The Asymmetric Response Concept explains ecological consequences of multiple stressor exposure and release.

Our capacity to predict trajectories of ecosystem degradation and recovery is limited, especially when impairments are caused by multiple stressors. Recovery may be fast or slow and either complete or partial, sometimes result in novel ecosystem states or even fail completely. Here, we introduce the Asymmetric Response Concept (ARC) that provides a basis for exploring and predicting the pace and magnitude of ecological responses to, and release from, multiple stressors. The ARC holds that three key mechanisms govern population, community and ecosystem trajectories. Stress tolerance is the main mechanism determining responses to increasing stressor intensity, whereas dispersal and biotic interactions predominantly govern responses to the release from stressors. The shifting importance of these mechanisms creates asymmetries between the ecological trajectories that follow increasing and decreasing stressor intensities. This recognition helps to understand multiple stressor impacts and to predict which measures will restore communities that are resistant to restoration.

Facing the Green Threat: A Water Flea's Defenses against a Carnivorous Plant.

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.

Determining freshwater pCO2 based on geochemical calculation and modelling using PHREEQC.

Fossil fuel combustion results in rising atmospheric carbon dioxide (CO2), which is known to impact the global climate and the oceans. Latest insights indicate that rising atmospheric CO2 levels also affect CO2 partial pressure (pCO2) in freshwaters, where pCO2 is controlled by a multitude of parameters. However, up to date there is no standardized method, which allows the determination of current and past freshwater pCO2 levels. Ideally methods should incorporate numerous hydrogeochemical and -physical factors to reflect the interplay of all interacting components and their effect on pCO2. We here describe the application of the geochemical program PHREEQC. This freeware serves as an easy method enabling a plausible and comprehensive analysis of pCO2 for field, laboratory, and especially long-term data. We present the use of the different input parameters of a laboratory- and a field long-term monitoring dataset including dissociation constants of carbonic acid measured as total inorganic carbon (TIC) and total CO2 concentration (TCO2) or total alkalinity (TA), together with hydrogeochemical and -physical parameters. Based on current literature and our analyses PHREEQC appears a solid strategy to determine freshwater pCO2 that can moreover be used for long-term datasets.•Comprehensive analysis of pCO2 for field, laboratory, and long-term data.•PHREEQC is not dependent on just one sampling method or parameter scheme.•PHREEQC includes testing the plausibility of a water analysis and enables the assessment of the quality of the laboratory analysis, as well as automatic calculation of all relevant aquatic complexes.

Thwarting predators? A three-dimensional perspective of morphological alterations in the freshwater crustacean Daphnia.

Predation is a major selective agent, so that many taxa evolved phenotypically plastic defensive mechanisms. Among them are many species of the microcrustacean genus Daphnia, which respond to an increased predation risk by developing inducible morphological alterations. Some of these features are obvious and easily recognized, e.g., crests in D. longicephala, while others are rather hidden, such as the bulkier shape of D. magna induced by the presence of the tadpole shrimp Triops. In this study we investigated the extraordinary diversity of morphological adaptations in the presence of predators with different foraging strategies in six predator-prey systems. For the first time we were able to analyze the unexposed and predator-exposed morphs comprehensively using three-dimensional scanning and reconstruction. We show that morphological changes are manifold in appearance between species and predators, and go beyond what has been known from previous 2D analyses. This further demonstrates the enormous trait flexibility of Daphnia. Interestingly, we found that among this variety some species share morphological strategies to counter a predator, while others use a different strategy against the same predator. Based on these intra- and interspecific comparisons, we discuss the mechanisms by which the respective defense might operate. These data therefore contribute to a deeper understanding of the inducible defenses' morphology as well as their diversified modes of operation in Daphnia, being a cornerstone for subsequent investigations, including the determination of costs associated with morphological change.

The history, biological relevance, and potential applications for polyp bailout in corals.

Corals have evolved a variety of stress responses to changing conditions, many of which have been the subject of scientific research. However, polyp bailout has not received widespread scientific attention, despite being described more than 80 years ago. Polyp bailout is a drastic response to acute stress in which coral colonies break down, with individual and patches of polyps detaching from the colony and the calcareous skeleton Polyps retain their symbiotic partners, have dispersal ability, and may undergo secondary settlement and calcification. Polyp bailout has been described worldwide in a variety of anthozoan species, especially in Scleractinia. It can be induced by multiple natural stressors, but also artificially. Little is known about the evolutionary and ecological potential and consequences of breaking down modularity, the dispersal ability, and reattachment of polyps resulting from polyp bailout. It has been shown that polyp bailout can be used as a model system, with promise for implementation in various research topics. To date, there has been no compilation of knowledge on polyp bailout, which prompted us to review this interesting stress response and provide a basis to discuss research topics and priorities for the future.

Snapshot prey spectrum analysis of the phylogenetically early-diverging carnivorous Utricularia multifida from U. section Polypompholyx (Lentibulariaceae).

Utricularia multifida is carnivorous bladderwort from Western Australia and belongs to a phylogenetically early-diverging lineage of the genus. We present a prey spectrum analysis resulting from a snapshot sampling of 17 traps-the first of this species to our knowledge. The most abundant prey groups were Ostracoda, Copepoda, and Cladocera. The genus cf. Cypretta (Cyprididae, Ostracoda) was the predominant prey. However, a high variety of other prey organisms with different taxonomic backgrounds was also detected. Our results indicate that U. multifida may potentially be specialized in capturing substrate-bound prey. Future approaches should sample plants from different localities to allow for robust comparative analyses.

Long-term effects of elevated pCO2 levels on the expression of Chaoborus-induced defences in Daphnia pulex.

Increased carbon dioxide from fossil fuel combustion results in an enrichment of CO2 in the global carbon cycle. Recent evidence indicates that rising atmospheric CO2 impacts the partial pressure of carbon dioxide (pCO2) in freshwaters. This affects freshwater biota by disrupting chemical communication between predator and prey. One such well-described predator-prey interaction is the phantom midge larva Chaoborus preying on the freshwater crustacean Daphnia pulex. To counter Chaoborus predation, D. pulex develops defensive neckteeth in response to chemical cues. The strength of neckteeth expression is reduced when D. pulex experience elevated pCO2 levels. This is discussed to directly impair predator perception and results in reduced defence expression. However, it is not known whether there are also long-term effects associated with continuous elevated pCO2. Here, we investigated the effect of long-term exposure of D. pulex to elevated pCO2 levels in a life-table experiment over three generations. Using a flow-through system, we continuously exposed D. pulex to cues released by the predatory larva Chaoborus and control or elevated pCO2 levels. We determined morphological defence expression in the 2nd juvenile instar and the number of neonates as a measure for life-history traits over three successive generations. We detected that elevated pCO2 significantly reduces the expression of predator-induced morphological defences (i.e. neckteeth) and life-history parameters (i.e. number of neonates) in successive generations. Our data clearly show that at least three generations become more vulnerable to predation without indications of transgenerational acclimation. As Daphnia is a keystone grazer of freshwater ecosystems, this may destabilise population growth rates. In conclusion, long-term effects of pCO2-induced reduction of predator-induced plasticity may significantly affect trophic interactions.

Linking local movement and molecular analysis to explore philopatry and population connectivity of the southern stingray Hypanus americanus.

Limited data pertaining to life history and population connectivity of the data-deficient southern stingray (Hypanus americanus) are available. To determine potential vulnerabilities of their populations, this study aimed to analyse their movement patterns and genetic variability. A population of southern stingrays encompassing nine sites around Cape Eleuthera, the Bahamas, has been monitored using mark-recapture, spanning a 2.5 year period. Out of 200 individual stingrays, more than a third were encountered again. The home range of the females appears to be restricted, which supports the notion of high site residency. As resident populations of stingrays could suffer from a lack of population connectivity and be predestined for genetic isolation and local extirpation, this study further investigated the genetic connectivity of four sample sites in the central and western Bahamas. A haplotype analysis from the mitochondrial D-loop region showed that no distinct population structure strictly correlated with the sample site. These findings were complemented by five microsatellite loci that revealed high degrees in genotypic variability and little population differentiation. The results suggest gene flow mediated by both males and females.

Elevated pCO2 affects behavioural patterns and mechano-sensation in predatory phantom midge larvae Chaoborus obscuripes.

Aquatic acidification is a major consequence of fossil fuel combustion. In marine ecosystems it was shown, that increasing pCO2 levels significantly affect behavioural and sensory capacities in a diversity of species. This can result in altered predator and prey interactions and thereby change community structures. Just recently also CO2 dependent acidification of freshwater habitats has been shown. Also here, increased levels of pCO2 change organisms' behaviour and sensory capacities. For example, the freshwater crustacean Daphnia's ability to detect predators and accurately develop morphological defences was significantly reduced, rendering Daphnia more susceptible to predation. It was speculated that this may have cascading effects on freshwater food webs. However, for a comprehensive understanding of how increased levels of CO2 affect trophic interactions, it is also important to study how CO2 affects predators. We tested this using the dipeteran phantom midge larva Chaoborus obscuripes, which is a world-wide abundant inhabitant of freshwater impoundments. We monitored activity parameters, predation parameters, and predation rate. Chaoborus larvae are affected by increased levels of pCO2 as we observed an increase in undirected movements and at the same time, reduced sensory abilities to detect prey items. This is likely to affect the larvae's energy budgets. Chaoborus is a central component of many freshwater food-webs. Therefore, CO2 effects on predator and prey levels will likely have consequences for community structures.

Prey capture analyses in the carnivorous aquatic waterwheel plant (Aldrovanda vesiculosa L., Droseraceae).

We investigated the predator-prey interactions between an Australian ecotype of the carnivorous waterwheel plant (Aldrovanda vesiculosa, Droseraceae) and its potential natural prey, the water flea Daphnia longicephala (Daphniidae), which also occurs in Australia. A. vesiculosa develops snap-traps, which close within ~10-100 ms after mechanical triggering by zooplankton prey. Prey capture attempts (PCAs) were recorded via high-speed cinematography in the laboratory. From 14 recorded PCAs, nine were successful for the plant (the prey was caught), and five were unsuccessful (prey could escape), resulting in a capture rate of ~64%. The prey animals' locomotion behaviour (antenna beat frequency and movement type) in trap vicinity or inside the open traps is very variable. Traps were mainly triggered with the second antennae. During trap closure, the animals moved only very little actively. A flight response in reaction to an initiated trap closure was not observed. However, several animals could escape, either by having a "lucky" starting position already outside the triggered trap, by freeing themselves after trap closure, or by being pressed out by the closing trap lobes. According to our observations in the successful PCAs, we hypothesize that the convex curvature of the two trap lobes (as seen from the outside) and the infolded trap rims are structural means supporting the capture and retention of prey. Our results are discussed in a broader biological context and promising aspects for future studies are proposed.

Red Queen revisited: Immune gene diversity and parasite load in the asexual Poecilia formosa versus its sexual host species P. mexicana.

In accordance with the Red Queen hypothesis, the lower genotypic diversity in clonally reproducing species should make them easier targets for pathogen infection, especially when closely related sexually reproducing species occur in close proximity. We analyzed two populations of clonal P. formosa and their sexual parental species P. mexicana by correlating individual parasite infection with overall and immune genotype. Our study revealed lower levels of overall genotypic diversity and marginally fewer MHC class I alleles in P. formosa individuals compared to sexually reproducing P. mexicana. Parasite load, however, differed only between field sites but not between species. We hypothesize that this might be due to slightly higher genotypic diversity in P. formosa at the innate immune system (toll like receptor 8) which is likely due to the species' hybrid origin. In consequence, it appears that clonal individuals do not necessarily suffer a disadvantage compared to sexual individuals when fighting parasite infection.

Zooplankters' nightmare: The fast and efficient catching basket of larval phantom midges (Diptera: Chaoborus).

Filter feeding zooplankton are a crucial component of limnic food webs. Copepods and cladocerans are important prey organisms for first-level predators like the common and abundant larvae of phantom midges (Chaoborus sp.). The latter possess a complex catching basket built of head appendages specialized to capture small crustaceans. The predator-prey-relationship of Chaoborus (Diptera, Nematocera) and Daphnia (Crustacea, Cladocera) has been studied in particular detail owing to the daphniids' ability to react upon the threat of predation with inducible defenses. Daphnia pulex expresses so-called 'neckteeth' in the presence of Chaoborus larvae that are discussed as a defensive trait that interferes with the larval head appendages and their effectiveness has been shown in several studies. Nonetheless, mode of function of these neckteeth is not understood and the hypothesis that they interfere with the predator's head appendages still has to be confirmed. To clarify the role of neckteeth in Daphnia, an understanding of the Chaoborus capture apparatus is essential. Here, we present a detailed three-dimensional analysis of Chaoborus obscuripes' larval head morphology as well as a kinematic analysis of the attack motion, which revealed an impressive strike velocity (14 ms to prey contact). The movement of the larvae's head appendages is reconstructed in the three-dimensional space using a combination of high-speed videography, micro-computed tomography and computer animation. Furthermore, we provide predation trial data to distinguish between pre- and post-attack defensive effects in D. pulex. Our findings suggest a combination of pre- and post-attack defenses with an average effectiveness of 50% each. With this study, we quantitatively describe prey capture kinematics of C. obscuripes and take a further step to reveal the neckteeth' mode of function in D. pulex.

Identification of Chaoborus kairomone chemicals that induce defences in Daphnia.

Infochemicals play important roles in aquatic ecosystems. They even modify food web interactions, such as by inducing defenses in prey. In one classic but still not fully understood example, the planktonic freshwater crustacean Daphnia pulex forms specific morphological defenses (neckteeth) induced by chemical cues (kairomones) released from its predator, the phantom midge larva Chaoborus. On the basis of liquid chromatography, mass spectrometry, and chemical synthesis, we report here the chemical identity of the Chaoborus kairomone. The biologically active cues consist of fatty acids conjugated to the amino group of glutamine via the N terminus. These cues are involved in Chaoborus digestive processes, which explains why they are consistently released despite the disadvantage for its emitter. The identification of the kairomone may allow in-depth studies on multiple aspects of this inducible defense system.

Scan, extract, wrap, compute-a 3D method to analyse morphological shape differences.

Quantitative analysis of shape and form is critical in many biological disciplines, as context-dependent morphotypes reflect changes in gene expression and physiology, e.g., in comparisons of environment-dependent phenotypes, forward/reverse genetic assays or shape development during ontogenesis. 3D-shape rendering methods produce models with arbitrarily numbered, and therefore non-comparable, mesh points. However, this prevents direct comparisons. We introduce a workflow that allows the generation of comparable 3D models based on several specimens. Translocations between points of modelled morphotypes are plotted as heat maps and statistically tested. With this workflow, we are able to detect, model and investigate the significance of shape and form alterations in all spatial dimensions, demonstrated with different morphotypes of the pond-dwelling microcrustacean Daphnia. Furthermore, it allows the detection even of inconspicuous morphological features that can be exported to programs for subsequent analysis, e.g., streamline- or finite-element analysis.

Rising pCO2 in Freshwater Ecosystems Has the Potential to Negatively Affect Predator-Induced Defenses in Daphnia.

Anthropogenically released CO2 accumulates in the global carbon cycle and is anticipated to imbalance global carbon fluxes [1]. For example, increased atmospheric CO2 induces a net air-to-sea flux where the oceans take up large amounts of atmospheric CO2 (i.e., ocean acidification [2-5]). Research on ocean acidification is ongoing, and studies have demonstrated the consequences for ecosystems and organismal biology with major impacts on marine food webs, nutrient cycles, overall productivity, and biodiversity [6-9]. Yet, surprisingly little is known about the impact of anthropogenically caused CO2 on freshwater systems due to their more complex biogeochemistry. The current consensus, yet lacking data evidence, is that anthropogenic CO2 does indeed affect freshwater carbon hydrogeochemistry, causing increased pCO2 in freshwater bodies [10-13]. We analyzed long-term data from four freshwater reservoirs and observed a continuous pCO2 increase associated with a decrease in pH, indicating that not only the oceans but also inland waters are accumulating CO2. We tested the effect of pCO2-dependent freshwater acidification using the cosmopolite crustacean Daphnia. For general validity, control pCO2-levels were based on the present global pCO2 average. Treatments were selected with very high pCO2 levels, assuming a continuous non-linear increase of pCO2, reflecting worst-case-scenario future pCO2 levels. Such levels of elevated pCO2 reduced the ability of Daphnia to sense its predators and form adequate inducible defenses. We furthermore determined that pCO2 and not the resulting reduction in pH impairs predator perception. If pCO2 alters chemical communication between freshwater species, this perturbs intra- and interspecific information transfer, which may affect all trophic levels.

Biomechanical properties of predator-induced body armour in the freshwater crustacean Daphnia.

The freshwater crustacean Daphnia is known for its ability to develop inducible morphological defences that thwart predators. These defences are developed only in the presence of predators and are realized as morphological shape alterations e.g. 'neckteeth' in D. pulex and 'crests' in D. longicephala. Both are discussed to hamper capture, handling or consumption by interfering with the predator's prey capture devices. Additionally, D. pulex and some other daphniids were found to armour-up and develop structural alterations resulting in increased carapace stiffness. We used scanning transmission electron microscopy (STEM) and confocal laser scanning microscopy (CLSM) to identify predator-induced structural and shape alterations. We found species specific structural changes accompanying the known shape alterations. The cuticle becomes highly laminated (i.e. an increased number of layers) in both species during predator exposure. Using nano- and micro-indentation as well as finite element analysis (FEA) we determined both: the structure's and shape's contribution to the carapace's mechanical resistance. From our results we conclude that only structural alterations are responsible for increased carapace stiffness, whereas shape alterations appear to pose handling difficulties during prey capture. Therefore, these defences act independently at different stages during predation.

Biomechanical analysis of prey capture in the carnivorous Southern bladderwort (Utricularia australis).

We recorded capture events (CEs) of the daphniid Ceriodaphnia dubia by the carnivorous Southern bladderwort with suction traps (Utricularia australis). Independent to orientation and behavior during trap triggering, the animals were successfully captured within 9 ms on average and sucked in with velocities of up to 4 m/s and accelerations of up to 2800 g. Phases of very high acceleration during onsets of suction were immediately followed by phases of similarly high deceleration (max.: -1900 g) inside the bladders, leading to immobilization of the prey which then dies. We found that traps perform a 'forward strike' during suction and that almost completely air-filled traps are still able to perform suction. The trigger hairs on the trapdoors can undergo strong bending deformation, which we interpret to be a safety feature to prevent fracture. Our results highlight the elaborate nature of the Utricularia suction traps which are functionally resilient and leave prey animals virtually no chance to escape.

The Flashlight Fish Anomalops katoptron Uses Bioluminescent Light to Detect Prey in the Dark.

Bioluminescence is a fascinating phenomenon occurring in numerous animal taxa in the ocean. The reef dwelling splitfin flashlight fish (Anomalops katoptron) can be found in large schools during moonless nights in the shallow water of coral reefs and in the open surrounding water. Anomalops katoptron produce striking blink patterns with symbiotic bacteria in their sub-ocular light organs. We examined the blink frequency in A. katoptron under various laboratory conditions. During the night A. katoptron swims in schools roughly parallel to their conspecifics and display high blink frequencies of approximately 90 blinks/minute with equal on and off times. However, when planktonic prey was detected in the experimental tank, the open time increased compared to open times in the absence of prey and the frequency decreased to 20% compared to blink frequency at night in the absence of planktonic prey. During the day when the school is in a cave in the reef tank the blink frequency decreases to approximately 9 blinks/minute with increasing off-times of the light organ. Surprisingly the non-luminescent A. katoptron with non-functional light organs displayed the same blink frequencies and light organ open/closed times during the night and day as their luminescent conspecifics. In the presence of plankton non-luminescent specimens showed no change in the blink frequency and open/closed times compared to luminescent A. katoptron. Our experiments performed in a coral reef tank show that A. katoptron use bioluminescent illumination to detect planktonic prey and that the blink frequency of A. katoptron light organs follow an exogenous control by the ambient light.

Different feeding strategies in Antarctic scavenging amphipods and their implications for colonisation success in times of retreating glaciers.

BACKGROUND: Scavenger guilds are composed of a variety of species, co-existing in the same habitat and sharing the same niche in the food web. Niche partitioning among them can manifest in different feeding strategies, e.g. during carcass feeding. In the bentho-pelagic realm of the Southern Ocean, scavenging amphipods (Lysianassoidea) are ubiquitous and occupy a central role in decomposition processes. Here we address the question whether scavenging lysianassoid amphipods employ different feeding strategies during carcass feeding, and whether synergistic feeding activities may influence carcass decomposition. To this end, we compared the relatively large species Waldeckia obesa with the small species Cheirimedon femoratus, Hippomedon kergueleni, and Orchomenella rotundifrons during fish carcass feeding (Notothenia spp.). The experimental approach combined ex situ feeding experiments, behavioural observations, and scanning electron microscopic analyses of mandibles. Furthermore, we aimed to detect ecological drivers for distribution patterns of scavenging amphipods in the Antarctic coastal ecosystems of Potter Cove. In Potter Cove, the climate-driven rapid retreat of the Fourcade Glacier is causing various environmental changes including the provision of new marine habitats to colonise. While in the newly ice-free areas fish are rare, macroalgae have already colonised hard substrates. Assuming that a temporal dietary switch may increase the colonisation success of the most abundant lysianassoids C. femoratus and H. kergueleni, we aimed to determine their consumption rates (g food x g amphipods-1 x day-1) and preferences of macroalgae and fish. RESULTS: We detected two functional groups with different feeding strategies among scavenging amphipods during carcass feeding: carcass 'opener' and 'squeezer'. Synergistic effects between these groups were not statistically verified under the conditions tested. C. femoratus switched its diet when fish was not available by consuming macroalgae (about 0.2 day-1) but preferred fish by feeding up to 80% of its own mass daily. Contrary, H. kergueleni rejected macroalgae entirely and consumed fish with a maximal rate of 0.8 day-1. CONCLUSION: This study reveals functional groups in scavenging shallow-water amphipods and provides new information on coastal intraguild niche partitioning. We conclude that the dietary flexibility of C. femoratus is a potential ecological driver and central to its success in the colonisation of newly available ice-free Antarctic coastal habitats.

Push or Pull? The light-weight architecture of the Daphnia pulex carapace is adapted to withstand tension, not compression.

Daphnia (Crustacea, Cladocera) are well known for their ability to form morphological adaptations to defend against predators. In addition to spines and helmets, the carapace itself is a protective structure encapsulating the main body, but not the head. It is formed by a double layer of the integument interconnected by small pillars and hemolymphatic space in between. A second function of the carapace is respiration, which is performed through its proximal integument. The interconnecting pillars were previously described as providing higher mechanical stability against compressive forces. Following this hypothesis, we analyzed the carapace structure of D. pulex using histochemistry in combination with light and electron microscopy. We found the distal integument of the carapace to be significantly thicker than the proximal. The pillars appear fibrous with slim waists and broad, sometimes branched bases where they meet the integument layers. The fibrous structure and the slim-waisted shape of the pillars indicate a high capacity for withstanding tensile rather than compressive forces. In conclusion they are more ligaments than pillars. Therefore, we measured the hemolymphatic gauge pressure in D. longicephala and indeed found the hemocoel to have a pressure above ambient. Our results offer a new mechanistic explanation of the high rigidity of the daphniid carapace, which is probably the result of a light-weight construction consisting of two integuments bound together by ligaments and inflated by a hydrostatic hyper-pressure in the hemocoel. J. Morphol. 277:1320-1328, 2016. © 2016 Wiley Periodicals, Inc.