The recent collapse of predatory sunflower sea stars ( Pycnopodia helianthoides ) owing to sea star wasting disease (SSWD) is hypothesized to have contributed to proliferation of sea urchin barrens and losses of kelp forests on the North American west coast. We used experiments and a model to test whether restored Pycnopodia populations may help recover kelp forests through their consumption of nutritionally poor purple sea urchins ( Strongylocentrotus purpuratus ) typical of barrens. Pycnopodia consumed 0.68 S. purpuratus d −1 , and our model and sensitivity analysis shows that the magnitude of recent Pycnopodia declines is consistent with urchin proliferation after modest sea urchin recruitment, and even small Pycnopodia recoveries could generally lead to lower densities of sea urchins that are consistent with kelp-urchin coexistence. Pycnopodia seem unable to chemically distinguish starved from fed urchins and indeed have higher predation rates on starved urchins owing to shorter handling times. These results highlight the importance of Pycnopodia in regulating purple sea urchin populations and maintaining healthy kelp forests through top-down control. The recovery of this important predator to densities commonly found prior to SSWD, whether through natural means or human-assisted reintroductions, may therefore be a key step in kelp forest restoration at ecologically significant scales.
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Survivors of Climate Driven Abalone Mass Mortality Exhibit Declines in Health and Reproduction Following Kelp Forest Collapse
Marine ecosystems are vulnerable to climate driven events such as marine heatwaves yet we have a poor understanding of whether they will collapse or recover. Kelp forests are known to be susceptible, and there has been a rise in sea urchin barrens around the world. When temperatures increase so do physiological demands while food resources decline, tightening metabolic constraints. In this case study, we examine red abalone ( Haliotis rufescens ) looking at sublethal impacts and their prospects for recovery within kelp forests that have shifted to sea urchin barrens. Abalone are a recreationally fished species that once thrived in northern California’s bull kelp forests but have recently suffered mass mortalities since the 2014–2016 marine heatwave. Quantitative data exist on the health and reproduction of abalone both prior to and after the collapse. The survivors of the mass mortality show a 2-year lag in body and gonad condition indices. After the lag, body and gonad indexes decreased substantially, as did the relationship between shell length and body weight. Production of mature eggs per female declined by 99% ( p < 0.001), and the number of eggs per gram of female body weight (2,984/g) declined to near zero (9/g). The number of males with sperm was reduced by 33%, and the sperm abundance score was reduced by 28% ( p = 0.414). We observed that these reductions were for mature eggs and sperm while immature eggs and spermatids were still present in large numbers. In the lab, after reintroduction of kelp, weight gains were quickly lost following a second starvation period. This example illustrates how climate-driven declines in foundation species can suppress recovery of the system by impacting body condition and future reproduction of surviving individuals. Given the poor reproductive potential of the remaining abalone in northern California, coupled with ongoing mortality and low kelp abundances, we discuss the need to maintain the fishing moratorium and implement active abalone restoration measures. For fished species, such as abalone, this additional hurdle to recovery imposed by changes in climate is critical to understand and incorporate into resource management and restoration.
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- Award ID(s):
- 2023664
- NSF-PAR ID:
- 10295552
- Date Published:
- Journal Name:
- Frontiers in Marine Science
- Volume:
- 8
- ISSN:
- 2296-7745
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Climate change is altering the intensity and variability of environmental stress that organisms and ecosystems experience, but effects of changing stress regimes are not well understood. We examined impacts of constant and variable sublethal hypoxia exposures on multiple biological processes in the sea urchin
Strongylocentrotus purpuratus , a key grazer in California Current kelp forests, which experience high variability in physical conditions. We quantified metabolic rates, grazing, growth, calcification, spine regeneration, and gonad production under constant, 3-hour variable, and 6-hour variable exposures to sublethal hypoxia, and compared responses for each hypoxia regime to normoxic conditions. Sea urchins in constant hypoxia maintained baseline metabolic rates, but had lower grazing, gonad development, and calcification rates than those in ambient conditions. The sublethal impacts of variable hypoxia differed among biological processes. Spine regrowth was reduced under all hypoxia treatments, calcification rates under variable hypoxia were intermediate between normoxia and constant hypoxia, and gonad production correlated negatively with continuous time under hypoxia. Therefore, exposure variability can differentially modulate the impacts of sublethal hypoxia, and may impact sea urchin populations and ecosystems via reduced feeding and reproduction. Addressing realistic, multifaceted stressor exposures and multiple biological responses is crucial for understanding climate change impacts on species and ecosystems. -
Kelp forests of the California Current System have experienced prolonged marine heatwave (MHW) events that overlap in time with the phenology of life history events (e.g., gametogenesis and spawning) of many benthic marine invertebrates. To study the effect of thermal stress from MHWs during gametogenesis in the purple sea urchin ( Strongylocentrotus purpuratus ) and further, whether MHWs might induce transgenerational plasticity (TGP) in thermal tolerance of progeny, adult urchins were acclimated to two conditions in the laboratory – a MHW temperature of 18°C and a non-MHW temperature of 13°C. Following a four-month long acclimation period (October–January), adults were spawned and offspring from each parental condition were reared at MHW (18°C) and non-MHW temperatures (13°C), creating a total of four embryo treatment groups. To assess transgenerational effects for each of the four groups, we measured thermal tolerance of hatched blastula embryos in acute thermal tolerance trials. Embryos from MHW-acclimated females were more thermally tolerant with higher LT 50 values as compared to progeny from non-MHW-acclimated females. Additionally, there was an effect of female acclimation state on offspring body size at two stages of embryonic development - early gastrulae and prism, an early stage echinopluteus larvae. To assess maternal provisioning as means to also alter embryo performance, we assessed gamete traits from the differentially acclimated females, by measuring size and biochemical composition of eggs. MHW-acclimated females had eggs with higher protein concentrations, while egg size and lipid content showed no differences. Our results indicate that TGP plays a role in altering the performance of progeny as a function of the thermal history of the female, especially when thermal stress coincides with gametogenesis. In addition, the data on egg provisioning show that maternal experience can influence embryo traits via egg protein content. Although this is a laboratory-based study, the results suggest that TGP may play a role in the resistance and tolerance of S. purpuratus early stages in the natural kelp forest setting.more » « less
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Abstract The terminal investment hypothesis (TIH) predicts that individuals with favorable prospects for future reproduction (i.e., high residual reproductive value, RRV) should moderate current reproductive investment in favor of growth, survival, and future reproduction, whereas those with low RRV should “terminally invest” by diverting somatic resources towards current reproduction at the expense of future reproduction. However, support for the TIH in wild animal populations is fragmentary, and the ecological contexts of terminal investment remain poorly known. We report a remarkable case of simultaneous terminal investment involving five sympatric species of the electric knifefish genus
Brachyhypopomus , from Amazonian floodplain and terra firme stream habitats. We found that terminal investment is synchronized by seasonal breeding, in response to circannual environmental variation in mortality risk. Four species exhibit a uniseasonal iteroparous (annual) life history with complete post‐reproductive mortality after a single breeding season. One species (Brachyhypopomus beebei ) exhibits a 2‐year multiseasonal iteroparous life history with breeding in two seasons and post‐reproductive mortality after the second. In mature females and (most) males of the annual species, as well as in both mature female and malesecond‐year (but not first‐year)B. beebei , we documented an increase in two metrics of reproductive effort (size‐adjusted gonad mass and electric signal amplitude) and a concomitant reduction in somatic condition (size‐adjusted somatic mass), all in response to proximity to the end of the common breeding season, when RRV approximates zero. In maturefirst‐year B. beebei , we documented neither an increase in reproductive effort nor a decline in somatic condition, implying an alternative strategy of reproductive restraint. Our findings support Kirkwood's disposable soma theory, which posits that death by reproductive exhaustion can be delayed if terminal investment is replaced by reproductive restraint, allowing individuals to survive and breed in a subsequent season. Deferral of the terminal investment response in annual species, and the origin of a gonadal regression‐regeneration sequence, may open pathways for rapid evolutionary transitions to multiseasonal iteroparity. Excepting the age (year‐group) dependency of terminal investment inB. beebei , we were unable to identify intrinsic cues or extrinsic environmental cues for the terminal investment response inBrachyhypopomus . -
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Abstract A critical tool in assessing ecosystem change is the analysis of long‐term data sets, yet such information is generally sparse and often unavailable for many habitats. Kelp forests are an example of rapidly changing ecosystems that are in most cases data poor. Because kelp forests are highly dynamic and have high intrinsic interannual variability, understanding how regional‐scale drivers are driving kelp populations—and particularly how kelp populations are responding to climate change—requires long‐term data sets. However, much of the work on kelp responses to climate change has focused on just a few, relatively long‐lived, perennial, canopy‐forming species. To understand how kelp populations with different life history traits are responding to climate‐related variability, we leverage 35 yr of Landsat satellite imagery to track the population size of an annual, ruderal kelp,
Nereocystis luetkeana , across Oregon. We found high levels of interannual variability inNereocystis canopy area and varying population trajectories over the last 35 yr. Surprisingly, OregonNereocystis population sizes were unresponsive to a 2014 marine heat wave accompanied by increases in urchin densities that decimated northern CaliforniaNereocystis populations. Some OregonNereocysti s populations have even increased in area relative to pre‐2014 levels. Analysis of environmental drivers found thatNereocystis population size was negatively correlated with estimated nitrate levels and positively correlated with winter wave height. This pattern is the inverse of the predicted relationship based on extensive prior work on the perennial kelpMacrocystis pyrifera and may be related to the annual life cycle ofNereocystis . This article demonstrates (1) the value of novel remote sensing tools to create long‐term data sets that may challenge our understanding of nearshore marine species and (2) the need to incorporate life history traits into our theory of how climate change will shape the ocean of the future.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fmars.2021.725134
