High sensitivity of a keystone forage fish to elevated CO2 and temperature

Abstract

Sand lances of the genus Ammodytes are keystone forage fish in coastal ecosystems across the northern hemisphere. Because they directly support populations of higher trophic organisms such as whales, seabirds or tuna, the current lack of empirical data and, therefore, understanding about the climate sensitivity of sand lances represent a serious knowledge gap. Sand lances could be particularly susceptible to ocean warming and acidification because, in contrast to other tested fish species, they reproduce during boreal winter months, and their offspring develop slowly under relatively low and stable pCO₂ conditions. Over the course of 2 years, we conducted factorial pCO₂ × temperature exposure experiments on offspring of the northern sand lance Ammodytes dubius, a key forage species on the northwest Atlantic shelf. Wild, spawning-ripe adults were collected from Stellwagen Bank National Marine Sanctuary (Cape Cod, USA), and fertilized embryos were reared at three pCO₂ conditions (400, 1000 and 2100 μatm) crossed with three temperatures (5, 7 and 10 ˚C). Exposure to future pCO₂ conditions consistently resulted in severely reduced embryo survival. Sensitivity to elevated pCO₂ was highest at 10 ˚C, resulting in up to an 89% reduction in hatching success between control and predicted end-of-century pCO₂ conditions. Moreover, elevated pCO₂ conditions delayed hatching, reduced remaining endogenous energy reserves at hatch and reduced embryonic growth. Our results suggest that the northern sand lance is exceptionally CO₂-sensitive compared to other fish species. Whether other sand lance species with similar life history characteristics are equally CO₂-sensitive is currently unknown. But the possibility is a conservation concern, because many boreal shelf ecosystems rely on sand lances and might therefore be more vulnerable to climate change than currently recognized. Our findings indicate that life history, spawning habitat, phenology and developmental rates mediate the divergent early life CO₂ sensitivities among fish species.

Keywords: Ammodytes dubius; climate change; early life-history; multi-stressor experiment; ocean acidification; ocean variability hypothesis.

Fig. 1

Map of SBNMS and the surrounding region. The red circle denotes the sampling location for spawning-ripe A. dubius.

Fig. 2

A. dubius. (A) Schematic of morphometric measurements made on newly hatched larvae from the main experiment. Measurements include hatch length (SL, nearest 0.01 mm), somatic body area (nearest 0.01 mm²), yolk sac area (nearest 0.001 mm²) and oil globule area (nearest 0.001 mm²). (B, C) Sea fertilization. Model-adjusted (±95% confidence interval) treatment PC scores of body size traits (B; PC 1; SL and somatic body area) and endogenous energy reserves (C; PC 2; yolk sac and oil globule area) per temperature and pCO₂ treatment (blue circles, 400 μatm; green squares, 1000 μatm; red triangles, 2100 μatm).

Fig. 3

A. dubius. Mean embryo survival (%) of offspring reared at 400 μatm (blue, left bar), 1000 μatm (green, central bar) and 2100 μatm pCO₂ (red, right bar) and two temperatures from the pilot trial.

Fig. 4

A. dubius. Hatching timelines from each fertilization event (2017: sea; 2017: laboratory) tested during the main experiment. Embryos were reared at 5°C (blue background) and 10°C (red background) crossed with three pCO₂ levels: 400 μatm (blue lines), 1000 μatm (green lines) and 2100 μatm (red lines). Traits presented are hatching success (A–D, %) and daily hatch frequencies (E–H, daily hatch/total final hatch within temperature treatment).

Fig. 5

Seasonal pH (NIST, blue) and temperature (°C, red) variability from spawning habitats of M. menidia (A; Mumford Cove, CT; 41° 19′ 25′′ N 72° 01′ 07″ W; Baumann, 2016) and A. dubius (B; Coastal Western Gulf of Maine Mooring; 43° 1′ 12′′ N, 70° 32′ 24′′ W; Sutton et al., 2014). The Gulf of Maine mooring is located ~ 100 km north of the sand lance collection site (~10 km offshore, 65 m depth). Faded circles, individual measurements; solid lines, smoothed data; shading, seasonal window of early life stages. (C) pH variability vs. pH/CO₂ sensitivity in M. menidia vs. A. dubius; average CO₂ effect (~2000 μatm) on embryo survival (LnRR±95% CI) plotted against the average pH range experienced during spawning season (ΔpH). Data for M. mendia (red circle) was taken from Baumann et al. (2018) . In both species, CO₂-driven reductions in embryo survival (negative LnRRs) are considered significant because 95% confidence intervals do not include 0 (Hedges et al., 1999).