Zooplankton responses to multiple threats within and across generations

In their natural environments, organisms are unlikely to be distributed randomly but instead they are constantly faced with multiple and variable threats. In order to maximise survival, they need to be able to perceive the present threat level and respond accordingly. In aquatic ecosystems, two common threats for crustacean zooplankton are predation and ultraviolet radiation (UVR). Despite the growing recognition that zooplankton can plastically respond to predation and UVR within a single generation, little is known on how they evolutionarily cope with these simultaneously occurring multiple threats over generations. In this thesis, I investigate the threat responses in zooplankton when exposed to multiple threats from predation and UVR based on short-term (within a single generation) and multigenerational exposure experiments.Alteration in behavioural traits is generally the first reaction in zooplankton to changed conditions, which allows them to escape from the threats instantly after exposure. One example of a common behavioural response in zooplankton is diel vertical migration (DVM), where they spend the day in deep, dark waters and migrate up to surface waters at night. I found that low-latitude copepods in Bahamian blue holes exhibited DVM to reduce predation risk from visually hunting fish, whereas no response was found to lake-specific differences in UVR transparency. Moreover, copepods also follow their food resources, so that they stay at the depth with rich food where predation risk and UVR may decrease to a negligible level. When exposed to conflicting threats from UVR and predation from either moving pelagic or benthic predators, Daphnia are able to make different risk assessments and thereby alter their behaviour in accordance with the actual threat level. I show that two Daphnia species respond strongly to UVR, whereas only the large prey species D. magna express a predator avoidance behaviour. In addition to alterations in behaviour, D. magna can also change its body size and life-history to deal with multiple threats from predation and UVR. I demonstrate that D. magna become smaller through generations in response to fish predation, whereas they change their behaviour to avoid UVR. Individuals who have previously experienced UVR respond more relaxed when exposed to such radiation again. These individuals also produce less offspring during the first generation after exposure but the number of offspring then gradually increases through generations. Therefore, D. magna adopt divergent strategies over generations and become adapted to the local environmental conditions after about three generations. Exposure to UVR can induce plastic phenotypic changes in D. magna including alterations in behaviour and life-history shifts. However, such transgenerational effects may be modified by the evolutionary history of stress that lead to different plastic responses to UVR across generations

Predation risk and the evolution of a vertebrate stress response: Parallel evolution of stress reactivity and sexual dimorphism

Predation risk is often invoked to explain variation in stress responses. Yet, the answers to several key questions remain elusive, including the following: (1) how predation risk influences the evolution of stress phenotypes, (2) the relative importance of environmental versus genetic factors in stress reactivity and (3) sexual dimorphism in stress physiology. To address these questions, we explored variation in stress reactivity (ventilation frequency) in a post-Pleistocene radiation of live-bearing fish, where Bahamas mosquitofish (Gambusia hubbsi) inhabit isolated blue holes that differ in predation risk. Individuals of populations coexisting with predators exhibited similar, relatively low stress reactivity as compared to low-predation populations. We suggest that this dampened stress reactivity has evolved to reduce energy expenditure in environments with frequent and intense stressors, such as piscivorous fish. Importantly, the magnitude of stress responses exhibited by fish from high-predation sites in the wild changed very little after two generations of laboratory rearing in the absence of predators. By comparison, low-predation populations exhibited greater among-population variation and larger changes subsequent to laboratory rearing. These low-predation populations appear to have evolved more dampened stress responses in blue holes with lower food availability. Moreover, females showed a lower ventilation frequency, and this sexual dimorphism was stronger in high-predation populations. This may reflect a greater premium placed on energy efficiency in live-bearing females, especially under high-predation risk where females show higher fecundities. Altogether, by demonstrating parallel adaptive divergence in stress reactivity, we highlight how energetic trade-offs may mould the evolution of the vertebrate stress response under varying predation risk and resource availability

Population connectivity, dispersal, and swimming behavior in Daphnia

The water flea Daphnia has the capacity to respond rapidly to environmental stressors, to disperse over large geographical scales, and to preserve its genetic material by forming egg banks in the sediment. Spatial and temporal distributions of D. magna have been extensively studied over the last decades using behavioral or genetic tools, although the correlation between the two has rarely been the focus. In the present study, we therefore investigated the population genetic structure and behavioral response to a lethal threat, ultraviolet radiation (UVR), among individuals from two different water bodies. Our results show two genetic populations with moderate gene flow, highly correlated with geographical location and with inheritable traits through generations. However, despite the strong genetic differences between populations, we show homogeneous refuge demand between populations when exposed to the lethal threat solar UVR

Ancestral environment determines the current reaction to ultraviolet radiation in Daphnia magna

An individual's phenotype can be altered by direct contact with its present environment but also by environmental features experienced by previous generations, that is, parental or grandparental effects. However, the strength and direction of these transgenerational effects may be highly variable according to the ecological conditions experienced by ancestral generations. Here, we performed a reciprocal split-brood experiment to compare transgenerational responses to the threat of ultraviolet radiation (UVR) in the zooplankter Daphnia magna, which had, or had not, been exposed to UVR for more than 150 generations. We found that the environment at which parents and grandparents were reared significantly influenced both behavior and life-history traits of their descendants. However, such transgenerational responses differed between D. magna individuals with contrasting ancestral stress history, that is, when exposed to UVR previously unexposed individuals rapidly changed their behavior and life-history traits, whereas individuals previously exposed to UVR showed less pronounced response when the UVR threat level relaxed. Hence, we here demonstrate an asymmetric transgenerational plasticity in response to UVR threat. The findings advance our understanding on the evolutionary ecology of such transgenerational effects and their potential role in response to changes in the local environment

Diverging responses to threats across generations in zooplankton

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

Energetic Asymmetry Connected with Energy Flow Changes in Response to Eutrophication : A Study of Multiple Fish Species in Subtropical Shallow Lakes

Energy flow is a central characteristic in all ecosystems, and it has attracted considerable scientific attention due to its significant effects on the stability of food webs. Lake ecosystems that undergo regime shifts (clear water phase, phytoplankton dominated changed into turbid water, macrophytes dominated or vice versa) are characterized by a series of transformation in trophic structure. Although previous studies have mainly focused on the causes and consequences of regime shifts in shallow lakes, studies about responses of energy flow changes to regime shifts is far from complete. In this paper, we estimated trophic position and benthivory (i.e. degree of benthivory) of seventeen fish species from seven shallow lakes. Our data show that the trophic position and benthivory of fish species in clear water phase are significantly higher than in turbid water. This finding might help spark some ideas for subtropical lake eutrophication treatment

Behavioural responses to co-occurring threats of predation and ultraviolet radiation in Daphnia

Organisms in the wild are faced with multiple threats and a common response is a change in behaviour. To disentangle responses to several threats, we exposed two differently sized species of the freshwater invertebrate Daphnia to solar ultraviolet radiation (UVR) and predation from either moving pelagic or benthic ambush predators. Using an advanced nanotechnology-based method, we tracked the three-dimensional movements of those mm-sized animals at the individual level. Each behavioural trial was performed both under conditions resembling night (no UVR) and day (UVR) and we examined patterns of the depth distribution and swimming speed by Daphnia across three treatments: no predator (control); bottom-dwelling damselfly (Calopteryx sp.); and fish (stickleback, Pungitius pungitius) predators. We also quantified the actual predation rate by the two predators on the two Daphnia species, Daphnia manga and Daphnia pulex. We show that individual Daphnia are able to identify predators with different feeding habitats, rank multiple and simultaneously occurring risks and respond in accordance with the actual threat; complex responses that are generally associated with larger animals. In a broader context, our results highlight and quantify how a cocktail of everyday threats is perceived and handled by invertebrates, which advances our understanding of species distribution in space and time, and thereby of population dynamics and ecosystem function in natural ecosystems

Diel vertical migration of copepods and its environmental drivers in subtropical Bahamian blue holes

Diel vertical migration (DVM) is the most common behavioral phenomenon in zooplankton, and numerous studies have evaluated DVM under strong seasonality at higher latitudes. Yet, our understanding of the environmental drivers of DVM at low latitudes, where seasonal variation is less pronounced, remains limited. Therefore, we here examined patterns of vertical distribution in copepods in six subtropical Bahamian blue holes with different food web structure and tested the role of several key environmental variables potentially affecting this behavior. Day and night samplings showed that copepods generally performed DVM, characterized by downward migration to deeper depths during the day and upward migration to surface waters at night. Across all blue holes, the daytime vertical depth distribution of calanoid copepods correlated positively with both predation risk and depth of food resources (Chlorophyll a), but was less affected by ultraviolet radiation (UVR). A potential explanation is that since UVR is a continuous threat across seasons, zooplankton have established photoprotective pigmentation making them less vulnerable to this threat. The copepods also showed a size-structured depth segregation, where larger individuals were found at deeper depths during the day, which further strengthens the suggestion that predation is a major driver of DVM in these systems. Hence, in contrast to studies performed at higher latitudes, we show that despite the constant exposure to UVR, predator avoidance and food availability are the most pronounced drivers of copepod DVM at those low latitudes, suggesting that the main driver of DVM may vary among systems, but also systematically by latitude

Turbidity data

Raw data and the script to determine how similar the UV threat will be across the three selected blue holes