Impacts of ocean acidification on sea urchin growth across the juvenile to mature adult life-stage transition is mitigated by warming

1. Introduction

Marine species are experiencing coasts and oceans that are simultaneously warming and decreasing in pH with the magnitude of change differing among world regions [1]. Climate warming is driving marked responses in many marine ectotherms including shifts in species distributions, as seen in the poleward range extension of species as they follow their thermal niche [2]; changes in phenology, as seen in the altered timing of spawning and plankton blooms [3]; and declining body size [4]. Ocean acidification is accompanied by covarying stressors; increasing pCO₂ causes organism hypercapnia and can result in metabolic suppression and energetic stress, while the accompanying decrease in calcium carbonate mineral saturation impairs calcification and growth, and hence decreasing body size, and a ‘dwarfing effect’ is reported and/or expected [5–7]. Where the synergy between warming and acidification has been investigated the outcomes for marine ectotherms can be complex, with some species being more vulnerable than others [6,8,9].

Marine calcifiers represent a vast diversity of species, and several meta-analyses show their high vulnerability to acidification, with reports of impaired growth of larval, juvenile and adult stages in studies involving single life stages of taxa that calcify in their larval and benthic life phases [6,9,10]. It is important to understand how warming and acidification will interact to affect survival, growth, size at maturity, reproductive output and other proxies of fitness. Temperature and pCO₂/pH can interact, as seen in the positive buffering effect of increased temperature on growth and calcification in near-future acidification in long-term (months) studies, or can act synergistically in a negative way when tolerance thresholds are breached [9,11–14]. Understanding how growth trajectories are affected by changing ocean conditions and prospects for population persistence requires acclimation experiments that follow the response to these factors across life-history transitions such as reaching reproductive maturity.

It is not known if it will be possible for marine species to acclimate to changing ocean conditions to maintain growth levels into the future. We used the fast-growing tropical sea urchin, Tripneustes gratilla as a model species to investigate the effects of acidification and warming on the life-stage transition from the post-metamorphic juvenile to the mature adult in a long-term acclimation study. The urchins were reared from the very early juvenile (5 mm test diameter, TD) through the gonad development stage (approx. 600 mm TD). This species is also an important fishery and aquaculture species, the latter due to its fast growth [15,16]. In T. gratilla the decrease in the thickness of the test and its crushing resistance following long-term rearing at pH 7.8 is mitigated by near-future warming, but not at greater acidification [17]. For the juveniles of calcifying species the interaction between increased acidification and temperature on skeleton formation is positive for some species [18–20], but not others [11,21]. For adult sea urchins, exposure to anthropogenic (CO₂ dosing experiments) and biogenic (respiratory CO₂) acidification can have a negative effect on body and gonad growth [16,22], although the negative effects of acidification on reproduction can be reduced in longer-term incubations [23,24]. Maintenance of organism acid–base balance is crucial for physiological function and is a significant energetic cost that affects energy partitioning between fitness traits such as growth and reproduction [25]. Several studies have shown that sea urchins can maintain their acid–base balance at near-future levels of acidification, but this is likely to be energetically costly [26,27], especially in combination with warming [28].

There are no studies that have reared post-metamorphic benthic calcifiers to reproductive maturity under ocean warming and acidification conditions to assess how chronic long-term exposure to these stressors interact to impact on body and gonad growth, as proxies of fitness. This knowledge gap is addressed here with T. gratilla reared to reproductive maturity in a factorial combination of three temperature and three pH/pCO₂ treatments, commensurate with projections for southeast Australia [29,30]. Survival, growth, internal pH and gonad production as a proxy of both nutritive condition and reproductive potential were determined. Given the negative effect of acidification on calcification and growth of echinoids on one hand, especially juveniles [31], and the positive effect of warming on the other [32], we expected to see a complex interplay between these factors with respect to the growth trajectories of T. gratilla. We predicted that impaired growth due to acidification would be ameliorated by near-future warming, as seen for T. gratilla larvae (e.g. [33]). However, if greater warming breached thermal tolerance limits, or if there is a negative effect of temperature on size even below thermal maxima such that the ‘temperature–size’ rule (TSR) applies for this species, we expect growth would be impaired [4,34]. The stunting effect of warming was expected to be exacerbated by acidification. As the gonad functions as the major nutrient storage organ in sea urchins [35], we predicted that energetic constraints imposed by acidification and warming would have a negative effect on its development. We also predicted that T. gratilla would be able to maintain its coelomic acid–base balance at moderate, but not more extreme acidification and warming.

2. Material and methods

3. Results

4. Discussion

As warming and acidification of marine habitats continues to unfold, it is not known how these combined stressors will interact to affect survival, growth, size at maturity and other proxies of fitness of marine ectotherms. In this first study to examine how these stressors interact to affect the juvenile to adult life-stage transition of a benthic calcifier, we show the utility of the multifactorial approach and the importance of considering the interplay between fitness traits in predicting species' responses to changing climate. In parallel with the trend seen for many calcifiers, near-future acidification reduced body size in T. gratilla, while near-future warming mitigated this effect. However, this mitigation was not as effective with respect to gonad growth, and not at all with respect to acid–base balance. Although the juveniles grew and survived in near-future warming and acidification conditions, chronic exposure to these stressors from an early age altered allocation to somatic and gonad growth in a positive or negative way, depending on the stressor combination.

Temperature alone had a positive effect on growth. Tripneustes gratilla in the 25°C and 28°C treatments were larger and heavier, and also had a more robust test, due to the increased skeletal growth and, as shown previously, potentially due to altered mineralogy (increased MgCO₃) [17]. As more tropical populations of this species experience these temperature levels, these outcomes might be expected. Our results contrast with those found for bivalves, where moderate warming reduced shell growth and strength [42]. Moderate warming had a positive effect on gonad growth in T. gratilla, while the warmest treatment showed evidence of reduced growth of this organ. Thus, while warming had a positive effect on body size, there was a limit to thermal facilitation of gonad production. Similarly, adult urchins in long-term warming (approx. +3°C) experiments (Paracentrotus lividus, 3 months; Echinometra sp., 2.5 months; Evechinus chloroticus 3 months) exhibit impaired gonad development [22,43,44]. Increasing temperatures are a major physiological stress for T. gratilla and other sea urchins with increased susceptibility to disease and mortality as the ocean warms [45,46].

Acidification alone, especially at pH 7.6, had a negative effect on body and gonad growth in T. gratilla, as also seen for calcification in this and other sea urchin species [17,22,25,31,47]. Moderate acidification (pH 7.8) was not so stressful, perhaps because this level approaches the conditions occasionally experienced in nature. Acidification was particularly deleterious to gonad growth. Along with reduced body size, this indicates an altered nutritive state and energy partitioning to development of this important storage organ.

The impacts of combined warming and acidification on body and gonad growth in T. gratilla were complex. Amelioration of the negative effect of acidification on growth in size and weight and calcification in T. gratilla [17] was limited to the near-future scenario (+3°C/pH 7.8). The negative effects of acidification on gonad growth were not mitigated by this level of warming. At higher stress levels T. gratilla were smaller and had poorly developed or no gonads, as seen for other sea urchins [25,44,47]. Despite being provided with excess food, it seems that T. gratilla was not able to maintain its growth and reproductive potential at high acidification and warming. This is counter to the observation that the deleterious effects of acidification can be compensated by high food conditions [48]. At pH 7.6, regardless of temperature, gonad development was reduced and in some individuals inhibited.

The T. gratilla were able to compensate their acid–base balance in moderate acidification but less so in the lowest pH treatment, as reported for other sea urchin species [22,25,27,49]. Increased temperature caused acidification of the coelomic fluid, probably due to increased respiratory acidosis of the coelom. The inability of T. gratilla reared to adulthood in warm–low pH conditions to compensate for internal acidosis is likely to have contributed to their reduced performance. Key functions such as growth and reproduction are negatively impacted by these stressors due direct impacts on metabolism and the energetic demands to maintain body acid–base balance for functions such as calcification and enzyme activity [25,26,31]. Increased temperature and acidification have an additive effect in increasing respiration in sea urchins [22,28]. It will be important to understand the metabolic responses of T. gratilla and other sea urchins reared to the adult stage in changing ocean conditions to determine if phenotypic adjustment over time is possible to maintain growth and production at present-day levels.

The duration of marine climate change experiments can influence outcomes as short-term incubations may overestimate effects when organisms do not have time to physiologically acclimatize to changing conditions [25]. For instance, acidification has a negative effect on gonad growth in sea urchins at 4-month but not 16-month exposure [23], although this would be influenced by the gametogenic state of the gonad at the onset of incubation. Adult urchins are able to adjust their reproductive output to control levels following long-term acclimation (years) to acidification and warming [24]. In both of these studies the experimental subjects were fully grown adult urchins with differentiated gonads. As shown here, the outcome is likely to differ when experiments involve juvenile urchins from first gonad development. We do not know if the urchins reared at pH 7.6 would eventually develop viable gonads with longer rearing. Given more time the controls would have developed larger gonads.

Reduced reproductive output of T. gratilla in response to warming and acidification have negative consequences for population persistence. This concern is compounded given the sensitivity of T. gratilla and other sea urchins to climate change stressors during their larval phase [10,33]. Given the sensitivity of invertebrate calcifiers to acidification and warming as larvae, decreased reproductive output by adults combined with poor larval survival may pose a serious bottleneck for survival of many benthic species in the future [9].

It is predicted that ocean acidification and warming will combine to exacerbate body size reductions in marine ectotherms as a universal impact of global change [4]. The ‘temperature–size’ rule (TSR) posits that ectotherms are smaller as adults when they develop through their life at elevated temperatures [50], as seen in the reduced body size of aquatic ectotherms due to contemporary warming [51]. Our results with T. gratilla do not support this and highlight that the TSR does not hold for all species [52], and may be context-dependent. Increasing temperatures have a nonlinear effect on ectotherms, initially elevating metabolic rates and facilitating growth with moderate warming up to thermal limits when growth decreases [4]. The expectation is that decreased body size will also be attributed to the impact of acidification where the energetic constraints to produce a skeleton under hypercapnic and lower carbonate mineral saturation conditions impair calcification and growth [4,6,7,10,31]. This is evident at CO₂ vent sites where calcifiers are smaller than in non-vent sites [52]. Our data for T. gratilla indicate that while warming can mitigate the stunting effects of acidification, there is a limit to this. Indeed, temperatures above the levels used here (29°C) impair growth of this species.

A major caveat of our results and much of current marine climate change research is that we tested how present-day genotypes respond to future stressors. It is likely that increased environmental stress will result in genetic change and possible adaptation [53]. A major challenge will be to understand how organisms might adapt to future multiple environmental stressors [54]. In addition, T. gratilla is a very widely distributed species with a large metapopulation across the tropics. Our juveniles were the progeny of high-latitude/range-edge parents with a comparatively ‘cool’ environmental history. It will be important to understand the tolerance of more tropical populations to increased temperature and acidification. However, in the absence of phenotypic adjustment, the interactive effects of warming and acidification on the benthic life phases of T. gratilla and other benthic calcifiers may compromise reproductive fitness and population maintenance as global climatic change unfolds.

Supplementary Material

Supplementary Material

Ethics

Under local guidelines no ethics approvals were needed to conduct this research.

Data accessibility

The datasets supporting this article are available in electronic supplementary material and from the Dryad Digital Repository (doi:10.5061/dryad.qc3m7) [55].

Authors' contributions

S.A.D. and M.B. conceived and designed the experiments, analysed the data and wrote the manuscript. S.A.D. preformed and managed the experiments.

Competing interests

We declare we have no competing interests.

Funding

This work was supported by grants from the New South Wales Environmental Research Trust and the Australian Research Council to S.A.D. and M.B.