Warmer, earlier, faster: Cumulative effects of Gulf of Alaska heatwaves on the early life history of Pacific cod

Abstract

Warming climates are creating unprecedented environmental conditions, such as more frequent and intense marine heatwaves (MHWs), that directly impact phenology and growth of fish and other marine organisms. Understanding individual phenological and growth responses to temperature is critical to predict species and population responses to climate change; however, doing so requires disentangling the effects of temperature on phenology, size, and growth in wild populations. We quantified the relationships between temperature and hatch timing, size-at-age, and early growth in a population of Pacific cod (Gadus macrocephalus) affected by recent MHWs in the Gulf of Alaska. Pacific cod juveniles were collected near Kodiak Island, Alaska, USA, across 11 years, categorized as before (2007, 2009–2010, 2012–2014), during (2015, 2016, 2019), and between (2017, 2018) multiple recent MHWs. We estimated age and growth with otolith structural analysis. Hatching occurred on average 14 days earlier during MHWs and 26 days earlier between than before MHWs. Approximately 53% and 16% of these respective shifts in timing were attributable directly to warmer temperatures during incubation. Size-at-age was similar across periods at younger ages (90 days), but approximately 7 mm and 11 mm larger than before MHWs at older ages (132 days) during and between MHWs, respectively. These differences in size-at-age were partially related to growth responses that differed among MHW periods. However, observed differences in growth rate could not account for the observed increases in size-at-age. We found that temperature alone could not explain the changes in growth and phenology; thus, factors such as parental effects, epigenetics, and selection likely contributed. Our results indicate that spawn timing, size, and growth relationships based on historical thermal responses should be questioned in population forecasting as the global climate continues to warm.

Marine heatwaves alter the nursery function of coastal habitats for juvenile Gulf of Alaska Pacific cod

“…Further, in direct contrast to the Temperature-Size Rule, our growth rates exhibited a negative relationship with water temperature. Instead, the larger body size during MHWs were predominantly a result of older ages due to shifting phenology 19 combined with modestly faster growth, and potentially other factors, including size-selective mortality 47 . It is also unlikely that decoupling between daily otolith increment formation and somatic growth contributed to higher than predicted sizes by August.…”

“…During the years between the MHWs, juvenile Pacific cod CPUE was among the highest we observed with greater demographic variation, including some of the broadest size distributions and slowest growing individuals. These trends may reflect persistent early spawning after the MHWs 19 , selective pressure for specific traits from the previous MHW years 25 , a shift in the parental stock contribution of Kodiak Island juveniles following the MHWs 75 , or a combination of these factors. Improved conditions in the nursery between the MHWs in 2017 and 2018 may illustrate some resilience of the species to periods of anomalous warming 76 ; however, less is known about how these cohorts fared through their first winter and beyond.…”

“…Dramatic declines of Pacific cod larval and age-0 juvenile abundances occurred almost immediately following the onset of MHW conditions, likely due to reduced hatch success 44 and potential mismatches in prey resources available to first-feeding larvae 23 . Follow-up studies found additional demographic changes in age-0 cohorts during MHWs, including a nearly 3-week shift to earlier hatch dates in the spring 19 , which contributed to predominantly larger and older juveniles entering coastal habitats in early summer 45 . During the MHWs, relatively large body size and low abundance of juvenile Pacific cod were observed post-settlement in coastal habitats across the GOA 46 .…”

“…This pattern, known as the ‘Temperature-Size Rule’, is regularly attributed to mechanisms such as faster growth rates 13 and elevated metabolism 14 early in life leading to maturation at smaller sizes. However, while increased size and growth rates of juvenile fishes at high temperatures are well-supported in the lab 15 , 16 , these patterns may be weakened or reversed in the field, where fish experience both the direct and indirect effects of elevated temperatures 17 – 19 . Increased temperatures can lead to earlier spawn timing for fishes 20 , resulting in fish that are both older and larger when they enter their first winter than conspecifics in cooler conditions.…”