological population to environmental changes via phenotypic plasticity and/or evolution can commonly occur in nature, which would in turn affect ecological processes (Agrawal 2001;Hairston et al. 2005). Laboratory experiments and field observation studies have revealed that freshwater zooplankton can adaptively change their life cycle, behavior, and morphology, when exposed to predators (reviewed in Harvell and Dodson 1999;Riessen and Gilbert 2018). However, only a few studies have examined the longterm phenotypic changes in zooplankton and their associated environmental changes for longer than one growing season (e.g., Hairston and Dillon 1990). ...
... Daphnia species can adaptively respond to predation through phenotypic plasticity and rapid evolution (e.g. Hairston et al. 1999;Cousyn et al. 2001;Stoks et al. 2016;Riessen and Gilbert 2018). D. pulex also change their body size and tail spine length as an inducible defense against their predators, Chaoborus larvae, and planktivorous fish (Dodson 1989;Riessen and Gilbert 2018;Nagano and Yoshida 2020), as well as their resource allocation to reproduction or growth depending on the predator (reviewed in Tollrian and Dodson 1999;Riessen and Gilbert 2018). ...
... Hairston et al. 1999;Cousyn et al. 2001;Stoks et al. 2016;Riessen and Gilbert 2018). D. pulex also change their body size and tail spine length as an inducible defense against their predators, Chaoborus larvae, and planktivorous fish (Dodson 1989;Riessen and Gilbert 2018;Nagano and Yoshida 2020), as well as their resource allocation to reproduction or growth depending on the predator (reviewed in Tollrian and Dodson 1999;Riessen and Gilbert 2018). ...
Article
How a population adapts to environmental changes is a central topic in ecology, but long-term changes in the phenotype of an organism have rarely been studied in aquatic systems. In this study, we examined the morphological changes in Daphnia pulex from the initial establishment stage, using paleolimnological analysis, in Lake Fukami-ike (Nagano Prefecture, Japan). We measured morphological traits of ephippia and subfossils of D. pulex and compared the results with the population dynamics assessed in an earlier study. D. pulex established a stable population in the lake in the early 2000s. The length of the ephippia significantly increased in the mid-2000s and then decreased more recently, whereas the length of the post-abdominal claw as a proxy of body size did not show significant changes. This suggests that their adult body size was larger, and the time to maturity was delayed or the shift to the dormant phase got later in the mid-2000s, although the mean body size did not change. Subfossils of Chaoborus and the historical records suggest that planktivorous fish were less abundant and Chaoborus larvae were more abundant in the mid-2000s than in more recent periods. These results suggest that D. pulex adaptively changed phenotypic traits in response to changes in the predator community in the studied lake.
... Growth of the neckteeth is thought to require exposure of Daphnia larval stages to Chaoborus kairomones (Riessen and Gilbert 2018). The neckteeth begin to form in the first larval instar and continue until the third instar. ...
... These findings agree with the behaviour of Daphnia under the natural condition of the pond Bodrio del pastore III, where in early spring there were nearly 80% of neckteethed juveniles while in late spring their frequency decreased below 40% (Rossi et al. 2014(Rossi et al. , 2015Maurone et al. 2018). Our results thus support that abiotic environmental factors are involved in the modulation of phenotypic plasticity and hence, assuming predation pressure is predictable in space and time, can be more reliable cues of predation risk than kairomones alone (Riessen and Gilbert 2018). For example, the spiny water flea Bythotrephes longimanus Leydig, 1860, responds to the increase of water temperature as a proxy for higher activity of fish in midseason by increasing spine and body length and by decreasing clutch size (Miehls et al. 2013). ...
... Here we supported that organisms respond not only to chemical cues from a predator but also to environmental factors that act as proximate cues signalling a change in the predation risk (Boeing 2006;Miehls et al. 2013;Le Blanc and Medlock 2015;Toyota et al. 2016;Fiorino and McAdam 2018;Riessen and Gilbert 2018). The fact that D. pulex produce antipredator defensive structures even in the absence of Chaoborus kairomones may explain why the frequency of the defensive morphotypes of D. pulex was not related to the density of Chaoborus larvae in the pond Bodrio del pastore III (Maurone et al. 2018). ...
Article
Daphnia pulex from a pond in Northern Italy shows four distinct defensive morphotypes, varying in the number, location and thickness of neckteeth, as the results of phenotypic plasticity. Because the frequency of the morphotypes was not related to the density of Chaoborus flavicans larvae, the main predators of D. pulex, it has been suggested that environmental factors such as long-day photoperiod, temperature or crowding might act as proximate cues for the predation risk. Here, we analysed the morphotypes of newborn D. pulex produced by mothers not exposed to chemical cues (kairomones) released by Chaoborus, but reared under environmental conditions simulating seasonal differences in predation risk. Three experimental treatments, low temperature and short-day photoperiod (16 °C 12:12 L:D), high temperature and long-day photoperiod (20 °C 14:10 L:D), and crowding under high temperature and long-day photoperiod, were compared for three clonal lineages. Almost 70% of neonates produced one or more neckteeth, but the frequencies of different morphotypes varied significantly among clones and treatments, indicating that both abiotic (temperature and photoperiod) and biotic (crowding) environmental factors affected the development of neckteeth. A characteristic S-shaped relationship between percentages of neckteethed and total juveniles per female further suggests an antipredator adaptation to high prey density. Our findings support that environmental conditions serve as proximate cues of predation risk in D. pulex contributing to the phenotypic plasticity of the neckteeth number.
... Conversely, low energy intake at low temperatures causes stunted growth and ultimately affects morphological defense and reproductive capacity (Chen et al., 2015;Havel, 1985). However, in the nature, low temperature also means low density and inactive invertebrate predators (Riessen and Gilbert, 2019), therefore, reduced defense at low temperatures may be a match for the dynamics of predators in nature. ...
Article
Full-text available
Cladocerans can recognize predation risk by sensing the chemical cues released by their predators, and adopt effective anti-predator defensive strategies to avoid being predated. In nature waters, temperature, as one of the key abiotic factors, fluctuates with day-night and seasons, especially under climate warming, which may impact the inducible anti-predator defenses of cladocerans. To investigate the effects of rising temperatures on the inducible anti-predator defenses of cladocerans, we cultured a common species Ceriodaphnia cornuta at presence or absence of Chaoborus sp. larvae kairomone at 15, 20, 25, and 30 °C for 15 days. Results showed that both the inducible anti-predator morphological responses and all the life history traits of C. cornuta were significantly affected by temperature changes. Specifically, rising temperature accelerated the inducible defense responses of the horn formation, but reduced the expression intensity of this morphological defense trait. With increasing temperature, the body size was increased, the time to first reproduction was decreased, and the reproduction was enhanced, indicating that C. cornuta tends to adopt K-selective strategy with maturity at relatively larger size and r-selective strategy with relatively earlier reproductive time and more offspring under warming conditions. These data demonstrated that the inducible anti-predator responses and the life history traits of C. cornuta can be shifted by temperature changes, which may indirectly affect top-down species interactions. Our study highlights the importance of incorporating species interactions when estimating the impact of rising temperature on species.
... The vast literature on rotifer phenotypic plasticity in response to predator presence includes the records of rotifers distinguishing kairomones of different threatening species (Gilbert 2009). Yet, it concerns almost exclusively monogont rotifers altering their morphology or life history (Gilbert 2013;Riessen and Gilbert 2019). ...
Article
Full-text available
Whether bdelloid rotifers can detect and respond to the chemical cues of predators has not been studied, and research on their behaviour is scarce in general. To test for such response, we observed the behaviour of Philodina megalotrocha rotifers in either control or copepod-conditioned water. We then introduced a mechanical disturbance to test if predator odour sensitises rotifers to subsequent cues. We found intensified swimming in P. megalotrocha exposed to Macrocyclops fuscus-conditioned water, i.e. the larger and more predatory of the tested copepods. Such response may be adaptive, depending on the predominant hunting mode of the predator in the particular habitat.
... By spending the light hours in deeper and darker waters, they reduce the risk of being detected by visually hunting predators, such as fish (Lampert 1989, Hays 2003, as well as avoid high exposure to harmful radiation (Rhode et al. 2001). Zooplankton may also respond phenotypically, that is, protecting themselves from predation threats by changing their morphology, such as growing larger spines, neck-teeth or helmets (Agrawal et al. 1999, Riessen andGilbert 2019). The size-efficiency hypothesis predicts that large individuals are stronger competitors because they are able to harvest more of the resources than small ones, whereas large individuals are generally a preferred prey for visually hunting predators, such as fish (Brooks andDodson 1965, Hall et al. 1976). ...
Article
Full-text available
Our understanding on how organisms evolutionarily cope with simultaneously occurring, multiple threats over generations is still elusive. In a long‐term experimental study we therefore exposed clones of a freshwater cladoceran, Daphnia magna, to threats from predation and ultraviolet radiation (UVR) during three consecutive parthenogenetic generations. We show that Daphnia can adapt to different sets of threats within three generations through modifying morphology, swimming behavior or life‐history traits. When faced with predator cues, D. magna responded with reduced body size, whereas exposure to UVR induced behavioral tolerance when again exposed to this threat. Such UVR‐tolerant behavior was initially associated with a reduced clutch size, but Daphnia restored the reproductive output gradually through generations. The findings advance our understanding on how those common invertebrates, with a global distribution, are able to persist and rapidly become successful in a changing environment.
... Daphnia (Arthropoda Crustacea) is an excellent model system for studying predator-induced plasticity (Lass & Spaak, 2003;Tollrian & Dodson, 1999), with alterations in their phenotype against predators including changes in body size, head shape, tail length, number of eggs, reproduction status, and distribution depth (Lass & Spaak, 2003). To express predator-induced plasticity, Daphnia need to perceive predatory kairomone (chemical substance) and/or other factors besides predators; the former is called primary factor and the latter secondary factor (Riessen & Gilbert, 2019). Riessen and Gilbert (2019) suggested in a review that secondary factors are related to increases or decreases in the degree of plasticity. ...
... To express predator-induced plasticity, Daphnia need to perceive predatory kairomone (chemical substance) and/or other factors besides predators; the former is called primary factor and the latter secondary factor (Riessen & Gilbert, 2019). Riessen and Gilbert (2019) suggested in a review that secondary factors are related to increases or decreases in the degree of plasticity. This suggests that predator-induced plasticity displays different trait values among individuals owing to the interaction between primary and secondary factors. ...
... The degree of expressed plasticity is thought to be both enhanced and suppressed in such environments and may be enhanced when Daphnia links periodic changes (i.e., seasons) in predator presence to physical stimuli and may be suppressed in the absence of relationships with cycles (Riessen & Gilbert, 2019 type of factor a "proxy cue" (Miehles et al., 2013). These factors are associated with local predator regimes and thereby cause intraspecific variation between populations. ...
Article
Full-text available
Phenotypic variation among individuals and species is a fundamental principle of natural selection. In this review, we focus on numerous experiments involving the model species Daphnia (Crustacea) and categorize the factors, especially secondary ones, affecting intraspecific variations in inducible defense. Primary factors, such as predator type and density, determine the degree to which inducible defense expresses and increases or decreases. Secondary factors, on the other hand, act together with primary factors to inducible defense or without primary factors on inducible defense. The secondary factors increase intraspecies variation in inducible defense, and thus, the level of adaptation of organisms varies within species. Future research will explore the potential for new secondary factors, as well as the relative importance between factors needs to be clarified. We identified seven secondary factors causing variations in inducible defense based on previous studies: abiotic factors, ecological and evolutionary traps, food, alarm substance, clone/genotypes, instars, and maternal effect.
... Researches on the inducible defense of genus Daphnia, freshwater zooplankton, have contributed to our understanding of the ecology and evolution of inducible defense (Tollrian and Harvel 1999, Lass and Spaak 2003, Riessen and Gilbert 2019. Predation pressure on Daphnia is characterized by its size-selective nature (Dodson 1974, Tollrian and Dodson 1999, Riessen and Trevett-Smith 2009, Weiss and Tollrian 2018, Riessen and Gilbert 2019. ...
... Researches on the inducible defense of genus Daphnia, freshwater zooplankton, have contributed to our understanding of the ecology and evolution of inducible defense (Tollrian and Harvel 1999, Lass and Spaak 2003, Riessen and Gilbert 2019. Predation pressure on Daphnia is characterized by its size-selective nature (Dodson 1974, Tollrian and Dodson 1999, Riessen and Trevett-Smith 2009, Weiss and Tollrian 2018, Riessen and Gilbert 2019. In general, Daphnia species are exposed to two different types of predation risk in lakes, by invertebrates that are usually gape size-limited predators (e.g., Chaoborus larvae) and by planktivorous fish that are visually hunting predators. ...
... The body length sometimes increases (Krueger and Dodson 1981, Havel and Dodson 1984, Riessen and Sprules 1990, Lüning 1992, Spitze 1992 which is thought to be adaptive against Chaoborus predation, or in other cases it decreases (Havel and Dodson 1987, Ketola and Vuorinen 1989, Boeing et al. 2006 which would be maladaptive. This contradictory pattern would be produced because of the development constraint or fitness cost (De Witt et al. 1998, Auld et al. 2010, Riessen and Gilbert 2019 that can obscure the induction of some specific defensive trait. Thus, the local adaptation to the local predators should be better examined in the multivariate phenotypic space as performed in this study and previous studies (Krueger and Dodson 1981, Parejko and Dodson 1991, Boersma et al. 1998, Boeing et al. 2006, Hammill et al. 2008, Dennis et al. 2011); otherwise, we may not be able to observe the actual nature of the induced defense (Kishida et al. 2010). ...
Article
Full-text available
Inducible defense is adaptive when prey organisms cope with fluctuations of predation risk, and there exists ample variations of inducible defense both within a species and between species even in a single habitat. Daphnia, a freshwater zooplankton genus, shows remarkable inducible morphological defense when exposed to predators. This study explored the intra‐ and inter‐specific variations of inducible defense of Daphnia and tested whether the variations can be explained by the size‐selective nature of predation. In Lake Fukami‐ike, Japan, Daphnia ambigua and Daphnia pulex coexist with planktivorous fish and Chaoborus larvae that have different preferences for prey size. We experimentally examined the ontogenetic change of inducible defense for ten clones of each of the two Daphnia species against the two different predators. The degree of defense expression evaluated based on the induction of multiple morphological traits showed remarkable differences between Daphnia species, instars and clones, and the intra‐ and inter‐specific variations were attributed to size‐selective predation from the different predators. The inducible defense of Daphnia showed the adaptive variations depending on the predation pressure that resulted from the size‐selective predation by the coexisting predators.