Folco Giomi

Improved heat tolerance in air drives the recurrent evolution of air-breathing

The transition to air-breathing by formerly aquatic species has occurred repeatedly and independently in fish, crabs and other animal phyla, but the proximate drivers of this key innovation remain a long-standing puzzle in evolutionary biology. Most studies attribute the onset of air-breathing to the repeated occurrence of aquatic hypoxia; however, this hypothesis leaves the current geographical distribution of the 300 genera of air-breathing crabs unexplained. Here, we show that their occurrence is mainly related to high environmental temperatures in the tropics. We also demonstrate in an amphibious crab that the reduced cost of oxygen supply in air extends aerobic performance to higher temperatures and thus widens the animals thermal niche. These findings suggest that high water temperature as a driver consistently explains the numerous times air-breathing has evolved. The data also indicate a central role for oxygen- and capacity-limited thermal tolerance not only in shaping sensitivity to current climate change but also in underpinning the climate-dependent evolution of animals, in this case the evolution of air-breathing.

A role for haemolymph oxygen capacity in heat tolerance of eurythermal crabs

Heat tolerance in aquatic ectotherms is constrained by a mismatch, occurring at high temperatures, between oxygen delivery and demand which compromises the maintenance of aerobic scope. The present study analyses how the wide thermal tolerance range of an eurythermal model species, the green crab Carcinus maenas is supported and limited by its ability to sustain efficient oxygen transport to tissues. Similar to other eurytherms, C. maenas sustains naturally occurring acute warming events through the integrated response of circulatory and respiratory systems. The response of C. maenas to warming can be characterized by two phases. During initial warming, oxygen consumption and heart rate increase, while stroke volume and haemolymph oxygen partial pressure decrease. During further warming, dissolved oxygen levels in the venous compartment decrease below the threshold of full haemocyanin oxygen saturation. The progressive release of haemocyanin bound oxygen with further warming follows an exponential pattern, thereby saving energy in oxygen transport and causing an associated leveling off of metabolic rate. According to the concept of oxygen and capacity limited thermal tolerance (OCLTT), this indicates that the thermal tolerance window is widened by the increasing contribution of haemocyanin oxygen transport and associated energy savings in cardiocirculation. Haemocyanin bound oxygen sustains cardiac performance to cover the temperature range experienced by C. maenas in the field. To our knowledge this is the first study providing evidence of a relationship between thermal tolerance and blood (haemolymph) oxygen transport in a eurythermal invertebrate.

Can respiratory physiology predict thermal niches

Predicting species responses to global warming is the holy grail of climate change science. As temperature directly affects physiological rates, it is clear that a mechanistic understanding of species vulnerability should be grounded in organismal physiology. Here, we review what respiratory physiology can offer the field of thermal ecology, showcasing different perspectives on how respiratory physiology can help explain thermal niches. In water, maintaining adequate oxygen delivery to fuel the higher metabolic rates under warming conditions can become the weakest link, setting thermal tolerance limits. This has repercussions for growth and scaling of metabolic rate. On land, water loss is more likely to become problematic as long as O2 delivery and pH balance can be maintained, potentially constraining species in their normal activity. Therefore, high temperatures need not be lethal, but can still affect the energy intake of an animal, with concomitant consequences for long‐term fitness. While respiratory challenges and adaptive responses are diverse, there are clear recurring elements such as oxygen uptake, CO2 excretion, and water homeostasis. We show that respiratory physiology has much to offer the field of thermal ecology and call for an integrative, multivariate view incorporating respiratory challenges, thermal responses, and energetic consequences. Fruitful areas for future research are highlighted.

Nothing in experimental biology makes sense except in the light of ecology and evolution – correspondence on J. Exp. Biol. 216, 2771-2782

‘Nothing in biology makes sense except in the light of evolution’ is a much cited message from a paper by Dobzhansky ([Dobzhansky, 1973][1]). It emphasizes that identifying the principles, similarities and differences of structures and functions between organisms, their families, phyla and

Quaternary structure and functional properties of Penaeus monodon hemocyanin

The hemocyanin of the tiger shrimp, Penaeus monodon, was investigated with respect to stability and oxygen binding. While hexamers occur as a major component, dodecamers and traces of higher aggregates are also found. Both the hexamers and dodecamers were found to be extremely stable against dissociation at high pH, independently of the presence of calcium ions, in contrast to the known crustacean hemocyanins. This could be caused by only a few additional noncovalent interactions between amino acids located at the subunit–subunit interfaces. Based on X‐ray structures and sequence alignments of related hemocyanins, the particular amino acids are identified. At all pH values, the p50 and Bohr coefficients of the hexamers are twice as high as those of dodecamers. While the oxygen binding of hexamers from crustaceans can normally be described by a simple two‐state model, an additional conformational state is needed to describe the oxygen‐binding behaviour of Penaeus monodon hemocyanin within the pH range of 7.0 to 8.5. The dodecamers bind oxygen according to the nested Monod–Whyman–Changeaux (MWC) model, as observed for the same aggregation states of other hemocyanins. The oxygen‐binding properties of both the hexameric and dodecameric hemocyanins guarantee an efficient supply of the animal with oxygen, with respect to the ratio between their concentrations. It seems that under normoxic conditions, hexamers play the major role. Under hypoxic conditions, the hexamers are expected not to be completely loaded with oxygen. Here, the dodecamers are supposed to be responsible for the oxygen supply.

The trade-off between heat tolerance and metabolic cost drives the bimodal life strategy at the air-water interface

The principle of oxygen and capacity limitation of thermal tolerance in ectotherms suggests that the long-term upper limits of an organisms thermal niche are equivalent to the upper limits of the organisms functional capacity for oxygen provision to tissues. Air-breathing ectotherms show wider thermal tolerances, since they can take advantage of the higher availability of oxygen in air than in water. Bimodal species move from aquatic to aerial media and switch between habitats in response to environmental variations such as cyclical or anomalous temperature fluctuations. Here we tested the prediction that bimodal species cope better with thermal stress than truly aquatic species using the crab Pachygrapsus marmoratus as a model species. When in water, oxygen consumption rates of P. marmoratus acutely rise during warming. Beyond a temperature threshold of 23 °C the crabs aerobic metabolism in air remains lower than in water. In parallel, the haemolymph oxygen partial pressure of submerged animals progressive decreases during warming, while it remains low but constant during emersion. Our results demonstrate the ability of a bimodal breathing ectotherm to extend its thermal tolerance during air-breathing, suggesting that there are temperature-related physiological benefits during the evolution of the bimodal life style.

Unusual oxygen binding behavior of a 24-meric crustacean hemocyanin.

Hemocyanins from Crustacea usually are found as 1x6 or 2x6-meric assemblies. An exception is the hemocyanin isolated from thalassinidean shrimps where the main component is a 24-meric structure. Our analysis of oxygen binding data of the thalassinidean shrimp Upogebia pusilla based on a three-state MWC-model revealed that despite the 24-meric structure the functional properties can be described very well based on the hexamer as allosteric unit. In contrast to the hemocyanins from other thalassinidean shrimps the oxygen affinity of hemocyanin from U. pusilla is increased upon addition of l-lactate. A particular feature of this hemocyanin seems to be that l-lactate already enhances oxygen affinity under resting conditions which possibly compensates the rather low intrinsic affinity observed in absence of l-lactate. The fast rate of oxygen dissociation might indicate that in this hemocyanin a higher cooperativity is less important than a fast response of saturation level to changes in oxygen concentration.

Thermal sensitivity of the crab Neosarmatium africanum in tropical and temperate mangroves on the east coast of Africa

Abstract Mangrove forests are amongst the tropical marine ecosystems most severely affected by rapid environmental change, and the activities of key associated macrobenthic species contribute to their ecological resilience. Along the east coast of Africa, the amphibious sesarmid crab Neosarmatium africanum (=meinerti) plays a pivotal role in mangrove ecosystem functioning through carbon cycling and sediment bioturbation. In the face of rapid climate change, identifying the sensitivity and vulnerability to global warming of this species is of increasing importance. Based on a latitudinal comparison, we measured the thermal sensitivity of a tropical and a temperate population of N. africanum, testing specimens at the centre and southern limit of its distribution, respectively. We measured metabolic oxygen consumption and haemolymph dissolved oxygen content during air and water breathing within a temperature range that matched the natural environmental conditions. The results indicate different thermal sensitivities in the physiological responses of N. africanum from tropical and temperate populations, especially during air breathing. The differences observed in the thermal physiology between the two populations suggest that the effect of global warming on this important mangrove species may be different under different climate regimes.

Temperature-induced phenotypic plasticity in the ovipositor of the invasive species Drosophila suzukii

Drosophila suzukii (Matsumura, 1931) is a highly successful invasive dipteran which represents a serious threat for global fruit industry. Among other adaptive traits, D. suzukii owes its success to the derived morphological features of its ovipositor, which allows the insect to exploit the exclusive ecological niche of fresh fruit, thus avoiding competition with other closely related species. With the aim of investigating temperature-induced phenotypic plasticity of D. suzukii ovipositor, we reared this insect in four different laboratory conditions, represented by the combination of two developmental temperatures and two diet regimes for the larvae. We recorded the effects of these two factors on ovipositor size and shape and overall body size through a combination of distance-based and geometric morphometric analyses. Results showed that insects attain the largest body sizes at lower temperature, whereas the diet does not determine significant difference in size. However, the effect on size of the two factors is less pronounced in the ovipositor, which shows a negative allometry with respect to body size in all treatments. At higher temperature, ovipositor shape tends also to co-vary with its own size. Neither temperature nor diet have significant effect on ovipositor bilateral fluctuating asymmetry. These results confirm the hypothesis that in D. suzukii the toughened valve of the ovipositor are subjected to effective morpho-functional constraints, while probably being under strong selection by reason of their mechanical role.

Prepupal diapause synchronizes adult emergence in the pine processionary moth Thaumetopoea pityocampa (Lepidoptera: Notodontidae): Processionary moth prepupal diapause

Insects with short‐lived adults must synchronize their emergence to maximize fitness. However, pre‐imaginal development time often varies among individuals as a result of exposure to varied abiotic and biotic factors; therefore, mechanisms adjusting pre‐imaginal development time are expected. Larvae of the pine processionary moth feed throughout the winter and conclude their development with characteristic processions in spring, leaving the trees to pupate in soil. The procession period can be as long as 2 months in some regions because of prior desynchronization of larval colonies, whereas the emergence period of the adults in summer remains short (less than 1 month). Through weekly sampling of larvae leaving trees to pupate in soil and subsequent rearing under field and laboratory conditions, it was observed that early prepupae waited longer than late prepupae before moulting into pupa. The differential duration of the prepupal stage was independent of temperature conditions and allowed resynchronization of colonies and overlapping emergences. The prepupal phase therefore appears to be critical for understanding the regulation of adult emergence of this important pest insect.