The effect of ambient oxygen on the thermal performance of a cockroach, Nauphoeta cinerea

Authors: Emily J Lombardi, Candice L Bywater, and Craig R White

Published in: Journal of Experimental Biology


The oxygen and capacity-limited thermal tolerance (OCLTT) hypothesis proposes that the thermal tolerance of an animal is shaped by its capacity to deliver oxygen in relation to oxygen demand. Studies testing this hypothesis have largely focused on measuring short-term performance responses in animals under acute exposure to critical thermal maximums. The OCLTT hypothesis, however, emphasises the importance of sustained animal performance over acute tolerance.

The present study tested the effect of chronic hypoxia and hyperoxia during development on moderate to long-term performance indicators at temperatures spanning the optimal temperature for growth in the speckled cockroach, Nauphoeta cinerea.

In contrast to the predictions of the OCLTT hypothesis, development under hypoxia did not significantly reduce growth rate or running performance, and development under hyperoxia did not significantly increase growth rate or running performance. The effects of developmental temperature and oxygen on tracheal morphology and metabolic rate were also not consistent with OCLTT predictions, suggesting that oxygen delivery capacity is not the primary driver shaping thermal tolerance in this species.

Collectively, these findings suggest that the OCLTT hypothesis does not explain moderate to long-term thermal performance in N. cinerea, which raises further questions about the generality of the hypothesis.

Lombardi EJ, Bywater CL, White CR (2020) The effect of ambient oxygen on the thermal performance of a cockroach, Nauphoeta cinerea. Journal of Experimental Biology PDF DOI

You are what you eat, but does it matter when you eat it?

We all know the expression “you are what you eat” but do juvenile diets determine your adult size or can adult diets change things? Gonçalo Poças, Alexander Crosbie and Christen Mirth have used a model organism – the fruit fly Drosophila melanogaster – to explore this question.

They found that while larval nutritional conditions play the dominant role in determining both adult body weight and appendage size in D. melanogaster, the adult diet can adjust body weight as the flies age.

The team manipulated both the quality and energy quantity of diets that larval and adult flies received in two experiments.

In the first experiment calorie content was held stable but the ratio of protein to carbohydrate was either 1:2 (high quality) or 1:10 (low quality). In the second experiment flies were fed a high quality diet but with two different calorie contents. The low calorie content diet was 25% of the high calorie diet.

Importantly, larvae were reared on one of the two diets in each experiment and then after “eclosing” (emerging as an adult) they either remained on the same diet or were switched to the alternative diet. This allowed the researchers to tease apart at what life-stage diet was most influential in determining measures of adult size.

Adult weights, wing area and femur size were measured at 3, 10 and 17 days old. The team predicted that adult weight would be more influenced by adult diet but that wing area and femur size would be determined by larval diet.

Schematic of the experimental design. Larvae were fed alternative diets in two experiments that looked at the quality of the diet or the energy content of the diet. Once flies emerged as adults they were kept on the same diet or switched to the other diet and measures of size were taken at 3, 10 and 17 days.

For the most part, the team found that the larval diet contributed more to differences in adult weight, wing area, and femur size in both males and females, but the quality of the larval diet had greater effects on adult size than the calorie content.

In addition to the effects of larval diet on adult size traits, Gonçalo and his colleagues found that animals subjected to poor larval nutrition were able to increase their body weight if maintained on good quality diets during the adult stages.

One surprising result the team uncovered was that the adult femur size changed with age, and depended on both the larval and adult diet. This suggests that the size of adult appendages might not be as fixed as previously thought.

So, to return to our initial question. Yes, the juvenile diet is very important in determining measures of adult size, but adult diets can make up for nutritional deficiencies in earlier life to some extent – in fruit flies at least.

This research is currently in press in the Journal of Insect Physiology.

Can communities minimise energy wastage over time?

Understanding how energy is used (or not used) in individuals, populations and communities has fascinated biologists for many years. Giulia Ghedini, an Australian Research Council research fellow in the Centre for Geometric Biology, is particularly interested in how communities use energy. Giulia and her colleagues have found that older communities of marine phytoplankton waste less energy than new or early successional communities.

In a previous post, we described how Giulia and her colleagues used marine invertebrates to test whether ‘older’ communities minimised energy wastage as predicted by Robert MacArthur in 1969. MacArthur basically said that, due to competition for resources, a community of species will, over time, maximise the efficiency with which it consumes resources meaning that older communities have very little energy (resource) wastage.

If MacArthur was right, then we can better understand and predict how disturbances that change the age or successional stage of a community might impact community function and invasion risk.  An older community might be able to sustain a greater biomass with the same resource requirements of a younger community. Not only that, but a community that efficiently uses all the energy or resources available makes it difficult for a new species to gain a foothold.

While the team found some support for MacArthur’s theory in their initial study, it was far from clear-cut and they thought that this might be because their experimental setup allowed for predation and immigration; MacArthur’s theory relates to a closed system where competition between species is the driving force for community structure and function.

To tackle this problem Giulia and her colleagues designed a new experimental setup using a completely different system: marine phytoplankton. They were able to create ‘starter’ assemblages of phytoplankton in the lab. They used six species and then followed these assemblages through time measuring energy inputs (light and nutrients) and energy use (photosynthesis, metabolism and overall production). This allowed them to work out how much energy from resources was not used and how much was lost to maintenance  – metabolism and mortality – the two components of MacArthur’s ‘wastage’. They also tracked changes in species composition and the size structure of the communities to understand their links with energy wastage.

The team found some marked changes in the phytoplankton communities. Larger species became more dominant over time and this was consistent in all 20 of the experimental communities. Surprisingly, neither changes in dominant species nor the homogenisation of communities were driving changes in energy flux.

So, while the composition of the species changed in a consistent way as the communities ‘aged’, the functioning of communities tracked less consistently, meaning that the oldest communities were not necessarily the most energy efficient. But there was a general pattern that fitted with MacArthur’s prediction that older more established communities would minimise energy wastage. And, as predicted, the changes were due to the two components of energy use changing in opposite directions.

The combined results from the team’s work suggest that overall patterns in community function might be predictable over time and that MacArthur’s minimisation principle might apply across very different systems.

Tracking species composition and energy use through time enabled Giulia and her colleagues to see that as the community was better able to harvest and use the available resources so that resource waste decreased over time (green), more energy was lost to metabolism and death (magenta). The black line represents the community trade off between the ability to uptake and use resources and the costs of maintenance that this competitive ability requires.

This research was published in the journal Ecology.

The Conversation: From crocodiles to krill, a warming world raises the ‘costs’ paid by developing embryos

By Dustin Marshall

This article is republished from The Conversation under a Creative Commons licence.

Apart from mammals and birds, most animals develop as eggs exposed to the vagaries of the outside world. This development is energetically “costly”. Going from a tiny egg to a fully functioning organism can deplete up to 60% of the energy reserves provided by a parent.

In cold-blooded animals such as marine invertebrates (including sea stars and corals), fish and reptiles, and even insects, embryonic development is very sensitive to changes in the temperature of the environment.

Thus, in a warming world, many cold-blooded species face a new challenge: developing successfully despite rising temperatures.

For our research, published today in Nature Ecology and Evolution, we mined existing literature for data on how temperature impacts the metabolic and development rates of 71 different species, ranging from tropical crocodiles to Antarctic krill.

We found over time, species tend to fine-tune their physiology so that the temperature of the place they inhabit is the temperature needed to minimise the “costs” of their embryonic development.

Temperature increases associated with global warming could substantially impact many of these species.

The perfect weather to grow an embryo

The energy costs of embryonic development are determined by two key rates. The “metabolic” rate refers to the rate at which energy is used by the embryo, and the “development” rate determines how long it takes the embryo to fully develop, and become an independent organism.

Both of these rates are heavily impacted by environmental temperature. Any change in temperature affecting them is therefore costly to an embryo’s development.

Generally, a 10°C increase in temperature will cause an embryo’s development and metabolic rate to more than triple.

This photo shows a developing sea urchin, from egg (top left) to larva, to a metamorphosed (matured into adult form) individual.

These effects partially cancel each other out. Higher temperatures increase the rate at which energy is used (metabolic), but shorten the developmental time.

But do they balance out effectively?

What are the costs?

For any species, there is one temperature that achieves the perfect energetic balance between relatively rapid development and low metabolism. This optimal temperature, also called the “Goldilocks” temperature, is neither too hot, nor too cold.

When the temperature is too cold for a certain species, development takes a long time. When it’s too hot, development time decreases while the metabolic rate continues to rise. An imbalance on either side can negatively impact a natural population’s resilience and ability to replenish.

As an embryo’s developmental costs increase past the optimum, mothers must invest more resources into each offspring to offset these costs.

When offspring become more costly to make, mothers make fewer, larger offspring. These offspring start life with fewer energy reserves, reducing their chances of successfully reproducing as adults themselves.

Thus, when it comes to embryonic development, higher-than ideal temperatures pack a nasty punch for natural populations.

Since the temperature dependencies of metabolic rate and development rate are fairly similar, the slight differences between them had gone unnoticed until recently.

Embryos at risk

For each species in our study, we found a narrow band of temperatures that minimised developmental cost. Temperatures that were too high or too low caused massive blow-outs in the energy budget of developing embryos.

This means temperature increases associated with global warming are likely to have bigger impacts than previously predicted.

Predictions of how future temperature changes will affect organisms are often based on estimates of how temperature affects embryo survival. These measures suggest small temperature increases (1°C-2°C) do not reduce embryo survival by much.

But our study found the developmental costs are about twice as high, and we had underestimated the impacts of subtle temperature changes on embryo development.

In the warming animal kingdom, there are winners and losers

Some good news is our research suggests not all species are facing rising costs with rising temperatures, at least initially.

We’ve created a mathematical framework called the Developmental Cost Theory, which predicts some species will actually experience slightly lower developmental costs with minor increases in temperature.

In particular, aquatic species (fish and invertebrates) in cool temperate waters seem likely to experience lower costs in the near future. In contrast, certain tropical aquatic species (including coral reef organisms) are already experiencing temperatures that exceed their optimum. This is likely to get worse.

It’s important to note that for all species, increasing environmental temperature will eventually come with costs.

Even if a slight temperature increase reduces costs for one species, too much of an increase will still have a negative impact. This is true for all the organisms we studied.

A key question now is: how quickly can species evolve to adapt to our warming climate?The Conversation

Developmental cost theory predicts thermal environment and vulnerability to global warming

Authors: Dustin J Marshall, Amanda K Pettersen, Michael Bode, and Craig R White

Published in: Nature Ecology & Evolution


Metazoans must develop from zygotes to feeding organisms. In doing so, developing offspring consume up to 60% of the energy provided by their parent.

The cost of development depends on two rates: metabolic rate, which determines the rate that energy is used; and developmental rate, which determines the length of the developmental period. Both development and metabolism are highly temperature-dependent such that developmental costs should be sensitive to the local thermal environment.

Here, we develop, parameterize and test developmental cost theory, a physiologically explicit theory that reveals that ectotherms have narrow thermal windows in which developmental costs are minimized (Topt).

Our developmental cost theory-derived estimates of Topt predict the natural thermal environment of 71 species across seven phyla remarkably well (R2⁓0.83).

Developmental cost theory predicts that costs of development are much more sensitive to small changes in temperature than classic measures such as survival. Warming-driven changes to developmental costs are predicted to strongly affect population replenishment and developmental cost theory provides a mechanistic foundation for determining which species are most at risk. Developmental cost theory predicts that tropical aquatic species and most non-nesting terrestrial species are likely to incur the greatest increase in developmental costs from future warming.

Marshall DJ, Pettersen AK, Bode M, White CR (2020) Developmental cost theory predicts thermal environment and vulnerability to global warming. Nature Ecology & Evolution PDF DOI

Community efficiency during succession: a test of MacArthur’s minimization principle in phytoplankton communities

Authors: Giulia Ghedini, Michel Loreau, and Dustin J Marshall

Published in: Ecology


Robert MacArthur’s niche theory makes explicit predictions on how community function should change over time in a competitive community. A key prediction is that succession progressively minimizes

the energy wasted by a community, but this minimization is a trade‐off between energy losses from unutilised resources and costs of maintenance. By predicting how competition determines community efficiency over time MacArthur’s theory may inform on the impacts of disturbance on community function and invasion risk.

We provide a rare test of this theory using phytoplankton communities, and find that older communities wasted less energy than younger ones but that the reduction in energy wastage was not monotonic over time. While community structure followed consistent and clear trajectories, community function was more idiosyncratic among adjoining successional stages and driven by total community biomass rather than species composition.

Our results suggest that subtle shifts in successional sequence can alter community efficiency and these effects determine community function independently of individual species membership.

We conclude that, at least in phytoplankton communities, general trends in community function are predictable over time accordingly to MacArthur’s theory. Tests of MacArthur’s minimization principle across very different systems should be a priority given the potential of this theory to inform on the functional properties of communities.

Ghedini G, Loreau M, Marshall DJ (2020) Community efficiency during succession: a test of MacArthur’s minimization principle in phytoplankton communities. Ecology PDF DOI

When does diet matter? The roles of larval and adult nutrition in regulating adult size traits

Authors: Gonçalo M Poças, Alexander E Crosbie, and Christen K Mirth

In press in: Journal of Insect Physiology (preprint)


Adult body size is determined by the quality and quantity of nutrients available to animals. In insects, nutrition affects adult size primarily during the nymphal or larval stages. However, measures of adult size like body weight are likely to also change with adult nutrition.

In this study, we sought to the roles of nutrition throughout the life cycle on adult body weight and the size of two appendages, the wing and the femur, in the fruit fly Drosophila melanogaster.

We manipulated nutrition in two ways: by varying the protein to carbohydrate content of the diet, called macronutrient restriction, and by changing the caloric density of the diet, termed caloric restriction. We employed a fully factorial design to manipulate both the larval and adult diets for both diet types.

We found that manipulating the larval diet had greater impacts on all measures of adult size. Further, macronutrient restriction was more detrimental to adult size than caloric restriction. For adult body weight, a rich adult diet mitigated the negative effects of poor larval nutrition for both types of diets. In contrast, small wing and femur size caused by poor larval diet could not be increased with the adult diet.

Taken together, these results suggest that appendage size is fixed by the larval diet, while those related to body composition remain sensitive to adult diet. Further, our studies provide a foundation for understanding how the nutritional environment of juveniles affects how adults respond to diet.

Poças GM, Crosbie AE, Mirth CK (2019) When does diet matter? The roles of larval and adult nutrition in regulating adult size traits. Journal of Insect Physiology PDF DOI


Are there any advantages to being smaller in higher temperatures?

Biologists have been familiar with a pattern of smaller body sizes with increasing temperatures for a long time, in fact, so familiar that Bergmann dubbed a “Temperature-Size Rule” in 1847.

Like many things to do with size, it is difficult to separate the effects of temperature on size from other traits that co-vary with size; metabolism for example. It may be that higher temperatures cause the evolution of faster metabolic rates and metabolic rate is genetically correlated with size. So that it is, in fact, metabolic rate that is the target of selection, not size.

Martino Malerba and Dustin Marshall were again able to take advantage of the evolved large and small algal cells to see if they could unambiguously assign any effects of temperature on size, to size alone. They wanted to find out if (and how) temperature affected fitness for different sized organisms.

To do this they used algal cells that had experienced 290 generations of artificial selection and where large selected cells were 13 times bigger than small selected cells. They then exposed these different lines (including the control lines) to three temperatures 18 °C, 22 °C and 26 °C and measured cell size, population density and cell production rates after three and six days.

They found that the smaller cells did better at higher temperatures; that is, the fitness proxies of cell production rate and population densities were both greater for small cells at higher temperatures. This means that Martino and Dustin have shown that size on its own can affect performance across different temperatures.

They then wanted to know why are cells smaller at higher temperatures; what is the advantage? It has long been thought that smaller cells do better in warmer temperatures because they have a greater surface-area to volume ratio. This would make them better able to take up resources such as nutrients, CO2 and light at the same time as increasing temperatures increase a cell’s demand for resources through increased enzyme activity and protein synthesis.

If this was the case, Martino and Dustin expected the large and small cells to show differences in performance at higher temperatures when resources were abundant (days 0 to 3) compared to when resources were depleted (days 3 to 6). But they found no difference in the fitness of large and small cells that related to resources suggesting that advantages of smaller cells at higher temperatures was not related to a greater surface-area to volume ratio.

Instead they measured the concentrations of reactive oxygen species in their selected lines of large and small cells. Reactive oxygen species are known to increase oxidative stress, damage DNA and so reduce the performance of a cell and also accumulate at higher temperatures. Martino found that the larger cells had almost five times more reactive oxygen species than smaller cells. And the larger cells had relatively smaller nuclei, meaning that there was twice the reactive oxygen species loading around the nuclei in large selected cells.

Martino and Dustin think that it is likely that small cells do better at higher temperatures, not because they are able to access more resources per unit volume, but because they are less prone to toxicity from reactive oxygen species.

This research was published in the journal Evolution.

Effects of two years of artificial size-selection (290 generations) on the cell volume of a phytoplankton species (Dunaliella tertiolecta).
Fitness increased with temperature (positive slope) in small-selected algae and decreased with temperature (negative slope) in large-selected algae. This finding confirms that reducing the size of a species automatically provides a fitness benefit at warmer temperatures.

Testing the drivers of the temperature-size covariance using artificial selection

Authors: Martino E Malerba, and Dustin J Marshall

Published in: Evolution


Body size often declines with increasing temperature. Although there is ample evidence for this effect to be adaptive, it remains unclear whether size shrinking at warmer temperatures is driven by specific properties of being smaller (e.g., surface to volume ratio) or by traits that are correlated with size (e.g., metabolism, growth).

We used 290 generations (22 months) of artificial selection on a unicellular phytoplankton species to evolve a 13‐fold difference in volume between small‐selected and large‐selected cells and tested their performance at 22 °C (usual temperature), 18 °C (−4), and 26 °C (+4).

Warmer temperatures increased fitness in small‐selected individuals and reduced fitness in large‐selected ones, indicating changes in size alone are sufficient to mediate temperature‐dependent performance.

Our results are incompatible with the often‐cited geometric argument of warmer temperature intensifying resource limitation. Instead, we find evidence that is consistent with larger cells being more vulnerable to reactive oxygen species. By engineering cells of different sizes, our results suggest that smaller‐celled species are pre‐adapted for higher temperatures.

We discuss the potential repercussions for global carbon cycles and the biological pump under climate warming.

Malerba ME, Marshall DJ (2019) Testing the drivers of the temperature-size covariance using artificial selection. Evolution PDF DOI

Water temperatures and viscosity will both change with ocean warming but how will they affect male fertility in the tubeworm Galeolaria?

Global warming will increase ocean temperatures at the same time as it reduces seawater viscosity and Evatt Chirgwin wanted to know how this combination of physiological and physical change would affect male fertility in a small tubeworm. He found that both these factors independently reduced male fertility, and together altered selection pressures on sperm morphology.

Most marine species release gametes into the water column and successful fertilisation depends on a sperm locating and fusing with an egg. This high-risk strategy is in stark contrast with many terrestrial species where sperm and eggs interact in the controlled environment of a female reproductive tract, making marine species more vulnerable to global warming.

Projected ocean temperature increases are expected to reduce male fertility because exposure to temperatures outside the usual range can disrupt physiological processes and cell function. But the viscosity or ‘thickness’ of the seawater will also change with increasing temperatures, and Evatt was interested in understanding how the fact that sperm are able to move more easily through the water would affect male fertility.

Because these two things tend to change together, up until now no one has considered how decreases in viscosity at higher temperatures might alter fertility as well as selection pressure on sperm structure. Sperm with larger heads have increased ‘drag’ while a long tail can increase swimming speeds – these might not matter so much when seawater is easier to pass through.

So how do temperature and viscosity affect male fertility and the selection forces acting on the size and shape of sperm? Evatt and his supervisors (Keyne Monro and Dustin Marshall) measured fertilisation success at three temperatures and used a hydrophilic polymer that allows warmer water to be adjusted to the same viscosity as cooler water (but not the other way around).

Evatt measured head size, midpiece size and tail length in the sperm of 157 males that had access to eggs from a variety of females in five different fertilisation environments.

Evatt manipulated both temperature and viscosity to give five fertilisation environments for the 157 males that he had measured head size, midpiece size and tail length in the sperm. Sperm from each male added to eggs from a number of different females in each of the five environments and fertilisation success recorded.

The team found that the isolated effects of temperature and viscosity each caused fertility to decline by around 5% from current to moderate warming and by another 5% from moderate to extreme warming. But temperature and viscosity acted together to alter selection on sperm morphology. The ‘midpiece’ that houses the mitochondria, was a target for selection at the projected, warmer environments. A shorter midpiece was favoured in moderate warming environments, while a wider midpiece was favoured at the more extreme, longer-term projections of warming.

Sperm midpiece size was a target of selection with both temperature and viscosity acting in combination. Narrower midpieces are favoured by current conditions, shorter midpieces are favoured by projected warming environments and more extreme or longer term warming favoured wider midpieces.

Evatt and his supervisors think that since the midpiece contain the mitochondria that provide energy, it is probable that changes in temperature and viscosity will change the energy requirements of sperm during the location and fertilisation of eggs.

For the first time, the team show how projected changes in water temperature and viscosity may impact the fertility of marine populations and expose sperm to novel evolutionary pressures that may drive them to adapt in response.

This research was published in the journal Functional Ecology.