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 After more than 15 years, the data of my only unpublished PhD chapter are now finally published.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
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!
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.
After just three years, Falko Buschke‘s Erasmus Mundus PhD fellowship came to an end. Just months later he succesfully defended his PhD thesis. Initially drawn to Belgium with the prospect of doing a thesis on community dynamics with a lot of empirical work, Falko soon settled into a different niche. Making use of the IUCN database he set out to explain the distribution patterns of terrestrial vertebrates in Africa. For this he used a very diverse set of statistical tools. He reconstructed biogeographical patterns in Africa based on how species present in different locations respond to spatial and environmental gradients. He experimented with novel ways to define regional species pools and investigated the drivers of patterns of alpha and beta diversity. Finally, he also experimented with spreading dye models and built a neutral metacommunity model to explain different biogeographical patterns in this realm. Overall, it was an exciting journey exploring the interface between community ecology and macro ecology. Falko, it was great having you here. We will miss your wit and humour now you have returned to South Africa… and will continue to follow your adventures on http://solitaryecology.com/
Just two weeks later, Tom Pinceel joined Falko in the league of doctors. After doing a MSc working on genetic patterns in rock pool fairy shrimp, Tom continued along this path and started to explore the hatching strategies of these enigmatic inhabitants of temporary pools worldwide. Tom showed adaptive variation in hatching strategies of pool invertebrates along a gradient of habitat stability. He also revealed that the ancient diversification of fairy shrimp on the Australian continent coincided with a period of intense aridification. When Australia lost most of its rainforests, desert adapted fauna like fairy shrimps seem to have benefited and responded with a spectacular adaptive radiation. This resulted in a nice little booklet with most of his chapters already published. Tom is now continuing his research into delayed hatching as a survival strategy in extreme environments as a prospective post doc. We can only hope he will be able to continue his work in the near future.
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: