Thermal and oxygen conditions during development cause common rough woodlice (Porcellio scaber) to alter the size of their gas-exchange organs

Antoł, Andrzej; Łabęcka, Anna Maria; Horváthová, Terézia; Zieliński, Bartosz; Szabla, Natalia; Vasko, Yaroslav; Pecio, Anna; Kozłowski, Jan; Czarnołęski, Marcin

doi:10.1016/j.jtherbio.2020.102600

Cited by 9 publications

(10 citation statements)

References 52 publications

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“…Yet they are not completely insurmountable. Organisms have evolved the capacity to: ( i ) increase surface area for resource uptake during growth, such as by changing body shape (Hirst, Glazier, & Atkinson, 2014; Glazier, Hirst, & Atkinson, 2015) or increasing the size of uptake organs (Antoł et al ., 2020) or their surfaces (gill re‐modelling; Nilsson, Dymowska, & Stecyk, 2012); ( ii ) increase rates at which they obtain and distribute resources (e.g. by increasing feeding activity or by active ventilation and circulation; Woods & Moran, 2020); and ( iii ) reduce rates of demand for resources (e.g.…”

Section: The Dependency Of T–s Responses On Growth and Developmentmentioning

confidence: 99%

Shrinking body sizes in response to warming: explanations for the temperature–size rule with special emphasis on the role of oxygen

et al. 2020

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Body size is central to ecology at levels ranging from organismal fecundity to the functioning of communities and ecosystems. Understanding temperature‐induced variations in body size is therefore of fundamental and applied interest, yet thermal responses of body size remain poorly understood. Temperature–size (T–S) responses tend to be negative (e.g. smaller body size at maturity when reared under warmer conditions), which has been termed the temperature–size rule (TSR). Explanations emphasize either physiological mechanisms (e.g. limitation of oxygen or other resources and temperature‐dependent resource allocation) or the adaptive value of either a large body size (e.g. to increase fecundity) or a short development time (e.g. in response to increased mortality in warm conditions). Oxygen limitation could act as a proximate factor, but we suggest it more likely constitutes a selective pressure to reduce body size in the warm: risks of oxygen limitation will be reduced as a consequence of evolution eliminating genotypes more prone to oxygen limitation. Thus, T–S responses can be explained by the ‘Ghost of Oxygen‐limitation Past’, whereby the resulting (evolved) T–S responses safeguard sufficient oxygen provisioning under warmer conditions, reflecting the balance between oxygen supply and demands experienced by ancestors. T–S responses vary considerably across species, but some of this variation is predictable. Body‐size reductions with warming are stronger in aquatic taxa than in terrestrial taxa. We discuss whether larger aquatic taxa may especially face greater risks of oxygen limitation as they grow, which may be manifested at the cellular level, the level of the gills and the whole‐organism level. In contrast to aquatic species, terrestrial ectotherms may be less prone to oxygen limitation and prioritize early maturity over large size, likely because overwintering is more challenging, with concomitant stronger end‐of season time constraints. Mechanisms related to time constraints and oxygen limitation are not mutually exclusive explanations for the TSR. Rather, these and other mechanisms may operate in tandem. But their relative importance may vary depending on the ecology and physiology of the species in question, explaining not only the general tendency of negative T–S responses but also variation in T–S responses among animals differing in mode of respiration (e.g. water breathers versus air breathers), genome size, voltinism and thermally associated behaviour (e.g. heliotherms).

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Section: The Dependency Of T–s Responses On Growth and Developmentmentioning

confidence: 99%

Shrinking body sizes in response to warming: explanations for the temperature–size rule with special emphasis on the role of oxygen

et al. 2020

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“…These places are relatively moist, but they are also expected to become oxygen deficient (hypoxic) during certain periods, such as floodings or heavy rainfall (Wright and Ting, 2006). With regard to the effect of hypoxia on isopods, there is evidence that hypoxia lowers their critical temperatures (Antoł et al, 2019;Klok et al, 2004;Stevens et al, 2010;Verberk et al, 2018), their thermal preference and performance (Antoł et al, 2019), their respiration rate (Wright and Ting, 2006) and slows down growth (Hoefnagel and Verberk, 2015, but see Antoł et al, 2020;Horváthová et al, 2015) as well as the development of their eggs and offspring (Horváthová et al, 2017). Furthermore, isopods enlarge the size of their lungs during development in chronic hypoxia (Antoł et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

“…With regard to the effect of hypoxia on isopods, there is evidence that hypoxia lowers their critical temperatures (Antoł et al, 2019;Klok et al, 2004;Stevens et al, 2010;Verberk et al, 2018), their thermal preference and performance (Antoł et al, 2019), their respiration rate (Wright and Ting, 2006) and slows down growth (Hoefnagel and Verberk, 2015, but see Antoł et al, 2020;Horváthová et al, 2015) as well as the development of their eggs and offspring (Horváthová et al, 2017). Furthermore, isopods enlarge the size of their lungs during development in chronic hypoxia (Antoł et al, 2020). The examples mentioned above show that isopods likely experience episodic hypoxia and that they are capable of responding to it, making hypoxia an important ecological factor driving their distribution along elevational gradients as well as microhabitat selection.…”

Section: Introductionmentioning

confidence: 99%

Effects of body size and lung type on desiccation resistance, hypoxia tolerance and thermal preference in two terrestrial isopods species

Antoł

Berg

Verberk

2021

Journal of Insect Physiology

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“…This work was part of a long‐term study of P. scaber , and its methods are already available elsewhere (e.g., Antoł et al, 2020; Horváthová et al., 2017; Horváthová, Antol, et al, 2015). Briefly, adults of P. scaber were collected in autumn (2013) and spring (2014) in an old backyard in Kraków, Poland (50°04ʹ15.9″N 19°56ʹ21.9″E).…”

Section: Methodsmentioning

confidence: 99%

Effects of thermal and oxygen conditions during development on cell size in the common rough woodlice Porcellio scaber

Antoł

Łabęcka

Horváthová

et al. 2020

Ecology and Evolution

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During development, cells may adjust their size to balance between the tissue metabolic demand and the oxygen and resource supply: Small cells may effectively absorb oxygen and nutrients, but the relatively large area of the plasma membrane requires costly maintenance. Consequently, warm and hypoxic environments should favor ectotherms with small cells to meet increased metabolic demand by oxygen supply. To test these predictions, we compared cell size (hindgut epithelium, hepatopancreas B cells, ommatidia) in common rough woodlice (Porcellio scaber) that were developed under four developmental conditions designated by two temperatures (15 or 22°C) and two air O2 concentrations (10% or 22%). To test whether small‐cell woodlice cope better under increased metabolic demand, the CO2 production of each woodlouse was measured under cold, normoxic conditions and under warm, hypoxic conditions, and the magnitude of metabolic increase (MMI) was calculated. Cell sizes were highly intercorrelated, indicative of organism‐wide mechanisms of cell cycle control. Cell size differences among woodlice were largely linked with body size changes (larger cells in larger woodlice) and to a lesser degree with oxygen conditions (development of smaller cells under hypoxia), but not with temperature. Developmental conditions did not affect MMI, and contrary to predictions, large woodlice with large cells showed higher MMI than small woodlice with small cells. We also observed complex patterns of sexual difference in the size of hepatopancreatic cells and the size and number of ommatidia, which are indicative of sex differences in reproductive biology. We conclude that existing theories about the adaptiveness of cell size do not satisfactorily explain the patterns in cell size and metabolic performance observed here in P. scaber. Thus, future studies addressing physiological effects of cell size variance should simultaneously consider different organismal elements that can be involved in sustaining the metabolic demands of tissue, such as the characteristics of gas‐exchange organs and O2‐binding proteins.

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Thermal and oxygen conditions during development cause common rough woodlice (Porcellio scaber) to alter the size of their gas-exchange organs

Cited by 9 publications

References 52 publications

Shrinking body sizes in response to warming: explanations for the temperature–size rule with special emphasis on the role of oxygen

Shrinking body sizes in response to warming: explanations for the temperature–size rule with special emphasis on the role of oxygen

Effects of body size and lung type on desiccation resistance, hypoxia tolerance and thermal preference in two terrestrial isopods species

Effects of thermal and oxygen conditions during development on cell size in the common rough woodlice Porcellio scaber

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