Colder rotifers grow larger but only in oxygenated waters

Czarnołęski, Marcin; Ejsmont-Karabin, Jolanta; Angilletta, Michael J.; Kozłowski, Jan

doi:10.1890/es15-00024.1

Cited by 38 publications

(44 citation statements)

References 38 publications

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“…This is consistent with the results of earlier studies of inter-specific differences in Hb concentrations in Daphnia (Heisey & Porter, 1977;Sell, 1998), which indicated that larger-bodied species have higher basal levels of Hb, and synthesise more Hb in hypoxic conditions. Although each of the two properties induces energetic costs, they could be treated as adaptations to both greater vulnerability to hypoxia, since diffusion distances are increased in a larger body (Czarnoleski et al, 2015;Seidl et al, 2005), and greater vulnerability to fish predation, since larger-bodied Daphnia are prone to dwell more deeply in the oxygen-deficient meta-and hypolimnetic water layers to avoid size-selective predation by planktivorous fish in the euphotic layers (Hansson & Hylander, 2009;Leibold & Tessier, 1991).…”

Section: Discussionmentioning

confidence: 99%

“…Hypoxia has been shown to reduce juvenile growth rate (Seidl et al, 2005), adult body size, and egg/neonate size (Hanazato & Dodson, 1995;Kobayashi & Hoshi, 1984;Lyu et al, 2013). Smaller adult body size in hypoxia could simply be attributed to slower juvenile growth, but it could also be treated as an adaptive response, since in a smaller body, diffusion distances are reduced, which contributes to an improved tolerance of hypoxia (Czarnoleski, Ejsmont-Karabin, Angilletta, & Kozłowski, 2015;Maszczyk & Brzeziński, 2018;Seidl et al, 2005). Moreover, due to smaller cell size, diffusion within tissues would be expedited (Woods, 1999), because oxygen more efficiently diffuses through a cell membrane than through the cytoplasm (Czarnoleski et al, 2015;Maszczyk & Brzeziński, 2018;Subczynski, Hyde, & Kusumi, 1989).…”

Section: Introductionmentioning

confidence: 99%

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The combined effects of hypoxia and fish kairomones on several physiological and life history traits of Daphnia

et al. 2019

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1. Numerous studies have tested the combined effect of the threat of predation by fish and low oxygen concentrations on the phenotypic plasticity of Daphnia.These studies assessed the trade-off between minimising predation risk and the negative effects of oxygen deficiencies in the context of depth selection behaviour. We tested whether this trade-off also affects physiological and life history traits. We expected an interactive effect between the threat of fish predation and low oxygen concentrations, such, that the net effect of both stressors would be antagonistic (lower than the sum of each of the stressors acting separately), rather than additive (or synergistic) on the majority of traits investigated, but we predicted synergistic effects on heat shock proteins (HSPs). 2. To test this, we performed life table experiments in different oxygen concentrations (normoxia and hypoxia) and levels of predation threat (the presence and absence of fish kairomones) on HSP70 and putative HSP110, haemoglobin concentration and life history traits with small-bodied Daphnia galeata and large-bodied Daphnia pulex originating from waterbodies where there were different risks of fish predation. 3. As predicted, the net effect of both stressors was antagonistic for most of the physiological and ecological variables studied. The presence of kairomones resulted in decreased body size of adults, egg size, egg size in relation to brood chamber volume, and in increased clutch size in relation to body size. These effects were weaker in hypoxia than in normoxia, which may suggest an existence of adaptive responses caused by a lower perceived risk in hypoxia than in normoxia, as the foraging abilities of fish are limited by oxygen deficiencies. 4. The presence of kairomones hampered the production of haemoglobin in hypoxia for the clones of larger-bodied species, which suggests the existence of a trade-off between reduced visibility under positive-size selective predation risk and increased efficiency of oxygen transport to body tissues. The presence of kairomones and hypoxia resulted in an increased level of putative HSP110, and the effect of kairomones was stronger in hypoxia than in normoxia. More complex results were obtained for the effect of both stressors on the level of HSP70. | 2205 WILCZYNSKI et al.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The combined effects of hypoxia and fish kairomones on several physiological and life history traits of Daphnia

et al. 2019

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“…Note that some panels have different units of x and y axes [Colour figure can be viewed at wileyonlinelibrary.com] Kolding, Haug, & Stefansson, 2008). Similarly, the amphipod Asellus aquaticus raised at warmer temperatures grew to smaller adult sizes only when oxygen was limited (Hoefnagel & Verberk, 2015), and rotifers in low-oxygen lakes reached smaller body sizes than those in similar temperature but well-oxygenated waters (Czarnoleski, Ejsmont-Karabin, Angilletta, & Kozlowski, 2015). In contrast, other studies show that oviparous fish can increase their mass-specific oxygen consumption by nearly 30% compared to post-spawning fish (Karamushko & Christiansen, 2002), suggesting that changes in oxygen supply are regulated by the internal demands rather than supply.…”

Section: Are Aquati C Org Anis Ms Limited By Their C Apacit Y To Upmentioning

confidence: 99%

Is oxygen limitation in warming waters a valid mechanism to explain decreased body sizes in aquatic ectotherms?

Audzijonytė

Barneche

Baudron

et al. 2018

Global Ecol Biogeogr

133

161

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Aim The negative correlation between temperature and body size of ectothermic animals (broadly known as the temperature‐size rule or TSR) is a widely observed pattern, especially in aquatic organisms. Studies have claimed that the TSR arises due to decreased oxygen solubility and increasing metabolic costs at warmer temperatures, whereby oxygen supply to a large body becomes increasingly difficult. However, mixed empirical evidence has led to a controversy about the mechanisms affecting species’ size and performance under different temperatures. We review the main competing genetic, physiological and ecological explanations for the TSR and suggest a roadmap to move the field forward. Location Global. Taxa Aquatic ectotherms. Time period 1980–present. Results We show that current studies cannot discriminate among alternative hypotheses and none of the hypotheses can explain all TSR‐related observations. To resolve this impasse, we need experiments and field‐sampling programmes that specifically compare alternative mechanisms and formally consider energetics related to growth costs, oxygen supply and behaviour. We highlight the distinction between evolutionary and plastic mechanisms, and suggest that the oxygen limitation debate should separate processes operating on short, decadal and millennial time‐scales. Conclusions Despite decades of research, we remain uncertain whether the TSR is an adaptive response to temperature‐related physiological (enzyme activity) or ecological changes (food, predation and other mortality), or a response to constraints operating at a cellular level (oxygen supply and associated costs). To make progress, ecologists, physiologists, modellers and geneticists should work together to develop a cross‐disciplinary research programme that integrates theory and data, explores time‐scales over which the TSR operates, and assesses limits to adaptation or plasticity. We identify four questions for such a programme. Answering these questions is crucial given the widespread impacts of climate change and reliance of management on models that are highly dependent on accurate representation of ecological and physiological responses to temperature.

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“…This mechanism was linked to the body size adjustment to temperature by Atkinson et al (2006). The hypothesis on the oxygen-driven size-to-temperature response has been positively verified both indirectly (Berner et al, 2007; Harrison et al, 2010; Rollinson and Rowe, 2018a; Rollinson and Rowe, 2018b; Santilli and Rollinson, 2018; Verberk and Atkinson, 2013) and directly (Czarnoleski et al, 2015; Frazier et al, 2001; Hoefnagel and Verberk, 2015). However, results relating this pattern directly to organismal fitness are scarce (Prokosch et al, 2019; Walczyńska et al, 2015a), while such a reference is the only way that enables reliable conclusions on the evolutionary meaning of TSR.…”

Section: Introductionmentioning

confidence: 81%

Aerobic scope does matter in temperature-size rule, but only under optimal conditions

Walczyńska

Łabęcka

Sobczyk

2020

Preprint

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3 1 exposure to hypoxia, (iii) this response enables us to keep the wide scope for aerobic 3 2 performance, and (iv) it prevents the decrease in fitness. We conducted our tests on three clones 3 3 of the rotifer Lecane inermis with different thermal preferences. These clones were exposed to 3 4 three experimental regimes: mild hypoxia, severe hypoxia driven by a too high temperature, and 3 5 severe hypoxia driven by an inadequate oxygen concentration. The results showed that our 3 6 causative reasoning was generally correct, but only under mildly hypoxic conditions. In more 3 7 stressful environments, rotifers had clone-and condition-specific responses, which in fact were 3 8 equally successful in terms of the levels of fitness. Our results join for the first time all factors 3 9 connecting the cause and effect in the temperature-size rule. They indicate the importance of the 4 0conditions under which it should be tested. The most important messages from this study was that 4 1 (i) a decrease in the body size was one of but not the only option for preventing fitness reduction 4 2 under hypoxia, and (ii) such a response to higher temperature fuelled the aerobic scope in clone-4 3 specific, thermally optimal conditions. 4 4 4 5 4 6 4 7 4 8 4 9 7 1 2018; Verberk and Atkinson, 2013) and directly (Czarnoleski et al., 2015; Frazier et al., 2001; 7 2 Hoefnagel and Verberk, 2015). However, results relating this pattern directly to organismal 7 3 fitness are scarce (Prokosch et al., 2019; Walczyńska et al., 2015a), while such a reference is the 7 4only way that enables reliable conclusions on the evolutionary meaning of TSR. 7 5In this study, we linked the hypothesized proximate and ultimate mechanisms behind the 7 6 phenotypically driven size decrease with increasing temperature for the case of the rotifer Lecane 7 7inermis. We aimed to thoroughly test the logic of the reasoning behind hypoxia driving body size 7 8shrinkage to prevent the reduction in fitness. Because the TSR has been empirically confirmed to 7 9 be condition-sensitive and to be performed only in an optimal thermal range (Walczyńska et al., 8 0 4 2016), we conducted our tests under optimal and suboptimal conditions; the latter was further 8 1 diversified between hypoxia driven by stress-inducing high temperatures or by the stress-8 2 inducing low oxygen levels. This distinction enabled inference on the possible border conditions 8 3 for TSR performance, linking the hypothesized proximate and ultimate factors with fitness. 8 4We examined the aerobic scope, our hypothesized ultimate mechanism, by estimating the specific 8 5 dynamic action (SDA). This measure refers to the increasing metabolic expenditures in animals 8 6 and is associated with ingestion, digestion, assimilation and absorption of food (McCue, 2006; 8 7 Secor, 2009), when the increasing oxygen consumption was mostly associated with the 8 8 biochemical transformation of food and the synthesis of the new proteins (Jordan and Steffensen, 8 92007). In practice, it was estimated as a difference in...

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Colder rotifers grow larger but only in oxygenated waters

Cited by 38 publications

References 38 publications

The combined effects of hypoxia and fish kairomones on several physiological and life history traits of Daphnia

The combined effects of hypoxia and fish kairomones on several physiological and life history traits of Daphnia

Is oxygen limitation in warming waters a valid mechanism to explain decreased body sizes in aquatic ectotherms?

Aerobic scope does matter in temperature-size rule, but only under optimal conditions

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