Always nice to deal with unfinished business. After more than 15 years, the data of my only unpublished PhD chapter are now finally published. In the end it took us a physical model, a demographic model, two field experiments and three lab experiments to show that fairy shrimp can avoid extinctions by ensuring that their dormant eggs can hatch at various moments in the future and that this is an evolutionary risk spreading strategy.
Pinceel, T., Buschke, F., Geerts, A., Vanoverbeke, J., Brendonck, L., & Vanschoenwinkel, B. (2021). An empirical confirmation of diversified bet hedging as a survival strategy in unpredictably varying environments. Ecology. (SCI: 5.499), Q1
Tough decision making is not restricted to human societies. While male mosquitoes happily feed on the nectar in our gardens, female mosquitoes invade our bedrooms at night attracted by the proteins in our blood. They need this resource to produce eggs that are subsequently deposited in freshwater habitats where the larvae grow. However, not every pond or ditch is a good breeding ground and therefore gravid mosquitoes tend to be very picky. This is because mosquito larvae feature prominently on the menu of a whole range of predators such as fish and voracious larvae of water beetles and dragonflies. To ensure survival of their offspring, mosquito mums must therefore deposit their eggs in habitats where these killers are absent. It was already known that mosquitoes avoid the smell of fish when they are looking for a place to lay their eggs. However, in a new study in the journal Ecology Letters, we show that mosquitoes do not only avoid reproduction in local ponds that smell fishy, but also in neighboring fishless ponds in the surrounding landscape. Although several researchers have suggested that the smell of predators can be used as a chemical repellent to prevent mosquitoes from reproducing , we show that this may not work very well. If the smell of fish is everywhere, mosquitoes seem to be smart enough to realize that there are no better alternatives and happily lay their eggs, even if the environment smells fishy. Just like politicians, mosquitoes seem to be able to make compromises and, in the absence of better options, will settle for a bad deal.
It was the first time that this process, which in the specialized literature is known as habitat compromise, could be demonstrated in nature. Releasing fish is a classical strategy to control mosquitoes. However, this approach is controversial as many biting mosquitoes reproduce in habitats where fish cannot survive such as ephemeral pools, gutters, buckets and other containers where rainwater accumulates. Additionally, releasing fish in ponds has negative effects on the diversity of other organisms. For instance, in Western Europe, a number of rare dragonfly species and amphibians such as the tree frog and the crested newt, can only successfully reproduce when their larvae are not consumed by fish. Yet, even when fish cannot be released, there are perspectives for the application of predator smell for mosquito control. Artificial fish smell chemicals might help to concentrate mosquitoes in a few selected water bodies in a landscape where the eggs and larvae can be eradicated locally. From an environmental perspective it will certainly be preferable to spray large areas with fish chemicals rather than insecticides. However, further research will be needed to confirm whether such an approach is practically feasible. The exact volatile fish chemicals to which mosquitoes respond are also still unknown.
Annual fishes of the genus Nothobranchius are endemic to temporary ponds. When exposed nonlethally to a predation risk, their reproductive efforts are increased, likely to reproduce as much as possible before being predated upon.
This experiment was done by Arnout Grégoir, who recently defended his PhD. We are learning more about the interesting life histories of these remarkable vertebrates, that, in terms of certain life history aspects, have more in common with aquatic invertebrates than fish.
In a new paper Tom Pinceel shows that crustaceans from ephemeral water bodies have different egg hatching frequencies depending on local climatic conditions. If the climate is harsher and less predictable, a lower percentage of eggs hatches after rains. This ensures that more long lived eggs are left that may grow during future conditions!
sTURN Working Group: Does time drive space? Building a mechanistic linkage between spatial and temporal turnover in metacommunities
Bram recently met up with an international selection of ecologists in Leipzig to develop new ways to study metacommunity dynamics and gave a lecture at the German Centre for Integrative Biodiversity Research (iDiv) https://www.idiv.de/
Zooplankton dormant eggs are time capsules that can transport offspring to distant futures. However, after decades of study we still don’t know very well how this mechanism has evolved and how it works from a mechanistic point of view.
In new paper, Tom and I decided to use the VUB’s micro CT scanner to have a look at the internal structures of zooplankton resting eggs. Why would we want to? Well, in the past, the only way to look inside them was to freeze dry them, cut them and look at them with a scanning electrone microscope. This means that you’d have to kill the embryo and that the procedure might result in artefacts. You might see structures that don’t look that way in real life. Given that we are doing a lot of experiments on the evolutionary importance of differential hatching from resting eggs we were really keen to have a look at exactly what’s going on inside these eggs before they decide to hatch.
This pilot experiment showed that the method can yield useful images although the resolution is less than SEM. In addition it turns out that the embryos in the eggs also don’t seem to suffer too much from the X rays and most of them still hatch afterwards. More information, is likely to follow as soon as we can start to link embryonic and egg traits to the hatching behavior of eggs.
3D reconstructions of resting eggs obtained via X ray scanning. Top left: a cyst of the fairy shrimp Branschipodopsis wolfi, Top right: a cyst of the tadpole shrimp Triops. Bottom: an ephippium with two resting eggs of the water flea Daphnia magna.
In a new paper out in Scientific Reports, we use a matrix population model to test how sensitive populations of fairy shrimps are to changes in climate. The stepwise modeling procedure allows to calculate the long term population growth as a measure of fitness. If it is positive, the population will survive, if it is negative it will not. It does this by calculating, for each generation, how many eggs would be produced based on known life history traits of the species and a measure of environmental quality of the inundation (in this case represented by inundation length).
For most species it is very difficult to know how they would respond to changes in climate. However, for our fairy shrimp we have a lot of background information that allows us to make educated guesses about which life history traits could be important. We know for this species that it requires a specific amount of time to reproduce which is related to how long a pool can hold water and on the conditions they need to hatch. We also know how much eggs they can produce per day, how many eggs hatch during each inundation etc…
Population of the fairy shrimp Branchipodopsis wolfi in a temporary rock pool on a mountaintop in South Africa
The length of these inundations is one environmental parameter (of many) that will change under changing climates. But it is an important one that is directly linked to fitness. Shorter inundations means less inundations that are long enough for reproduction.
We were – and are – still ignorant about how these species will respond to these changes. However, the model does allow us to test which life history traits could be important to maintain long term survival of the populations. As such it shows which traits could help populations to survive.
One of the conclusions of the study is that, when inundations are short, it would be beneficial to make sure that a lower fraction of eggs would hatch during a given inundation. Such a mechanism could be an example of a risk spreading theory that is consistent with predictions of evolutionary bet hedging theory.
It is still a simplistic model, so it does not tell us how things will go in the future. It does not capture tradeoffs among life history traits nor the evolutionary potential of the populations. Yet, it still narrows down the range of possible future scenarios of these populations by showing what the consequences for population survival would be if populations could respond adaptively or plastically and change there life history traits.
In a new paper published in Freshwater Biology, PhD student Karen Tuytens builds further on a hydrological model for temporary pools I developed in my PhD. Temporary pools are expected to be strongly impacted by the effects of global environmental change. Being directly dependent on precipitation (and occasionally ground water) for filling, changes in precipitation and/or evaporation will have an impact on the length (hydroperiod) and the frequency of inundations.
The model that was developed is a realistic simulation model which can be parametrized for individual pools and which can predict the water levels on a day to day basis based on nothing but pool morphometry and precipitation and evaporation data. By making use of historic climate it is possible to reconstruct the inundation history of a pool and, hence, reconstruct the long term disturbance regime which is relevant to explain both patterns of diversity as well as adaptive trait variation among populations.
However, the main advantage explored in this paper is the ability to simulate the effects of different IPCC climate change scenarios on inundation patterns. Karen did not only show that inundations are likely to be become shorter resulting in shorter growing seasons for aquatic fauna, she also modeled connections that are formed between pools during heavy rains. Under future scenarios that include less precipitation and higher evaporation, these connections formed less frequently. Overall, this shows that climate change can not only affect habitat suitability but also connectivity in clusters of aquatic habitats. This is relevant since different levels of connectivity can have pronounced effects, not only on the persistence of populations but also on diversity and the functioning of metacommunities.
The code of the model is optimized for the R programming environment and is readily available in the appendix of the paper. At the moment, the model is optimized to work in very simple aquatic habitats such as rock pools which have no groundwater influence and don’t leak water. However, Karen is currently extending the model to make it applicable for more complex temporary aquatic habitats such as temporary wetlands.
In freshwater zooplankton, that survive unfavorable periods of winter cold or drought as dormant eggs in the sediment, light is an important cue that may activate the embryo to hatch. If no light is detectable then the egg is probably buried and it would be a bad idea to hatch. We investigated the light-activation process of zooplankton resting eggs using a rock-pool fairy shrimp as a model. We showed that light activation entails a relatively simple mechanism involving a light-energy threshold. These results illustrate the potential adaptive value of light activation but also highlighted the possible role of variation in eggshell pigmentation as a risk-spreading strategy. How does this work?
Much like a pair of sunglasses, the egg shell modulates how much light is absorbed. Consequently embryos in eggs with a darker egg shell should be less responsive to light. This is exactly what we found. In darker eggs, the embryo responds later, presumably because the light energy threshold is reached later. Given that there is often strong variation in the color of eggs in populations and in clutches of eggs, this simple ‘sunglasses effect’ can ensure that not all eggs will hatch at the same time. As a result the emerging larvae that use different food sources when they get older are less likely to compete with one another. As such, it could represent a simple, yet potentially effective risk spreading strategy.
While the effectiveness of this strategy within inundations was demonstrated, its potential role in spreading hatching over different inundations remains unknown. Tests are needed to assess whether degradation of pigments over time may be an adaptive mechanism that prevents resting eggs from becoming locked in diapause. Additionally, given the similarities in observed responses to light activation in both crustacean resting eggs and plant seeds, parallel patterns in these taxonomically distant groups might possibly reflect an old evolutionary mechanism tapping the same biochemical pathways, but this hypothesis also remains to be confirmed.
Picture of an adult male fairy shrimp of the species Branchipus schaefferi taken by Aline Waterkeyn
Fairy shrimp re-discovered in Belgium
Fairy shrimps (Crustacea, Anostraca) are specialized inhabitants of inland water bodies that periodically dry or freeze over. Tipped of by local conservationists we traveled to Hainaut and were able to confirm the first observation since 1997 of a member of this basal crustacean order in Belgium and the first sighting of the species Branchipus schaefferi Fischer, 1834 since 1930. Nineteen populations were found in a restricted area. The current study illustrates that populations of fairy shrimp can remain undetected, although individuals are relatively large (1 – 4 cm) and conspicuous and often characterized by bright coloration, and even in relatively well-studied and monitored regions, such as Belgium. Large branchiopods are threatened in many parts of the world and notably in Western Europe. The main reason for this is the loss of temporary aquatic habitats as a result of intensive agriculture and urbanisation, and the few remaining habitats are often degraded.
Fairy shrimp wheel track habitat
While public incentive to conserve a rare group of crustaceans may be limited, it is important to realize that temporary ponds not only house a unique crustacean fauna, but are also of vital importance for other endangered species of plants and animals (Williams, 2006). These include macrophytes, dragonflies and amphibians specifically linked with temporary waters. Substantial efforts and financial support have been directed at protecting certain endangered amphibians that use temporary ponds for breeding, such as the natterjack toad (Bufo calamita) and the fire bellied toad (Bombina bombina). Temporary pond restoration and construction projects performed for these ‘flagship’ species (e.g. EU life project Bombina) are likely to be beneficial for other typical temporary pond organisms too. For instance, different rare macrophytes were shown to re-emerge from old seed banks during pond restoration projects (Hilt et al., 2006). Due to the prolonged viability of their dormant eggs (Brendonck, 1996), it is not unlikely that large branchiopods may emerge from old egg banks present in the sediment. Consequently, a habitat oriented conservation strategy protecting the few remaining high quality temporary ponds and increasing temporary pond densities in the landscape is likely to be most beneficial as a large number of organism groups, including large branchiopods, will benefit from them.
Checking out wheel tracks and farmland ponds in the Binche area in Hainaut
Low predation pressure in combination with plenty of nutrients ensure that fairy shrimps can reach high population densities in temporary pools
Read more about the ecology of fairy shrimp and the remaining populations in Belgium in these publications: