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14 Dec 2023
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Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxia

Future oceanic conditions could leave sponge holobionts breathless – but they won’t let that stop them

Recommended by ORCID_LOGO based on reviews by Maria Lopez Acosta and 2 anonymous reviewers

It is now widely accepted that anthropogenic climate change is a severe threat to biodiversity, ecosystem function and associated ecosystem services. Assessing the vulnerability of species and predicting their response to future changes has become a priority for environmental biology (Williams et al. 2020).

Over the last few decades, oxygen concentrations in both the open ocean and coastal waters have been declining steadily as the result of multiple anthropogenic activities. This global trends towards hypoxia is expected to continue in the future, causing a host of negative effects on marine ecosystems. Oxygen is indeed crucial to many biological processes in the ocean, and its decrease could have strong impacts on biogeochemical cycles, and therefore on marine productivity and biodiversity (Breitburg et al. 2018).

Whenever facing such drastic environmental changes, all organisms are expected to have some intrinsic ability to adapt. At shorter than evolutionary timescales, ecological plasticity and the eco-physiological processes that sustain it could constitute important adaptive mechanisms (Williams et al. 2020)

Marine sponges seem particularly well-adapted to oxygen deficiency, as some species can survive seasonal anoxia for several months. This paper by Strehlow et al. (2023) examines the mechanisms allowing this exceptional tolerance. Focusing on two species of sponges, they used transcriptomics to assess how gene expression by sponges, by their mitochondria, or by their unique and species-specific microbiome could facilitate this trait. Their results suggest that sponge holobionts maintain metabolic activity under anoxic conditions while displaying shock response, therefore not supporting the hypothesis of sponge dormancy. Furthermore, hypoxia and anoxia seemed to influence gene expression in different ways, highlighting the complexity of sponge response to deoxygenation. As often, their exciting results raise as many questions as they provide answers and pave the way for more research regarding how anoxia tolerance in marine sponges could give them an advantage in future oceanic environmental conditions.

References

Breitburg et al. (2018): Declining oxygen in the global ocean and coastal waters. Science 359, eaam7240. https://doi.org/10.1126/science.aam7240 

Strehlow et al. (2023): Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxia. bioRxiv, 2023.02.27.530229, ver. 4 peer-reviewed and recommended by Peer Community in Zoology.  https://doi.org/10.1101/2023.02.27.530229 

Williams et al. (2008) Towards an Integrated Framework for Assessing the Vulnerability of Species to Climate Change. PLOS Biology 6(12): e325. https://doi.org/10.1371/journal.pbio.0060325 

Williams et al. (2020):  Research priorities for natural ecosystems in a changing global climate. Global Change Biology 26: 410–416. https://doi.org/10.1111/gcb.14856 

Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxiaBrian W Strehlow, Astrid Schuster, Warren R Francis, Lisa Eckford-Soper, Beate Kraft, Rob McAllen, Ronni Nielsen, Susanne Mandrup, Donald E Canfield<p>Deoxygenation can be fatal for many marine animals; however, some sponge species are tolerant of hypoxia and anoxia. Indeed, two sponge species, <em>Eurypon </em>sp. 2 and <em>Hymeraphia stellifera</em>, survive seasonal anoxia for months at a ...Biology, Ecology, Genetics/Genomics, Invertebrates, Marine, SymbiosisLoïc N. Michel Maria Lopez Acosta2023-05-12 16:22:47 View
27 Apr 2023
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Brood thermoregulation effectivenessis positively linked to the amount of brood but not to the number of bees in honeybee colonies

Precision and accuracy of honeybee thermoregulation

Recommended by ORCID_LOGO based on reviews by Jakob Wegener and Christopher Mayack

The Western honeybee, Apis mellifera L., is one of the best-studied social insects. It shows a reproductive division of labour, cooperative brood care, and age-related polyethism. Furthermore, honeybees regulate the temperature in the hive. Although bees are invertebrates that are usually ectothermic, this is still true for individual worker bees, but the colony maintains a very narrow range of temperature, especially within the brood nest. This is quite important as the development of individuals is dependent on ambient temperature, with higher temperatures resulting in accelerated development and vice versa. In honeybees, a feedback mechanism couples developmental temperature and the foraging behaviour of the colony and the future population development (Tautz et al., 2003). Bees raised under lower temperatures are more likely to perform in-hive tasks, while bees raised under higher temperatures are better foragers. To maintain optimal levels of worker population growth and foraging rates, it is adaptive to regulate temperature to ensure optimal levels of developing brood. Moreover, this allows honeybees to decouple the internal developmental processes from ambient temperatures enhancing the ecological success of the species. 

In every system of thermoregulation, whether it is endothermic under the utilization of energetic resources as in mammals or the honeybee or ectothermic as in lower vertebrates and invertebrates through differential exposure to varying environmental temperature gradients, there is a need for precision (low variability) and accuracy (hitting the target temperature). However, in honeybees, the temperature is regulated by workers through muscle contraction and fanning of the wings and thus, a higher number of workers could be better at achieving precise and accurate temperature within the brood nest. Alternatively, the amount of brood could trigger responses with more brood available, a need for more precise and accurate temperature control. The authors aimed at testing these two important factors on the precision and accuracy of within-colony temperature regulation by monitoring 28 colonies equipped with temperature sensors for two years (Godeau et al., 2023).

They found that the number of brood cells predicted the mean temperature (accuracy of thermoregulation). Other environmental factors had a small effect. However, the model incorporating these factors was weak in predicting the temperature as it overestimated temperatures in lower ranges and underestimated temperatures in higher ranges. In contrast, the variability of the target temperature (precision of thermoregulation) was positively affected by the external temperature, while all other factors did not show a significant effect. Again, the model was weak in predicting the data. Overall colony size measured in categories of the number of workers and the number of brood cells did not show major differences in variability of the mean temperature, but a slight positive effect for the number of bees on the mean temperature. 

Unfortunately, the temperature was a poor predictor of colony size. The latter is important as the remote control of beehives using Internet of Things (IoT) technologies get more and more incorporated into beekeeping management. These IoT technologies and their success are dependent on good proxies for the control of the status of the colony. Amongst the factors to monitor, the colony size (number of bees and/or amount of brood) is extremely important, but temperature measurements alone will not allow us to predict colony sizes. Nevertheless, this study showed clearly that the number of brood cells is a crucial factor for the accuracy of thermoregulation in the beehive, while ambient temperature affects the precision of thermoregulation. In the view of climate change, the latter factor seems to be important, as more extreme environmental conditions in the future call for measures of mitigation to ensure the proper functioning of the bee colony, including the maintenance of homeostatic conditions inside of the nest to ensure the delivery of the ecosystem service of pollination.

REFERENCES

Godeau U, Pioz M, Martin O, Rüger C, Crauser D, Le Conte Y, Henry M, Alaux C (2023) Brood thermoregulation effectiveness is positively linked to the amount of brood but not to the number of bees in honeybee colonies. EcoEvoRxiv, ver. 5 peer-reviewed and recommended by Peer Community in Zoology. https://doi.org/10.32942/osf.io/9mwye 

Tautz J, Maier S, Claudia Groh C, Wolfgang Rössler W, Brockmann A (2003) Behavioral performance in adult honey bees is influenced by the temperature experienced during their pupal development. PNAS 100: 7343–7347. https://doi.org/10.1073/pnas.1232346100

Brood thermoregulation effectivenessis positively linked to the amount of brood but not to the number of bees in honeybee coloniesUgoline Godeau, Maryline Pioz, Olivier Martin, Charlotte Rüger, Didier Crauser, Yves Le Conte, Mickael Henry, Cédric Alaux<p style="text-align: justify;">To ensure the optimal development of brood, a honeybee colony needs to regulate its temperature within a certain range of values (thermoregulation), regardless of environmental changes in biotic and abiotic factors....Biology, Conservation biology, Demography/population dynamics, Ecology, InsectaMichael Lattorff Mauricio Daniel Beranek2022-07-06 09:20:10 View
02 Nov 2021
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Cuckoo male bumblebees perform slower and longer flower visits than free-living male and worker bumblebees

Cuckoo bumblebee males might reduce plant fitness

Recommended by ORCID_LOGO based on reviews by Patrick Lhomme, Silvio Erler and 2 anonymous reviewers

In pollinator insects, especially bees, foraging is almost exclusively performed by females due to the close linkage with brood care. They collect pollen as a protein- and lipid-rich food to feed developing larvae in solitary and social species. Bees take carbohydrate-rich nectar in small quantities to fuel their flight and carry the pollen load. To optimise the foraging flight, they tend to be flower constant, reducing the flower handling time and time among individual inflorescences (Goulson, 1999). Males of pollinator species might be found on flowers as well. As they do not collect any pollen for brood care, their foraging flights and visits to flowers might not be shaped by the selective forces that optimise the foraging flights of females. They might stay longer in individual flowers, take up nectar if needed, but might unintentionally carry pollen on their body surface (Wolf & Moritz, 2014).
 
Bumblebees are excellent pollinators (Goulson, 2010), and a few species are exploited commercially for their delivery of pollination services (Velthuis & van Doorn, 2006). However, a monophyletic group of socially parasitic species – cuckoo bumblebees – has evolved amongst the bumblebees, lacking a worker caste. Cuckoo bee gynes usurp nests of free-living bumblebees, kill the resident queen, and forces the host workers to rear their offspring consisting of gynes and males (Lhomme & Hines, 2019). The level of affected colonies in an area can be up to 42% (Erler & Lattorff, 2010).
 
The behaviour of the cuckoo bumblebees, especially that of the males, has been rarely studied. The present study by Fisogni et al. (2021) has targeted the flower-visiting behaviour of workers and males of free-living bumblebees and males of the cuckoo species. They used behavioural observations of flower-visiting insects on Gentiana lutea, a plant from south-eastern Europe with yellow flowers arranged in whorls. While all three groups of bees visited the same number of plants, males of both types visited more flowers within a whorl, but cuckoo males spent more time on flowers within a whorl and the whole plant than the free-living bumblebees.
 
The flower visits of bumblebee workers are optimised, aiming at collecting as much pollen as possible within a short time frame. This, in turn, has consequences for the pollination process by enhancing cross-pollination between different plants. By contrast, males and especially cuckoo bumblebee males, are not selected for an optimised foraging pattern. Instead, they spend more time on flowers, eventually resulting in higher levels of pollen transfer within a plant (geitonogamy), which might lead to reduced plant fitness. This is the first study to relate the foraging behaviour of cuckoo bumblebees to pollination and plant fitness.
 
References
 
Erler, S., & Lattorff, H. M. G. (2010). The degree of parasitism of the bumblebee (Bombus terrestris) by cuckoo bumblebees (Bombus (Psithyrus) vestalis). Insectes sociaux, 57(4), 371-377. https://doi.org/10.1007/s00040-010-0093-2
 
Fisogni, A., Bogo, G., Massol, F., Bortolotti, L., Galloni, M. (2021). Cuckoo male bumblebees perform slower and longer flower visits than free-living male and worker bumblebees. Zenodo, 10.5281/zenodo.4489066, ver. 1.2 peer-reviewed and recommended by PCI Zoology. https://doi.org/10.5281/zenodo.4489066
 
Goulson, D. (1999). Foraging strategies of insects for gathering nectar and pollen, and implications for plant ecology and evolution. Perspectives in plant ecology, evolution and systematics, 2(2), 185-209. https://doi.org/10.1078/1433-8319-00070
 
Goulson, D. (2010). Bumblebees. Behaviour, Ecology, and Conservation, 2nd edn. Oxford University Press, Oxford.
 
Lhomme, P., Hines, H. M. (2019). Ecology and evolution of cuckoo bumble bees. Annals of the Entomological Society of America, 112, 122-140. https://doi.org/10.1093/aesa/say031
 
Velthuis, H. H. W., van Doorn, A. (2006). A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie, 37, 421-451. https://doi.org/10.1051/apido:2006019
 
Wolf, S., Moritz, R. F. A. (2014). The pollination potential of free-foraging bumblebee (Bombus spp.) males (Hymenoptera. Apidae). Apidologie, 45, 440-450. https://doi.org/10.1007/s13592-013-0259-9

Cuckoo male bumblebees perform slower and longer flower visits than free-living male and worker bumblebeesAlessandro Fisogni, Gherardo Bogo, François Massol, Laura Bortolotti, Marta Galloni<p>Cuckoo bumblebees are a monophyletic group within the genus Bombus and social parasites of free-living bumblebees, upon which they rely to rear their offspring. Cuckoo bumblebees lack the worker caste and visit flowers primarily for their own s...Behavior, Biology, Ecology, Insecta, Invertebrates, TerrestrialMichael Lattorff Patrick Lhomme, Seth Barribeau , Silvio Erler, Denis Michez2021-02-02 01:41:35 View