Is the temperature-size rule mediated by oxygen in aquatic ectotherms?

Hoefnagel, K. Natan; Verberk, Wilco C. E. P.

doi:10.1016/j.jtherbio.2014.12.003

Cited by 89 publications

(85 citation statements)

References 41 publications

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“…In ectotherm species, one might predict that warming in cities might induce evolution of a fast life cycle involving small individuals that develop fast and produce many, smaller eggs. This prediction is in line with the temperature–size rule (Atkinson, ; Forster, Hirst, & Atkinson, ; Hoefnagel & Verberk, ) and complements the earlier observation that small organisms have a higher thermal tolerance, as was also reported for Daphnia (Brans, Jansen, et al., ; Geerts et al., ). The occurrence of disturbances linked to management (e.g., clearance of the litter layer on the bottom of the pond and addition of water; Hassall, ; personal observations) and extreme temperature events in cities (Brans et al., ; Ward et al., ; Wouters et al., ) might also select for a fast life cycle (Atwell et al., ; Charmantier et al., ; Evans, Boudreau, & Hyman, ).…”

Section: Introductionsupporting

confidence: 89%

City life on fast lanes: Urbanization induces an evolutionary shift towards a faster lifestyle in the water flea Daphnia

Brans

Meester

2018

Functional Ecology

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Multiple species show significant trait shifts in response to urbanization. Yet, the impact of anthropogenic warming linked to the urban heat island effect is remarkably understudied. In addition, the relative contributions of phenotypic plasticity and genetic change underlying trait shifts in response to urbanization are poorly known. A common garden study with the water flea Daphnia magna revealed that both genetic differentiation in response to urbanization and phenotypic plasticity in response to higher rearing temperature (24°C) induced significant parallel multivariate shifts in life‐history strategy along the slow–fast pace‐of‐life axis. Urban animals and animals reared at higher temperatures are characterized by fast maturation, early release of progeny, a smaller size at maturity, increased fecundity and higher performance (given by maximal population growth rate “r”) compared to genotypes isolated from rural ponds and animals reared at lower temperatures, respectively. Evolution in response to urbanization accounted for 30% of the total observed shift in life history and caused a significant change in mean trait values, while plasticity responses to experimental warming were unaltered between urban and rural populations. The total trait change achieved through both plasticity and evolution ranged from 8% to 56% depending on the trait. Our results provide clear evidence for evolution underlying an increase in pace of life of populations in response to urbanization. Given the pivotal role of Daphnia in aquatic ecosystems, this shift potentially feeds back to population structure, top‐down control of algae and food web dynamics in urban freshwater ecosystems. In addition, we argue that adaptation to urban heat islands might render these populations preadapted in a context of future climate change. http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13184/suppinfo is available for this article.

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Section: Introductionsupporting

confidence: 89%

City life on fast lanes: Urbanization induces an evolutionary shift towards a faster lifestyle in the water flea Daphnia

Brans

Meester

2018

Functional Ecology

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“…While these effects were generally small, there is evidence for mayflies that small effects of oxygen on lethal limits become more pronounced for sublethal limits manifested at lower temperatures under field conditions (Verberk, Durance, et al., ). Previous work on A. aquaticus , one of the most heat‐ and hypoxia‐resistant species in our study, also showed strong interactive effects of temperature and oxygen on growth (Hoefnagel & Verberk, ), while employing temperatures (14–24°C) and oxygen levels (10–40 kPa) more moderate than those used in the present study. Still in half of the species we studied, thermal tolerance was not affected by hypoxia or by hyperoxia, reflecting the mixed results reported earlier (Ern et al., ; Frederich & Pörtner, ).…”

Section: Discussionsupporting

confidence: 61%

Thermal limits in native and alien freshwater peracarid Crustacea: The role of habitat use and oxygen limitation

et al. 2018

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In order to predict which species can successfully cope with global warming and how other environmental stressors modulate their vulnerability to climate‐related environmental factors, an understanding of the ecophysiology underpinning thermal limits is essential for both conservation biology and invasion biology.Heat tolerance and the extent to which heat tolerance differed with oxygen availability were examined for four native and four alien freshwater peracarid crustacean species, with differences in habitat use across species. Three hypotheses were tested: (1) Heat and lack of oxygen synergistically reduce survival of species; (2) patterns in heat tolerance and the modulation thereof by oxygen differ between alien and native species and between species with different habitat use; (3) small animals can better tolerate heat than large animals, and this difference is more pronounced under hypoxia.To assess heat tolerances under different oxygen levels, animal survival was monitored in experimental chambers in which the water temperature was ramped up (0.25°C min−1). Heat tolerance (CTmax) was scored as the cessation of all pleopod movement, and heating trials were performed under hypoxia (5 kPa oxygen), normoxia (20 kPa) and hyperoxia (60 kPa).Heat tolerance differed across species as did the extent by which heat tolerance was affected by oxygen conditions. Heat‐tolerant species, for example, Asellus aquaticus and Crangonyx pseudogracilis, showed little response to oxygen conditions in their CTmax, whereas the CTmax of heat‐sensitive species, for example, Dikerogammarus villosus and Gammarus fossarum, was more plastic, being increased by hyperoxia and reduced by hypoxia.In contrast to other studies on crustaceans, alien species were not more heat‐tolerant than native species. Instead, differences in heat tolerance were best explained by habitat use, with species from standing waters being heat tolerant and species from running waters being heat sensitive. In addition, larger animals displayed lower critical maximum temperature, but only under hypoxia. An analysis of data available in the literature on metabolic responses of the study species to temperature and oxygen conditions suggests that oxygen conformers and species whose oxygen demand rapidly increases with temperature (low activation energy) may be more heat sensitive.The alien species D. villosus appeared most susceptible to hypoxia and heat stress. This may explain why this species is very successful in colonizing new areas in littoral zones with rocky substrate which are well aerated due to continuous wave action generated by passing ships or prevailing winds. This species is less capable of spreading to other waters which are poorly oxygenated and where C. pseudogracilis is the more likely dominant alien species. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13050/suppinfo is available for this article.

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“…The driving role of oxygen in temperature-size rule was hypothesized by Atkinson et al (2006). Since then, it was confirmed in several other studies Hoefnagel & Verberk, 2015;Horne et al, 2015;Walczyńska et al, 2015) and rejected in one meta-analysis (Klok & Harrison, 2013). In the context of adaptive phenotypic plasticity, the temperature-size rule can be considered as being ''responsive'' (sensu Whitman & Agrawal, 2009) with regard to temperature, but ''anticipatory'' with regard to oxygen, possibly because mechanisms of response to temperature are better developed than those of response to oxygen, as was previously suggested by Walczyńska et al (2015).…”

Section: Discussionmentioning

confidence: 59%

Empirical evidence for fast temperature-dependent body size evolution in rotifers

Walczyńska

Franch‐Gras

2017

Hydrobiologia

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Organisms tend to decrease in size with increasing temperature by phenotypic plasticity (the temperature-size rule; ectotherms) and/or genetically (Bergmann's rule; all organisms). In this study, the evolutionary response of body size to temperature was examined in the cyclically parthenogenetic rotifer Brachionus plicatilis. Our aim was to investigate whether this species, already known to decrease in size with increasing temperature by phenotypic plasticity, presents a similar pattern at the genetic level. We exposed a multiclonal mixture of B. plicatilis to experimental evolution at low and high temperature and monitored body size weekly. Within a month, we observed a smaller size at higher temperature, as compared to body size at lower temperature. The pattern was consistent for the size of both mature females and eggs; rotifers kept at high temperature evolved to be on average 14% (after 2 weeks) and 3% (after 3 weeks) smaller than the ones kept at low temperature (10 and 5% in the case of eggs, respectively). We therefore found that B. plicatilis is genetically programmed to adjust its body size-toenvironmental temperature.

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Is the temperature-size rule mediated by oxygen in aquatic ectotherms?

Cited by 89 publications

References 41 publications

City life on fast lanes: Urbanization induces an evolutionary shift towards a faster lifestyle in the water flea Daphnia

City life on fast lanes: Urbanization induces an evolutionary shift towards a faster lifestyle in the water flea Daphnia

Thermal limits in native and alien freshwater peracarid Crustacea: The role of habitat use and oxygen limitation

Empirical evidence for fast temperature-dependent body size evolution in rotifers

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