Combined effects of elevated temperature and Deepwater Horizon oil exposure on the cardiac performance of larval mahi-mahi, Coryphaena hippurus

Abstract

The 2010 Deepwater Horizon oil spill coincided with the spawning season of many pelagic fish species in the Gulf of Mexico. Yet, few studies have investigated physiological responses of larval fish to interactions between anthropogenic crude oil exposure and natural factors (e.g. temperature, oxygen levels). Consequently, mahi mahi (Coryphaena hippurus) embryos were exposed for 24 hours to combinations of two temperatures (26 and 30°C) and six concentrations of oiled fractions of weathered oil (from 0 to 44.1 μg ∑50PAHs·L-1). In 56 hours post-fertilization larvae, heart rate, stroke volume and cardiac output were measured as indicators of functional cardiac phenotypes. Fluid accumulation and incidence of edema and hematomas were quantified as indicators of morphological impairments. At both 26 and 30°C, oil-exposed larvae suffered dose-dependent morphological impairments and functional heart failure. Elevation of temperature to 30°C appeared to induce greater physiological responses (bradycardia) at PAH concentrations in the range of 3.0-14.9 μg·L-1. Conversely, elevated temperature in oil-exposed larvae reduced edema severity and hematoma incidence. However, the apparent protective role of warmer temperature does not appear to protect against enhanced mortality. Collectively, our findings show that elevated temperature may slightly decrease larval resilience to concurrent oil exposure.

Fig 1. Experimental design.

Mahi embryos (eight hpf) were exposed to HEWAF solutions during 24 hours and subsequently transferred to clean seawater for an additional 24 hours of development. Exposures were performed at two temperatures: a “normal” temperature of 26°C and an “elevated” temperature 30°C. Each temperature trial included a control group raised in seawater only. hpf; hours post-fertilization.

Fig 2. Morphological impairments associated with edema.

(A) Edema area (mm²), (B) sinus venosus-yolk mass gap (μm) and (C) total incidence of intrapericardial hematomas measured at two rearing temperatures 26°C (N = 20–39) and 30°C (N = 20–56). Data for edema area and SV-YM gap are expressed as mean±SEM. Incidence of intrapericadial hematomas is expressed in total percent of hematomas scored in oil—exposed individuals. Simple linear regressions are given for graphical representation at both exposure temperatures. * (26°C) and # (30°C) indicate significant differences of oil exposure concentrations compared to respective control groups (P<0.05).

Fig 3. Cardiac variables measured in mahi larvae under combined oil and temperature exposures.

(A) Heart rate (beat.min^-1), (B) stroke volume (nL) and (C) cardiac output (nL·min^-1) measured at two rearing temperatures 26°C (N = 20–39) and 30°C (N = 20–56). Data are presented as Mean±SEM. Simple linear regressions are given for graphical representation at both temperature exposures. * for 26°C and # for 30°C indicate significant differences of oil exposure concentrations compared to respective control groups (P<0.05).

Fig 4. Correlation between cardiac variables and extent of edema in mahi larvae under combined oil and temperature exposures.

N = 20–39 at 26°C and N = 20–56 at 30°C. Data are presented as Mean±SEM. Solid and dashed lines represent linear regressions at 26°C and 30°C, respectively.