Elsevier

Aquatic Toxicology

Volume 237, August 2021, 105904
Aquatic Toxicology

Effects of short-duration oil exposure on bay anchovy (Anchoa mitchilli) embryos and larvae: mortality, malformation, and foraging

https://doi.org/10.1016/j.aquatox.2021.105904Get rights and content

Highlights

  • Higher latent mortality post-larval than post-embryo exposure.

  • Malformation of the yolk-sac, finfold, notochord and cranio-facial structure.

  • Relationships among blue-sac disease malformations of exposed larvae and embryos.

  • Time in motion, swim speed, and the number of bursts increased during larval foraging.

  • Burst speed, burst distance, and pause duration decreased during first-foraging.

Abstract

The Deepwater Horizon oil spill highlighted the need to understand the effects of oil exposure on marine eggs and larvae. To determine how short-duration exposure impacts the survivability of early life stages of the bay anchovy, Anchoa mitchilli, embryos and larvae ≤ 3-days-post-hatch (dph) were exposed to high-energy water accommodated fractions of weathered crude oil for 2 or 6 h. Lethal and sublethal effects of short-duration oil exposure were observed, including crippling malformations and altered optimal swimming and foraging behavior of larvae without malformation. The probability of mortality for larvae exposed as embryos (37.37 and 77.31 µg L−1 total polycyclic aromatic hydrocarbons or ‘TPAH’), assessed 48 h after exposure, increased from 0.06 to 0.15 (2 h) and 0.10–0.23 (6 h) relative to unoiled controls. When exposed as 1-dph larvae (8.80–37.37 µg L−1 TPAH) and assessed 24 h after exposure, the probabilities increased from 0.20 to 0.76 (2 h) and 0.28–0.99 (6 h). Among surviving larvae, probabilities of yolk-sac, finfold, notochord, and cranio-facial malformations increased with exposure concentration, duration, and time after exposure by up to 0.07 immediately following exposure of 1-dph larvae and 0.55 24 h after exposure. When assessed 48 h after exposure as embryos, the probability of larval malformation reached 0.43. First-feeding (3-dph) foraging behavior was altered immediately and 24 h after 2 h exposures (8.80–77.31 µg L−1 TPAH). Time spent in motion and swim speed increased with exposure concentration by up to 331% and 189%, respectively. The number of bursts min−1 increased by 293% immediately and 152% 24 h after exposure. Burst distance decreased by 201%. Pause duration and burst speed decreased by 391% and 250% immediately and 124% and 109% 24 h after exposure. No effects were found for burst duration or tortuosity. Our results suggest potential cascading effects on fitness and trophic interactions.

Introduction

Maritime oil production and transport occasionally result in environmental contamination such as the 2010 failure of an offshore drilling platform in the northern Gulf of Mexico (nGOM) known as Deepwater Horizon. The nGOM is home to a wide diversity of tropical and subtropical marine fishes that were spawning when Deepwater Horizon occurred. Consequently, an unprecedented number of marine fish and other larvae became exposed to crude oil. This led to a vast number of studies testing the lethality, altered physiology, and ecological consequences of crude oil exposure on many larval taxa (Pasparakis et al., 2019). Despite this massive ecosystem assessment, relatively few studies have focused on the effects of short-duration exposure (< 24 h) for early life stages of forage fishes, such as the bay anchovy, Anchoa mitchilli (Pasparakis et al., 2019). Assessment of short-duration exposures are important because at high temperatures, many subtropical marine larvae hatch in less than 24 h and undergo other rapid changes in development. Without short duration exposures it is impossible to separate the effects of exposure on embryos (pre hatch) and newly-hatched larvae or those associated with other significant developmental changes, like the onset of first feeding, that occur post-hatch (Grosell et al., 2020). Additionally, while the current standards for toxicological studies promote comparison between taxa, the methodology used can lead to results that are overly conservative for sensitive species, such as the bay anchovy and don't always necessarily reflect exposure scenarios in the environment.

High fecundity, early maturity, and a spawning season that extends from early spring through autumn make bay anchovy embryos and larvae the most common and abundant species of ichthyoplankton within the bays and nearshore waters of the nGOM (Lyczkowski-Shultz et al., 1990; Raynie and Shaw 1994; Peebles et al., 1996; Hernandez et al., 2010; Carassou et al., 2012). Their dominant presence in the ichthyoplankton is reflected by the tremendous biomass of the adult population which has long been among the most abundant estuarine species of the nGOM (Gunter 1941; Din and Gunter 1986; Rakocinski et al., 1992; Baltz et al., 1993; Chesney et al., 2000; Schrandt et al., 2018) and Mid-Atlantic Region (Houde and Zastrow 1991), with a range extending from the Yucatan to the Gulf of Maine (Morton (1989)). Their great abundance within these systems makes bay anchovy an important forage species that constitutes substantial components of the diets of piscivorous fishes and coastal birds (Hartman and Brandt 1995; Jung and Houde 2004; Simonsen and Cowan 2013). As zooplanktivores (Darnell 1958; Din and Gunter 1986), bay anchovy are an important link in the transfer of energy to these higher trophic levels. As a forage species, bay anchovy serve as a vector for bioaccumulation among predators that exploit them in contaminated environments (Xia et al., 2015). These aspects make this species particularly relevant to multispecies management and comprehensive ecosystem assessments, such as the National Resource Damage Assessment (NRDA) (Oil Pollution Act 1990) in the United States and other similar programs around the world.

Upon hatching, larval bay anchovy are small (< 3 mm standard length and 10 µg dry weight), fragile, and reliant upon the energy stored within a yolk sac to develop until they reach a first-feeding stage at approximately 2–3 days post-hatch (dph) (Chesney 2008). Generally, larval anchovy are poor predators at first feeding due to limited visual acuity and the fact that their small mass and the constraints of water viscosity make ‘cruise-searching’ energetically inefficient (Vlymen 1974; Weihs 1980). Instead, they use a ‘pause-travel’ foraging strategy. This short and choppy search pattern involves alternating periods where the larva remains still while identifying prey, followed by a burst to engage prey or a ‘tail flick’ that changes their orientation to present a new field of view to search (Chesney 2008). At this stage, successful feeding is critical for larval survival (Hunter 1972; Houde and Schekter 1978, 1980; Tucker 1989). Growth to approximately 5 mm can be reached by 5 dph (Houde and Schekter 1978; Chesney 2008), which typically relates to a sufficient body mass to allow larval bay anchovy to cope with water viscosity and transition from the ‘pause-travel’ to the ‘cruise-searching’ swimming and foraging strategy (Chesney 2008). Sublethal impacts of oil exposure affecting movement and foraging during this important life stage can result from malformations or impaired sensory or cognitive capability and reduce the survivability of bay anchovy larvae beyond the direct effects of toxicity-induced mortality (Blaxter and Hallers-Tjabbes 1992; Carvalho et al., 2008; Hicken et al., 2011; Johansen et al., 2017; Magnuson et al., 2018; Rowsey et al., 2019; Schlenker et al., 2019a).

Past studies have established total polycyclic aromatic hydrocarbon concentrations in crude oil high-energy water accommodated fractions (HEWAFs) resulting in 50% mortality (LC50) of 5- and 21-dph larval bay anchovy exposed for 24 h (0.69 and 1.61 µg L−1) (Duffy et al., 2016) and bay anchovy embryos exposed for 24 and 48 h (9.71 and 1.48 µg L−1) (O'Shaughnessy et al., 2018). These previous studies also assessed latent mortality to better understand long-term effects on survival of bay anchovy larvae following sublethal oil exposure. Our study builds upon that research by evaluating the mortality and malformation rates in larval bay anchovy exposed to oil during their most sensitive stages of development. Embryos and 1-dph larvae were exposed to weathered crude oil HEWAF of environmentally relevant concentrations for 2 or 6 h durations. Larvae exposed as embryos were assessed 48 h after exposure and larvae exposed at 1-dph were assessed immediately and 24 h after exposure in order to determine the effects of exposure concentration, duration, and time after exposure on larval mortality and malformation rates. Determination of LC50 concentrations was not a goal of this study and we report the predicted probabilities of mortality from these experiments to contextualize the sublethal effects. We also evaluated the swimming and foraging behavior of 3-dph first-feeding larval bay anchovy exposed for 2 h, both immediately and 24 h after exposure. Specifically, we hypothesized that exposure concentration would significantly affect the time spent in motion, the number of bursts (or pauses) min−1 (where a burst was a single instance of continuous movement followed by a pause), burst and pause durations, the average swim speed including pauses, the average burst speed and distance, and the tortuosity, or path efficiency.

Section snippets

Bay anchovy culture

Bay Anchovy embryos were collected from a captive wild-caught adult spawning population kept at the Louisiana Universities Marine Consortium (LUMCON). The broodstock was housed in a 2176 L recirculating seawater system with a 1500 L sump tank. The system was maintained at a salinity of 25 psu using Gulf of Mexico seawater (approximately 36 psu) collected and transported from offshore by the R/V Pelican, filtered at 5 µm, UV sterilized, and diluted to 25 psu using carbon filtered, dechlorinated

Mortality following exposure of embryos and 1-day-post-hatch larvae

Embryonic and larval bay anchovy are delicate. It is not unusual to experience high mortality within control or reference treatments (Duffy et al., 2016; O'Shaughnessy et al., 2018), especially during the first days of development which has been described as a critical period (Hjort 1914; Houde 1987; Chesney 2005). Excluding moribund larvae, mortality rates within the unoiled reference seawater groups were 6.33% for embryos assessed 48 h after exposure (Fig. 2), 0.87% for 1-dph larvae assessed

Discussion

Short-duration exposure of bay anchovy embryos and larvae to oil HEWAF caused substantial latent mortality and sublethal effects within a 24–48-h period. The general standard for toxicological studies is to determine LC50 levels that are usually based upon exposure durations of ≥ 24 h (Pasparakis et al., 2019; Grosell et al., 2020). While important, this can lead to conclusions founded on overly-conservative time endpoints for sensitive species early in development (Grosell et al., 2020). Bay

CRediT authorship contribution statement

Ryan T. Munnelly: Conceptualization, Methodology, Formal analysis, Investigation, Data curation, Writing – original draft, Visualization, Project administration. Claire C. Windecker: Conceptualization, Methodology, Investigation, Data curation, Writing – review & editing, Visualization. David B. Reeves: Formal analysis, Writing – review & editing, Visualization. Guillaume Rieucau: Writing – review & editing. Ralph J. Portier: Conceptualization, Formal analysis, Writing – review & editing,

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We thank the Gulf of Mexico Research Initiative for funding (project number GoMRI-021; principle investigators Edward Chesney and Ralph Portier) and Sarah Webb for insights regarding larval malformations. This work adhered to The Code of Ethics of the World Medical Association. This work has not been previously published. The views and conclusions contained in this document are those of the authors and should not be interpreted as representing the opinions, views, or policies of the National

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