Attention:The NSF Public Access Repository (PAR) system and access will be unavailable from 11:00 PM ET on Thursday, October 15th until 12:00 AM ET on Friday, October 16th due to maintenance. We apologize for the inconvenience.


Title: Temperature-dependent hypoxia tolerance of purple sea urchin Strongylocentrotus purpuratus across biogeography and ontogeny
Ocean warming is increasing organismal oxygen demand, yet at the same time the ocean’s oxygen supply is decreasing. For a patch of habitat to remain viable, there must be a minimum level of environmental oxygen available for an organism to fuel its metabolic demand—quantified as its critical oxygen partial pressure (pO2crit). The temperature-dependence ofpO2critsets an absolute lower boundary on aerobically viable ocean space for a species, yet whether certain life stages or geographically distant populations differ in their temperature-dependent hypoxia tolerance remains largely unknown. To address these questions, we used the purple sea urchinStrongylocentrotus purpuratusas a model species and measuredpO2critfor 3 populations of adult urchins (Clallam Bay, WA [n = 39], Monterey Bay, CA [91], San Diego, CA [34]) spanning 5-22°C and for key embryonic and larval developmental phases (blastula [n = 11], gastrula [21], prism [31], early-pluteus [21], late-pluteus [14], settled [12]) at temperatures of 10-19°C. We found that temperature-dependent hypoxia tolerance is consistent among adult populations exposed to different temperature and oxygen regimes, despite variable basal oxygen demands, suggesting differential capacity to provision oxygen. Moreover, we did not detect evidence for a hypoxia tolerance bottleneck for any developmental phase. Earlier larval phases are associated with higher hypoxia tolerance and greater temperature sensitivity, while this pattern shifts towards lower hypoxia tolerance and reduced temperature sensitivity as larvae develop. Our results indicate that, at least forS. purpuratus,models quantifying aerobically viable habitat based onpO2crit-temperature relationships from a single adult population will conservatively estimate viable habitat.  more » « less
Award ID(s):
1922966 2108566
PAR ID:
10550196
Author(s) / Creator(s):
; ; ; ; ;
Publisher / Repository:
Marine Ecology Progress Series
Date Published:
Journal Name:
Marine Ecology Progress Series
Volume:
739
ISSN:
0171-8630
Page Range / eLocation ID:
129 to 146
Subject(s) / Keyword(s):
Hypoxia tolerance Deoxygenation Strongylocentrotus purpuratus Purple sea urchin Warming threshold Climate change
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Giant kelpMacrocystis pyriferaprovides the foundation for immense biodiversity on the coast of California, USA. Kelp forests can change seawater retention time, altering water chemistry, including pH and dissolved oxygen (DO), as well as the magnitude and predictability of variability in the same properties. Environmental heterogeneity across space and time could drive organismal performance and processes such as transgenerational plasticity (TGP), where parental experience modifies the offspring phenotype, potentially conferring tolerance to future environmental stress. We monitored environmental variability by deploying temperature, pH, and DO sensors inside and outside a temperate kelp forest in the Santa Barbara Channel (SBC) throughout the gametogenesis period of a key herbivore, the purple urchinStrongylocentrotus purpuratus. Over the 6 mo period, pH and temperature were slightly elevated inside the kelp forest, accompanied by more predictable, low-frequency variability relative to outside. AdultS. purpuratuswere conditioned inside and outside the kelp spanning gametogenesis. The urchins were spawned and their larvae were raised under high (1053 µatm) and lowpCO2(435 µatm) at 15°C in the laboratory to assess their physiological response to the maternal and developmental environments. Larvae raised under highpCO2were more susceptible to acute thermal stress; however, within each larval treatment, progeny from outside-conditioned mothers had a 0.4°C higher lethal temperature (LT50). Our results indicate that heterogeneity in abiotic factors associated with kelp can have transgenerational effects in the field, and interactions between factors, including temperature and pH, will impact purple urchins as local variability associated with marine heatwaves and upwelling evolves with climate change. 
    more » « less
  2. Abstract Estuaries supply a critical habitat to many ecologically and commercially valuable fish species, providing safety and food availability during the larval and juvenile stages. However, dissolved oxygen is naturally dynamic in these systems, varying from complete anoxia to hyperoxia. In some species, the larval stage may be particularly vulnerable to low‐oxygen stress due to incomplete development of oxygen transport systems, high metabolic cost associated with early feeding and a narrow aerobic scope to support additional activity. Increasing seawater temperatures further increase oxygen demand in poikilothermic species and are amplified in shallow inshore habitats. In teleost fish, estuarine hypoxia and warming may lead to recruitment bottlenecks at the larval stage, which often requires a narrower range of environmental conditions than juveniles or adults. Here, we compared the physiological oxygen supply capacity (α) and aerobic scope of late‐larval and early‐juvenile common snookCentropomus undecimalis(Bloch 1792), a coastal marine species found in the Gulf of Mexico, Caribbean and western Atlantic from Florida to Brazil. We hypothesized that larvae would be more hypoxia sensitive than juveniles but instead found that routine and maximum metabolic rates scaled similarly with body mass, resulting in size independence of factorial aerobic scope and critical oxygen partial pressure between life stages. Theαvalue matched maximum demand across the transition from larval to juvenile stages, suggesting thatC. undecimaliscan effectively regulate the supply of oxygen from the environment to their tissues as early as 17 days post hatching. Additionally,C. undecimalisexhibited aPcmaxvalue of 18.63 kPa, indicating that their full aerobic potential can be met only at oxygen pressures near air saturation. Although this is the expectedPcmaxbased on their previously reported prevalence in surface waters, this may lead to reduced habitat availability as estuarine deoxygenation worsens in the Gulf of Mexico. 
    more » « less
  3. It is well established that adult vertebrates acclimatizing to hypoxic environments undergo mitochondrial remodeling to enhance oxygen delivery, maintain ATP, and limit oxidative stress. However, many vertebrates also encounter oxygen deprivation during embryonic development. The effects of developmental hypoxia on mitochondrial function are likely to be more profound, because environmental stress during early life can permanently alter cellular physiology and morphology. To this end, we investigated the long-term effects of developmental hypoxia on mitochondrial function in a species that regularly encounters hypoxia during development—the common snapping turtle ( Chelydra serpentina ). Turtle eggs were incubated in 21% or 10% oxygen from 20% of embryonic development until hatching, and both cohorts were subsequently reared in 21% oxygen for 8 months. Ventricular mitochondria were isolated, and mitochondrial respiration and reactive oxygen species (ROS) production were measured with a microrespirometer. Compared to normoxic controls, juvenile turtles from hypoxic incubations had lower Leak respiration, higher P:O ratios, and reduced rates of ROS production. Interestingly, these same attributes occur in adult vertebrates that acclimatize to hypoxia. We speculate that these adjustments might improve mitochondrial hypoxia tolerance, which would be beneficial for turtles during breath-hold diving and overwintering in anoxic environments. 
    more » « less
  4. Environments with fluctuating oxygen are intense challenges for organisms both on land and in the water. Aquatic organisms can be exposed to especially stressful bouts of hypoxia that come on rapidly and to extreme levels. The copepodTigriopus californicusinhabits supralittoral rocky pools and appears tolerant of hypoxia levels considered lethal for other aquatic organisms despite lacking molecular components typically used by animals to detect and respond to low environmental oxygen. Here, we quantified the natural regime of dissolved oxygen (DO) pools inhabited byT. californicusvia deployment of continuous oxygen sensors in copepod pools in Oregon, USA. Using wild-derived cultures from northern (Oregon) and southern (Californian) populations, we exposed copepods to hypoxia and anoxia and assayed loss of equilibrium (LOE) and survival. We also quantified respiratory regulation via critical oxygen tension, oxygen supply capacity, and regulation index. The pools underwent extreme daily cycles of DO, and near anoxia often persisted for up to 6 h. Respiratory statistics indicated individuals could regulate oxygen consumption even near anoxia, predicting a species with hypoxia tolerance ranking high among aquatic taxa. Copepods survived hypoxia below 0.3 mg O2l-1for up to 72 h with some individuals not showing any LOE. Survival was high following even 6 and 15 h exposure to anoxia. We observed sex and population differences in lethality and LOE, with southern populations exhibiting higher resilience. Intraspecific variation in tolerance makes this system a candidate for future studies to investigate alternative molecular and physiological pathways of hypoxia response. 
    more » « less
  5. Ocean warming due to climate change can affect the metabolism, performance, and survival of ectothermic marine species. On the US Northeast continental shelf (US NES), waters are warming faster than the global average, leading to elevated mean temperatures and an increased risk of marine heatwave exposure in the region. Thus, it is critical to understand the effects of warming on the region’s living marine resources. Here, we quantified the acute temperature sensitivity of metabolic traits to evaluate their role as possible drivers of acute thermal tolerance and viable habitat in the spiny dogfish sharkSqualus acanthiason the US NES. From 10-23°C, the standard metabolic rate increased more rapidly than the maximum metabolic rate, resulting in a reduction in factorial aerobic scope at warmer temperatures. However, the oxygen supply capacity increased with temperature in proportion to maximum metabolic rate, and neither metric declined at the warmest temperatures, suggesting oxygen supply capacity does not limit performance within the tested range. Although behavioral observations revealed overt thermal stress via loss of equilibrium at ≥20°C and estimated lethal temperature at ∼24°C, sharks retained the ability to regulate their resting metabolic rate, achieve maximum activity, and peak absolute aerobic scope at warm temperatures. Results suggest that factors other than oxygen supply or aerobic scope are constraining thermal tolerance inS. acanthiasand support the notion that aerobic scope cannot be universally applied to determine optimal or viable metabolic habitat. 
    more » « less