Category: Research

Prescription rates for antidepressants are increasing year-by-year worldwide. At the same time, patients consuming antidepressants excrete a large proportion of these chemicals during their bowel movements. They thus end up in the sewage system, and wastewater treatment plants are unable to filter out these small molecules before forwarding the water into natural water bodies. Consequently, antidepressants and their metabolites are constantly accumulating in natural aquatic ecosystems. Two of the most widespread antidepressants at the moment are fluoxetine and venlafaxine. These chemicals are selective serotonin uptake inhibitors.

Many people are unaware of the consequences of the presence of antidepressants in freshwater ecosystems. Fish are vertebrates that have similar serotonergic systems as humans, making them susceptible to fluoxetine and venlafaxine. These antidepressants decrease the ability of fish to cope with predators, which gets them eaten frequently. They also negatively affect social behaviors – they make fish avoid conspecifics such as potential mates, and can furthermore make them display inappropriate aggression behaviors. The presence of these chemicals also prevents fish from reproducting properly – which leads to fewer offspring.

Furthermore, the consequences of antidepressant exposure are not restricted to a single generation – they are also passed down through the germline and can induce similar effects even in offspring that are themselves unexposed to antidepressants.

Such effects have concerning effects on fish populations in freshwater ecosystems – certain species may hardly reproduce anymore and disappear entirely. Predator populations that are then unable to find prey items may collapse shortly afterwards. This also concerns fishermen that may be unable to catch fish, which may be essential for their livelihood. Algal blooms may take over whole freshwater ecosystems if populations of fish species that forage on algae collapse.

Making people aware of these issues so as to curb the introduction of more antidepressants into freshwater ecosystems is thus of paramount importance.

Therefore, I would like to invite you to read our current review on this issue, which was recently published in Science of the Total Environment.

Photo: © Ajale/pixabay.com

Recently, I was able to publish a correspondence in Nature on the needs of deaf and hard-of-hearing researchers. After having read several published pieces in Nature that advertise virtual conferences as being more inclusive (see R. Joo, Nature 598, 257 (2021) and K. Powell, Nature 598, 221–223 (2021)), I felt that I had to clarify that virtual conferences can be exclusive to people with other disabilities as needs vary. Technological limitations concering camera quality particularly constrain deaf and hard-of-hearing researchers from participating in virtual conferences. Inclusiveness could thus be bolstered by meeting organizers including live captions during presentations and discussions. The article has already garnered attention on international social media.

Find the full article here: https://doi.org/10.1038/d41586-021-03487-2

Logo image: © nature.com

Transgenerational plasticity is a useful ability. To enable this process, parents collect information about their environment during their lifetime, and then pass this information down to offspring. This information then allows young animals to prepare themselves ideally to live in the same environment.

Over the last decades, many different ways how information can be transmitted across generations have been identified. For example, both mothers and fathers can transmit epigenetic marks (epialleles) together with their DNA within sperm and eggs. Mothers can also embed hormones within the eggs. Fathers can alter their seminal fluid. Furthermore, parents can communicate information to eggs by handling them differently during parental care. And lastly, offspring can also perceive their environment themselves.

Now, which information is more important? This has been a long unresolved question that I wanted to tackle in my research. For this purpose, I conducted a large experiment with the model system Pimephales promelas that forms shoals as a distinct social behavior. Under high predation risk, shoals are dense so that individuals are not getting eaten. However, as in other social animals, forming dense shoals also has disadvantages as it leads to more competition, less food and to greater transmission risk of pathogens – doing so is clearly not always optimal. Hence, like other animals these fish are known to adjust their shoaling density dependent on the level of perceived risk.

This trade-off between the costs and benefits of antipredator responses is what leads to a hypothesis developed by Lima and Bednekoff in 1999. This theory is called the risk allocation hypothesis. It predicts that when predation risk is constantly high, it is beneficial for individuals to respond with clear antipredator defenses only during immediate predator attacks, and not all the time as this would not allow individuals to gather enough food. In contrast, when predation risk is usually low, and individuals can forage all the time, which allows them to be full, it is better to respond to sudden predation events with clear, long-term antipredator responses. In a shoaling context, that means that when predation risk is believed to be high, shoals should be less responsive to a single risky event, but the opposite pattern should emerge in low-risk environments.

I exposed mothers, fathers, males that provided parental care (in this species parental care is solely provided by fathers) and offspring themselves to either high predation risk as communicated through exposure to alarm cues – or to low predation risk as simulated by exposure to tap water. Some of these treatments involved parental care while offspring were still inside eggs, others did not. By combining these treatments, I reached 12 different combinations and tested shoaling behavior in 2810 one-month old offspring. For this purpose, I assessed how close offspring swam to each other before and after a simulated predator attack.

Interestingly, treatments that involved parental care consistently caused offspring to form densest and least dense shoals, respectively. When the caring individual did not experience risk, offspring shoals were loose and were very sensitive to the simulated predator attack. However, when the male that provided care had perceived high predation risk prior to the care period, offspring formed dense shoals and were less sensitive to the simulated predator attack.

Without parental care, maternal experience with high risk was more important than paternal experience, but offspring responded most appropriately when both parents were exposed to either high or low risk. The risk information that offspring assessed themselves was only important when no risk information was transmitted from parents (i.e., when parents were never exposed to risk).
Taken together, this research highlights the high relative importance of parental care during the embryonal period (while offspring are still within their eggs) for the formation of optimal social behavior in the next generation. Many studies on transgenerational plasticity explicitly exclude parental care from their experimental design, and the results here show that this practice may lead to incorrect consequences regarding the relevance of transgenerational plasticity in allowing animals to cope with environmental change.

This study was published in Open Access format at BMC Ecology and Evolution. That means, it is freely available to everyone, and you are welcome to take a peek if you are interested in reading more details. It is the first transgenerational plasticity study that has arisen from my stay at the University of Saskatchewan, Canada – and more are to come.

Our immune systems are very effective at protecting us from many pathogens that can cause diseases. When we get injured or when foreign matter enters our bodies, the immune system reacts by producing cells and antibodies that attack and eliminate pathogens. As the vertebrate immune system can take many forms and shapes dependent on what is required for effective defenses against pathogens, it is clearly plastic.

But are vertebrate immune systems also able to prepare themselves for possible future injury long before injury, before any pathogen enters the bloodstream? To address this question, I conducted a long-term experiment on the cichlid Pelvicachromis taeniatus. Predator attacks are clearly known to cause injury, and it would be beneficial for individual immune systems to prepare ahead of time before a predator attack actually occurs – so they can respond faster to injury.

Over a four-year period, we exposed cichlids to either perceived high predation risk as communicated through conspecific alarm cues – which are perceived as an odor – or to a control treatment. Then, we sampled their blood, and assessed the number of different white blood cells.

Individuals that had been exposed to perceived predation risk had more white blood cells than controls. This was because they had almost twice as many lymphocytes as controls. Lymphocytes are the most frequent white blood cell type and include cells that directly attack and kill pathogens as well as those that produce antibodies. Thus, the presence of more lymphocytes in risk-exposed individuals suggests the immune system prepared itself for future injury.

However, the greater production of lymphocytes is not without cost. Greater cell multiplication rates also increase the risk of cancer such as leukemia. This is why it makes sense to boost lymphocyte production only when odors are perceived that suggest future attacks on the individual.

More detail about this study can be found at Oecologia, where it was recently published.

As a consequence of my successful application to the Bielefelder Nachwuchsfonds at Bielefeld University, I am pleased to announce that I have been awarded a one-year Bielefeld Young Researcher’s fund. This “career-bridge” stipend from Bielefeld University will allow me to prepare and submit proposals for 6-year future research projects on the snail Physella acuta and to complete the analysis as well as the publication of the vast amount of data that I have collected during my previous two-year research fellowship at the University of Saskatchewan in Canada.

Bisphenol A was widely used as an additive in the production of plastics until people became aware that it leaches from plastics into food and water, and has estrogen-disrupting effects in vertebrates. Thus, large parts of the plastics industry have replaced Bisphenol A with Bisphenol S (BPS), while sometimes explicitly advertising these products as “BPA-free”.

However, mounting evidence suggests that BPS may likewise have estrogen-mimicking effects and have detrimental effects on vertebrates. At the same time, incomplete elimination of this chemical by wastewater treatment plants led to the accumulation of BPS in aquatic ecosystems throughout the world.

We thus ventured out to test whether BPS concentrations that are present in natural environments have detrimental effects on the social behavior of zebrafish (Danio rerio).
For this purpose, we exposed adult zebrafish to different concentrations of BPS, to estradiol, and to a water control for 75 days. Afterwards, we investigated their shoaling behavior, their group preference and their activity. In addition, we assessed the effects of these treatments on mRNA expression of important neuropeptide signaling pathways within the zebrafish brain.
We found that exposure to Bisphenol S decreased shoaling density of exposed zebrafish. Furthermore, exposed fish were less interested in associating with conspecifics. This decreases the benefits of shoaling, which is, similar to other forms of animal grouping, mainly protection from predators. Activity was unaffected by BPS exposure.

Analysis of mRNA expression revealed that these changes may be consequences of BPS-disrupted isotocinergic and vasotoncinergic neuro-endocrine systems. Isotocin is the fish equivalent to oxytocin (a human hormone that is relevant for social bonding, reproduction, childbirth and the period following childbirth), and vasotocin is the fish equivalent of vasopressin (a human hormone suggested to also play a role in social behavior, sexual motivation and pair bonding).

If BPS-exposed fish are unable to cope with the presence of predators, whole fish populations may be eradicated, which is likely to have cascading effects on higher food-web levels. This showcases how the ubiquitous presence of BPS may have devastating effects on aquatic ecosystems – which may, among other consequences – crucially affect the livelihood of fishermen. We thus need to strive to reduce the use of not only BPA but also of BPS during the manufacturing process of plastics.

The detailed report of this experiment and a more specialized discussion can be found in our recent publication in Environmental Pollution.

Photo: © Steven Depolo

Happy new year!

This year, I will switch from my last research project at the University of Sackatchewan in Canada to a new host university: The Bielefeld University.

Here, in the Faculty of Biology – Evolutionary Biology I will be able to extend my research on the topic phenotypic plasticity by studying not only the phenotypic but also the genetic level. Here, I will be using the freshwater gastropod Physella acuta as a model system.

For this purpose, I will be working together with the world-renowned evolutionary biologist Prof. Klaus Reinhold as well as the likewise renowned evolutionary geneticist Prof. Joe Hoffman.

If you are interested in joining me at this lab, please feel free to contact me.

Following one of my last discoveries – that morphological plasticity follows age- and sex-specific patterns in the cichlid Pelvicachromis taeniatus – I was interested in whether the same patterns occur in the fathead minnow Pimephales promelas.

In my newest experiments, I exposed sibling groups of minnows to either alarm cues or a control treatment. Then I photographed individual fish at 18 days (at the end of larval development) and 180 days (at the onset of sexual maturation) age. Afterwards, I performed geometric morphometrics by using the IMP suite.

By using these tools I revealed first that already at the end of their larval development after just 18 days, juvenile minnows exposed to alarm cues had a distinctly deeper body as well as noticeably longer dorsal fin base lengths than did control fish. At 180 days age, we were able to observe a sex-specific response with only male but not female minnows responding morphologically to the presence of alarm cues. Males developed a deeper body shape as well as larger eyes. Females showed no morphological response at all. Interestingly, when we pooled results from both males and females, the effect of alarm cue exposure on fish morphology was still pronounced. This suggests first that the results from juvenile fish may be driven by a male-specific response as well. Second, the results from many previous studies on fish morphology where sexes had been pooled should be questioned – it may have been a strong sex-specific response in many of these cases as well. Nevertheless, most of these results match the outcome of our previous study, confirming our assumption that the observed age- and sex- specific patterns in morphology are likely to be a general pattern and not just an observation that is restricted to a single species.

This study has just been published in the open-access journal Scientific Reports. It is the third published study that has arisen from my stay at the University of Saskatchewan, Canada.

Boldness is a personality trait of animals that is widespread across many different species. The boldness-shyness continuum represents a fundamental axis of behavioral variation and has been in the center of attention of behavioral ecologists. When relating boldness to a predation context, differences in boldness between individuals can lead to a range of responses from predator ignorance to complete predator avoidance. While it has been known that boldness has a genetic component, it has also evolved to be markedly influenced by the environment, which makes boldness a plastic trait. This is because for example, it is not always advantageous to be bold in a predator-rich environment due to the risk of being eaten. Likewise, being shy in a predator-free environment does not offer many advantages due to the risk of losing when competing over food or mates with bolder individuals. At the same time, the ideal level of boldness also depends on body size. Small animals are growing quickly, have a small stomach and few fat reserves; thus they have a metabolic need to constantly search for food – this is not the case for larger individuals that have ample reserves. At the same time, smaller individuals have a higher risk of getting eaten – many different predators will readily feed on small animals. This is not the case for large animals, which may have only few predators, if any. Consequently, there is a relationship between body size and boldness, which has been theoretically predicted and observed in previous studies on natural fish populations. In predator-free rivers and lakes, boldness is size-dependent; smaller fish are bolder than larger individuals due to their increased need of finding food. However, in predator-rich ecosystems, the higher predation risk for smaller fish balances out this size-dependency, making small and large fish equally bold.

As previous studies on this topic have only been performed in natural habitats, they could not control for various confounding factors that may influence this result. First, predators may have eaten all the fish of a specific personality or a specific body size beforehand so that these fish could not be tested at the time of the experiments. Second, direct experience with predators, such as attacks that followed an inappropriate boldness response and were just narrowly escaped, may be responsible for shifts in personality. Third, as fish grow throughout their whole life, older fish are also larger and the observed “size-dependent” effects may be an effect of age instead. Older fish in natural predator-rich habitats simply have more experience with dealing with predators and are the only large fish that were actually able to survive until the time of the experiments.

To investigate whether the theoretically predicted and previously observed size-dependent boldness response is consistent even in the absence of these potentially confounding factors, I conducted a laboratory study. Here, I raised fathead minnows, Pimephales promelas under either simulated presence or absence of predators. To simulate predation risk, I applied alarm cues, which are released by injured fish and signal the presence of predators to conspecifics. From hatching onwards, I raised siblings under either continuous exposure to alarm cues or a control treatment. At 4 months age, I then assessed the boldness of individual fish in both treatments. I found that boldness was size-dependent only in fish from the control treatment. In alarm cue-exposed fish, this pattern was not present. These results are consistent with theoretical predictions and the previous studies in natural ecosystems and confirm that perceived predation risk alone can cause a plastic shift in boldness.

This study is the first published one that I have conducted during my abroad research fellowship at the University of Saskatchewan in Canada. The complete study is available in the journal Animal Behaviour. I hope you enjoyed the read!

When a fish is injured by a predator, its injuries release a cue that is recognized and avoided by conspecifics. This phenomenon was first observed by Karl von Frisch in 1938. In exploratory research, he cut the fish’s skin with a knife and found that other fish avoided the injured individual. Then, he also tested extracts from the fish liver, spleen, gonads or the heart with the same shoal and did not observe any response. An extract of fish muscle or the intestine instead caused intermediate responses. Numerous following efforts to reveal the chemical identity of these alarm cues have thus been focused on skin extracts and their chemical components. In 1961, Wolfgang Pfeiffer observed that the presence of club-shaped cells in the skin correlates with exploratory observations of an avoidance response towards skin extracts across species. These cells were now referred to as “club cells” and for decades assumed to contain these alarm cues.

However, recent studies have suggested that fish likewise show an avoidance or other anti-predator responses towards fish blood and fish muscle tissue. Hence, I set out to reveal the location of the alarm cues in the cichlid fish Pelvicachromis taeniatus. For this purpose, I prepared extracts from seven different tissue types (see above figure) and exposed conspecifics to these extracts. As a response, I measured individual activity, which usually decreases in the presence of predators so as to be less conspicuous. I also examined the skin of this species histologically. The results revealed that despite the presence of club cells in its skin, Pelvicachromis taeniatus responded most strongly towards muscle tissue extract. However, responses to muscle tissue were not very different from responses to the other extracts. This suggests that alarm cues are not located in only one part of the body but – in different concentrations – present throughout the whole fish body. This makes sense from an ecological perspective as attacking predators are unlikely to injure only one tissue in their prey.

These findings have been published in a special issue of Evolutionary Ecology Research as a contribution in honor of my recently retired doctorate supervisor Theo C.M. Bakker. I welcome you to also read the other articles within this special issue, all impressive studies written by former students of his.