Elsevier

Progress in Oceanography

Volume 198, November 2021, 102676
Progress in Oceanography

Impact of extreme environmental conditions: Foraging behaviour and trophic ecology responses of a diving seabird, the common diving petrel

https://doi.org/10.1016/j.pocean.2021.102676Get rights and content

Highlights

  • Successive summer marine heatwave events in south-eastern Australia.

  • Bottom-up effect inducing major impact on the breeding and foraging ecology of a zooplanctivorous seabird.

  • Common diving petrels exhibited abnormally low breeding success, increased foraging effort and shifted to lower quality prey following marine heatwave events.

  • Results indicate the relevance of such species to monitor the effects of changing oceanographic conditions.

Abstract

The reproductive success of birds is strongly driven by environmental conditions at different time scales. Thus, during periods of low food availability, breeding success is constrained by the ability of adults to adapt their foraging effort and feeding behaviour to maintain regular incubation shifts and chick provisioning. However, while large seabirds can buffer disruptions in prey availability, the ecophysiological constraints of smaller species may limit their behavioural flexibility. By combining information on at-sea movements, foraging habitat, trophic niche, and breeding success, this study evaluated the effects of intense variability in oceanographic conditions on common diving petrels (Pelecanoides urinatrix) at the northern extent of their range in south-eastern Australia during four consecutive breeding seasons. Unusually low breeding success (6 and 0%) was observed during two years with intense heatwave events, which were associated with higher foraging effort (foraging trips twice longer) and a substantial shift in trophic niche (lower blood δ15N values). These findings suggest that common diving petrels in Bass Strait may have reached a critical threshold above which buffering the effects of environmental variability on their reproductive output is not possible. The clear cascading impacts that marine heatwaves have on zooplankton feeders illustrate the profound bottom-up effect induced by such extreme environmental variations, and suggest strong impact on higher-trophic levels. The wide, circumpolar breeding distribution of the common diving petrel, and its high sensitivity to variations in oceanographic conditions, suggest that this species may be a suitable model to study short-term and long-term behavioural responses to the effects of climate change throughout the Southern Ocean.

Introduction

Seabirds forage in a patchy and dynamic environment where prey is unevenly distributed (Hunt, 1990, Weimerskirch, 2007). The variation in physical characteristics of the ocean such as temperature, salinity or currents, strongly influence the distribution and availability of prey which, in turn, determine the foraging behaviour of consumers (Franks, 1992). Individuals must be flexible in their foraging behaviour and diet, according to spatio-temporal variations in the abundance and distribution of prey species. Thus, seabirds should adapt their strategy at different time scales (i.e. daily, seasonally or annually) to ensure survival and maximise reproductive output (Haury et al., 1978, Weimerskirch et al., 1993). However, climate change is likely to challenge species, as the anticipated increased alterations in the distribution, abundance and diversity of prey should affect their capacity to cope with environmental variability (Chambers et al., 2011).

Seabirds have been extensively used as ecological indicators of the impacts of environmental variations (Cairns, 1992, Piatt et al., 2007, Bost et al., 2008). During periods of low prey abundance, breeding seabirds can adjust their behaviour by increasing their foraging effort and/or adapting their diet (Harding et al., 2007, Cohen et al., 2014). However, behavioural plasticity varies greatly between species and/or populations (Gilmour et al., 2018), and seabirds with less flexible foraging strategies or capabilities may not cope with drastic environmental variability (Quillfeldt and Masello, 2013, Jakubas et al., 2020). Due to their relatively easier access for data collection, the majority of studies have focused on large iconic species, resulting in knowledge being mostly restricted to species of higher trophic level, broad diet and/or large foraging range (Chiaradia et al., 2010, Price et al., 2020). Consequently, our understanding of the links between seabird parameters and variation in oceanographic conditions is limited (Grémillet & Charmantier, 2010), with little information available for species feeding locally on low trophic level prey.

This is exemplified by small pursuit-diving seabirds with high flight costs that might be less able to buffer the consequences of reduced prey availability and longer foraging trips (Elliot et al., 2013). While significant advances have been made in recent years for small Northern Hemisphere alcids (e.g. Grémillet et al., 2012, Amélineau et al., 2019, Jakubas et al., 2020), information on the at-sea movements and foraging behaviour of Southern Hemisphere diving petrels (Procellaridae), and their capacity to adapt, is deficient (Chastel et al., 1995, Cherel et al., 2014). This is of concern considering the wide distribution and large biomass the species comprises (Marchant & Higgins, 1990). For example, the common diving petrel (Pelecanoides urniatrix, study species) is a ubiquitous species of the Southern Ocean estimated to 20–30 million individuals (conservative estimation based on the estimated breeding pairs; Marchant and Higgins, 1990, Brooke, 2004) and contributing to 600–900,000 tonnes of crustacean biomass consumption annually (estimation based on the average consumption per individual; Guinet et al., 1996).

During the breeding season, common diving petrels exhibit a unimodal foraging trip duration strategy. This contrasts with most of the other small Procellariiformes that display a dual foraging strategy by alternating short and long foraging trips (Weimerskirch et al., 1994, Chastel et al., 1995). Across its wide distribution encompassing different environmental conditions, the common diving petrel consistently does short daily trips, during both the incubation (Navarro et al., 2013, Zhang et al., 2019, Dunphy et al., 2020) and chick-rearing periods (Roby, 1989, Weimerskirch et al., 1994, Fromant et al., 2020a). This consistent behavioural pattern between populations and across breeding stages could highlight a very high efficiency in foraging and illustrate the species adaptation capacity to different local environments. Conversely, this could indicate a low behavioural plasticity resulting in common diving petrels breeding only where this unimodal foraging behaviour can persist.

Throughout the species range, common diving petrels show differences in breeding phenology (Fromant et al., 2020b), diet (Reid et al., 1997, Bocher et al., 2000, Fromant et al., 2020c) and diving behaviour (Bocher et al., 2000, Navarro et al., 2014, Dunphy et al., 2015), showing how populations adapt to specific conditions. However, it is uncertain if these variations demonstrate behavioural flexibility at the species and/or population level. In particular, the absence of combined multi-year datasets on the trophic and foraging behaviour at a given locality impedes our understanding of how small, abundant seabirds such as diving petrels adapt to inter-annual environmental changes.

Despite its relatively low primary productivity, Bass Strait, the shallow (50–100 m) continental shelf area between mainland Australia and Tasmania, hosts 60% of Australian seabirds (Ross et al., 2001). Currents within Bass Strait are complex and dynamic, fluctuating spatially, seasonally and annually, and being influenced by tides, winds and density-driven flows (Sandery & Kämpf, 2007). This region is also one of the most rapidly changing areas of the global ocean, characterised by warming waters and changing currents (Cai et al., 2005, Poloczanska et al., 2007). These ongoing changes are likely to deeply influence the abundance and distribution of cold water zooplanktonic communities (Evans et al., 2020), and could potentially affect zooplanktivorous species such as common diving petrels (Chambers et al., 2011, Evans et al., 2021). In particular, coastal krill (Nyctiphanes australis), the main prey of common diving petrel in Bass Strait (Schumann et al., 2008, Fromant et al., 2020c), exhibits high sensitivity to increased ocean temperatures (Young et al., 1993, Mills et al., 2008). Furthermore, Bass Strait represents the northern extent of the common diving petrel range, and the predicted modification of oceanographic parameters in the region are likely to have a profound effect on this small and geographically isolated population (Schumann et al., 2014). Exploring the foraging and trophic ecology of common diving petrels in such a challenging environment will provide valuable information on the extent of its behavioural flexibility and contribute to our understanding of the capacity of small planktonic feeders to buffer contrasted environmental fluctuations.

The present study was conducted over four consecutive years on common diving petrels breeding in Bass Strait. Its aims were to determine: (1) their at-sea movements and habitat use; (2) trophic niche; and (3) inter-annual variation in relation to environmental parameters and reproductive output. Specifically, south-eastern Australia experienced over the last decade successive intense summer marine heatwaves (prolonged periods where ocean temperatures are above the climatological average; Oliver et al., 2017, Perkins-Kirkpatrick et al., 2019). If these extreme rises in sea surface temperature induce major shifts in zooplankton population structure (Evans et al., 2020), the cascading effect that marine heatwaves have on upper trophic levels remains unknown. We predicted that (1) diving petrel trip duration and foraging area would increase in response to the negative effect of marine heatwaves on cold-water zooplanktonic prey; (2) the shifts in prey availability would induce a modification in the birds’ trophic niche; and (3) the resultant increased in foraging effort would negatively impacts their breeding success.

Section snippets

Study site and animal instrumentation

The study was conducted during the incubation and chick-rearing periods over four consecutive years (2017–2020) on Kanowna Island (39°15′S 146°30′E) in northern Bass Strait, south-eastern Australia. This island is a breeding site for seven seabird species (Fromant et al., 2020d), including 250–500 pairs of common diving petrels (2–4% of the northern Bass Strait population; Schumann et al., 2014). Some study nests (20–30 per year) were randomly located at the start of each breeding season to

Inter-annual variations of oceanographic conditions

During the whole study period, SST varied strongly, ranging from 10.9 to 21.5 °C, exhibiting an annual cycle with significant differences between the seasons (ANOVA, F641.1 = 69.925, P < 0.001), and significant inter-annual variations (ANOVA, F197.63 = 58.194, P < 0.001). Importantly, the average temperature in summer preceding the common diving petrel breeding season in 2018 (18.5 ± 0.9 °C) and 2019 (18.2 ± 1.1 °C) were significantly warmer than in 2017 (17.1 ± 1.0 °C) and 2020

Discussion

Using a combination of GPS tracking and stable isotope analyses, the present study documented for the first time substantial variations over four successive breeding cycles in the at-sea movements, foraging behaviour and trophic niche of a small planktonic forager, the common diving petrel. The salient features of the results can be summarized as following: (i) these inter-annual variations coincided with drastic fluctuations in reproductive success and were associated with intense summer

Declaration of Competing Interest

The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: John Arnould reports financial support was provided by Sea World Research and Rescue Foundation. Aymeric Fromant reports financial support was provided by BirdLife Australia. John Arnould reports a relationship with Sea World Research and Rescue Foundation that includes: funding grants. Aymeric Fromant reports a relationship with BirdLife Australia that

Acknowledgements

Fieldwork was conducted on Wamoon country, land of the Boon Wurrung, Bunurong and Gunaikurnai people. The authors thank the numerous volunteers for their help in the field, and G. Guillou from the Plateforme Analyses Isotopiques of the LIENSs laboratory for running stable isotope analysis. Thanks to the CPER (Contrat de Projet Etat-Région) and the FEDER (Fonds Européen de Développement Régional) for funding the IRMS of LIENSs laboratory. The IUF (Institut Universitaire de France) is

Author contributions

AF conceived the study, collected field data, did the statistical analyses and drafted the manuscript; KD and JAB participated in the data analysis, helped drafting the manuscript and critically revised it; YHE, AL, JAB, BRG participated to the data collection, helped drafting the manuscript and critically revised it; MBF, PB and YC were involved in stable isotopes analysis, helped drafting the manuscript and critically revised it;

JPYA, CAB participated in the conception and coordination of the

Funding statement

This study was supported logistically and financially by Sea World Research and Rescue Foundation Inc. and Birdlife Australia.

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