Thermal bottlenecks in the life cycle define climate vulnerability of fish

Abstract

<jats:p>Species’ vulnerability to climate change depends on the most temperature-sensitive life stages, but for major animal groups such as fish, life cycle bottlenecks are often not clearly defined. We used observational, experimental, and phylogenetic data to assess stage-specific thermal tolerance metrics for 694 marine and freshwater fish species from all climate zones. Our analysis shows that spawning adults and embryos consistently have narrower tolerance ranges than larvae and nonreproductive adults and are most vulnerable to climate warming. The sequence of stage-specific thermal tolerance corresponds with the oxygen-limitation hypothesis, suggesting a mechanistic link between ontogenetic changes in cardiorespiratory (aerobic) capacity and tolerance to temperature extremes. A logarithmic inverse correlation between the temperature dependence of physiological rates (development and oxygen consumption) and thermal tolerance range is proposed to reflect a fundamental, energetic trade-off in thermal adaptation. Scenario-based climate projections considering the most critical life stages (spawners and embryos) clearly identify the temperature requirements for reproduction as a critical bottleneck in the life cycle of fish. By 2100, depending on the Shared Socioeconomic Pathway (SSP) scenario followed, the percentages of species potentially affected by water temperatures exceeding their tolerance limit for reproduction range from ~10% (SSP 1–1.9) to ~60% (SSP 5–8.5). Efforts to meet ambitious climate targets (SSP 1–1.9) could therefore benefit many fish species and people who depend on healthy fish stocks.</jats:p>

From gametogenesis to spawning: How climate‐driven warming affects teleost reproductive biology

“…As most teleosts are poikilotherms, ambient temperature directly impacts metabolic rate, reproductive performance (Vagner et al ., 2019; Wang et al ., 2010), body growth, natural mortality and recruitment success (so‐called “vital parameters” in population dynamics), and thereby ultimately population (stock) productivity (Kjesbu et al ., 2014). Depending on the species and life stages, fish sensitivity to thermal fluctuations varies due to their window of thermal tolerance (Pörtner & Farrell, 2008; Dahlke et al ., 2020). For instance, most sensitive stages to thermal stress, spawning and early life correspond to the narrowest thermal windows.…”

Warming winters threaten peripheral Arctic charr populations of Europe

“…The narrower temperature tolerance of the egg stage is related to a reduced aerobic capacity (and ability to supply oxygen to tissues), which improves from egg to adult with the development of the cardiorespiratory system (e.g. Dahlke et al 2020). Charr eggs also have immature homeostatic capacities to tolerate adverse thermal conditions.…”

“…In aquatic ectotherms, the spawning adult and embryonic egg stages have the narrowest thermal tolerance range and are therefore most vulnerable to warming temperatures (Elliott and Elliott 2010;Dahlke et al 2020). Warm winters can subject fertilised embryos to adverse conditions, leading to smaller egg sizes, lower hatch success, and smaller emergent larvae (Farmer et al 2015).…”

Climate risk to European fisheries and coastal communities

“…Note that we explicitly avoid the use of the term "stock" to refer to this unit of analysis, as this has clear implications in fisheries management but is not entirely the same as our definition "population". Secondly, we place the degree of warming experienced by these populations in a physiological context using thermal-safety margins (TSM) 26,27,64,65 . TSM is defined as the difference between the maximum temperature that the species can sustain and the temperature of the environment: high TSMs indicate a high capacity to tolerate warming.…”