Decline and recovery of pelagic acoustic backscatter following El Niño events in the Gulf of California, Mexico

Highlights

• Timeseries of acoustic backscatter as a proxy for midtrophic biomass in the Gulf of California.

• ENSO explained more variability than regional temperature or chlorophyll concentration.

• Backscatter decreased significantly during the positive phase of ENSO (El Niño).

• Mean backscatter took more than two years to recover to pre-El Niño levels.

Abstract

Climatic variability exerts enormous pressures on the structure and function of open ocean ecosystems. Although the responses of primary producers and top predators to these pressures are being increasingly well-documented, little is known about how midtrophic communities respond to oceanographic and climatic variability. We address this knowledge gap through a study of the effects of El Niño Southern Oscillation (ENSO) and local environmental conditions on acoustic proxies of the midtrophic community in the Gulf of California, Mexico. We quantified the intensity and distribution of nighttime acoustic backscatter (120 kHz) in the upper 200 m of the water column during 10 oceanographic cruises (2007–2017) and described its response to environmental variability using generalized additive models. ENSO conditions were the strongest drivers of variability in backscatter after accounting for seasonal increases in backscatter with sea surface temperature and chlorophyll-a concentration. Acoustic backscatter in the central Gulf of California decreased significantly during the positive phase of ENSO. Following El Niño events in 2009–10 and 2015–16, mean backscatter declined by an order of magnitude and remained depressed for more than two years before recovering to pre-El Niño levels. Scattering layer density increased with total backscatter, likely an influential factor determining prey availability for pelagic predators. Our findings demonstrate large and sustained impacts of El Niño on the midtrophic community in the Gulf of California and further highlight the need to better understand the responses of midtrophic communities to environmental variability.

Introduction

Over the past century, marine capture fisheries production has quadrupled (FAO, 2016) and human activities, particularly greenhouse gas emissions, have contributed to warming of the global ocean by ∼ 0.6 °C (Levitus et al., 2001, Gleckler et al., 2016). Our observations and understanding of the ways pelagic organisms respond to these pressures are heavily skewed toward primary producers and top predators. On average, the global biomass of primary producers in the ocean is decreasing in response to ocean warming (Polovina et al., 2008, Boyce et al., 2010, Rykaczewski and Dunne, 2011). Predatory fishes, birds, and mammals are also rapidly changing in abundance and distribution, often in response to the combined pressures of fishing and warming (Veit et al., 1997, Lewison et al., 2004, Polovina et al., 2009, Hazen et al., 2013, Woodworth-Jefcoats et al., 2015).

Food-web models suggest anthropogenic pressures on pelagic ecosystems are not simply additive, but that top-down and bottom-up effects of these pressures may be modulated by the midtrophic organisms in pelagic food webs (Woodworth-Jefcoats et al., 2015, Choy et al., 2016). Midtrophic biomass is composed of diverse fishes, crustaceans, gelatinous organisms, and cephalopods, many of which aggregate into relatively dense communities that are observable as acoustic scattering layers within the upper 1000 m of the water column (Kloser et al., 2009, Ritz et al., 2011, Klevjer et al., 2016). In addition to linking production at the base of food webs (phytoplankton) to top predators, midtrophic organisms help to link surface to deep pelagic habitats through diel vertical migration (Ducklow et al., 2001, Ambriz-Arreola et al., 2017). Daily movement between nighttime feeding grounds at the ocean surface and daytime refuge at depth actively contributes to carbon sequestration as part of the pelagic biological pump. This ‘mesopelagic-migrant pump’ component accounts up to 50% of the total downward carbon transport (Zhang and Dam, 1997, Hidaka et al., 2001, Schukat et al., 2013), and is surpassed only by the gravitational pump component with respect to carbon export rates (Boyd et al., 2019).

Changes in the abundance of midtrophic organisms are thus expected to impact both the ecological and biogeochemical functions of pelagic ecosystems. Variability in the biomass of midtrophic organisms has been observed at coarse spatial scales (e.g. across ocean basins, Kloser et al., 2009, Irigoien et al., 2014) and fine temporal scales (e.g. days to weeks; McClatchie and Dunford, 2003), but there are few time series that can demonstrate the responses of these communities to large-scale environmental variability over a prolonged period (Godø et al., 2014, Koslow et al., 2019, Proud et al., 2017).

Climatic conditions define baseline ocean heat content and atmosphere interactions and mitigate seasonal oceanographic variability in pelagic habitats. El Niño Southern Oscillation (ENSO) is a recurring climate pattern that describes heat content distribution in the tropical Pacific Ocean and is quantified by the multivariate ENSO Index (MEI.v2, NOAA Physical Sciences Laboratory, https://psl.noaa.gov/enso/mei/). Over the past four decades (1980–2020), there have been eight El Niño events (positive ENSO extremes defined as at least five consecutive months of MEI.v2 > 0.5), characterized by a major redistribution of heat content from west to east – in 1982–83, 1986–87, 1991–94, 1997–98, 2002–03, 2006–07, 2009–10, and 2015–16 (https://psl.noaa.gov/enso/mei/). Regional conditions in the Gulf of California, Mexico, a marginal sea located in the northeastern subtropical Pacific, are greatly impacted by the water masses available for exchange at the mouth of the gulf (Herrera-Cervantes et al., 2007, Staines-Urías et al., 2009, Portela et al., 2016). During El Niño events, tropical water masses become more available for exchange (Baumgartner et al., 1985, Frawley et al., 2019) and the Gulf of California experiences increased sea surface temperature (SST) and subsurface warming (Lluch-Cota et al., 2007, Lluch-Cota et al., 2010), as well as overall diminution and redistribution of phytoplankton biomass (Kahru et al., 2004, Robinson et al., 2016).

Strong El Niño events (MEI.v2 > 1) in 1982–83 and 1997–98 were associated with changes in abundance of anchovy, sardines, and other midtrophic organisms in the Gulf of California (Lavaniegos et al., 1989, Lavaniegos-Espejo and Lara-Lara, 1990, Sánchez-Velasco et al., 2004, Velarde et al., 2013, Velarde et al., 2015, Petatán-Ramírez et al., 2019, Arreguín-Sánchez et al., 2021). A range of responses was observed for predators at higher trophic levels in conjunction with events in 1997–98 and 2009–10. Elegant terns (Thalasseus elegans) failed to nest on their specific site on Isla Raza in the central Gulf of California and instead shifted north to nest well outside the Gulf (Velarde et al., 2013, Velarde et al., 2015). Humboldt squid (Dosidicus gigas) show a more complex response: squid biomass redistributed from neritic to pelagic habitats; lifespan was severely reduced (> 1.5 years to < 0.5 year); and size at maturity was reduced (> 60 cm mantle length (ML) and 10 kg body mass to < 20 cm ML and 0.1 kg body mass) (Hoving et al., 2013, Robinson et al., 2016). Although both predators recovered rapidly after the strong El Niño of 1997–98, recovery after the 2009–10 event was erratic and further hindered by the strong 2015–16 El Niño (Velarde, pers. comm.; Frawley et al., 2019). Prey biomass and density are both important determinants of habitat selection and foraging success for marine predators (Benoit-Bird, 2009, Hazen and Johnston, 2010, Benoit-Bird et al., 2013, Carroll et al., 2017), and prey availability may mitigate predator responses to climatic events. However, the responses of midtrophic prey in the Gulf of California to El Niño events are poorly described and represent a critical gap in our understanding of the effects of environmental variability on pelagic food webs.

To estimate the response of midtrophic communities to environmental variability, we quantified acoustic backscatter intensity and distribution in the central Gulf of California based on ten oceanographic surveys carried out between January 2007 and June 2017. This period included warm- and cool-season sampling as well as three El Niño events (2006–07, 2009–10, and 2015–16). The goals of the present study were 1) to assess sensitivity of nighttime acoustic backscatter in the upper 200 m of the water column to ENSO conditions, sea surface temperature, and sea surface chlorophyll-a concentrations, and 2) to determine the time scales over which El Niño events impacted the midtrophic assemblages that contribute to backscatter. This work provides unique insight into the relative impacts of local environmental and ENSO conditions on midtrophic biomass inferred from acoustic backscatter in the Gulf of California and may help us understand how projected increases in the frequency and intensity of El Niño events will affect midtrophic organisms in the eastern Pacific Ocean.