A general pattern in morphological antipredator plasticity? It is age- and sex-specific in the fathead minnow as well!

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 – a personality trait that is modified through perceived predation risk in the fathead minnow Pimephales promelas

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!

The location of alarm cues in Pelvicachromis taeniatus

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.

The variation of morphological plasticity across development and between sexes

Organisms can adapt their body to their environment within a single generation. This ability is called morphological plasticity (from old greek morphé „shape“ and lógos „study“ = „study of shape“). Examples for this ability in humans would be muscle development after exercise or getting a tan after sunbathing (melanin production).

Scientists have long assumed that the degree of this plasticity is something that remains constant across individual development and between sexes. However, new theories have recently been developed: following what would be optimal in nature, the degree of plasticity should be different at different developmental stages and dependent on the environment, either males or females should be able to change their morphology to a greater extent. As to date, no empirical research addressing this question existed, I used the slender krib (Pelvicachromis taeniatus) to test these assumptions in the context of morphological changes induced by alarm cues.

Alarm cues are passively released from injured fish and warn conspecifics about the presence of predators. The presence of alarm cues does not only lead to behavioral changes but in the long-term also modifies fish morphology. In the presence of alarm cues, the crucian carp (Carassisus carassius, Fig. a) develops a markedly different body shape characterized by a distinct increase in body depth (Fig. b). This makes it much more difficult for predators to handle and feed on such “defended” fish. Consequently, crucian carp with deep bodies have a lower risk to get eaten.

In my experiments, I exposed siblings of Pelvicachromis taeniatus from hatching onwards to either alarm cues or a control treatment, a treatment that was continued for their whole life in order to simulate the permanent presence of predators. Then, by taking photographs at pre-defined ages, I tracked fish body shape as well as fish color patterns at six developmental stages. Three of them were juvenile fish, the other three stages adults.

We found that alarm cue-exposed Pelvicachromis taeniatus altered both their body shape as well as their color pattern development. However, these changes were observable at only two developmental stages. First, they appeared at an early juvenile stage, only two weeks after hatching. Afterwards, these modifications disappeared, only to re-appear at the onset of sexual maturation and disappear again afterwards. This pattern matches the previously mentioned theoretical assumptions and thereby confirms the corresponding theories. Surprisingly, we also observed that only male fish altered their body whereas females did not. This may be because male Pelvicachromis taeniatus are larger than females and have to defend their territory from other animals. The most important morphological changes were accelerated growth in alarm cue-exposed juveniles and males as well as a paler color in males. A larger body makes it – similar to a deeper body – more difficult for predators to handle these fish. At the same time, the pale color makes the fish less conspicuous, which makes them more difficult to find to predators.

These results were published in the renowned journal The American Naturalist. Lay summaries of the article can be found in a press release of the same journal as well as in a press release of the University of Bonn. Moreover, this paper has been mentioned as an example for the excellence of research in Germany according to the German Federal Ministry of Education and Research .

Photo: © Christer Brönmark/Proceedings of the Royal Society B

Group living in animals – cooperation and conflict

Children are standing in front of the monkey enclosure at the zoo and watch a group of monkeys sitting together. They yell “How cute!”. Animals living together are not only cute to look at but group-living can also be beneficial. Animals that live in groups can better protect themselves from danger, find food together and support each other.

More animals, more eyes and ears
A lion stalking through high grass is almost invisible. However, with the help of several dozen eyes, antelopes can detect even such tiny movements. Numerous open ears can perceive the dry grass that is being crushed by the lion’s paws. A single antelope can’t do that because it has to lower its head to the ground to feed. In a group of antelopes, however, another animal can raise its head at the same time and monitor the area. If just a single animal notices a suspicious rustle in the grass, it can warn the other group members. Monkeys do the same – they warn each other of approaching leopards by screaming or noticeable movements. Sometimes, animals can even listen to warning calls of other species. In the rainforest, birds warn each other with alarm calls when leopards approach. Monkeys and other animals can listen in to these signals and are then informed about the leopard as well. The most common response to the presence of a predator is to escape.

Predator confusion through joint escape
Hundreds of legs, trampling in all directions at once – this view will confuse every predator. The predator needs to decide which prey to pursue. However, in large groups of escaping animals, individual animals are difficult to follow. So the predator needs time to focus, and this time is incredibly precious for the escaping animals. Every single step further away lowers the probability of being eaten. Additionally, a big group decreases the probability to get caught simply because of its numbers. If a predator catches a single animal from a group of ten, the risk for each animal to be that one is one tenth. However, if the size of the herd is a hundred animals, the probability to get caught and eaten is that much lower. Large aggregations of animals also prevent predators from finding them easily. This is because the groups gather within a few square meters in an area that may be several hectares in size. Roaming predators will thus less frequently find prey. However, even if a group is found, the group members will not always flee. Some species know how to defend themselves – be it with teeth, horns or claws.

Expelling predators through joint attack
Species armed with weapons are often able to hold their own against predators – especially when they are present in large numbers. One example is the buffalo, which can use its sturdy, large horns to put lions to flight. A single buffalo can be brought down by several lions. However, a dozen buffalos attacking can make even a group of lions leave without them having achieved anything. More intelligent animals like great apes know how to use tools for defence. With the help of long and tough sticks, groups of adult and aggressive chimpanzees even hunt leopards. In a study, researchers set up leopard dummies by covering a wooden scaffold with leopard skin. Subsequently, chimpanzees hit it aggressively with sticks and destroyed it completely. If this model had been a living leopard, its spine would have been shattered. Other apes throw objects for self-defence. They use stones, branches, fruits or any other tangible object to keep predatory cats or other dangerous animals away from their trees. The same happened to a researcher who was looking for monkeys. He found himself in a hail of fruit and eventually even a small monkey that was just within the reach of the angry ape was thrown at him. Hence, even as a predator, you cannot easily fool around with angry animals joining together in groups.

Finding food gets easier but also more difficult
More eyes make finding food easier. When food sources have high yield and are sparsely distributed, a single animal may have no hope of finding them on its own. Multiple animals however, can spread over a big area much more easily. However, if a tasty food source is found, an animal may try to benefit from it personally instead of telling other group members about it. This is especially pronounced if the amount of food is little. A quantity enough for a single animal can be only a drop in the ocean for a large group, leading to quarrels and aggressions over the meal. However, a cheating animal might easily be found out – after all, it smells like food after having enjoyed a tasty meal. The next time when the group looks for food, some other animals may inconspicuously follow the cheater and steal the next meal from it. Thus, living together can also cause conflicts and endanger the basic needs of individuals.

Fighting over mates
Not only food is a basic need of every living being. Reproduction is another. To continue the existence of its genes, every animal aims to have as many children as possible. In groups, this leads to single animals trying to monopolize the access to mates – strong and dominant individuals are likely to claim all fertile mates. This is because in the disputes over mates within a group, only the strongest animals will persevere. The dispute does not stop there. As soon as the strongest animals falls sick, becomes weak or gets old, the dispute starts anew. Living together thus is a never-ending source of conflicts – an issue that lone animals are not faced with.

Support in communities
Despite this competition, peaceful coexistence is possible. This is because in animal groups, members are often related to each other. Individual group members support each other in raising children and researchers have long wondered why they help so readily. When considering kinship, this is easy to explain. Relatives share genes and thus benefit from helping to raise offspring as well. Lonely siblings, aunts and grandmothers can thus use this opportunity to maximize the spread of their genes.

A paradise for parasites
Even when there are no squabbles between group members, other issues arise. One of these are tiny bacteria and parasites that make animals sick. Constant interaction between animals is exactly what these microbes like. Touching, sneezing , coughing or contact with poop transmits these parasites between individuals, which can then easily spread among the whole group. This phenomenon can collapse entire communities – which is what happened with the black plague during the Middle Age. On the other hand, continued contact with less lethal parasites in a group can lead to the formation of resistances within immune systems, causing all members to become immune to this disease easily.

The optimal group size
The advantages and disadvantages of group living are traded-off against each other, leading to an optimal group size for every population and its ecosystem. This number is affected by the amount of predators present, the abundance of food and potential mates as well as the incidence of disease, which can vary greatly even within nearby areas. Thus, in one area, a species can build solitary nests whereas in another, the same species can breed in groups of many hundreds of individuals.

In a zoo, however, good care can prevent most of the downsides of group living. Animal keepers stop predators from attacking the population, provide food in plentiful amounts and an even sex ratio. Additionally, veterinarians eradicate pathogens. Only this makes it possible for animals to be kept in large groups even within relatively small enclosures – much to the enjoyment of small children.

Transgenerational phenotypic plasticity – a DFG-funded research fellowship

As a consequence of my successful application to the German Research Foundation (DFG), I am pleased to announce that I have been awarded a two-year research fellowship (2017-2019) for the project “Transgenerational phenotypic plasticity in the cyprinid Pimephales promelas“, which I will tackle during a stay abroad in Canada.

While phenotypic plasticity – the adaptation of the appearance (phenotype) to the environment within a single generation has already been well researched – examples are the melanin production of the skin induced by solar radiation (UV radiation) or muscle growth induced by exercise – not much is known about transgenerational phenotypic plasticity. This term refers to the effects of an organism’s current environment on the phenotypes of future generations. This mechanism allows offspring to adapt to the environmental conditions of previous generations, to which they are likely exposed as well.

A well-known example of transgenerational plasticity in humans is a study published in the European Journal of Human Genetics by Kaati and colleagues in 2007. They found that men whose paternal grandfathers suffered from hunger as children during World War II have a shorter life expectancy. Transgenerational responses have also been observed in other animals and plants. In the presence of predators, the water flea Daphnia cucullata forms a large helmet and tail spine that prevents it from fitting into the mouth of predators easily. These effects are also observable in subsequent generations, as shown by a study from Nature by Agrawal and colleagues in 1999. The authors also found a similar effect in the field radish Raphanus raphanistrum: In the presence of herbivores, this plant produces more secondary plant substances that make it less palatable. This effect continued over generations even when no herbivore was present anymore.

In my previous research, I have studied the effects of predation risk on the behaviour and morphology of the cichlid Pelvicachromis taeniatus. Now I will be able to investigate in the fathead minnow Pimephales promelas to what extent the adaptations to predation risk affect future generations. To this end, I plan a large-scale breeding program in which clutches are split between two treatments in each generation over multiple generations. The offspring will be reared either under simulated high predation risk or under control conditions. First, in my experiments, I will separate the predator-induced transgenerational effects mediated by sperm and oocytes from the effects of an altered brood care caused by simulated high predation risk. Secondly, I will investigate the consequences of transgenerational plasticity over several generations. Here I will test the hypothesis that phenotypic plasticity favors the development of (genetic) adaptations. Third, I will compare the effects of paternal and maternal exposure to simulated predation to determine sex-specific inheritance during the transgenerational response. I will also compare the effects of directly perceived predation risk on offspring with the inherited transgenerational response.

I will carry out this project at the University of Saskatchewan in the workgroup of Prof. Douglas P. Chivers. More information can be found in the project description on GEPRIS (the “Funded Projects Information System” of the DFG) and the publications resulting from this project can be found in my profile on ResearchGate.


Logo: Official logo of the German Research Foundation (DFG)

Smoke and mirrors during the spider wedding

Prior to marriage, men often have to make an effort to convince their beloved. This is also the case with some animals – before they are willing to mate, some female animals demand a gift in the form of a dead prey animal from their admirers. The nursery web spider presents this nuptial gift inside a package of spider silk. Current research revealed that some clever spider males take advantage of this circumstance and wrap inedible objects in silk so as to obtain access to females with little effort. The Danish biologist Maria J. Albo and her colleagues investigated this interesting behaviour and reported on their findings in the scientific journal “BMC Evolutionary Biology”. In their experiments, they caught several young nursery web spiders (Pisaura mirabilis) and raised them in the laboratory. Subsequently, male spiders were given either a fresh fly or inedible objects of the same size such as a cotton ball, an apple blossom or the empty shell of an already eaten fly. The males wrapped each of these objects in silk and presented these gifts to females that were added shortly afterwards. When the females noticed that the male was carrying a gift, they approached it and allowed it to mate. However, the swindlers didn’t profit the same as honest spiders – females that found a worthless object after unwrapping the gift immediately stopped mating. Only the males that packaged fresh, juicy flies were allowed to mate with the females for a long time. Obviously, females attempt to punish cheating males. However, finding and catching an attractive piece of prey requires a lot of diligence and effort – which weak spider males rarely manage to do. If those instead wrap a worthless object, they may be able to exchange at least a little sperm with a female. Similarly, in humans, men often try to entrance women by offering fake objects as for example worthless jewellery – but until the women find out the truth, they may already be pregnant with the cheaters having escaped long ago.


Photo: © Lukas Jonaitis/flickr.com