Changes in habitat use by a deep-diving predator in response to a coastal earthquake

Highlights

• Sperm whales responded to earthquake-triggered changes in a submarine canyon.

• Surface intervals between dives increased by 25% for one year after the earthquake.

• Return to pre-earthquake levels after one year suggested recovery of foraging efficiency.

• Whales exhibited long-lasting changes in distribution of core foraging areas.

Abstract

Earthquakes can significantly impact ecosystem function and survivability of marine organisms, however their effect on marine predators remains unknown. In November 2016, a 7.8 magnitude earthquake triggered a ‘canyon flushing’ event in the submarine canyon of Kaikōura (New Zealand), a year-round foraging ground for sperm whales (Physeter macrocephalus). Underwater landslips and turbidity currents caused significant changes to the seafloor and removed large quantities of benthic biomass from the canyon. To investigate the potential impact of the earthquake on habitat use by sperm whales, we used a multi-year dataset to quantify changes in their behaviour, foraging distribution and use of food resources before and after the earthquake. The diving locations and behaviour of individual whales were recorded during summer and winter from January 2014 to January 2018, and samples of sloughed skin were collected for bulk and amino acid specific stable isotope analyses. While blow rates remained unchanged, the mean surface interval between dives was 25% longer for about one year after the earthquake, potentially reflecting increased effort searching for prey. Stable isotope ratios of sperm whale skin provided no evidence for change in diet. However, significant changes in the distribution of core foraging areas indicated shifts in habitat use for at least one year, potentially driven by changes in the seafloor and prey availability following the canyon flushing. Overall, our observations suggested that the earthquake caused alterations in the foraging patterns of sperm whales over a period of at least 12 months. This was the first study to quantify the impact of an earthquake on a marine mammal population, providing new insights into how top predators react and adapt to large-scale events of natural disturbance.

Introduction

Extreme natural events, such as earthquakes, hurricanes and volcanic eruptions are rare, but can profoundly impact ecosystems through modifications to habitat and mortality of plants and animals (Bell and Hall, 1994; Fraile-Nuez et al., 2012; Kitahashi et al., 2014). Knowledge of how animal populations respond to such events is important for understanding the ecological impacts of large-scale disturbances and the risks they pose to population viability. The effects of earthquakes on marine species, especially mobile organisms, are poorly understood. With the exception of observations of a fin whale (Balaenoptera physalus) immediately following a 5.5 magnitude earthquake (Gallo-Reynoso et al., 2011), the effects on marine mammals are undocumented. Because earthquakes are infrequent and unpredictable, the opportunities to assess their impact on marine mammal populations are extremely rare.

In November 2016, a 7.8 magnitude earthquake hit Kaikōura, New Zealand, and was described as one of the most complex crustal earthquakes ever recorded (Hamling et al., 2017). Strong ground shaking triggered widespread underwater mudslides in the submarine canyon off Kaikōura, causing a full flushing event and powerful turbidity currents, as well as changes in bathymetry of up to 50 m (Mountjoy et al., 2018). The Kaikōura Canyon is a highly productive deep-sea habitat (De Leo et al., 2010) and a foraging ground for male sperm whales (Physeter macrocephalus; Childerhouse et al., 1995), deep-diving predators that use echolocation to find their prey (Watkins et al., 1993; Madsen et al., 2002). Sperm whales have an important ecological role as top predators (Heithaus et al., 2008; Rosenblatt et al., 2013) and are a key natural asset for the local tourism industry, which is the main driver of Kaikōura's economy (Curtin, 2003). The abundance of sperm whales foraging in the area has almost halved over the last three decades (Somerford, 2018), but the causes for the decline remain unknown. The decline makes the population particularly vulnerable to additional impacts, highlighting the importance of monitoring the whales' responses to disturbance events. The sperm whales of Kaikōura have been studied since 1990. Data on abundance (Childerhouse et al., 1995; Somerford, 2018), behaviour (Jaquet et al., 2000, 2001; Miller et al., 2013; Guerra et al., 2017), distribution (Jaquet et al., 2000) and trophic ecology (Guerra, 2018) gathered prior to the earthquake provided a unique opportunity to assess the earthquake's impact on the population.

There are several ways in which earthquakes and subsequent aftershocks could affect sperm whales. In the short-term (hours to days), potential impacts include noise and re-suspension of sediment. Odontocete cetaceans, including sperm whales, depend on sound for communication, detection of prey and navigation, and are also highly sensitive to noise (e.g. Richardson et al., 1995; Southall et al., 2007). Earthquakes produce among the loudest underwater sounds, characterised by low-frequency noise similar to anthropogenic explosions (Hildebrand, 2009). Demonstrated impacts of underwater noise on cetaceans include injury, hearing damage, displacement and behavioural modifications (Ketten et al., 1993; Richardson et al., 1995; Nowacek et al., 2007). Re-suspension of sediment has the potential to interfere with the whales’ echolocation, as increased turbidity can impede propagation and processing of sound (Krahforst et al., 2012). Over longer periods (months to years), potential impacts include changes in distribution or foraging brought on by physical and biological alterations to deep-sea habitats. In the case of the Kaikōura earthquake, the large-scale erosion and sediment flow through the canyon had a dramatic impact on the seafloor structure and benthic ecosystem (Mountjoy et al., 2018). Of particular importance was the removal of benthic invertebrate communities which previously existed in the upper canyon (De Leo et al., 2010), with an estimated 39 × 10⁶ kg of biomass removed due to sediment flushing (Mountjoy et al., 2018). Such impacts on benthos are likely to have significant consequences for the canyon food web, and thus may impact the top predators, including sperm whales, which forage on both demersal and pelagic prey (Miller et al., 2013; Guerra et al., 2017).

In the present study we aimed to identify the ecological impact of the Kaikōura earthquake on the sperm whale population by assessing pre-vs. post-earthquake patterns in diving behaviour, spatial distribution, and utilisation of food resources. Specifically, we quantified the temporal variability in: (1) ventilation and echolocation behaviour, including the time spent at the surface between dives, intervals between blows, and time taken to start echolocating after diving. These variables are related to metabolic rate and diving strategy (e.g., Richter et al., 2006; Fais et al., 2015), and can thus reflect changes in foraging efficiency; (2) spatial distribution, by examining the location of high-use areas; and (3) food resources utilised by sperm whales, using bulk and amino acid specific stable isotope analyses of sloughed whale skin. To address these questions, we analysed data gathered before and after the earthquake over a period of four years, and partitioned seasonal and annual variability.