Samuel Hylander

Escape from UV threats in zooplankton : A cocktail of behavior and protective pigmentation

In order to avoid environmental threats, organisms may respond by altering behavior or phenotype. Using experiments performed in high-latitude Siberia and in temperate Sweden, we show for the first time that, among freshwater crustacean zooplankton, the defense against threats from ultraviolet radiation (UV) is a system where phenotypic plasticity and behavioral escape mechanisms function as complementary traits. Freshwater copepods relied mainly on accumulating protective pigments when exposed to UV radiation, but Daphnia showed strong behavioral responses. Pigment levels for both Daphnia and copepods were generally higher at higher latitudes, mirroring different UV threat levels. When released from the UV threat, Daphnia rapidly reduced (within 10 days) their UV protecting pigmentation-by as much as 40%--suggesting a cost in maintaining UV protective pigmentation. The evolutionary advantage of protective pigments is, likely, the ability to utilize the whole water column during daytime; conversely, since the amount of algal food is generally higher in surface waters, unpigmented individuals are restricted to a less preferred feeding habitat in deeper waters. Our main conclusion is that different zooplankton taxa, and similar taxa at different latitudes, use different mixes of behavior and pigments to respond to UV radiation.

Effects of ultraviolet radiation on pigmentation, photoenzymatic repair, behavior, and community ecology of zooplankton

In this report, we provide a perspective on how zooplankton are able to respond to present and future levels of ultraviolet (UV) radiation, a threat that has been present throughout evolutionary time. To cope with this threat, zooplankton have evolved several adaptations including behavioral responses, repair systems, and accumulation of photoprotective compounds. Common photoprotective compounds include melanins and carotenoids, which are true pigments, but also mycosporine-like amino acids (MAAs) and several other substances, and different taxa use different blends of these compounds. It is not only the level of UV radiation, however, that determines the amount of photoprotective compounds incorporated by the zooplankton, but also other environmental factors, such as predation and supply rate of the compounds. Furthermore, compared to taxa that are less pigmented, those taxa with ample pigmentation are generally less likely to exhibit diel migration. The photoenzymatic repair of UV damages seems to be more efficient at intermediate temperature than at low and high temperatures, suggesting that it is less useful at high and low latitudes, where UV radiation is often extremely high. While predicted future increases in UV radiation are expected to substantially affect many processes, recent studies show that most zooplankton taxa are well adapted to cope with such increases, either by UV avoidance behavior or by incorporation of photoprotective compounds. Hence, we conclude that future increase in UV radiation will have only moderate direct effects on zooplankton biomass and community dynamics.

Size-structured risk assessments govern Daphnia migration.

Abstract One of the more fascinating phenomena in nature is animal mass migrations and in oceans and freshwaters, diel variations in depth distribution of zooplankton are a phenomenon that has intrigued scientists for more than a century. In our study, we show that zooplankton are able to assess the threat level of ultraviolet radiation and adjust their depth distribution to this level at a very fine tuned scale. Moreover, predation risk induces a size-structured depth separation, such that small individuals, which we show are less vulnerable to predation than larger, make a risk assessment and continue feeding in surface waters during day, offering a competitive release from down-migrating larger animals. Hence, we mechanistically show that such simple organisms as invertebrate zooplankton are able to make individual, size-specific decisions regarding how to compromise between threats from both predators and UV radiation, and adjust their diel migratory patterns accordingly.

Characteristic Sizes of Life in the Oceans, from Bacteria to Whales

The size of an individual organism is a key trait to characterize its physiology and feeding ecology. Size-based scaling laws may have a limited size range of validity or undergo a transition from one scaling exponent to another at some characteristic size. We collate and review data on size-based scaling laws for resource acquisition, mobility, sensory range, and progeny size for all pelagic marine life, from bacteria to whales. Further, we review and develop simple theoretical arguments for observed scaling laws and the characteristic sizes of a change or breakdown of power laws. We divide life in the ocean into seven major realms based on trophic strategy, physiology, and life history strategy. Such a categorization represents a move away from a taxonomically oriented description toward a trait-based description of life in the oceans. Finally, we discuss life forms that transgress the simple size-based rules and identify unanswered questions.

Rapid Enzymatic Response to Compensate UV Radiation in Copepods

Ultraviolet radiation (UVR) causes physical damage to DNA, carboxylation of proteins and peroxidation of lipids in copepod crustaceans, ubiquitous and abundant secondary producers in most aquatic ecosystems. Copepod adaptations for long duration exposures include changes in behaviour, changes in pigmentation and ultimately changes in morphology. Adaptations to short-term exposures are little studied. Here we show that short-duration exposure to UVR causes the freshwater calanoid copepod, Eudiaptomus gracilis, to rapidly activate production of enzymes that prevent widespread collateral peroxidation (glutathione S-transferase, GST), that regulate apoptosis cell death (Caspase-3, Casp-3), and that facilitate neurotransmissions (cholinesterase-ChE). None of these enzyme systems is alone sufficient, but they act in concert to reduce the stress level of the organism. The interplay among enzymatic responses provides useful information on how organisms respond to environmental stressors acting on short time scales.

Foraging success of juvenile pike Esox lucius depends on visual conditions and prey pigmentation

Young-of-the-year pike Esox lucius foraging on copepods experienced different foraging success depending on prey pigmentation in water visually degraded by brown colouration or algae. Both attack rate and prey consumption rate were higher for E. lucius foraging on transparent prey in brown water, whereas the opposite was true in algal turbid water. Pigments in copepod prey may have a cryptic function in brown water instead of a photo-protective function even if prey-size selectivity was stronger than selection based on pigmentation in juvenile E. lucius.

Adult and offspring size in the ocean over 17 orders of magnitude follows two life history strategies

Explaining variability in offspring vs. adult size among groups is a necessary step to determine the evolutionary and environmental constraints shaping variability in life history strategies. This is of particular interest for life in the ocean where a diversity of offspring development strategies is observed along with variability in physical and biological forcing factors in space and time. We compiled adult and offspring size for 407 pelagic marine species covering more than 17 orders of magnitude in body mass including Cephalopoda, Cnidaria, Crustaceans, Ctenophora, Elasmobranchii, Mammalia, Sagittoidea, and Teleost. We find marine life following one of two distinct strategies, with offspring size being either proportional to adult size (e.g., Crustaceans, Elasmobranchii, and Mammalia) or invariant with adult size (e.g., Cephalopoda, Cnidaria, Sagittoidea, Teleosts, and possibly Ctenophora). We discuss where these two strategies occur and how these patterns (along with the relative size of the offspring) may be shaped by physical and biological constraints in the organisms environment. This adaptive environment along with the evolutionary history of the different groups shape observed life history strategies and possible group-specific responses to changing environmental conditions (e.g., production and distribution).

Fitness costs and benefits of ultraviolet radiation exposure in marine pelagic copepods

Summary 1. Life-history theory predicts that organisms should allocate energy throughout their life such that they maximize their fitness. Copepod zooplankton are known to accumulate sunscreens (so-called mycosporine-like amino acids, MAAs) and antioxidant carotenoids to mitigate negative effects of ultraviolet radiation (UVR), but it is not well known how this affects their fitness. 2. We followed cohorts of the marine copepod Acartia tonsa and assessed how fitness was affected by UVR exposure and a diet rich in UVR-protective sunscreens. 3. Several fitness components including somatic growth, egg quality and nauplii production (larvae) were negatively affected by UVR, whereas other components such as size at maturity, survival and length of life were not. Nauplii production through low egg quality was the most influential life-history parameter that changed in response to UVR. 4. There was interaction between fitness costs and food source. If copepods were fed a diet rich in UVR-screening MAAs, they were able to maintain and even increase their fitness even though they were exposed to otherwise detrimental radiation. Levels of UVR-protective carotenoids were low in the studied species and a meta-analysis revealed that marine copepods in general have much lower – by an order of magnitude – levels of carotenoids than freshwater species, while levels of MAAs are similar between the two habitats. 5. We conclude that allocation to different fitness components to some extent is plastic although egg quality is by far the most influential factor, and this is an example of how environmental variability affects overall fitness. Fitness costs associated with UVR exposure in the absence of UVR-screening MAAs were present. Other costs such as costs for accumulating MAAs were not detected, and if present, they were outweighed by a stimulated fitness in combined UVR and MAA treatments challenging the common model that inducible defences (such as accumulation of MAAs) should come with a cost. Low levels of carotenoids in marine systems suggest high predation pressures on pigmented specimens. Accumulation of nonpigmented MAAs could hence be a key adaptation for surface-dwelling marine zooplankton to maintain or even increase their fitness when exposed to detrimental radiation.

Induced tolerance expressed as relaxed behavioural threat response in millimetre- sized aquatic organisms

Natural selection shapes behaviour in all organisms, but this is difficult to study in small, millimetre-sized, organisms. With novel labelling and tracking techniques, based on nanotechnology, we here show how behaviour in zooplankton (Daphnia magna) is affected by size, morphology and previous exposure to detrimental ultraviolet radiation (UVR). All individuals responded with immediate downward swimming to UVR exposure, but when released from the threat they rapidly returned to the surface. Large individuals swam faster and generally travelled longer distances than small individuals. Interestingly, individuals previously exposed to UVR (during several generations) showed a more relaxed response to UVR and travelled shorter total distances than those that were naive to UVR, suggesting induced tolerance to the threat. In addition, animals previously exposed to UVR also had smaller eyes than the naive ones, whereas UVR-protective melanin pigmentation of the animals was similar between populations. Finally, we show that smaller individuals have lower capacity to avoid UVR which could explain patterns in natural systems of lower migration amplitudes in small individuals. The ability to change behavioural patterns in response to a threat, in this case UVR, adds to our understanding of how organisms navigate in the ‘landscape of fear’, and this has important implications for individual fitness and for interaction strengths in biotic interactions.

Instantaneous threat escape and differentiated refuge demand among zooplankton taxa

Most animals, including aquatic crustacean zooplankton, perform strong avoidance movements when exposed to a threat, such as ultraviolet radiation (UVR). We here show that the genera Daphnia and Bosmina instantly adjust their vertical position in the water in accordance with the present UVR threat, i.e., seek refuge in deeper waters, whereas other taxa show less response to the threat. Moreover, Daphnia repeatedly respond to UVR pulses, suggesting that they spend more energy on movement than more stationary taxa, for example, during days with fluctuating cloud cover, illustrating nonlethal effects in avoiding UVR threat. Accordingly, we also show that the taxa with the most contrasting behavioral responses differ considerably in photoprotection, suggesting different morphological and behavioral strategies in handling the UVR threat. In a broader context, our studies on individual and taxa specific responses to UVR provide insights into observed spatial and temporal distribution in natural ecosystems.