The Foraging Ecology of Caspian Terns (Hydroprogne Caspia) on Peel-Harvey Estuary, South-Western Australia

Home , Birds of Australia, Caspian tern, Chinese crested tern, Eastern osprey, Inca tern, Lari

The foraging ecology of Caspian Terns (Hydroprogne caspia) on Peel-Harvey Estuary, south-western Australia.

Submitted by Susie Stockwell

This Thesis is presented for the degree of Bachelor of Science Honours School of Veterinary and Life Sciences, Murdoch University, 2019

Declaration

I declare that this Thesis is my own account of my research and contains as its main content work, which has not previously been submitted for a degree at any tertiary education institution.

Susie Jill Stockwell

Acknowledgements

I am filled with gratitude for the baalap (people), boodja (places) and kaadadjan (knowledge), as well as the beautiful birds themselves, which have been integral to the success of this project. Firstly, to my incredible supervisors, Professor Neil Loneragan, Dr. Nic Dunlop and Claire Greenwell, thank you for your support, your time and your generosity in sharing ideas, advice, and opportunities throughout the project. Your passion for ecological sciences and conservation has been inspiring, and I am so grateful for your encouragement, understanding, and support throughout our Caspian project. Thank you especially to Claire Greenwell, my fellow ‘ternologist,’ you have been an academic inspiration and such an amazing friend, I am so grateful for your love and support and our birdy adventures throughout the project. I have been overwhelmed with gratitude for the community support for the Caspian Tern project, in particular to Bob Patterson, Dave Martin, and Jesse Steele. Your passion for the birdlife of Peel-Harvey Estuary, and your knowledge, friendship, and photographic contributions have been invaluable throughout the field season. Thank you also to Dr. Peter Coulson, Dr. James Tweedley, Katherine Stockwell, and Kate Born, for your time and enthusiasm with the otolith, PRIMER and GIS components of the project. To my wonderful family, friends, and all who have been part of my journey from the central Kimberley to the south-west coast and everywhere in between. I am thankful for your love, support, and friendship. I am also grateful and acknowledge the Wadjuk-Noongar people as Traditional Custodians of Peel-Harvey Estuary, and pay respects to all Elders past and present. Finally, I would like to express my gratitude for all who invest their hearts and minds in the love and conservation of our natural world, not only on the Peel-Harvey but across the world. Sir David Attenborough is famously quoted, saying: "No one will protect what they don't care about, and no one will care about what they have never experienced." While I’ve always believed this to be the case, this project has reminded me time again of the beauty of nature and the power of humanity in contributing towards its protection.

Abstract

Terns and noddies (subfamily Sterninae), comprising almost 15% of all seabird species, are largely piscivorous predators found from temperate to tropical regions in both coastal and pelagic systems. The largest species, the Caspian Tern (Hydroprogne caspia) has a cosmopolitan distribution, but despite this they are largely understudied, especially the finer- scale patterns of their distribution, abundance and foraging ecology throughout non-breeding periods. In south-western Australia, most H. caspia populations are restricted to two or three pairs, except for a large group of approximately 120 birds that breed annually on Penguin

Island, Shoalwater Bay. This study investigated the foraging ecology of H. caspia over the first five months of their non-breeding season, from October 2018 to February 2019 on the Ramsar- listed Peel-Harvey Estuary. A single overnight roosting site for H. caspia was identified on the

Estuary where a maximum of 147 birds were recorded in mid-February 2019. Tern foraging activity was concentrated at six main areas across the estuary, although tern counts and foraging activity varied between these areas, and foraging activity also differed significantly with time of day throughout the study period – it was greatest in the morning block. Overall, H. caspia were recorded taking 17 prey species (16 fish and one crustacean) on the Estuary, the most common being whitings (Sillaginidae), mullets (Mugilidae) and Eight-lined Trumpeter

(Pelates octolineatus), comprising 35.0%, 33.9% and 14.4% respectively of their observed catch. The results of this study highlight the significance of the Peel-Harvey Estuary for the conservation of H. caspia in south-western Australia and the connectivity between the birds on the Estuary in the non-breeding period and those on Penguin Island during the breeding season.

In addition, H. caspia appear to be strong candidates as biological indicators of Estuary health.

The results of this study provide a basis for an ongoing monitoring plan to contribute towards the conservation and management of the birds and the environment at this Ramsar-listed site.

Table of Contents

Declaration ...... 2 Acknowledgements ...... 2 Abstract ...... 3 Table of Contents ...... 4 Chapter 1. General introduction ...... 6 1.1 Foraging ecology of seabirds ...... 7 1.2 Caspian Terns (Hydroprogne caspia) ...... 8 1.3. Seabirds as indicators of ecosystem health ...... 12 1.4. Study aims and research questions ...... 14 Chapter 2. Literature review: the foraging ecology and energetic requirements of seabirds with a focus on the larger terns ...... 15 Summary ...... 15 2.1. Introduction ...... 16 2.1.1 Larger terns ...... 17 2.1.2 Aims of the review ...... 19 2.2. Foraging ecology of larger terns ...... 21 2.2.1 Foraging area ...... 22 2.2.2 Diet ...... 27 2.2.3 Foraging behaviour ...... 28 2.3. Energetic requirements ...... 31 2.3.1 Estimating field metabolic rates ...... 32 2.3.2 Energetic requirements of terns ...... 33 2.4. The significance of understanding foraging ecology ...... 34 2.4.1 Seabird conservation ...... 34 2.4.2 Seabirds as biological indicators ...... 36 2.5. Knowledge gap ...... 36 2.6. Conclusion ...... 37 Chapter 3. Patterns of distribution, abundance and foraging ecology of Caspian Terns (Hydroprogne caspia) on the Peel-Harvey Estuary, south-western Australia...... 39 Summary ...... 39 3.1. Introduction ...... 40 3.1.1. Seabird foraging ecology ...... 40 3.1.2. Caspian Terns in south-western Australia...... 41 3.2. Methods...... 45 3.2.1 Study area ...... 45

3.2.2 Tern abundance and distribution ...... 48 3.2.3 Foraging activity ...... 51 3.2.4 Determining diet from bill-loaded images and regurgitation pellets ...... 54 3.3. Results ...... 60 3.3.1 Environmental conditions in the Peel-Harvey Estuary ...... 60 3.3.2 Abundance and distribution ...... 62 3.3.3 Foraging activity ...... 67 3.3.4 Diet ...... 71 3.4 Discussion ...... 80 3.4.1. Abundance and distribution ...... 80 3.4.2 Foraging activity ...... 86 3.4.3 Diet ...... 89 3.4.4 Energetic requirements of non-breeding terns ...... 91 3.4.5 Conclusion ...... 93 Chapter 4. Conclusions and recommendations ...... 95 4.1. Conclusions ...... 95 4.2. Recommendations: the use of Caspian Terns as bio-indicators on the Ramsar-listed Peel- Harvey Estuary, south-western Australia ...... 98 4.2.1 Caspian Terns as bio-indicators on Peel-Harvey Estuary ...... 98 4.2.2 Proposed monitoring program ...... 101 References ...... 104 Appendix 1. Summary of larger terns featured in this literature review and their foraging ecology...... 110 Appendix 2. Identification guide to prey species in Caspian Tern (Hydroprogne caspia) diet, as recorded between October 2018 and February 2019 across Peel-Harvey Estuary from (a) bill-loaded images and (b) otoliths in regurgitation pellets, with reference images. . 112 Appendix 3. Observations of foraging behaviour of Caspian Terns (Hydroprogne caspia) on Peel-Harvey Estuary during their non-breeding period...... 117 Appendix 4. Proposed monitoring plan for Caspian Terns (Hydroprogne caspia) as a biological indicator of ecosystem health on Peel-Yalgorup Ramsar site 482...... 122

Chapter 1. General introduction

This Thesis investigates the distribution, abundance and foraging ecology of a large seabird, the Caspian Tern, Hydroprogne caspia, in a large, temperate Australian estuary, during their non-breeding period. Seabirds are high-level predators feeding mainly on fish and cephalopods in marine ecosystems worldwide (Serventy et al. 1971; Burger et al. 1996). The overall aim of this Thesis is to gain a greater understanding of the ecology of large terns, particularly H. caspia, and its foraging ecology during their non-breeding period. This has been achieved by reviewing the foraging ecology and energetic requirements of larger terns (Chapter

2) and investigating the distribution, abundance, foraging ecology and diet of the largest tern species, H. caspia, in the Peel-Harvey Estuary in south-western Australia (Chapter 3). In this

Chapter, I provide an overview of predation, seabird foraging ecology, the biology of H. caspia, and the value of seabirds as indicators, and introduce the overarching aims of the Thesis.

Predation is a key ecological and evolutionary process in determining the structure and function of ecosystems worldwide (Estes et al. 2011). Top predators exert a top-down influence on lower trophic levels in food webs and in doing so, play an essential role in maintaining the trophic balance and health of their ecosystem (Myers et al. 2007). As occupants of high positions in the food web, they regulate the abundance of species at lower trophic levels by direct (predation) and indirect ecological interactions e.g., by reducing numbers for smaller predators or species with greater competitive abilities (Bornatowski et al. 2018). This allows other species to co-exist (Bornatowski et al. 2018), and in doing so, shapes the structure and function of their community (Collar et al. 2017). They can create niches and resources within the ecosystem for other species such as scavengers, and drive natural selection of prey species by removing older or weaker individuals (Paterson et al. 2018). Despite their relatively low abundance within food webs, top-predators exert a disproportionate influence over these environments (Collar et al. 2017). Consequently, the loss of these species from an environment,

6 which can result in an overabundance of prey, meso-predator release and trophic cascades, all of which alter ecosystem composition (Estes et al. 2011; Heupel et al. 2014).

Marine ecosystems are naturally dynamic, and frequent changes in abiotic conditions and trophic composition lead to fluctuations and unpredictability in prey availability (Gaglio 2017).

Most predatory species have evolved flexible foraging strategies and broad diets in order to meet their energetic requirements and maximise foraging efficiency (Green et al. 2015). The capacity for prey switching is a behavioural adaptation by predators to buffer scarcity and variation in food resource availability across their stochastic marine environments (Ferreira et al. 2017). Seabirds, cetaceans, and large pelagic fish species fill higher-level predatory roles across marine ecosystems worldwide (Ferreira et al. 2017). These marine predators share several unifying characteristics including long lifespans, slow growth rates and delayed maturity, and low clutch sizes with high levels of parental care in seabirds and cetaceans (Berg et al. 2010). The potential for replacement among these k-strategists (that is, populations fluctuating at carrying capacity) is achieved over numerous breeding attempts over their lives

(Furness & Monaghan 2011; Greenwell et al. 2019). While these life-history traits enhance their capacity to buffer fluctuations across their environment, there is significant variation between predators in their response to changing conditions (Gaglio 2017).

1.1 Foraging ecology of seabirds

Seabirds form a diverse group of 329 species worldwide (Croxall et al. 2012) and have important roles as predators across coastal and pelagic marine ecosystems (Barrett et al. 2007;

Green et al. 2015). They are predominantly piscivorous and consume an estimated 70 million tonnes of low- to mid-trophic level prey species each year (Brooke 2004). Many seabird species are generalists, and while they can switch between prey and adjust their foraging areas to buffer

7 changing ecosystem conditions, changes in resource availability can impact their populations over time (Crawford et al. 2014; Ferreira et al. 2017).

Foraging efficiency is an important consideration when investigating foraging ecology, involving the balance of energetic requirements with nutritional gain from prey (Campos et al.

2017). It has important implications for daily individual foraging patterns, as well as long-term population trends. Optimal foraging is achieved by maximising the energy obtained from food while minimising the energy expenditure in obtaining food (Campos et al. 2017).

Consequently, taking prey of lower nutritional quality and reducing foraging efficiency (higher energy expenditure or lower energy uptake) can lower recruitment rates and cause population decline over the longer-term (Crawford et al. 2006). The foraging ecology of seabirds can be considered in terms of diet, foraging area, and foraging strategy or behaviour (Zimmer et al.

2008). The energetic and time allocations to different behaviours, such as foraging, has important consequences for the overall energy budgets of seabirds. Energy budgets dictate the capacity of seabirds to adapt their foraging strategies and maintain their energetic requirements, as the energy expenditure associated with foraging can increase under altered ecosystem conditions (Collins et al. 2016; Gaglio 2017). In this way, seabird populations are intimately linked to the condition of their environment and can offer insight into ecosystem health and fish availability (Einoder 2009). The foraging ecology and energetic requirements of seabirds, with a focus on larger terns and noddies (family Laridae, sub-family Sterninae) are explored further in Chapter 2.

1.2 Caspian Terns (Hydroprogne caspia)

Terns and noddies (family Laridae, subfamily Sterninae) form a group of 46 medium- sized seabirds, that are characteristically slender and often pale-coloured (except noddies who are brown and grey in appearance), with the adults of most species adorning a brighter “head-

8 cap” and bill in breeding plumage (Figure 1.1; Menkhorst et al., 2017). Caspian Terns,

Hydroprogne caspia, are the world’s largest species of tern, with a weight range between 530-

780 g, body lengths from 48-54 cm and a wingspan of 127-145 cm (Burger et al. 1996;

Menkhorst et al. 2017). While H. caspia display many features characteristic of the Sterninae, they can be distinguished from other tern species by their size, large, red-coloured bill

(especially while in breeding plumage), and dark panels at their wingtips when in flight (Figure

1.1). Both sexes are superficially similar in appearance, and undergo the same seasonal changes in their plumage once they become adults (Gould 1848). Hydroprogne caspia also has an iconic call that distinguishes it from other species, described by Gould (1848) as “…[a] clamorous, cackling, screeching note which it constantly utters while flying over”.

Figure 1.1. Caspian Tern (Hydroprogne caspia) identification on plumage: a. breeding adult; b. non-breeding adult; c. fledged juvenile; d. tern in flight (note: dark panels under wingtips). (Photographs by Susie Stockwell)

Distribution and habitat

Hydroprogne caspia has a cosmopolitan but scattered worldwide distribution

(Figure 1.2) where they occupy a range of marine, brackish and freshwater environments including coastal, wetland, estuarine and fluvial systems (IUCN 2019). Urban and peri-urban areas can also be significant for breeding and foraging birds like H. caspia (McKinney & Paton

2009). Birds in the northern hemisphere are annual breeding migrants, whereas those in

Australia tend to be more sedentary, and undergo much shorter movements between their breeding colonies and non-breeding foraging sites (Burger et al. 1996). Although most colonies around Australia comprise small groups of one to three pairs, H. caspia can form larger, monospecific colonies in areas with more abundant food (Burger et al. 1996; Lyons et al. 2005;

Dunlop & McNeill 2017).

Figure 1.2. Global distribution of H. caspia throughout tropical, subtropical and temperate waters of the world (source: IUCN 2019).

Reproductive ecology

Most adult H. caspia breed annually in springtime, between April and June in the northern hemisphere, and August and October in the southern hemisphere (Serventy et al. 1971;

Burger et al. 1996). During this period, they exhibit strong philopatry by returning to their birth colony to breed (Serventy et al. 1971). In general, colonies are located on promontories of small, rocky peninsulas and nearshore islands, or on the sandy flats surrounding large river mouths (Gould, 1848; Burger et al. 1996). Like many seabirds, H. caspia display pair-bonding activities prior to copulation, and in some cases, mate fidelity between breeding years (Serventy et al. 1971). Females lay two speckled eggs in a shallow depression on the ground (Burger et

10 al. 1996), and both parents share the roles of egg incubation, chick provisioning and nest defence (Serventy et al. 1971).

Foraging ecology

The foraging ecology of larger terns and noddies is described in detail in Chapter 2, while that of H. caspia, is summarised briefly here. Hydroprogne caspia usually forage in shallow, sheltered waters, by characteristically plunge-diving for various prey species (Serventy et al.

1971). Their larger size enables them to penetrate the water to greater depths whilst foraging to take benthic forage fish such as mullet, herring and anchovies (Lyons et al. 2005; Dunlop &

McNeill 2017) up to 25 cm in length (Burger et al. 1996). While they are mostly piscivorous predators (Menkhorst et al. 2017), H. caspia have been recorded taking crustaceans, carrion, the eggs and young of other birds as well as insects and earthworms (Burger et al. 1996).

Similar to other tern species, H. caspia are central place foragers throughout their annual breeding season, including the period when incubating their eggs and provisioning their chicks

(Lyons et al. 2005; Monticelli et al. 2008). Adults can forage up to 60 km from the colony during this period to catch fish and meet their elevated energetic requirements at this time

(Whittow & Rahn 1984; Burger et al. 1996; Balance et al. 2008). The length and frequency of foraging trips, as well as relative time spent foraging or attending chicks, changes with food resource availability (Dunlop & McNeill 2017), which has a direct influence on chick survival and the overall recruitment within the population (Anderson et al. 2007). Towards the end of the breeding season, adult birds and their fledgling chicks move away from the colony in order to exploit richer foraging areas (Serventy et al. 1971; Dunlop & McNeill 2017). Aside from this, little is known of the foraging ecology of H. caspia, or other Sterninae throughout non- breeding periods.

1.3. Seabirds as indicators of ecosystem health

Marine environments are increasingly being recognised as a global priority for conservation. However, these systems are vast and can be logistically challenging to monitor

(Parsons et al. 2008). Seabirds, such as shearwaters, puffins, terns and noddies, have been used as sentinel species to provide indicators of ecological health for marine systems (Cairns 1988), as many aspects of their behaviour and life history can be used to monitor changes in marine environments over time (Burger & Gochfeld 2004).

Most seabirds are relatively large in size, diurnally active and long-lived (Burger &

Gochfeld 2004), which makes them good subjects for long-term research, both at individual and population levels. As top predators within marine food webs, they accumulate pollutants such as heavy metals, plastics, and chemicals in their body tissues through their prey, exposing them to elevated contaminant levels from all lower trophic levels (Burger & Gochfeld 2004;

Dunlop 2017). Unlike other marine predators, seabirds return to terrestrial breeding colonies on a regular (often annual) basis, making them reliable and accessible candidates for generating long-term datasets, based on biological parameters (Parsons et al. 2008). For these reasons, monitoring programs for seabirds are being used to enhance the management and conservation of marine ecosystems worldwide (Einoder 2009). However, the use of seabirds as indicators of ecosystem condition and change relies on a sound understanding of their foraging and reproductive ecology (Burger & Gochfeld 2004).

Plasticity in their foraging behaviour and diet over varying temporal scales facilitates the use of seabirds as real-time indicators of forage-fish distribution and abundance, as they have the capacity to find and follow prey species (Sydeman, Thompson, et al. 2017). Additionally, their high energetic requirements, particularly throughout the breeding season, make seabirds especially sensitive to fluctuations in prey availability (Green et al. 2015). By understanding this, seabirds can be used to track changes in fisheries productivity as well as pollutant levels,

12 climatic shifts and altered abiotic conditions (Furness & Camphuysen 1997; Einoder 2009;

Mallory et al. 2010). The connection between seabirds, prey availability and ecosystem condition are reflected in their diet, foraging activity (including time-activity budgets) and recruitment rates at both individual and population levels (Gaglio 2017).

Caspian Terns as bio-indicators on the Peel-Harvey Estuary

As high-level predators, seabirds may be exposed to the accumulation of contaminants in their prey species from the natural system (Furness & Camphuysen 1997; Bond & Diamond

2009). A study of heavy metals in H. caspia tail feathers found elevated levels of methyl- mercury in feathers taken from approximately one-third of adult birds at the Penguin Island breeding colony in south-western Australia (Dunlop & McNeill 2017). The mean mercury concentration was 2.27 mg.kg-1 with values ranging between 0.9 and 5.9 mg.kg-1 (Dunlop &

McNeill 2017). Another species nesting on the same island, the Bridled Tern, Onychoprion anaethetus, had a much lower mean mercury concentration of 0.71 mg/kg-1 ( SD 0.53, n = 10;

Dunlop & McNeill 2017). The differences in the foraging ecology of these two seabird species could explain the differences in mercury accumulation. Hydroprogne caspia forage in shallow water for benthic fish species whereas O. anaethetus forage over the coastal shelf targeting different forage fish species including larval fish associated with seaweed rafts and squid

(Serventy et al. 1971; Dunlop 2017; Dunlop & McNeill 2017).

Detection of contaminants in seabird body tissue, such as mercury in H. caspia, can be a useful indicator of contaminant levels in prey species and their ecosystems (Burger &

Gochfeld 2004). Dunlop and McNeill (2017) offered insight into the foraging and reproductive ecology of this population of H. caspia throughout the breeding period. However, relatively few published studies explore the foraging ecology of seabirds during their non-breeding periods, and even fewer have focussed on H. caspia, despite their cosmopolitan distribution

(Serventy et al. 1971). Prior to this study, information on the foraging ecology of H. caspia during the non-breeding season had not been explored in south-western Australia.

1.4. Study aims and research questions

This study aims to understand the overall foraging ecology of large terns (Chapter 2) and fill the knowledge gap identified by Dunlop and McNeill (2017) on the ecology of the largest tern¸ Hydroprogne caspia, during the non-breeding period in south-western Australia

(Chapter 3). The foraging ecology and energetic requirements of seabirds, with a focus on larger terns and noddies (family Laridae, sub-family Sterninae), is explored in Chapter 2, while

Chapter 3 investigates patterns in the distribution, abundance, and foraging ecology of

H. caspia, in the Peel-Harvey Estuary (Figure 3.1) during the non-breeding season. Here, foraging ecology is considered in terms of three main components: foraging area (range and habitat), behaviour (or strategy) and diet (Zimmer et al. 2008). Chapter 4 presents the conclusions and recommendations from these studies and proposes the use of H. caspia as an indicator of ecosystem health for monitoring the greater Peel-Yalgorup Ramsar-listed site. Key ecological characteristics for the Ramsar site must be monitored, and data provided to a

Technical Advisory Group established to ensure any fluctuation is within the limits of acceptable change set for each component of ecological health (RAMSAR 1971; Hale &

Butcher 2007; Hale 2008). Such a program would provide information for enhancing the management and conservation of H. caspia and the condition of the Peel-Harvey Estuary and its associated wetlands.

Chapter 2. Literature review: the foraging ecology and energetic requirements of seabirds with a focus on the larger terns

Summary

Seabirds form a diverse group of 329 species across the world. Despite their prevalence and importance within their ecosystems, they are amongst the most threatened bird taxa globally, with over one-third of species vulnerable to extinction. Terns and noddies (subfamily

Sterninae) comprise almost 15% of all seabird species; they are largely piscivorous and have a wide distribution: from temperate to tropical regions in both coastal and pelagic systems.

This review has three aims: first, to explore similarities and differences in the foraging ecology of terns and noddies of different body size, in regard to diet, behaviour and foraging area; secondly, to compare their energetic requirements; and thirdly, to highlight key gaps in our knowledge of their foraging ecologies. Terns and noddies employ one of two main foraging strategies, either plunge-diving or surface feeding in order to meet their energetic requirements.

These requirements are largely correlated with body size, although they are also dependent on demographic factors (i.e. the age and sex of birds), as well as ecological factors, including colony latitude and breeding stage. Seabird resource needs increase dramatically during the breeding season as parents invest significant energy in raising their chicks.

Like most seabirds, the foraging ecology of terns and noddies, especially outside their breeding season, is relatively understudied, and yet these birds have significant ecological and anthropogenic value. Seabirds play important roles as top predators within their ecosystems and also hold potential for use as time- and cost-effective ‘indicators’ of changing ecosystem condition or fisheries productivity. This relies upon a sound understanding of their foraging ecology and life history. Studying seabirds, such as terns and noddies, could improve conservation and management of both the birds themselves and their marine ecosystems worldwide.

2.1. Introduction

Seabirds are a diverse group of medium-sized, long-lived birds, with representatives distributed worldwide (Serventy et al. 1971). While there is no conclusive definition to unite all seabirds as one group, they are linked by three main morphological and behavioural characteristics. First, most seabirds are fish-eaters and inhabit marine (coastal and pelagic) environments, although some occupy brackish or freshwater systems including wetlands, inland lakes and rivers (Croxall et al. 2012). Secondly, seabirds spend relatively long periods of time foraging for fish and marine invertebrates, usually alone or in small groups, but are tied to the land for reproduction (Balance et al. 2008). Thirdly, most adult seabirds return annually to breeding colonies on offshore islands or coastal-mainland environments, and many species display strong nest-site philopatry and even mate fidelity (Serventy et al. 1971). In addition to these activities, pair-bonding activities, such as courtship and parental care for small clutches of one to two young, are also typical of most seabirds (Serventy et al. 1971).

While seabirds exhibit great diversity in their form and distribution, they share unifying characteristics in their physiology, behaviour and the roles they play within their respective ecosystems, making them functionally similar. For the purpose of this literature review, a functional, rather than a phylogenetic classification of seabirds has been applied to investigate the foraging ecologies of seabirds and the respective roles they play within their ecosystems.

Following Croxall et al. (2012), 329 species of described, extant species from five orders and eleven families are considered as seabirds; birds that make a living, largely, from marine resources (Table 2.1; Croxall et al., 2012, IOC 2018).

Like most birds, seabirds first evolved from ancestors in the Cretaceous Period, between

145 and 67 million years ago (Prum et al. 2015) and have since diversified to fill marine ecosystems worldwide, with many distinct lineages represented today (Jetz et al. 2012). Despite this phylogenetic diversity between seabirds, they have many structural and functional

16 similarities in appearance, behaviour and strategies employed for foraging and reproduction.

This convergent evolution is largely a result of adaptations to occupy sympatric ecological niches and exploit similar resources (Prum et al. 2015).

Table 2.1. Taxonomic classification of seabird species considered in this literature review, modified from Croxall et al. 2012 and BirdLife and International Ornithological Congress’s master world bird list (v8.2, 2018) (IOC 2018).

Order Family Number of Species Extant Extinct Charadriiformes Alcidae Auks 23 1 (Clade: Lari) Laridae Gulls, Terns & 100 0 Noddies Stercorariidae Skuas & Jaegars 8 0

Phaethintiformes Phaethontidae Tropicbirds 3 0

Procellariformes Diomeidae Albatrosses 22 0 Hydrobatidae Storm-petrels 22 0 Pelecanoididae Diving-petrels 4 0 Procellaridae Petrels & Shearwaters 80 2

Spheniciformes Spheniscidae Penguins 18 0

Suliformes Fregalidae Frigatebirds 5 0 Phalacrocoracidae Cormorants 34 0 Sulidae Gannets & Boobies 10 0

Total: 5 13 329 3

2.1.1 Larger terns

The family Laridae is comprised of gulls, kittiwakes, terns, noddies and skimmers, with an estimated 100 extant species occurring worldwide (Table 2.1). Terns and noddies (family

Laridae, subfamily Sterninae) form a group of medium-sized seabirds, comprising 46 species from 11 genera (Table 2.2; IOC 2018). They are widespread across most tropical and temperate marine systems and are well-adapted to breeding and foraging in these environments (Ashmole

& Ashmole 1967). Most terns are top piscivorous predators and feed on various forage-fish or

17 invertebrates by plunge-diving or surface foraging (Serventy et al. 1971). Like other seabirds, terns return to annual breeding colonies, often on exposed, near-shore islands and are central- place foragers during the breeding season. Adults form pair bonds and often display strong mate fidelity (Serventy et al. 1971). Most seabirds are faithful to their natal colony, while some species such as Bridled Terns (Onychoprion anaethetus) and the Common Noddy (Anous stolidus) also exhibit nest-site philopatry (Serventy et al. 1971). The small terns (genus

Sternula) commonly shift nesting sites from one breeding attempt to the next; driven by a range of factors including past breeding success, habitat stability and resource availability (Burger

2008).

Table 2.2. Genera, common names and size ranges of all terns and noddies (Menkhorst et al., 2017; IOC 2018). Group Genus Common name No of Size Range Species (cm) Noddies Anous “Noddies” 5 25-45

Larger Terns Gelochelidon Gull-billed Tern 1 36-42 Hydroprogne Caspian Tern 1 48-54 Larosterna Inca Tern 1 40 Onychoprion “Brown-backed terns” 4 30-36 Phaetusa Large-billed Tern 1 38-42 Sterna “White terns” 13 30-43 Thalasseus “Crested terns” 8 38-48

Smaller Terns Chlidonias “Marsh terns” 4 20-25 Gygis White Tern 1 30-33 Sternula “Little terns” 7 20-28

Total 11 46 20-54

Terns are characteristically slender and often pale-coloured (except noddies) with the adults of most species adorning a brighter “head-cap” and bill in breeding plumage (Menkhorst et al. 2017). As a group, they vary in size (Figure 2.1) with the larger terns (> 35cm in body length) represented in eight genera (Table 2.2) that comprise 24 species (IOC 2018). This review focusses on investigating the foraging ecology of representative species from each

18 genus of larger terns, including the Common Noddy (A. stolidus), Gull-billed Tern

(Gelochelidon nilotica), Caspian Tern (Hydroprogne caspia), Inca Tern (Larosterna inca),

Bridled Tern (O. anaethetus), Sooty Tern (Onychoprion fuscatus), Large-billed Tern (Phaetusa simplex), Roseate Tern (Sterna dougallii) and Crested Terns (Thalasseus bergii) (Figure 2.2).

The largest tern, H. caspia, has a body length of 48-54 cm (Table 2.2; Serventy et al. 1971), while the world’s smallest tern, the Least Tern (Sternula antillarum), has a body length of 22-

24 cm (Gochfeld & Burger 1992).

Figure 2.1. Images of 15 species of terns and noddies representing all 11 genera and arranged by size from smallest (left) to largest (right; images by Morcombe and Stewart, 2010).

2.1.2 Aims of the review

This review aims to synthesise existing knowledge of seabird foraging ecology across marine environments worldwide, focussing on the larger terns and noddies. Foraging ecology is considered in terms of diet, foraging area and the foraging behaviours employed to optimize feeding success. This review has three main aims: first, to explore the similarities and differences in the foraging ecology of terns and noddies of different body size, in regard to diet, behaviour and foraging area; secondly, to compare the energetic requirements of birds in each genus; and thirdly, to highlight key gaps in our knowledge of their foraging ecology, as priorities for future research.

Figure 2.2. Images of representative species of each genus of larger terns featured in this literature review (and some smaller species for comparison) (photos: Susie Stockwell, unless otherwise stated)

Common Noddy Whiskered Tern Gull-billed Tern White Tern (Gygis alba) (Anous stolidus) (Chlidonias hybrida) (Gelochelidon nilotica) Source: Wikipedia

Caspian Tern Inca Tern (Larosterna inca) Sooty Tern Bridled Tern (Hydroprogne caspia) Source: Wikipedia (Onychoprion fuscatus) (Onychoprion anaethetus)

Large-billed Tern (Phaetusa simplex) Crested Tern (Thalasseus bergii) Roseate Tern (Sterna dougallii) Fairy Tern (Sternula nereis) Source: Wikipedia

2.2. Foraging ecology of larger terns

Foraging is the process of searching for, and acquiring food resources from the environment, and is an integral component of an organism’s capacity to survive and reproduce

(Whittow & Rahn 1984). Consequently, many species evolve structural and behavioural adaptations to optimize their foraging success within their ecosystem (Balance et al. 2008). At one end of the spectrum, these adaptations involve specialisations to exploit a specific ecological niche or narrow set of resources, while at the other end, strategies such as “prey- swapping” are used by generalists to exploit a broader niche; buffer against fluctuations in resource availability or changing conditions (Balance et al. 2008). Niche breadth a reflection of foraging plasticity, which is the range of resources used by an animal and includes ecosystem parameters such as habitat use, home range and latitudinal position, as well as foraging area, behaviour and diet (Donovan & Welden 2002). The degree of specialisation within each of these parameters can provide information on their ‘flexibility’ or ‘rigidity’ to activities such as foraging (Donovan & Welden 2002). In this way, foraging is largely governed by niche breadth: all species must meet daily energetic requirements by taking prey of various size, quantity and nutritional value within their niche to match their energetic expenditure (Baltz &

Morejohn 1977; Collins et al. 2016; Fasola et al. 2009). Additionally, the temporal and spatial segregation of foraging resources by seabirds, such as the size and species of prey items (Baltz

& Morejohn 1977), and selection of foraging area or macrohabitat (Fasola et al. 2009), can reduce the severity of competition for food (Baltz & Morejohn 1977). Therefore, the niche breadth of a species determines their foraging ecology, as well as the degree of their foraging plasticity within these parameters (Baltz & Morejohn 1977; Donovan & Welden 2002).

Adopting flexible foraging strategies provides a mechanism for enhancing individual survival, the persistence of populations under fluctuating conditions, and intra- and interspecific competition for limited resources (Boyd et al. 2014). Additionally, the time

21 allocated to different behaviours, such as foraging, has important consequences for an animal’s overall energy budget (Collins et al. 2016). When considering top predators like seabirds, energetic budgets and niche breadth can offer insight into ecosystem health and resource availability (Collins et al. 2016; Einoder 2009). Optimal foraging involves maximising the energy obtained from food whilst minimising the energy expenditure in obtaining food

(Campos et al. 2017).

Terns and noddies, like other seabirds, are structurally and behaviourally well-adapted to optimise their foraging success in order to meet their daily energetic requirements and maximise energy uptake from their catch (Balance et al. 2008; Campos et al. 2017; Serventy et.al 1971). Their foraging ecology can be considered in terms of three main components: foraging area (range and habitat); behaviour (or strategy); and diet (Zimmer et al. 2008).

Despite similarities in their appearance and behaviour, terns and noddies are diverse in all aspects of their foraging, which will be explored in this review.

2.2.1 Foraging area

Terns are widespread across most tropical and temperate marine ecosystems, with several species represented in most seabird communities (Catry et al. 2009). In contrast, some species occupy brackish or freshwater systems; for example, the Large-billed Tern (Phaetusa simplex) is restricted to some South American rivers (Zarza et al. 2013), and the Gull-billed Tern

(Gelochelidon nilotica) is widespread across marine and freshwater systems including wetlands and tidal mudflats on most continents (Serventy et al. 1971; Dies et al. 2006). While some terns, such as the Caspian Tern (Hydroprogne caspia) and Roseate Tern (Sterna dougallii) are distributed globally (Serventy et al. 1971), other species have a restricted geographic range. For example, the Inca Tern (Larosterna inca) is confined to coastal areas off

Peru and Chile (Velando et al. 2001), where it feeds mostly on protein-rich anchovies

(Engraulis ringens) in the very productive Humboldt Current (Duffy 1983; Thiel et al. 2007).

Consequently, L. inca forages over relatively small areas to meet their energetic requirements, despite their large size and high energy demand ( Table 2.2; Whittow and Rahn, 1984).

Tropical terns forage in naturally oligotrophic waters (Ashmole 1971) and yet many sympatric species co-exist within these environments (Catry et al. 2009). To facilitate this overlap in distribution and to overcome competition, all terns can exhibit high levels of specialisation to partition limited resources and fill different ecological niches (Donovan &

Welden 2002; Surman & Wooller 2003; Robertson et al. 2014). For example, nine sympatric terns including Caspian Tern (Hydroprogne caspia), Bridled Tern (Onychoprion anaethetus),

Sooty Tern (Onychoprion fuscatus), Roseate Tern (S. dougallii), Fairy Tern (Sternula nereis),

Crested Tern (Thalasseus bergii), Common Tern (Anous stolidus) and Lesser Noddy (Anous tenuirostris) breed on the Houtman Abrolhos Islands in the Indian Ocean (Table 2.3; Surman and Wooller, 2003). All species exhibit strong resource partitioning by foraging for prey (of various species and size) across different areas (Surman & Wooller 2003; Collar et al. 2017).

In this way, there is some segregation in niche breadth between sympatric species (Donovan &

Welden 2002; Surman & Wooller 2003). The five most abundant forage-fish species were studied by Surman & Wooller (2003) (Table 2.3) to understand the mechanisms behind their sympatry.

In coastal areas, the larger T. bergii forage in shallow reef habitats, feeding on reef fish such as parrotfish (Scaridae), blennies (Blennidae) and wrasses (Labridae) while S. dougallii targeted larval fish in deeper waters within the same area (Table 2.3; Surman and Wooller,

2003). However, these terns are flexible in their diet, and exhibit high foraging plasticity with changing prey availability and environmental conditions (Gaglio et al. 2018). In contrast, wider-ranging pelagic species of terns and noddies capitalise on opportunistic encounters with forage fish and squid (Weimerskirch et al. 2004). Of these, the larger terns exhibit more

23 pronounced segregation in foraging area and the use of prey resources, presumably because of the greater energetic requirements associated with travelling greater distances. For example, O. fuscatus forage farthest (480-600 km) from their colonies and target both squid and fish, especially lanternfish (Myctophidae) (Table 2.3; Surman and Wooller, 2003). Conversely, the closely-related, but smaller, O. anaethetus (30-32 cm; 130g) forage over smaller areas than O. fuscatus (33-36 cm; 157g) and can occupy coastal areas and shallow waters around island colonies (Serventy et al. 1971).

The energetic requirements of seabirds are closely correlated with their mass (Ellis &

Gabrielsen 2002; Dunn et al. 2018) and consequently, the body size of terns dictates their required daily prey intake or mass of prey they require (Surman & Wooller 2003). Larger terns such as T. bergii tend to take a small number of longer and heavier forage-fish to meet their energetic requirements, whilst smaller species such as S. dougallii take more fish of smaller size (Table 2.3; Surman and Wooller, 2003). Similarly, sympatric species such as A. stolidus and A. tenuirostris overlap through much of their pelagic foraging range, targeting productive areas along the continental shelf 180 km from their colony off the mid-Western Australian coast (Shephard et al. 2018). Although both noddies often forage for the same fish species

(Surman & Wooller 2003), A. stolidus usually take larger forage fish to meet their energetic requirements, possibly due to their greater size (183g; 40-45cm in length, Menkhorst et al.,

2017) than A. tenuirostris (112g; 30-35cm in length, Menkhorst et al., 2017) . Anous stolidus forage for larger fish, often twice the length of A. tenuirostris’ prey, including Beaked Salmon

(Gonorhynchus greyii), Hawaiian Bellowfish (Macroramphosus scolopax) and the Australian

Anchovy (Engraulis australis), although they can supplement their diet with squid spp. when it is available (Surman & Wooller 2003). In contract, A. tenuirostris tend to target goatfish

(Mullidae), especially Upereus and Parupeneus spp. (Monticelli et al. 2008) as well as larval and post-larval fish in the surface layer (Dunlop 2017). This resource partitioning based on

prey size reduces inter-specific competition between A. stolidus and A. tenuirostris and

promotes their co-existence when they are sympatric (Surman & Wooller 2003).

Table 2.3. Resource partitioning by five sympatric terns on Abrolhos Islands, Western Australia (summarised from: Surman and Wooller, 2003)

Mean Mean Mean Tern Estimated mass no prey prey body colony size Species Diet Foraging area /sample items length mass (breeding (g) /sample (mm) (g) pairs) Common Noddy, Fish sp. (69%), Squid Pelagic foragers 12.5 27.8 51.3 183 130,000 Anous stolidus (10%), Black-spotted 180km off ± 0.4 ±0.9 ± 0.2 Goatfish (8%) colony

Lesser Noddy, Fish sp. (46%), Beaked Pelagic foragers 5.8 26.2 33.5 112 35,000 Anous tenuirostris Salmon (27%), Black- 180km off ± 0.1 ±0.9 ± 0.1 spotted Goatfish (8%), colony Hawaiian Bellowfish (5%)

Sooty Tern, Squid (61%), Beaked Pelagic foragers 11.1 8.6 27.8 157 250,000 Onychoprion Salmon (7%), fish sp. (off continental ± 0.5 ± 0.6 ± 0.6 fuscatus (6%), Lanternfish (5%) shelf) 480- 600km from the colony

Roseate Tern, Fish sp. (37%), Coastal areas in 3.3 2.4 47.8 108 1000 Sterna dougallii Australian Anchovy close proximity ± 0.5 ± 0.4 ± 1.1 (12%), Sole (12%), to colony, over Beaked Salmon (11%), deeper waters Blue Spart (8%), Slender Spart (7%), Black-spotted Goatfish (6%)

Crested Tern, Reef fish: Parrotfish Coastal reefs in 23.0 1.1 100.5 324 1000 Thalasseus bergii (23%), Blennies (15%), close proximity ± 1.6 ± 0.1 ± 1.6 Cluepid sp. (14%), to colony, over Wrasses (12%) shallower waters

In temperate and polar regions, sympatric species such as Common Terns (Sterna

hirundo) and Arctic Terns (Sterna paradisaea) forage over relatively small areas, but take a

wide variety of forage fish, many of which are protein-rich, including sand-eels (predominately

Ammodytes marinus) (Monaghan et al. 1989). These similar-sized terns, (both 32-37cm in

length, Table 2.2; Menkhorst et al., 2017) have similar energetic requirements and breed

25 sympatrically on island colonies across the northwest and northeast Atlantic, such as Coquet

Island in the North Sea and Country Island off Nova Scotia, Canada respectively (Rock et al.

2007; Robertson et al. 2014). Although these terns exploit similar food resources (Mallory et al. 2017), they forage across different habitats within the same region, with S. hirundo targeting shallower waters and S. paradisaea the deeper areas, respectively (Rock et al. 2007). The partitioning of foraging areas reduces interspecific competition and provides a mechanism for accommodating their sympatry (Robertson et al. 2014). This phenomenon is consistent across all sympatric tern colonies and is important for reducing interspecific competition and promoting coexistence between species (Rock et al. 2007).

Most seabirds have elevated energy requirements whilst incubating and feeding chicks

(Collins et al. 2016). Therefore, their foraging range is usually contract during their breeding season to reduce their energy expenditure from flight, permitting increased parental care (Boyd et al. 2014). This concentrated seabird foraging in the immediate area of the breeding colony is known as ‘central place foraging’ (Boyd et al. 2014). Central-place foraging produces seasonal variation in the trophic interactions across all marine ecosystems and can increase interspecific competition for food resources within these small areas surrounding the colony site (Monticelli et al. 2008). For example, the normally wide-ranging S. dougallii contract their foraging area whilst breeding and overlap with the sympatric A. tenuirostris on island colonies in the Seychelles during the breeding season (Monticelli et al. 2008). Similarly, H. caspia are central place foragers whilst incubating eggs and provisioning chicks (Lyons et al. 2005;

Monticelli et al. 2008) but outside the breeding season, forage over much larger spatial scales.

During the breeding period, the length of foraging trips and relative time spent foraging or attending chicks, changes with food resource availability. This has a direct influence on chick mortality and the overall recruitment within the population (Anderson et al. 2007).

2.2.2 Diet

Most terns and noddies are generalist piscivores and feed on a broad diet of small- to medium-sized forage fish or squid in order to meet their energetic requirements. While open ocean species in pelagic environments are reliant on prey in the surface layer (mostly within one metre of the surface), terns in shallower, coastal ecosystems can access fish throughout the water column. Larger species, such as Caspian (Hydroprogne caspia) and Crested (Thalasseus bergii) terns penetrate the water column to greater depths (0-2 m of surface) than do smaller ones, such as Fairy Terns (Sternula nereis) which target schooling baitfish at the surface (within

0.5m, Ismar et al., 2014). In doing so, H. caspia and T. bergii are able to target benthic forage- fish from coastal areas dominated by seagrass and reef substrate respectively (Surman &

Wooller 2003; Lyons et al. 2005; Dunlop & McNeill 2017). As generalists, variation in the diet of each species tends to reflect changes in abundance and availability of fish within their foraging area (Lyons et al. 2005). However, many terns and noddies exhibit resource partitioning in their diets and foraging areas (see Table 2.3; section 2.1 above). This interspecific variation in foraging ecology between terns and noddies reduces competition for often limited food resources and facilitates the co-existence of sympatric species within seabird communities.

Most terns and noddies forage for adult and larval fish species and squid relative to their size (Surman & Wooller 2003; Rock et al. 2007; Dunlop 2017). Some species, such as L. inca and G. nilotica have relatively specialised diets, feeding mostly on anchovies (Engraulis ringens) and crustaceans respectively (Duffy 1983; Dies et al. 2006). Smaller, wetland specialists such as the Black Tern (Chlidonias niger) can pluck small fish from the surface layer of wetlands. However, C. niger are also able to capture insects on the wing as part of their diet because of their small size and agility (Steen & Powell 2012).

2.2.3 Foraging behaviour

All seabirds have developed strategies or behaviours in order to optimise their success whilst foraging and meet their energetic requirements (Balance et al. 2008). Most seabirds employ one of six main strategies: surface-feeding, pursuit-diving, plunge-diving, kleptoparasitism or piracy (scavenging and predation), filter feeding and general feeding strategies (Table 2.4). Terns and noddies use predominantly two of these foraging strategies: surface-feeding and plunge-diving, to exploit various resources or ecological niches within their environment (Table 2.4; Serventy et al. 1971). All terns have long, narrow, pointed wings for efficient flight, forked tails to steer, and large, pointed bills used to snatch prey (Menkhorst et al. 2017). Thus, terns are well adapted for surface-feeding and plunge diving.

Surface-feeding

Surface-feeding is a common foraging strategy amongst seabirds for exploiting food resources in the surface layer of the water column (0-0.2 m below the surface) across a variety of ecological niches. This feeding style involves dipping the bill beneath the surface to catch prey, either in flight or whilst paddling (Balance et al. 2008). Many seabird species that occupy tropical, pelagic environments, such as the Common Noddy (Anous stolidus) and Sooty Tern

(Onychoprion fuscatus) are surface feeders whilst in flight and swoop down over the ocean, dipping their heads to catch forage fish and squid at the surface (Shephard et al. 2018). This strategy is ideal for wide-ranging, generalist species, especially those in oligotrophic environments (Weimerskirch et al. 2004). Additionally, ocean currents can concentrate krill, forage-fish and squid in the surface layer of upwelling zones, and large marine predators (such as cetaceans and tuna) can also push shoaling fish toward the surface (Weimerskirch et al.

2004). Anous species often rely on these oceanographic features and feeding events to meet their energetic requirements (Surman & Wooller 2003). The Gull-billed Tern (Gelochelidon

Table 2.4. Summary of the six main foraging styles of seabirds, synthesised from Balance et al. (2008). Foraging style Characteristics Typical groups Prey types

1. Surface-foraging Dipping the bill beneath Frigatebirds (Fregatidae) (Weimerskirch et al. Small surface- the surface to catch prey 2004), gadfly petrels (Pterodromas spp.) (Leal dwelling fish, squid in the surface layer, et al. 2017), some terns & noddies (Sterninae) and other marine either in flight or whilst (Dunlop et al. 2001) invertebrates (Dunlop paddling (Balance et al. et al. 2001; Storm-petrels (Hydrobatidae) by seemingly 2008). Weimerskirch et al. “walking on water” (Menkhorst et al. 2017) 2004). Skimmers (Rhynchops spp.) by “ploughing” the surface with bill (Rojas et al. 1997).

2. Pursuit-diving Sub-surface foot or wing • Auks (Alcidae) Mostly krill, fish, propulsion to catch prey • Diving-petrels (Pelecanoides spp.), squid & crustaceans at greater depths • Cormorants (Phalacrocoracidae), at greater depths (Balance et al. 2008). • Shearwaters (Procellaridae) (Holm & Burger • Penguins (Sphenicidae) 2002).

(Zimmer et al. 2010; Watanabe et al. 2012)

3. Plunge-diving Patrolling high above the • Tropicbirds (Phaethon spp.) (Sommerfeld Mostly fish and water until prey is & Hennicke 2010; Campos et al. 2017) marine invertebrates sighted. Plunge divers form beneath surface • Most terns (Sterninae) (Dunlop et al. will hover then plummet (or benthic layer in 2001) rapidly to the surface to shallow habitats) seize their prey before • Gannets and boobies (Sulidae) (Dunlop et al. 2001). returning with it to the (Weimerskirch et al. 2005) air (Balance et al. 2008).

4. Kleptoparasitism Piracy by one seabird of Mostly jaegars and skuas (Stercorarius spp.) Flexible; mostly another’s catch. (Wood et al. 2015), other species (e.g. gulls) stolen fish (Jakubas et opportunistically (Washburn et al. 2013). al. 2018).

5. Filter feeding “Hydroplaning” or Three species of prion, for example broad- Krill and copepods paddling on the surface billed prion (Pachyptila vittata) (Klages & Cooper with head submerged, (Klages & Cooper 1992). 1992). seizing and filtering food (Klages & Cooper 1992).

6. Generalist Opportunistic acquisition Mostly albatrosses (Diomedeidae), large Scavenging: carrion strategies of prey by predation or petrels (Procellaria spp.) (Phillips et al. 2016), (Phillips et al. 2016), scavenging dead or fulmars (Fulmarus spp.) (Donnelly-Greenan et Predation: fish, discarded food (Balance al. 2014), gulls (Laridae) (Washburn et al. mammals, (e.g. et al. 2008). 2013) and other species opportunistically lemmings), other Skuas and jaegars (Stercorarius spp.) predate seabirds (adults, upon other seabirds (Jakubas et al. 2018). chicks and eggs) (Jakubas et al. 2018).

29 nilotica) also employs surface-feeding in coastal and freshwater systems, including tidal mudflats, to forage for crustaceans and small fish (Dies et al. 2006).

Plunge-diving

Plunge-diving is a common foraging behaviour amongst terns across open ocean, coastal, estuarine and freshwater habitats to target forage fish at various depths between 0-2 m beneath the surface. It involves patrolling high above the water until prey are sighted, then hovering briefly before plummeting rapidly to catch their prey beneath the surface, then returning to the air with their catch (Balance et al. 2008). Plunge divers can capture faster-moving forage-fish at greater depths as the momentum from their dive temporarily combats their natural buoyancy.

Plunge diving is the dominant foraging strategy amongst pelagic and coastal terns (Balance et al. 2008).

Plunge-diving terns exhibit a wide variation in body size (Table 2.2; Figure 2.1), and consequently, they can reach different depths whilst foraging. Coastal terns, such as H. caspia,

T. bergii, and S. nereis, forage by plunge-diving (Ismar et al. 2014; Dunlop & McNeill 2017;

Gaglio et al. 2017) and their size differences require them to exploit different forage-fish species at different depths within their ecosystem. The largest, H. caspia (48-54 cm, Table 2.2), forages in shallow waters for small- to medium-sized benthic, estuarine fish such as Perth

Herring (Nematolosa vlaminghii) and Sea Mullet (Mugil cephalus) in Western Australia’s

Peel-Harvey Estuary (Dunlop & McNeill 2017). In the Columbia River Estuary, the United

States of America, salmonids (Oncorhynchus spp.), Californian Anchovy (Engraulis mordax), and Pacific Herring (Clupea pallasi) make up the large majority of food resources (Lyons et al. 2005).

Smaller species like S. nereis (22-27 cm, Table 2.2) target smaller, juvenile and larval forage fish in the surface layer such as gobies (Gobiidae), other bait-fish and small crustaceans

30 to meet their energetic requirements (Ismar et al. 2014). Their small size reduces the capacity of S. nereis to take larger prey species and penetrate the water column whilst plunge-diving.

Open-ocean species such as S. dougallii, S. hirundo and S. paradisaea also exploit forage fish in the surface layer by plunge-diving (Mallory et al. 2017).

2.3. Energetic requirements

Seabirds forage to meet their energetic requirements and must balance their energy expenditure with the energy they obtain from prey (Whittow & Rahn 1984; Dunn et al. 2018).

Optimal foraging involves maximising prey uptake (higher quantity, size or nutritional value of prey) whilst minimising foraging effort (reduced distance travelled and time spent foraging)

(Whittow & Rahn 1984). Consequently, the time allocated to foraging and other activities that make up the energy budget are an important consideration in seabird energetics. Seabird foraging ecology is comprised of a number of components, including time spent foraging, foraging behaviour, prey type, foraging area and distance travelled, each dictated by adult energy requirements (Zimmer et al. 2008). The energy requirements vary between species, sexes (Pinet et al. 2012; Phillips et al. 2016) and with life stage (Fayet et al. 2015), and change significantly between breeding and non-breeding periods (Collins et al. 2016).

Foraging efficiency is constrained by the rate at which prey are encountered as well as the success of each foraging attempt (Zimmer et al. 2008), which is dependent on the resource availability and environmental conditions within marine ecosystems (Campos et al. 2017).

Seabirds must make judicious foraging decisions; responding to environmental cues and learnt behaviours (Fayet et al. 2015) in order to exploit “foraging hotspots” or areas of reliably high productivity (Bradshaw et al. 2004) to meet their energetic requirements. Foraging hotspots are important, predictable areas for marine predators to optimise their foraging success

(Sommerfeld & Hennicke 2010). They are created by favourable physical and bathymetric

31 conditions that support high biomass of production across multiple trophic levels and can be static e.g. around seamounts and upwellings; or nomadic e.g. follow schooling predators like tuna or dolphins, fishing boats or environmental fronts (Kokubun et al. 2015).

2.3.1 Estimating field metabolic rates

Seabird energetics are closely related to bird size and life history (Figure 2.3; Whittow and Rahn, 1984; Dunn, White and Green, 2018). While energy expenditure is most closely linked to physiological characteristics, especially body mass (Nagy 2005), there is also a positive correlation between seabird energetics and ecological and contextual factors (Dunn et al. 2018). That is, seabird energy demands increase both with colony latitude, and as the breeding season progresses (Dunn et al. 2018). Seabirds provide high levels of parental care for sustained periods (Serventy et al. 1971) and chicks require increasing sustenance as they grow and develop (Dunn et al. 2018). Simple calculations can be used to estimate energy expenditure for free-ranging seabirds when only the mass of the bird is known, using the general equation: Energy expenditure = 16.69 x mass0.651 (Ellis & Gabrielsen 2002). This allometric approach is based on the relationship between avian field metabolic rates (or sum of an individual’s energy expenditure over a specific period) and some morphological characteristics of seabirds (Fort et al. 2011; Dunn et al. 2018). Ellis & Gabrielsen (2002) developed this equation using data from many species across all orders of seabirds (Table 2.1), and it can be applied to estimate energy expenditure when few biometric parameters are known.

However, this approach should be applied judiciously for seabird species that were not included in the development of this equation (Ellis & Gabrielsen 2002), as well as when estimating energetic expenditure outside the breeding season (Fort et al. 2011).

2.3.2 Energetic requirements of terns

The energetic expenditure of terns of varying body size has been estimated using the allometric approach (Table 2.5; Ellis and Gabrielsen, 2002). Estimates from allometric equations indicate a strong positive correlation between body mass and energy expenditure

(Figure 2.2; Nagy, 2005). All seabirds must meet their daily energetic requirements when foraging in order to survive and reproduce successfully. Time-energy budgets can be developed for seabirds that break down their daily activities, and calculate the energy gained or lost whilst completing each activity (Gremillet et al. 2003). For tern species with more specialised diets or foraging areas, birds can meet these requirements by obtaining a minimum quantity of their preferred prey species and, where possible, reducing foraging trip parameters (distance travelled or time spent foraging). However, most terns and noddies are generalists (Serventy et al. 1971) and can meet these requirements by taking prey species of varying size and nutritional quantity opportunistically (Whittow & Rahn 1984). Over time, these budgets can reflect changes in seabird energetic requirements (Collar et al. 2017) as well as changing prey availability or environmental condition (Rishworth et al. 2014). Seabirds are top predators in marine environments and understanding their energetics is an essential component to studying both their role within the ecosystem (Fort et al. 2011) and potential use as indicators of environmental condition (Rishworth et al. 2014).

1400 1200

1000

) 1 - 800

600 (kJ (kJ d 400

200 Energetic Expenditure Energetic Expenditure 0 0 100 200 300 400 500 600 700 800 Mass (g) Figure 2.3. The estimated energetic expenditure of free-ranging seabird species (included in Table 2.5), using allometric calculations (Ellis & Gabrielsen 2002), using average mass (Fort et al. 2011). A polynomial trendline illustrates the relationship between seabird energetics.

Table 2.5. Daily predicted energetic expenditure for free-ranging seabirds during the breeding season, based on the average mass of adult birds (Serventy et al. 1971; Surman & Wooller 2003; Gochfeld & Burger 1992) and allometric calculations (Ellis & Gabrielsen 2002). Energetic Expenditure Species name Common name Mass (g) (kJ d-1)

Larger species (≥35cm body length)

Anous stolidus Common Noddy 183 495.81 Gelochelidon nilotica Gull-billed Tern 291 670.58 Hydroprogne caspia Caspian Tern 700 1187.45 Larosterna inca Inca Tern 195 516.74 Onychoprion fuscatus Sooty Tern 157 448.73 Phaetusa simplex Large-billed Tern 228 572.10 Sterna dougallii Roseate Tern 108 351.73 Sterna hirundo Common Tern 99 332.36 Sterna paradisaea Arctic Tern 128 392.87 Thalasseus bergii Crested Tern 324 719.15

Smaller species (<35cm body length)

Anous tenuirostris Lesser Noddy 112 360.16 Chlidonias niger Black Tern 62 245.08 Gygis alba White Tern 120 376.71 Onychoprion anaethetus Bridled Tern 130 396.86 Sternula nereis Fairy Tern 70 265.23

2.4. The significance of understanding foraging ecology

2.4.1 Seabird conservation

Seabirds are one of the most vulnerable groups of birds (Croxall et al. 2012), with many documented declines in the abundance and distribution of species. Almost one-third of extant seabirds are threatened (Spatz et al. 2014), and three species, Pterodroma rupinarum, Bulweria bifax and Pinguinus impennis have become extinct within the last 200 years (IUCN Red List

2017). Globally, a majority of recent avian extinctions have occurred on oceanic islands, which has been attributed to the effects of invasive species, hunting and habitat alteration (Szabo et al. 2012). Although they spend long periods at sea, seabirds return annually to breeding colonies on oceanic islands and most colonial species have evolved without the threat of predation or disturbance (Spatz et al. 2014). Predation by introduced mammals such as cats

(Felis catus), foxes (Vulpes vulpes) and rats (Rattus rattus) pose an immediate threat to the 34 survival of eggs, chicks and adult breeding seabirds (Spatz et al. 2017). Changing oceanic conditions as well as ingestion of, and entanglement in marine debris have directly and indirectly caused declines in many seabird populations worldwide (Phillips et al. 2016).

In addition to the above threats, their typical life-history strategies make them susceptible to population decline and slow recovery: that is, most are species are long-lived, slow to reach sexual maturity and produce few young at each breeding opportunity (Phillips et al. 2016).

These life history traits, coupled with the specific breeding and foraging requirements of seabirds, exaggerates their vulnerability to threatening processes and reduces their capacity for rapid population recovery (Phillips et al. 2016). For this reason, a sound understanding of their foraging and reproductive ecology is crucial towards delivering effective conservation for seabirds and their environments.

The foraging (and reproductive) success of terns has significant implications for their conservation and that of their ecosystems. Currently, four species of tern are classified as threatened species by the IUCN; the Fairy Tern (Sternula nereis) as ‘Vulnerable’ (Birdlife

International: S. nereis 2017), the Black-fronted Tern (Chlidonias albostriatus) and Peruvian

Tern (Sternula lorata) as ‘Endangered’ (Birdlife International: C. albostriatus 2016; Birdlife

International: S. lorata 2016) and the Chinese Crested Tern (Thalasseus bernsteini) as

‘Critically Endangered’ (Birdlife International: T. bernsteini 2017). This is largely a result of the destruction or alteration of habitat required for breeding colonies, associated with large- scale anthropogenic development in coastal areas, as well as disturbance to, or predation upon eggs, chicks and breeding adult birds (BI C. albostriatus 2016; BI S. lorata 2016; BI S. nereis

2017; BI T. bernsteini 2017). The long-term monitoring of population trends, as well as research focused on threat mitigation and better understanding their foraging and reproductive ecologies, are high priorities for tern conservation and developing recovery plans.

2.4.2 Seabirds as biological indicators

Seabirds play an integral role in both marine and terrestrial (at breeding colonies) ecosystems as top, piscivorous predators (Spatz et al. 2014) and an understanding of their role in marine ecosystems are important for the conservation of seabirds and their ecosystems

(Kokubun et al. 2015). Seabirds also have exceptionally high anthropogenic value as potential biological indicators (‘bio-indicators’) of the structure and function of coastal and pelagic marine systems, and can provide insight into shifts in marine ecosystems such as changes in fisheries productivity, pollutant levels, climatic shifts and abiotic conditions (Einoder 2009;

Mallory et al. 2010). Marine environments are increasingly recognised as a global priority for conservation. However, these systems are vast and can be logistically challenging and expensive to monitor (Parsons et al. 2008). The distribution and foraging pathways of seabirds, particularly during the breeding season when most species are colonial, provides a direct reflection of habitat quality, as well as biotic and abiotic conditions within the ecosystem

(Dunlop 2017; Shephard et al. 2018). Research on seabirds, therefore, provides a low-cost and resource effective mechanism for collecting data and tracking changes in marine health, provided there is a sound understanding of their foraging and reproductive ecology (Burger &

Gochfeld 2004; Dunlop 2017)

2.5. Knowledge gap

In recent decades, seabirds and their foraging ecology have been the focus of an increasing number of research projects and monitoring programs worldwide, although many of these studies have been relatively isolated, specific or short-term in their nature (Phillips et al. 2016). There is a growing need for longer-term and broader-focused dietary studies of more seabird taxa including terns and noddies, as well as greater connectivity and collaboration between projects. Additionally, some groups of seabirds, such as storm-petrels (Hydrobatidae)

36 remain largely understudied, and seabird populations in less accessible, or remote areas with fewer anthropogenic uses, have historically been given less attention.

Furthermore, most research projects have focused on monitoring seabirds at breeding colonies. Less attention has been given to their foraging ecology, especially outside the reproductive season, despite the importance of year-round food availability for seabird population persistence. A sound understanding of the foraging ecology of seabirds facilitates their use as time- and cost-effective indicator species to monitor changing conditions across marine environments. Knowledge of seabird foraging ecology and its’ mechanisms also provides an important opportunity to improve their conservation, as well as the management of marine ecosystems. This project aims to contribute towards the greater knowledge by filling a gap in understanding the foraging ecology of a widespread tern, H. caspia, during its non- breeding season.

2.6. Conclusion

All seabirds play important roles within marine ecosystems as top predators. Terns and noddies (Sterninae) as a group comprise 46 representatives (almost 15% of all seabird species) and provide an interesting lens through which to consider seabirds. They are widespread through tropical and temperate marine ecosystems, with several species represented worldwide. Terns and noddies are largely piscivorous seabirds, well-adapted to foraging across these environments to meet their daily energetic requirements. Their foraging ecology can be considered in terms of foraging range and habitat, behaviour (or strategy), and diet. Terns and noddies employ two of the six main foraging strategies; surface-feeding or plunge diving, to take a variety of forage fish. While open-ocean species in pelagic environments are reliant on prey in the surface layer, terns in shallower, coastal ecosystems can access fish at varying depths of the water column, with larger species, such as Caspian (Hydroprogne caspia) and

Crested (Thalasseus bergii) terns able to take benthic forage-fish such as mullet, herring and anchovies. The interspecific variation between terns and noddies in their foraging ecology reduces competition for often limited food resources and facilitates the co-existence of sympatric species within seabird communities.

All seabirds must make judicious decisions whilst foraging to optimise their success and meet their daily energetic requirements. These requirements are closely linked to body size, and in this way, larger terns and noddies have greater energy demands than smaller ones. Larger terns and noddies exhibit a combination of adaptations, from specialisation to high plasticity whilst foraging to meet their larger energetic requirements. Although their greater mass often facilitates their access to larger or more nutritional prey species at greater depths, they require a higher biomass of prey to meet their energetic requirements. Therefore, reductions in distances travelled and the time spent foraging ensure their energetic expenditure doesn’t exceed their daily energetic requirements. Furthermore, these requirements can vary with age, sex and life stage of these birds, with marked elevation throughout breeding periods when parents incubate eggs and provision chicks.

Knowledge of seabird foraging ecology is important for improving their conservation and furthering our understanding of seabirds and marine ecosystems. The global distribution of terns and noddies, coupled with their size, longevity and role as top piscivorous predators within their ecosystems make them ideal candidates as time- and cost-effective sentinels of changing marine conditions worldwide. A sound understanding of their foraging ecology and energetic requirements is crucial for interpreting and developing their use as ‘biological indicators’ of marine health and fisheries productivity. In this way, terns and noddies can be used to improve the monitoring of marine environments for more effective management and conservation.

Chapter 3. Patterns of distribution, abundance and foraging ecology of Caspian Terns

(Hydroprogne caspia) on the Peel-Harvey Estuary, south-western Australia.

Summary

Despite their large size and cosmopolitan distribution, Caspian Terns (Hydroprogne caspia) have been largely understudied, especially the finer scale patterns of their distribution, abundance and foraging ecology throughout their non-breeding periods. In south-western

Australia, the largest population of approximately 120 H. caspia breed annually on Penguin

Island, Shoalwater Bay and were thought to be resident on the Ramsar-listed Peel-Harvey

Estuary throughout their non-breeding season. This study has two main aims: first, to investigate the patterns in abundance and distribution of H. caspia; and secondly, to explore their foraging ecology by examining change in foraging area and diet over time throughout their non-breeding season. These aims were achieved by a program of direct field observations from October 2018 to February 2019 to examine patterns of distribution, abundance and foraging activity and how they vary spatially and temporally. Following methods outlined in

Dunlop & McNeill (2017), the diet of H. caspia was determined through photographs (images) of prey items in tern beaks and identifying otoliths in tern pellets (regurgitations of undigested prey) to determine food composition. A single overnight roosting site for H. caspia was identified, with a maximum number of 147 birds recorded in mid-February 2019. Tern foraging was concentrated in six main areas across the estuary especially around the mouths of channels, tributaries and drains. The number of terns, foraging birds and foraging activity differed between these six areas of the Estuary, and foraging activity also differed significantly with time of day – it was greatest in the morning block (04:30 to 09:30). Overall, 17 prey species

(16 fish and one crustacean) were recorded in the diet of H. caspia whilst foraging on the

Estuary, the most common being whitings (Sillaginidae), mullets (Mugilidae) and Eight-lined

Trumpeter (Pelates octolineatus), comprising 35.0%, 33.9% and 14.4% respectively of their observed catch. These results suggest that H. caspia could be an ideal biological indicator of the condition of the Peel-Harvey Estuary and its associated Ramsar wetlands during their non- breeding season.

3.1. Introduction

3.1.1. Seabird foraging ecology

Dietary studies are essential for understanding seabird ecology, as well as the structure and function of marine ecosystems, and how these change over different spatial and temporal scales (Jordan 2005; Barrett et al. 2007). The foraging ecology of seabirds in the sub-family

Sterninae (terns and noddies) has been discussed in detail in Chapter 2 and a brief overview is provided here as background to the aims and objectives of the research. Studying the foraging ecology of seabirds provides valuable information about variation in their prey, including prey size, quantity and species as well as foraging range, habitat and behaviour (Chapter 2; Barrett et al. 2007). These insights into the foraging ecology of seabirds, in turn, offer insight into the health and trophic structure of their marine ecosystems (Jordan 2005). A number of methodologies are used to examine seabird diets, with less invasive sampling methods being ideal (Barrett et al. 2007). The development and application of simple, non-invasive methodologies, that are time- and cost-efficient and appropriate to a diverse suite of species, are essential for deriving results that reflect natural behaviours and are comparable between studies (Gaglio 2017). The results of these dietary studies are important for gaining a deeper understanding of seabird ecology and the connectivity and composition of ecosystems. In addition, they can be used to enhance natural resource management and to develop the use of seabirds as indicators of the condition of their marine ecosystems (Burger & Gochfeld 2004).

Thus, dietary studies can play an important role in the conservation of both seabirds and the environments in which they live (Chapter 2; Croxall 1987; Estes et al. 2011; Szabo et al. 2012).

3.1.2. Caspian Terns in south-western Australia

Caspian Terns (Hydroprogne caspia) are large seabirds with a cosmopolitan distribution and an increasing population trend worldwide (IUCN 2019). Despite this, relatively few published studies have focussed on this species worldwide. One exception is a large breeding colony of approximately 9,700 pairs on the Columbia River Estuary in the United States of

America which has been the subject of detailed, ongoing research (Lyons et al. 2005). Another population in south-western Australia has also been studied throughout the breeding period

(see Dunlop & McNeill 2017). Withstanding these exceptions, H. caspia populations worldwide have been largely understudied, especially the finer scale patterns of their distribution, abundance and foraging ecology throughout their non-breeding periods.

In south-western Australia, H. caspia are found across most of the coastline as well as estuary, wetland and river systems (Serventy et al. 1971). Most breeding colonies within this region are limited to several pairs (Dunlop & McNeill 2017), except for Penguin Island, in

Shoalwater Bay (Figure 3.1), which hosts the largest breeding colony in south-western

Australia of approximately 60 pairs. The terns breed on this island each year between August and October and are thought to travel 30 km south to the Peel-Harvey Estuary (-32.40, 115.40) after their chicks develop and eventually fledge (Dunlop and McNeill, 2017, Figure 3.1). A study of the resighting of Caspian Terns banded on Penguin Island found that 98.6% of the re- sightings were from the Peel-Harvey Estuary, suggesting that the birds may be resident in this region throughout the non-breeding season (Figure 3.1; Dunlop and McNeill, 2017).

Figure 3.1. Map indicating the location of the breeding colony (-32.305°, 115.690°; Penguin Island, Shoalwater Bay) and non-breeding foraging grounds (-32.40, 115.40; Peel-Harvey Estuary) of the largest Caspian Tern, Hydroprogne caspia, population in south-western Australia.

As highlighted in Chapter Two, seabirds have great potential to act as indicators of marine ecosystem health (Cairns 1988; Einoder 2009; Mallory et al. 2010). They forage high in the marine food web and are tied to specific, terrestrial areas during the reproductive season, where they are easily studied. A sound knowledge of their foraging ecology and reproductive success can be used to provide indicators of fish recruitment and support studies of contamination; identifying potential risks of human consumption (Bond & Diamond 2009;

Einoder 2009; Mallory et al. 2010). For example, a recent study using H. caspia from this population found elevated levels of methyl-mercury (mean = 2.27 mg.kg-1, range = 0.9-5.9 mg.kg-1, n = 39) in R5 tail feather samples collected from breeding adults in this population

(Dunlop & McNeill 2017). Heavy metals such as mercury can enter the body tissue via prey ingestion, and this effect is magnified with each successive trophic level (Bond & Diamond

2009). Consequently, top predatory seabirds such as H. caspia (Balance et al. 2008; Spatz et

42 al. 2014) can accumulate larger quantities of heavy metals because of their position within the food web (Bond & Diamond 2009).

3.1.3. Study Aims

This study investigates the patterns of distribution and abundance and foraging ecology of a top-predator, the Caspian Tern (Hydroprogne caspia) in their non-breeding season. It examines spatial and temporal variation in their abundance and distribution during this time, and aspects of their foraging ecology, including foraging area and habitat, and diet composition and foraging behaviour. This Thesis focusses on the following three research questions:

1. Abundance and distribution: how many H. caspia use the Peel-Harvey Estuary and

which parts of this system are most significant?

2. Foraging area (spatial): where do H. caspia forage within the system?

3. Diet: what are the main prey types of H. caspia, and to what extent do they vary

between locations in the estuary and how do they differ from Penguin Island?

Based on the literature and preliminary observations of foraging terns, the main hypotheses investigated were that:

1. Population: individuals of H. caspia will be concentrated at one location during the

evening (a night roost) that has the potential to provide estimates of the population size

during the non-breeding period (Dunlop 2018).

2. Distribution and abundance: the distribution and abundance of H. caspia will be

heterogeneous across the estuary, with greater concentrations in areas with extensive

shallows and sandy spits (Serventy et al. 1971; Burger et al. 1996).

3. Diet: H. caspia will forage on a similar selection of fish species to that recorded at their

breeding colony on Penguin Island (Dunlop & McNeill 2017), as well as abundant

species of small- to medium-sized benthic fish in the Peel-Harvey Estuary (Potter,

Loneragan, et al. 1983; Lenanton et al. 1984; Loneragan et al. 1986; Potter et al. 2016).

4. Foraging area: the foraging ecology of H. caspia is linked to the distribution of

shallow water, sandy habitats, and the terns will favour these parts of the Estuary for

foraging, particularly around the mouths of tributary rivers (Burger et al. 1996).

3.2. Methods

Data were collected on H. caspia numbers and foraging activities at sites across the

Peel-Harvey Estuary in south-western Australia (Figure 3.1) between October 2018 and March

2019. The period of this study immediately follows the terns’ annual breeding season, which typically spans the months of August to October (Dunlop & McNeill 2017). The Peel-Harvey

Estuary and its ecological values are briefly described below (Section 3.2.1), followed by the methodological approaches used to investigate the foraging ecology of H. caspia. This includes approaches used to determine the distribution and abundance of terns (3.2.2), their foraging patterns (3.2.3), dietary composition (3.2.4), and their foraging behaviours (Appendix 3).

3.2.1 Study area

The Peel-Harvey Estuary is the largest and most diverse estuarine system in south- western Australia and forms part of the greater Ramsar-listed Peel-Yalgorup system (Hale &

Butcher 2007). It is recognised as having significant economic, social and ecological value

(O’Malley & Willmott 2015; Del Marco & Willmott 2017) but has long been exposed to contaminants from industry, agriculture and urban development (Hale & Butcher 2007).

Additionally, there is limited ecological monitoring data available for some components of these wetlands (Hale & Butcher 2007).

Geography and climate

The Peel-Harvey Estuary is a large, micro-tidal system comprising two shallow connected basins; the Peel Inlet and the Harvey Estuary, covering an area of 136 km2 (Figure

3.1). The depth of the estuary ranges from 0 to 3.9 m at the lowest water level (Department of

Transport, 2006), with a daily tidal fluctuation of ≥ 1 m (Bureau of Meteorology, 2019). The dominant benthic habitats are seagrass on sandy substrates and green macroalgae (Hale &

Butcher 2007). The system is fed by three tributary rivers; the Serpentine and the Murray enter

45 in the north-east, and the Harvey in the south (Figure 3.1). It has two openings to the Indian

Ocean in the north-western region; one natural channel in the north and the Dawesville Channel in the south, which that was opened in 1994 (Figure 3.1). The Peel-Harvey Estuary is surrounded by an extensive network of lakes and wetlands to the north, south and east

(O’Malley and Willmott, 2015), that comprise the greater Peel-Yalgorup system. The region experiences a Mediterranean climate, with hot, dry summers (December to February), cool, wet winters (June to August) with moderate rainfall (average rainfall = 880 mm per year) and persistent winds year-round (average wind speed = 12 to 16 km h-1) (Hale and Butcher, 2007;

Bureau of Meteorology, 2019).

Ecological significance

The greater Peel-Yalgorup wetland system covers 26,530 ha and is recognised as a wetland of international importance (Hale & Butcher 2007). In 1990, the system was formally listed as Ramsar site 482 under the Convention on Wetlands of International Importance (the

Ramsar Convention), having met seven of the nine criteria for recognition (Ramsar, 1971; Del

Marco and Willmott, 2017; Table 3.1). Initially, H. caspia was one of six bird species included under criterion six (i.e. the wetland regularly supports 1% of the individuals in a population of a species or subspecies of waterbird) that contributed towards site 482’s initial Ramsar listing.

However, H. caspia was later removed, as revised waterbird population estimates suggested that the system did not regularly support at least 1% of individuals within the Australia-wide

H. caspia population (Hale and Butcher, 2007; O’Malley and Willmott, 2015; Del Marco and

Willmott, 2017; Table 3.1).

The Peel-Harvey Estuary supports a diverse flora and fauna including migratory shorebirds, endemic and threatened taxa (Hale & Butcher 2007). A total of 65 species of estuarine and marine fish have been recorded in Peel-Harvey Estuary (Potter et al. 2016), many of which are commercially and recreationally important (Potter, Chrystal, et al. 1983; Lenanton

et al. 1984). In addition, the estuary supports several meso-predator species, including seabirds

and a population of Indo-Pacific Bottlenose Dolphins (Tursiops aduncus), that use the area for

breeding, foraging and travelling (Raeside 2012).

Table 3.1. Criteria for Ramsar-listing of the Peel-Yalgorup wetland system in south-western Australia, synthesised from Del Marco & Willmott (2017) and RAMSAR (1971).

RAMSAR Criteria Peel-Yalgorup compliance 1. The wetland contains a representative, rare The site includes the largest and most diverse estuarine complex in or unique example of (near-) natural wetlands south-western Australia and exemplifies coastal saline lake and found within the bioregion. freshwater marsh wetland types. 2. The wetland supports vulnerable, The site supports a breeding population of the Vulnerable Fairy Tern endangered or critically endangered species, or (Sternula nereis nereis) (IUCN 2019). The Lake Clifton thrombolite threatened ecological communities. microbial community has also been listed as critically endangered (EPBC 1999). 3. The wetland supports populations of plant The site is one of only two locations in south-western Australia and and/or animal species important for one of very few global sites where living thrombolites occur in inland biodiversity of the bioregion. waters. 4. The wetland supports plant and/or animal The site supports many species at critical life stages: feeding species at a critical stage in their life cycle or migratory shorebirds as well as breeding waterbird, fish, crab and provides them with refuge through adverse prawn species. conditions. The site is a refuge for waterbirds, fish and invertebrates in drought, and waterfowl (e.g. Musk Ducks, Biziura lobata and Australian Shelducks, Tadorna tadornoides) when moulting. 5. The wetland regularly supports >20,000 The site is the most important for waterbirds within the region and waterbirds. regularly supports >20,000 individuals. 6. The wetland regularly supports 1% of the Currently, fourteen species meet this criterion on site. This list individuals in a population of a species or includes an additional eight species over and above the initial list of subspecies of waterbird. six birds included under criterion six: • Grey Teal (Anas gracilis) • Australasian Shoveler (Anas rhynchotis) • Musk Duck (Biziura lobata) • Sharp-tailed Sandpiper (Calidris acuminata) • Curlew Sandpiper (Calidris ferruginea) • Red-necked Stint (Calidris ruficollis) • Red-capped Plover (Charadrius ruficapillus) • Banded Stilt (Cladorhynchus leucocephalus) • Eurasian Coot (Fulica atra) • Pied Stilt (Himantopus himantopus) • Red-necked Avocet (Recurvirostra novaehollandiae) • Fairy Tern (Sternula nereis nereis) • Hooded Plover (Thinornis rubricollis) 8. The wetland is an important area for fish The site is an important nursery, breeding and/or feeding ground for feeding, spawning, nursery or migration. at least 50 fish species. Peel-Harvey Estuary is a migratory route for the Pouched Lamprey (Geotria australis).

Anthropogenic connections and land use

The Peel-Harvey Estuary holds significant anthropogenic value for the local Wadjuk

Noongyar people of south-western Australia and the wider community (O’Malley & Willmott

2015). Its close proximity to the City of Mandurah (population: 85,300; Australian Bureau of

Statistics, 2018) has provided residents and visitors, alike, with access to the estuary’s natural assets. However, tourism and population growth throughout the region is predicted to increase the anthropogenic pressure on the Peel-Harvey Estuary in the future (O’Malley & Willmott

2015). Today, the major land-uses surrounding the Estuary include mining (estimated annual value = $3.4 billion), agriculture (estimated annual value = $324 million), commercial fisheries

(estimated annual value = $4.38 million from 12 licenses in circulation), land development, logging and tourism/recreation activities (O’Malley & Willmott 2015).

3.2.2 Tern abundance and distribution

Roost counts

The number of birds using a night roost within a region can be used to generate a population estimate (Dunlop 2018). A search was initiated to locate the H. caspia night roost on the Peel-Harvey Estuary, primarily by watching and listening for birds as they left foraging areas in the late afternoon and following them to the night roost site. Once the night roost was discovered in mid-November 2018, all birds were counted there at approximately two-weekly intervals. Each count was conducted by a concealed observer in the ten-minute period before last light, once all birds had assembled for the night (Figure 3.2). All H. caspia were counted with no attempt to distinguish among numbers of juvenile, one-year-old or adult terns as these stages are difficult to distinguish under the dusk light conditions. The flock was counted three times within a ten-minute period on each occasion and the average number of birds from these three counts was recorded.

Figure 3.2. Counting conditions at the night roost site for the Caspian Tern, Hydroprogne caspia, (pictured in foreground) on the Peel-Harvey Estuary in January 2019.

Estuary-wide census

Hydroprogne caspia were counted and their foraging activity was recorded at 20 accessible sites around the perimeter of the estuary every fortnight between 5 October 2018 and 17 February 2019 (Figure 3.3). The total number of H. caspia (total terns) and the number of birds foraging (foragers) were counted over a 10-minute period at each site. The time that the terns spent foraging, i.e. from the time a bird started foraging until no more birds were foraging, was recorded using a stopwatch. The proportion of time when any bird within the group was observed foraging within the ten-minute period was then calculated as a percentage.

Each site was surveyed on 10 occasions at varying times of day (from early morning to late afternoon) in an attempt to reduce any time bias. From these counts, as well as opportunistic observations of terns, areas with high levels of foraging activity were identified and sampled at higher intensity using focal sampling (see Section 3.2.3 below) and photographs of prey carried in the bills of the terns were taken – “digiscoping” (see 3.2.4).

Opportunistic observations

Opportunistic observations of tern presence and activity were recorded on Penguin Island

(the breeding colony), and around the Peel-Harvey Estuary, its tributaries and surrounding wetlands during the study. Records of colour-banded birds, interactions with Indo-Pacific

Table 3.2. The number and total duration (hours) of focal samples of H. caspia carried out at 13 forage sites (numbered blue dots in Figure 3.3) in six areas across the Peel-Harvey Estuary. Each monitoring period spanned either time block AM (morning; 4:30 – 9:30); MD (midday; 9:30 – 14:30); or PM (afternoon; 14:30 – 19:30) within the non-breeding period, October ’18 to February ’19. Site number refers to numbered blue dots in Figure 3.3.

Time Block Duration Monitoring site by area Total (hours) (and site number) AM MD PM 1. Murray 6 6 6 18 90 1. Austin Bay 2 2 2 6 30 2. Yunderup 2 2 2 6 30 3. Murray River 2 2 2 6 30 2. Serpentine 32 22 14 68 340 4. Nairns 30 20 12 62 310 5. Serpentine River 2 2 2 6 30 3. Mandurah Channel 4 4 4 12 60 6. Chimneys 2 2 2 6 30 7. Mandurah Channel 2 2 2 6 30 4. Dawesville Cut 12 12 12 36 180 8. Ward Pt 6 6 6 18 90 9. Wannanup 2 2 2 6 30 10. Pt Grey 2 2 2 6 30 11. Dawesville 2 2 2 6 30 5. Southern Estuary 2 2 2 6 30 12. Heron/Island Pts 2 2 2 6 30 6. Mealup Drain 2 2 2 6 30 13. Mealup Drain 2 2 2 6 30 Grand Total 58 48 40 146 730

Figure 3.3. Map of the Peel-Harvey Estuary (-32.40°S, 115.40°E), in south-western Australia with locations of census (red) and numbered monitoring sites (blue) within each foraging area.

The known night roost location is indicated by a yellow star (-32.5638°S, 115.7351°E). Bottlenose Dolphins (Tursiops aduncus), incidents of birds stealing prey from other birds, i.e. kleptoparasitism, and other observations of foraging behaviour, were noted. When dolphins were sighted within the foraging area, the pod was observed to assess whether or not H. caspia interacted with them. The number of terns and time of day were recorded for each interaction event. These foraging observations are recorded in Appendix 3.

As part of a separate project based at the Penguin Island breeding colony, H. caspia are banded or ringed (by J. N. Dunlop, Conservation Council of Western Australia), a common technique used in ornithological research that enables individual birds to be recognized following re-sighting or recapture. A total of 50 breeding adults were metal- and colour- banded, and 45 fledglings banded with a metal identification ring only, between 2012 and 2018.

Colour-banded birds have a unique combination of three “roll-on” colour-bands, in addition to a unique eight-digit metal band. Most colour bands have since been lost, possibly due to the force exerted upon them when the terns plunge-dive for fish (Chapter 2). However, some terns still retain between one and three of their original colour-bands and some of these birds can still be identified individually at a distance. When colour-banded terns were sighted, their colour combination, area of sighting and time of day were recorded.

3.2.3 Foraging activity

Studies of foraging activity were carried out using focal sampling, which involves the targeted, direct observation of individuals in situ as they perform an activity (Altman 1974).

This is a preferred method for bird dietary and foraging studies when conditions permit (Real

1996), as it is comprehensive and non-invasive. Focal sampling requires minimal expense and technology to implement, is non-invasive and, thus, provides an effective means of studying population-scale foraging patterns over time (Nye & Dickman 2005).

Focal sampling

Thirteen sites with high levels of H. caspia foraging activity were identified during exploratory surveys on the Peel-Harvey Estuary. These sites were grouped into six main foraging areas (Figure 3.3; Table 3.2). The influence of time of day on foraging activity was investigated by dividing the diurnal period into three 5-hour periods termed “blocks”: the morning (‘AM’; 04:30-09:30), midday (‘MD’; 09:30-14:30) and afternoon (‘PM’; 14:30-

19:30) periods. Observations were made from a kayak or the shoreline. The total number of terns present, the number foraging and total time spent foraging were recorded every hour during each observation block; light conditions permitting. A stopwatch was started at the first sign of foraging activity and stopped when no terns were foraging at the site. All sites were surveyed at least twice in each time block (Table 3.2). Overall, the study ‘effort’ totalled 730 observation hours in 146 ‘time blocks’ across the thirteen forage sites (Figure 3.3; Table 3.2).

Hydroprogne caspia were identified in situ according to their physical and behavioural characteristics (Figure 1.1), and their activity was described following an ethogram, developed from Nye and Dickman (2005; Table 3.3). Three types of foraging activity were recognised and recorded – scanning, hovering and plunge diving (Table 3.3; Nye and Dickman, 2005).

Data analyses

The time of first light and last light was recorded for each day of monitoring (Bureau of

Meteorology, 2019) in order to calculate the proportion of each time block available to terns for foraging. Abiotic data for tide height, air temperature, rainfall, wind speed and direction, from the Mandurah Channel (station 009977) were downloaded from the Bureau of

Meteorology for each day of the study period (www.bom.gov.au/climate/dwo/ Bureau of

Meteorology, 2019). Wind roses were created using wind speed and direction data in R studio

(R Core Team 2011). Salinity, water temperature and chlorophyll-a data were obtained from the Department of Water and Environmental Regulation from monitoring sites in close proximity to all six main foraging areas (Dep. of Water & Environmental Regulation, 2019).

Table 3.3. Ethogram for identifying observed H. caspia “activities”, developed from Nye & Dickman (2005). Grey shading indicates those behaviours categorised as foraging activities.

Mutually Exclusive Behaviour Description Loafing: Resting Standing on sand spit with head “exposed” Loafing: Roosting Standing on sand spit with head “tucked away” Bathing, stretching or cleaning feathers and body, with bill deep in Loafing: Preening dorsal plumage, often whilst standing Rapid, direct flight through an area, low levels of ‘engagement’ (no Travelling ‘scanning’ with neck or undulation in flight), flaps wings Controlled flight on ‘horizontal plane’, head held strong, occasionally Foraging: Scanning, on wing scans neck back and forth Flaps wings in ‘upright’ body ‘stance’, remains in a ‘self-actuated’ Foraging: Hovering stationary position mid-air (motivated, powered) Foraging: Plunge-diving Plummets from air (rapid drop) to water’s surface Fish-carrying Fish held in bill during direct flight to sand spit Consumption of prey, either in the air (post plunge-dive) or whilst Feeding: Self-feeding standing on sand spit Feeding: Chick-feeding Feed prey to chick, either regurgitated or directly Feeding: Year-old Begging Year-old tern “crying” to adults for fish Prey offered to adult (usually mate) whilst on nest or as part of Feeding: Adult-feeding courtship Adult terns (in breeding plumage) perform and display to attract and Courtship ‘bond’ with one another Pairs of terns come together and copulate, often following courtship Mating and/or the construction of a nest Pair of adult terns build nest on ground level where they lay and Nesting incubate a small clutch of eggs.

Two-way analyses of variance (ANOVA) were used to test whether the total number of

terns (total terns), number of foragers (foragers) and proportion of time spent foraging differed

among areas and blocks of time. The proportion of the total mean squares for each factor in the

ANOVA was calculated and used to determine the main sources of variation in these analyses

(Rogers et al. 2019). Before analysis, diagnostic plots (histograms and QQ plots) were

examined to assess the distribution of the data and investigate whether the variance was

homogenous. As the data did not meet the underlying assumptions for ANOVA, a square-root

transformation was applied to data for the total number of terns and number of foragers (Zuur

53 et al. 2010). No outliers were identified and a subsequent Levene’s test found that the variance was homogeneous across the different levels of factors in the ANOVA. No transformation was necessary for the proportion of foraging time. Where significant differences were found, posthoc Tukey’s HSD (honestly significant difference) tests were used to investigate which treatments different significantly (Chang et al. 2004; Rogers et al. 2019). Correlation analyses was used to examine the relationships between environmental variables (i.e. wind speed and tide height) and the total number of terns, foragers and proportion of time spent foraging by terns between October 2018 and February 2019 (Zuur et al. 2010). Additionally, data from the

Nairns foraging site, which was sampled most intensively due to continuously high numbers of birds present throughout the study period, was investigated further to test temporal variation in the total numbers, number of foragers and proportion of foraging time.

3.2.4 Determining diet from bill-loaded images and regurgitation pellets

Two primary methods were used to determine the diet of Hydroprogne caspia on Peel-Harvey

Estuary throughout the non-breeding season: fish identification from bill-loaded images and otolith identification in regurgitation pellets. These methods were selected as they are non- invasive, so as not to interrupt the natural foraging behaviour of birds, and to replicate a previous study by Dunlop & McNeil (2017) that successfully studied the diet of this same population of H. caspia at their breeding colony using the same approach.

Image analysis

Hydroprogne caspia are fish-carriers, often holding prey crosswise in their bill (“bill- loading”), prior to ingestion, chick-feeding or presenting the prey to mates (courtship feeding)

(Serventy et al. 1971; Gaglio et al. 2017). This behaviour allows the prey to be identified by direct observation or photography (Larson & Craig 2006). Bill-loaded birds were photographed using a Nikon D3500 camera (lens 70-300 mm) when the birds returned to sand spits with their

54 catch following plunge-dives (Figure 3.4). Photographs or ‘digi-vouchers’ of prey species were collated for identification, and the location, time and date of each digi-voucher was recorded.

Opportunistic photographs, taken by community members, were also included in the image analysis. Of the 495 digi-vouchers collated, 35 (7%) were provided by seven community members, who were encountered on the Estuary and submitted their photos for analysis.

Figure 3.4. A ‘digi-voucher’ of a bill-loaded tern taken at Point Ward, Peel-Harvey Estuary (photographer: S. Stockwell). The prey species is identified as the Eight-lined Trumpeter, Pelates octolineatus (estimated length: 117 mm, or 1.5 bill lengths). All digi-vouchers were collated with their associated metadata to create a catalogue for identification. A fish identification key was created with reference images of all fish species known to inhabit the Peel-Harvey Estuary (e.g. Loneragan et al., 1986, 1987; Potter et al.,

2016), and known to be consumed by H. caspia within south-western Australia (Dunlop and

McNeill, 2017). All digi-vouchers were analysed to identify prey to the lowest taxonomic level possible. Any prey species that could not be identified from the digi-vouchers was recorded as

“unidentified fish sp.”. The identification of each prey species was confirmed twice by the observer and checked with one of several fish ecologists at Murdoch University (Dr. Peter

Coulson, Prof. Neil Loneragan, Dr. Nic Dunlop, Dr. James Tweedley).

Prey size was estimated by comparing the length of prey with the average bill length to the nearest quarter bill length (± 19.5 mm ) of adult H. caspia (78.1 ± 3.40 mm, range = 71.8 -

87.1 mm), calculated from culmen measurements from 53 birds at their breeding colony on

Penguin Island between 2012 and 2016 (J.N. Dunlop, Conservation Council of WA,

55 unpublished data). The length of the fish was estimated in terms of number of bill lengths to the nearest ¼ bill and then converted to length in mm using the average bill length (Dunlop &

McNeill 2017). The error in these estimates includes deviation in size of the culmen length from the mean culmen length (CV = 30.2%, range of values within 11% of the mean) and error in estimation of the number of culmens equivalent to the fish length in the bill. However, this method provides a valuable approximation of fish size (Dunlop & McNeill 2017). The total number of fish from each taxa and the percentage contribution of each taxa was calculated for each area of the estuary and Penguin Island (breeding area), where opportunistic photos were collected in October and November 2018.

Regurgitation pellet analysis

Pellets of undigested prey parts are regurgitated by H. caspia whilst loafing on sandspits, sometime after prey has been consumed. These pellets consist of hard waste products from prey that are more resistant to digestion, including scales, bones and otoliths (Dowling,

Brown and Lek, unpublished report). All fish have three pairs of otoliths, or ear bones, used for balance and sound detection (Popper & Lu 2000). The largest, and most morphologically distinct of these is the sagittae, which can be used to identify prey species (Campana 1999;

Furlani et al. 2007) and provide information about their life history and ecosystem composition

(Mazloumi et al., 2017).

Figure 3.5. a) Pellet regurgitation by a Caspian Tern, Hyrdoprogne caspia, on Nairns sand spit, Peel- Harvey Estuary; b) the pellet prior to collection, c) assorted hard structures dissected from one pellet and; d) pair of otoliths, identified as Sillaginodes punctata.

Only four regurgitations were observed throughout the study period, despite over 730 hours of H. caspia observations, indicating this is an inconspicuous behaviour (Figure 3.4).

However, 218 pellets were collected opportunistically from sandspits at aggregation and foraging sites across the Peel-Harvey Estuary between October 2018 and February 2019 (Table

3.4) and two pellets were also collected at the Penguin Island breeding colony in October and

November 2018. Most pellets were uncovered at low tide in the latter part of the day.

Table 3.4. Location of sandspits and number of pellets collected at each monitoring site within six main Hydroprogne caspia foraging areas on Peel-Harvey Estuary. Latitude Longitude Number of Forage Area Monitoring Site Sandspit (S) (E) Pellets 1. Murray Murray Mouth -32.5912 115.7628 7 Austin Bay -32.5982 115.7732 0 Austin Bay Boodalan Island* -32.5933 115.7512 0 Murray River - - 0

2. Serpentine Close Spit -32.5723 115.7620 30 Far Spit -32.5772 115.7622 149 Nairns Serpentine Channel* -32.5740 115.7617 0 Murray Channel* -32.5787 115.7609 0 Serpentine River - - 0 3. Mandurah Chimneys -32.5609 115.7128 14 Channel Mandurah Channel -32.5533 115.7152 0

4. Dawesville Ward Pt -32.5939 115.6726 9 Dawesville - - 0 Pt Grey -32.6156 115.6666 0 Wannanup -32.6039 115.6541 7

Island Pt Reserve -32.7549 115.6971 2 5. Southern Herron Pt (closer) -32.7432 115.7110 0 Estuary Southern Estuary Herron Pt (beyond) -32.7451 115.7098 0 (Harvey River) Brunswick Island -32.7495 115.7062 0 North of Herron Pt -32.7348 115.7128 0

Mealup Drain -32.6921 115.6972 0 6. Mealup Drain Mealup Drain Fallen Tree Pt -32.7020 115.7005 0

Total 218 * Spits that are available to H. caspia only at lower tides (< 0.7m)

All pellets were placed in clean, individual zip-lock bags and frozen prior to analysis

(Figure 3.5). Each pellet was air dried on absorbent paper towel, weighed and separated into its components. The remains were weighed, and the otoliths were removed and examined under

57 a dissecting microscope to identify the fish species to the lowest taxonomic order possible, using a reference collection (Figure 3.5; Dowling et al., unpublished report; Furlani et al. 2007).

The number of otoliths for each prey species in each pellet was counted, then otolith pairs were divided by two to estimate the number of individual fishes caught (Dunlop & McNeill 2017).

Dietary item data analyses

The total number of each taxa recorded in each region was determined and the proportional contribution of each taxa to the total fish recorded in the region calculated. Each otolith was identified to the lowest taxonomic level possible, often to species. The number of otoliths for each species was counted and divided by two to estimate the number of fish consumed and the percentage contribution of each species to the diet of H. caspia in each region

(Dunlop & McNeill 2017). The relationship between the number of different prey species detected and the number of samples collected (recorded from bill-loaded images) was plotted as a species accumulation curve in PRIMER 7 (Ugland et al. 2003; Clarke & Gorley 2015) for the three areas where most samples were recorded (Nairns, near Serpentine and Point Ward, near Dawesville on the Peel-Harvey Estuary and the breeding colony on Penguin Island). The species accumulation curves were constructed by randomly ordering samples within each region and plotting the curve of cumulative frequency of all different species calculated (e.g.

Potter et al., 2016). This computation was repeated for a further 999 random orderings of the samples, and the resulting curves averaged and plotted following Potter et al. (2016).

Bill-loaded images from the three key areas – Serpentine River, Point Ward and Penguin

Island – where at least 70 images had been lodged, were randomly grouped into equal ‘samples’ for further analysis (Clarke et al. 2014). From this, multidimensional scaling (MDS) ordination plots were constructed to provide a visual representation of similarities between grouped samples using the Bootstrap Average Routine (Clarke & Gorley 2015; Greenwell et al. 2019).

Averages of repeated bootstraps for grouped samples were used to create a metric MDS

58 ordination plot (Greenwell et al. 2019). A shade plot (i.e. a colour-gradient representation of a frequency matrix) was constructed to highlight the most significant components of H. caspia diet from random samples of bill-loaded images between three key areas (Clarke et al. 2014).

On this plot, white spaces indicated the prey item wasn’t recorded in that sample, while the shade colour increased in intensity from pale blue to deep red in proportion to the frequency of each prey type in each ‘sample’ (Greenwell 2017).

Commercial fisheries data

Catch and effort data for commercial fisheries operating on the Peel-Harvey Estuary between 2013 and 2018 were obtained from the Department of Primary Industries and Regional

Development, Western Australia in April 2019. The total catch (kg), proportion of catch (%) and effort (mean number of vessels per month) was calculated for each species over these five years.

3.3. Results

3.3.1 Environmental conditions in the Peel-Harvey Estuary

The air temperature between October 2018 and February 2019 ranged between 9.0 and

35.8 oC with a mean of 21.0 °C across all sites (Figure 3.6a). Mean daily rainfall across all sites during monitoring was 0.37 mm (2d.p.; ±1.15 mm) although 85% of monitoring days had no rainfall recorded (Figure 3.6a). Wind speed and direction varied between months across all monitoring sites on the Peel-Harvey Estuary. During the October to February period, winds across all sites blew most frequently from a south-westerly direction, with wind speeds ranging from 0 to 40 km h-1 (mean = 16.1 km h-1; Figure 3.7a). Winds from the south-east were present through to February but were weaker than those from the south-west (Figure 3.7b-f).

The Department of Water (2019) data for chlorophyll-a at three sites in the Harvey

Estuary and three in the Peel Inlet showed that values were greatest over winter and spring

(from June to September), with the highest readings of 0.007 and 0.008 mgL-1 in Southern

Estuary and Mealup Drain, respectively, in August 2018 (Figure 3.6b). Salinity was relatively consistent across all sites with a significant decline following the winter period (June to

August) in 2018. Particularly in Murray, Serpentine and Southern Estuary that were closest to river mouths, where salinities 8.3 and 11.3 were recorded. In comparison, the mean salinity across all other sites within this period was of 31.7 mgL-1. Water temperature was similar between all areas ranging between 13.8 oC in winter (June to August) to 25.9 oC in summer

(December to February), with an average value of 18.7oC between May 2017 and January 2019

(Figure 3.6d).

60 a 40 Rainfall Minimum Maximum 16 35 14

C) 30 12 ° ( 25 10 20 8 15 6

10 4 Rainfall (mm) Temperature 5 2 0 0 1/10/2018 1/11/2018 1/12/2018 1/01/2019 1/02/2019 Date

MUR 0.010 b /SER 0.008 MCH

0.006 DAW

0.004 SOU

0.002 MEA

0.000 Chlorophyll Chlorophyll (mg/L) a 5 6 7 8 9 10 11 12 1 2 3 4 5 6 7 8 9 10 11 12 1 2017 2018 2019 Month and Year c 500 MUR /SER 400 MCH

300 DAW

200 SOU

Salinity Salinity (ppt) 100 MEA

0 5 6 7 8 9 10 11 12 1 2 3 4 5 6 7 8 9 10 11 12 1 2017 2018 2019 Month and Year

30 MUR

d /SER C) ° 25 MCH 20 DAW 15 SOU 10 5 MEA

WaterTemperature ( 0 5 6 7 8 9 10 11 12 1 2 3 4 5 6 7 8 9 10 11 12 1 2017 2018 2019 Month and Year Figure 3.6. Values for (a) minimum and maximum daily air temperature and daily rainfall from October 2018 to February 2019 and values for (b) chlorophyll a, (c) salinity and (d) water temperature for each area of the Peel-Harvey Estuary between May 2017 and January 2019. Data for (b) to (d) provided by the Department of Water and Environmental Regulation from sites within each area: MUR/SERP = Murray and Serpentine; MCH = Mandurah Channel; DAW = Dawesvill; SOU = Southern Harvey; MEA = Mealup Drain. Data on air temperature and rainfall from Mandurah station 009977 by the Bureau of Meterology

Figure 3.7. Wind roses showing the frequency of wind speed in each direction across all sites between October 2018 and February 2019 (a), and for each month within the study period (b to f). Data from Bureau of Meteorology (www.bom.gov.au/climate/dwo/)

3.3.2 Abundance and distribution

Roost counts The numbers of H. caspia at the night roost on the Peel-Harvey Estuary increased from

84 birds in mid-November to an average of 107 birds in mid-December. In mid-January, an average of 132 birds (± 1.42 birds) were counted before reaching a maximum of 147 terns in mid-February 2019, five months after the end of their breeding season (Figure 3.8). However, on 21 and 22 February, the roost count dropped significantly from 147 birds to 71 (21st

February 2019) (Figure 3.8) and then 0 birds (22nd February 2019; Figure 3.8).

160 140 120 100 80 60 40 20

Count Count Caspian of Terns 0 14-Nov 28-Nov 12-Dec 26-Dec 9-Jan 23-Jan 6-Feb 20-Feb 6-Mar

Date Figure 3.8. Total count (± 1 standard error) of Caspian Terns Hydroprogne caspia at the night roost site on the Peel-Harvey Estuary between 15 November 2018 and 21 February 2019. No birds were seen at the night roost on 21 February.

Estuary census Proximate census sites within six areas were identified with high tern counts, greater than the overall average of 4.1 birds (± 7.1 birds; Table 3.5). These sites were later monitored at higher intensity using focal sampling to investigate the influence of area and time of day on total numbers, numbers of foragers and foraging behaviour. While tern counts varied across foraging sites, the number of total terns on Peel-Harvey was relatively consistent during

November and December 2018, before dropping in early January 2019 and climbing again in mid-February 2019 (Figure 3.9). Sites within Serpentine and Mandurah Channel (areas two and three) remained relatively consistent throughout the study period (Figure 3.9).

100 1 Murray 80 2 Serpentine 60 3 Mandurah Channel 4 Dawesville

terns 40 5 Southern Estuary 6 Mealup 20

Accumulated Accumulated count totalof 0 12-Nov 26-Nov 11-Dec 23-Dec 7-Jan 20-Jan 4-Feb 17-Feb Date

Figure 3.9. The total number of Caspian Terns, Hydroprogne caspia, counted during Estuary Census at sites within each of the six main foraging areas in the Peel-Harvey Estuary between 12 November 2018 and 17 February 2019 as an accumulation curve.

Throughout the study period, the highest mean counts of total terns (± 1 SD) were recorded at sites within areas three (20.6 ± 11.8 terns at ISL) and two (10.3 ± 5.4 and 11.8 ±

6.7 birds at NAN and SEM respectively; Table 3.5). The mean number of foragers was highest across areas one (MUM: 2.1 ± 1.4 birds), two (NAN: 2.2 ± 2.2 & SEM: 2.5 ± 2.5 birds) and four (LHS: 2 ± 1.4 birds; Table 3.5). The proportion of time spent foraging by terns was highest in area two (NAN: 61.1% ± 50.1 & SEM: 60.9% ± 46.2). All sites on tributary rivers and channels (site MUR in area one, SER in area two and MCH in area three) recorded lower tern counts than corresponding sites at their mouths (site MUM in area one, NAN and SEM in area two and ISL in area three; Figure 3.3; Table 3.5).

Table 3.5. Mean values of total terns, foragers and proportion of time spent foraging across all census sites (to one decimal place, with standard deviation) from fortnightly counts on the Peel-Harvey Estuary between October 2018 and February 2019.

Area Site Total Foragers %Time Foraging 1 Murray MUM 6.5 (±5.7) 2.1 (±1.4) 55.0 (±36.7) MUR 0.1 (±0.4) 0.1 (±0.3) 2.1 (±6.5) 2 Serpentine COW 0.9 (±1.5) 1.1 (±1.7) 24.7 (±41) NAN 10.3 (±5.4) 2.2 (±2.2) 61.1 (±50.1) SEM 11.8 (±6.7) 2.5 (±2.5) 60.9 (±46.2) SER 0 0 0 3 Mandurah Channel ISL 20.6 (±11.8) 0.7 (±1.1) 5 (±8.9) LHN 1.5 (±1.6) 0.8 (±0.9) 18.9 (±23.5) MCH 1 (±1.4) 0.9 (±1.4) 18.2 (±29.4) 4 Dawesville DAW 0.1 (±0.4) 0.5 (±0.8) 7.8 (±15.8) LHS 7.3 (±9.6) 2 (±1.4) 49 (±41.9) WAR 0.6 (±0.7) 0.5 (±0.7) 11.8 (±17.4) 5 Southern Estuary HEP 6.1 (±3.6) 0.8 (±0.9) 24.9 (±35.2) IPR 4 (±2.7) 1.3 (±1.6) 46.7 (±43.7) 6 Mealup Drain MMR 8 (±11.7) 0.9 (±1.3) 36.6 (±42.2) Sites outside these areas

CRI 0.3 (±0.7) 0.5 (±1.1) 14.6 (±31.1)

CRW 0.1 (±0.4) 0.2 (±0.4) 4.1 (±12)

PRF 1 (±1.1) 0.3 (±0.7) 18.6 (±31)

PRR 0.4 (±0.7) 0.1 (±0.3) 4.9 (±15.4)

ROB 1.3 (±1.8) 0.2 (±0.4) 2.6 (±5.9) Overall Mean 4.1 (±7.1) 0.9 (±1.4) 23.5 (±35.6)

Foraging activity of H. caspia fluctuated with time across census sites between October

2018 and February 2019 (Figure 3.9). Consistently high numbers of terns were recorded at sites within Serpentine (NAN and SEM) where counts ranged from 5 to 34 with an average of 21 (±

10.2) birds (Figure 3.9). Similarly, the ISL site at Mandurah Channel had tern counts between

5 and 43, with an average of 20.6 (± 11.8) birds. Southern Estuary recorded higher numbers of terns in November and December 2018 (range 9 to 18 birds), but dropped off in January and

February (range 1 to 10 birds; Figure 3.9) whereas Mealup Drain followed an opposite trend with low bird counts in November and December 2018 (range 0 to 1 bird), increasing in January and February 2019 to 29 terns (Figure 3.9). Both Murray and Dawesville recorded their highest number of terns in December with respective maximum counts of 19 and 29 birds (Figure 3.9).

The pattern of tern counts and foraging activity observed at frequently focal-sampled foraging sites, such as Nairns (in area two, Serpentine), followed the same pattern of change during the study period as those censuses at the same site (Figure 3.10).

60 Focal Sampling 50 Estuary Census 40 30 20 10

Count of total terns totalof Count 0 5/10/2018 5/11/2018 5/12/2018 5/01/2019 5/02/2019 Date

Figure 3.10. The total count of Caspian Terns, Hydroprogne caspia, at Nairns site (area two) during estuary censuses (NAN, SEM & COW sites combined; Figure 3.3) and counts of total terns at the same site during focal sampling.

The total number of terns summed across all 20 census sites (44 to 104 birds) was very similar to the sum of counts at sites within the six focal sampling areas (Figure 3.11). The roost count was lower than both the total estuary-census count and the combined counts from the six main sites in late November (84). Roost counts increased at the end of November and were

65 markedly higher that estuary counts in January and early February (104 to 147 birds). However, the roost count declined markedly in mid-February and no birds were seen on 22 February

2019 (Figure 3.11).

160 140 120 TOP SIX 100 80 ALL 60 ROOST Number Number terns of 40 COUNT 20 0

Date

Figure 3.11. Temporal variation in tern counts from all census sites (black), the six most popular areas (dashed line) and counts at the night roost (light grey) on the Peel-Harvey Estuary between November 2018 and February 2019.

Individual foraging patterns

Nine individual birds were recognised by their colour bands throughout the study period on sand spits across the Estuary (Figure 3.12). Some birds were re-sighted frequently in a limited number of locations, for example, orange-white and its fledged chick were only sighted on Wannanup spit (Figure 3.12), and appeared reluctant to leave even when disturbed by dogs and kite surfers. Other birds such as white-red-lime green and yellow-grey were re-sighted at sites across the entire Peel-Harvey Estuary (Figure 3.12). The most frequently re-sighted individual, red-yellow-grey was sighted on Peel Inlet most frequently across Yunderup and

Nairns sites, as well as Chimneys on the Mandurah Channel and Pt Ward near the Dawesville

Cut (Figure 3.12).

Figure 3.12. Location and number of resights of colour-banded individuals at monitoring sites across Peel-Harvey Estuary (October 2018 to February 2019), and photographs of each colour-banded tern.

3.3.3 Foraging activity

Population-level foraging patterns The foraging activity of H. caspia was focussed on six main areas of Peel-Harvey Estuary during the non-breeding period: Murray, Serpentine, Mandurah Channel, Dawesville, Southern

Estuary and Mealup Drain. The total number of terns differed significantly amongst areas of the Peel-Harvey Estuary (P < 0.0001) but not between times of day (P = 0.56) and the area- block interaction was not significant (P = 0.87, Table 3.6a). The Tukey HSD posthoc test

67 showed that the mean number of terns was significantly greater at Mealup Drain (5.09) and

Serpentine (4.51) than Mandurah Channel (3.23), Murray (3.22) and Dawesville (2.95), while no significant difference was found between these sites and the Southern Estuary (4.42;

Figure 3.13a). The mean number of foragers differed significantly amongst areas (P = 0.001) and blocks of time (P = 0.037), but the area-block interaction was not significant (P = 0.378,

Table 3.6b). The mean number of foragers was significantly greater at Mealup Drain (3.34),

Southern Estuary (3.16) and Serpentine (3.08) than Murray, Dawesville and Mandurah

Channel (2.40 to 2.49, Figure 3.13b). Similarly, the proportion of time spent foraging by terns also differed significantly amongst areas (P < 0.0001) and blocks of time (P = 0.023), and the area-block interaction was not significant (P = 0.43, Table 3.6c). The proportion of time spent foraging was significantly greater at Serpentine (98%) than all other areas (35 to 58%), except

Mealup Drain (59.3%, Figure 3.13c).

Table 3.6. Mean squares, F-values and P-values from two-way ANOVAs to test for differences in (a) total terns (b) number of foragers and (c) proportion of time spent foraging among Areas and Blocks of time. Df = degrees of freedom. P values < 0.05 are in bold.

Source of variation df MS %MS F P a) Total terns Area 5 18.464 82.5 10.04 < 0.0001 Block of Time 2 1.08 4.8 0.58 0.560 Area x Block 10 0.963 4.3 0.52 0.874 Error 128 1.8750 8.4 Total 22.382 b) Foragers Area 5 3.615 44.6 4.40 0.001 Block of Time 2 2.782 34.3 3.38 0.037 Area x Block 10 0.893 11.0 1.09 0.378 Error 128 0.8220 10.1 Total 8.112 c) Time spent foraging (%) Area 5 5177 70.1 13.79 < 0.0001 Block of Time 2 1452 19.7 3.87 0.023 Area x Block 10 385 5.2 1.03 0.426 Error 128 375 5.1 Total 7389

(a) a 6 a ab 5.09 4.51 5 4.42 b b b 4 3.22 3.23 2.95 3

Number Number totalof terns 1

0 Murray Serpentine Mandurah Dawesville Southern Estuary Mealup Drain Channel Area

(b) 5 a 4 ab a 3.16 3.34 ab 3.08 ab a 3 2.49 2.46 2.40 2

1 Number Number foragers of 0 Murray Serpentine Mandurah Dawesville Southern Estuary Mealup Drain Channel Area a (c) 98.0 100 90 b ab 80 59.0 b 59.3 70 54.8 b b 60 40.5 50 35.9 40 30 20 10 Time spent foraging Time foraging spent (%) 0 Murray Serpentine Mandurah Dawesville Southern Estuary Mealup Drain Channel Area

(d) (e) 5 a ab 84.3 a 100 74.8 4 b 3.05 b ab 80 56.3 3 2.59 2.69 60 2 40

1 20 Number Number foragers of 0 0

AM MD PM AM MD PM Time spent foraging Time foraging spent (%) Time Block Time Block Figure 3.13. Mean values (± 1 SE) and results for Tukey's HSD tests (shown by letters, denoting the differences between means) to test for differences amongst areas in (a) total tern counts, (b) forager counts and (c) time spent foraging, and amongst times of day for (d) forager counts and (e) time spent foraging.

The Tukey HSD test showed that the mean number of foragers in the morning block

(3.05) was significantly greater than in the midday block (2.59) but not the afternoon (2.69;

Figure 3.13d). The proportion of time spent foraging was also significantly greater in the morning (84.3%) than the afternoon (56.3%) and did not differ significantly from midday

(mean 74.8%; Figure 3.13e).

At Nairns (within area two), the mean total number of terns increased from 18.1 in

October 2018 to a peak of 36.3 in January 2019, before dropping to 24.3 in February

(Table 3.7). The mean number of foragers was consistently 30-45% of all birds present. The mean proportion of time spent foraging at Nairns declined during the study period: terns foraged 63.7% of the time in October 2018, which decreased to 52.9% in December 2018 and

40.1% in February 2019 (Table 3.7).

Table 3.7. Monthly variation in mean (± 1 SD) total number of terns, number of foragers and proportion of time spent foraging (%), at a frequently sampled foraging site, Nairns (area two) on the Peel-Harvey Estuary. 2018 2019 Oct Nov Dec Jan Feb Overall Number of blocks sampled 19 25 11 4 3 62 18.1 29.2 29.1 36.3 24.3 26.0 (±9.8) Total Terns (±6.8) (±6.5) (±11.9) (±13.9) (±2.1) 7.4 12.7 13.5 11.8 9.3 11.0 (±5.6) Foragers (±3.4) (±6.8) (±3.7) (±0.5) (±5.5) 63.7 61.6 52.9 59.5 40.1 59.5 (±14.7) Times spent foraging (%) (±12.5) (±15.0) (±13.4) (±14.7) (±16.4)

Preliminary correlation analyses showed that wind speed was correlated with the total number of terns at foraging sites but accounted for only 5.2% of the total variation in total terns

(R2 = 0.052, P = 0.029, n = 75; Table 3.8). Similarly, the wind speed was also correlated with the proportion of time spent foraging but, again, accounted for only a small proportion of the total variation (R2 = 0.045, P = 0.006, n = 147; Table 3.8). None of the correlations between tern counts or proportions of time spent foraging, and tidal height were significant (Table 3.8).

Table 3.8. Summary table showing p-values and coefficients of determination (R2) from correlation analyses using square-root transformed data for total and foraging terns, and un-transformed data for foraging rates. P-values < 0.05 are in bold. Variable Tide Wind speed R2 P n R2 P n a) Total terns 0.011 0.652 75 0.052 0.029 75 b) Foragers 0.011 0.546 59 0.017 0.843 59 c) Time spent foraging 0.005 0.188 147 0.045 0.006 147

3.3.4 Diet

In total, 21 different prey taxa were identified from 495 bill-loaded images and 220 regurgitation pellets collected from the Peel-Harvey Estuary and Penguin Island (breeding colony) between October 2018 and February 2019. Overall, 18 taxa were identified in bill- loaded images and seven in the otoliths from regurgitation pellets. On the Peel-Harvey Estuary only, 16 fish species and one crustacean were identified (two records of Blue Swimmer Crab,

Portunus armatus, were recorded; Table 3.9). The most common species from photographs were whiting species (Sillaginidae, 35.0%) including King George Whiting (Sillaginodes punctatus; 8.2%), Southern School Whiting (Sillago bassensis; 2.3%), Trumpeter Whiting

(Sillago maculata; 6.7%) and Yellowfin Whiting (Sillago schomburgkii; 10.3%). Mullets

(Mugilidae, 33.9%) including Yellow-eyed Mullet (Aldrichetta forsteri; 22.1%) and Sea

Mullet (Mugil cephalus; 11.8%) were the second most common prey species (Table 3.9). Eight- lined Trumpeter (Pelates octolineatus) comprised 14.4% of all forage fish identified from image analysis, and 42% of all fish captured at Dawesville (Table 3.9). Overall, fish could not be identified in 23 bill-loaded images, accounting for 5.7% of photos. Bill-loaded images from

Penguin Island also showed high proportions of mullets (44.5%), whitings (23.6%) and P. octolineatus (19.4%) (Table 3.9). Three prey species of marine fish identified from Penguin

Island images; Rainbow Cale (Heteroscarus acroptilus), Brown Spotted Wrasse (Notalabrus parilus) and a goatfish species (Mullidae), were not seen in images from the Peel-Harvey

Estuary (Table 3.9).

Table 3.9. Proportion of each prey species (%) recorded from image and pellet analysis of Hydroprogne caspia in each area of the Peel-Harvey estuary (Areas 1 to 6) and Penguin Island (Area 7). Areas 1 to 6 as defined in Figure 3.3. Number of samples from each area is noted in brackets in the parentheses. IMAGE ANALYSIS PELLET ANALYSIS Area Area Family Fish Species 1 2 3 4 6 7 1 2 3 4 7 (14) (250) (5) (114) (6) (71) (6) (108) (8) (21) (2) Hemiramphidae Hyporhamphus melanochir 8.1 1.8 16.7 1.4 Gobiidae Goby spp. 0.4 4.2 All mullet spp. 14.3 42.3 20.0 14.9 16.7 44.5 16.7 43.5 25.0 33.3 Mugilidae Aldrichetta forsteri 14.3 26.0 20.0 10.5 16.7 15.3 25.9 12.5 4.8 Mugil cephalus 16.3 4.4 29.2 16.7 17.6 12.5 28.6 Arripidae Arripis georgianus 0.4 Gerreidae Gerres subfasciatus 0.9 Heteroscarus 1.4 Labridae acroptilus Notolabrus parilus 2.8 Mullidae Goatfish sp. 1.4 All whiting spp. 78.6 32.5 60.0 35.1 16.7 23.6 66.7 26.9 75.0 52.4 50.0 Sillaginodes punctatus 14.3 8.5 20.0 5.3 16.7 16.7 14.3 Sillago bassensis 14.3 1.2 3.5 Sillaginidae Sillago maculata 14.3 6.1 7.9 Sillago schomburgkii 28.6 9.4 20.0 10.5 2.8 Whiting sp. 7.1 7.3 20.0 7.9 6.9 66.7 24.1 75.0 38.1 50.0 Amniataba caudavittata 0.4 Terapontidae Pelates octolineatus 2.4 20.0 42.1 16.7 19.4 6.5 Paralichthyidae Pseudorhombus jenynsii 1.2 0.9 Plotosidae Cnidoglanis macrocephalus 1.6 Monacanthidae Leatherjacket sp. 0.4 1.8 Tetraodontidae Torquigener pleurogramma 33.3 Unidentified fish spp. 7.1 9.4 2.6 0.0 1.4 16.7 21.3 14.3 50.0 Portunidae Portunus armatus 0.8 1.9

Of the 220 regurgitation pellets collected, 109 contained otoliths. Many of the otoliths

were broken into smaller shards (Figure 3.14a), possibly from the impact of plunge-diving terns

on the dorsal surface of the prey species. The mean number of otoliths per pellet was 0.83

otoliths, corresponding to 0.59 fish, with the number of otolith pairs ranging from none to three

individual fish per pellet. In total, 125 prey captures from three families were identified from

otoliths in regurgitation pellets. Mullet species, A. forsteri and M. cephalus comprised 45.6%,

while whiting species, S. punctatus and whiting spp. comprised 40% (Table 3.9). Pelates

octolineatus accounted for 5.6% of prey species identified in regurgitation pellets. 8.8% of all

otoliths were unable to be identified (unidentified fish spp., Table 3.9).

a) b)

Figure 3.14 Photographs of otoliths dissected from regurgitation pellets collected in the Peel-Harvey estuary (a) in shards, identified as Pelates octolineatus and (b) complete pair of otoliths, identified as Sillago schomburgkii

Table 3.10. Proportion of each prey species (%) in Hydroprogne caspia diet in each month recorded from image analysis on the Peel-Harvey Estuary between October 2018 and February 2019. Month October November December January February Fish Species (32) (197) (161) (74) (13) Hyporhamphidae Hyporhamphus melanochir 4.3 1.8 1.6 16.9 0 Gobiidae Goby spp. 4.3 0.4 0 0 0 All mullet spp. 47.8 53.3 29.1 28.1 43.8 Mugilidae Aldrichetta forsteri 34.8 30.7 17.5 11.2 18.8 Mugil cephalus 13.0 22.7 11.6 16.9 25.0 Arripidae Arripis georgianus 0 0.4 0 0 0 Gerreidae Gerres subfasciatus 0 0 0.5 0 0 All whiting spp. 21.7 35.1 48.1 23.6 43.8 Sillaginodes punctatus 4.3 12.9 6.9 5.6 0 Sillago bassensis 0 0.4 4.2 0 0 Sillaginidae Sillago maculata 0 2.7 10.1 1.1 0 Sillago schomburgkii 0 6.7 12.7 4.5 0 Whiting spp. 17.4 12.4 14.3 12.4 43.8 Amniataba caudavittata 4.3 0 0 0 0 Terapontidae Pelates octolineatus 17.4 6.7 18.0 27.0 0 Paralichthyidae Pseudorhombus jenynsii 0 0.4 1.1 0 0 Plotosidae Cnidoglanis macrocephalus 0 0.4 0 2.2 12.5 Monacanthidae Leatherjacket sp. 0 0.4 1.1 0 0 Tetraodontidae Torquigener pleurogramma 0 0.4 0 2.2 0 Portunidae Portunus armatus 0 0.4 0.5 0 0 TOTAL 100 100 100 100 100

The proportion of prey species recorded in the diet of H. caspia from image analysis varied between the months in the Peel-Harvey Estuary. For example, mullet species, A. forsteri and M. cephalus, comprised approximately half of all prey species taken in October and

November 2018 (Table 3.10). However, in December 2018 and January 2019, mullets only contributed to approximately 30% of all photographic captures. Whiting species were most frequently taken by H. caspia in December 2018 (48.1% of images) and February 2019 (43.8% of images; Table 3.10). The proportion of P. octolineatus ranged between 6.7 and 27% between

October 2018 and January 2019 but this species was not recorded in images from February

2019 (Table 3.10). Other species such as Hyporhamphus melanochir and C. macrocephalus contributed to a relatively small proportion of the H. caspia diet except in January and

February, where their contributions were 16.9% and 12.5%, respectively (Table 3.10).

On average, the longest prey species taken by H. caspia was C. macrocephalus, which had an estimated mean length of 244 mm (±37.9) or 3.1 bill lengths, followed by H. melanochir

(202 mm (±59.5) or 2.6 bill lengths; Table 3.11). The estimated mean prey length for the other species ranged from 117 to 195 mm, or 1.5 to 2.5 bill-lengths (Table 3.11). Overall, the mean length of mullets, whitings and Eight-lined Trumpeter (Pelates octolineatus) caught by H. caspia were 167 mm (±53.0; 2.1 bill lengths), 170 mm (±49.6; 2.16 bill lengths) and 120 mm

(±16.5; 1.5 bill lengths), respectively (Table 3.11). The mean length of mullets, A. forsteri, M. cephalus, from gill net trawls (deeper areas) in Peel-Harvey Estuary was 246 and 267 mm respectively, and from beach seine trawls (shallow areas) was 136 and 143 mm respectively

(Potter, Loneragan, et al. 1983). Similarly, the mean lengths of whitings, S. punctatus and S. schomburgkii from gill net trawls in Peel-Harvey Estuary were 278 and 229 mm respectively, and from beach seine trawls were 162 and 108 mm (Potter, Loneragan, et al. 1983). Beach seines in shallow water found P. octolineatus had a mean length 84 mm and gill nets in deeper water revealed fish of mean length 169 mm (Potter, Loneragan, et al. 1983). The mean length

of whitings, mullets and P. octolineatus caught by H. caspia falls within these values for fish

length at shallower and deeper parts of Peel-Harvey Estuary.

Table 3.11. The estimated mean length (± 1 SD) of fish (mm) for each area of the Peel-Harvey Estuary (areas 1 to 6) and Penguin Island (area 7), and an overall mean bill to fish length ratio from bill-loaded images, taken October 2018 to February 2019. Areas 1 to 6, as defined in Figure 3.3. Area Family Fish Species 1 2 3 4 6 7 Overall Bill Ratio (14) (250) (5) (114) (6) (71) Hemiramphidae Hyporhamphus 188.3 273 172 352 202 2.6 melanochir (±48.2) (±0) (±59.5) Gobiidae Goby spp. 78 98 88 1.1 Mugilidae All mullet spp. 156.5 161.5 214 136 117 187 167 2.1 (±27.6) (±52.0) (±46.2) (±44.7) (±52.7) (±53.0) Aldrichetta forsteri 156.5 149.2 214 151 117 155 151 1.9 (±27. 6) (±45.8) (±42.5) (±25.4) (±42.9) Mugil cephalus 173.8 121 219 184 2.3 (±58.5) (±8.9) (±49.7) (±59.9) Arripidae Arripis georgianus 117 117 1.5

Gerreidae Gerres subfasciatus 117 117 1.5

Labridae Heteroscarus 137 137 1.7 acroptilus Notolabrus parilus 117 117 1.5 (±0) (±0) Mullidae Goatfish sp. 78 78 1 Sillaginidae All whiting spp. 186.6 170.24 182 165 273 189 170 2.16 (±64.2) (±47.0) (±21.9) (±50.4) (±51.1) (±49.6) Sillaginodes 234.5 197.8 195 147 273 143 179 2.3 punctatus (±166.2) (±56.4) (±66.0) (±50.8) (±66.4) Sillago bassensis 176 (±0) 169.3 166 169 2.1 (±29.6) (±33.5) (±25.6) Sillago maculata 176 (±0) 175.5 189 180 2.3 (±19.5) (±57.7) (±36.3) Sillago schomburgkii 151.5 160 195 182 167 2.1 (±36.9) (±41.0) (±43.5) (±41.6) Whiting sp. 195 148.6 157 143 234 155 2 (±49.4) (±22.5) (±46.6) (±25.3) Terapontidae Amniataba 117 117 1.5 caudavittata Pelates octolineatus 100.8 98 122 117 120 120 1.5 (±19.2) (±15.4) (±15.0) (±16.5) Paralichthyidae Pseudorhombus 130 98 122 1.5 jenynsii (±29.5) (±28.9) Plotosidae Cnidoglanis 244.3 244.3 3.1 macrocephalus (±37.9) (±37.9) Monacanthidae Leatherjacket sp. 195 195 2.5

Tetraodontidae Torquigener 117 117 117 1.5 pleurogramma (±0) (±0) Unidentified fish 126.5 98 117 1.5 spp. (±13.4) (±19)

The estimated mean prey length from bill-loaded images of H. caspia varied with the area. For example, the largest mullets (A. forsteri) were caught in Mandurah Channel (area 3) with a mean length of 214 mm (±46.2) or 2.75 bill lengths (Table 3.11). In contrast, the largest whiting (S. punctatus, 352 mm or 4.5 bill lengths) was caught at Murray (area 1), while the smallest (S. punctatus and whiting spp.) came from Penguin Island and Dawesville respectively

(areas 7 and 4), both with a length of 143 mm or 1.75 bill lengths (Table 3.11).

The species-accumulation curve constructed for prey species shows that 250 ‘samples’ were required to find 90% of species recorded in H. caspia photo-images (18 species) on the

Peel-Harvey Estuary and Penguin Island combined (Figure 3.15). After 100 images, an estimated 15 species were accumulated (68% of all recorded species), which increased to 18 species (82% of all recorded species) after 200 images (40.4% of all images; Figure 3.15).

Figure 3.15. Prey species accumulation curve showing the representation of all prey species at two sites on Peel-Harvey Estuary and Penguin Island. Each ‘sob’ is a collection of randomly grouped photos to create a ‘sample’. Metric multi-dimensional scaling (MDS) plots showed that the composition of “replicate” photo-image samples in each of the three regions with sufficient samples for analysis, i.e. the

Serpentine, Dawesville and Penguin Island, were distinct from each other and did not overlap

(Figure 3.16a). The separation of the two Peel-Harvey regions from each other was similar in

76 magnitude to that of each Peel-Harvey site from Penguin Island. The shade plot illustrates that the most significant contribution to H. caspia diet in the Serpentine was A. forsteri, followed by M. cephalus, S. schomburgkii and S. punctatus (Figure 3.16b). In Dawesville, P. octolineatus dominated the H. caspia diet while birds on Penguin Island most frequently consumed M. cephalus (Figure 3.16b).

(a)

Penguin Island

Dawesville Cut

Serpentine

(b)

Figure 3.16. Comparison of diets from bill-loaded images of H. caspia at two areas on Peel-Harvey (Serpentine and Dawesville) and Penguin Island (a) bootstrapped average nMDS ordination plots constructed showing contributions of main dietary categories from randomly-constructed prey samples using bill-loaded images (b) shade plots showing contributions of main dietary categories from randomly-constructed prey samples using bill-loaded images. 77

Commercial fisheries data

Ten species of teleost fish and one crustacean, the Blue Swimmer Crab (Portunus armatus) were recorded during this time (Table 3.13; Department of Primary Industries and

Regional Development, 2019). The commercial catch data showed that M. cephalus and P. armatus each comprised approximately 40.0% of the total catch, followed by S. schomburgkii with 9.3% and A. forsteri with 6.0% over the five-year period (Table 3.13). The P. armatus fishery had the highest fishing effort of 8.4 vessels per month, compared to the average of 4.7 vessels per month across all other species (Table 3.13). The total monthly catch, including

P. armatus, was highest in January and lowest in November (Figure 3.17a), noting that the estuary is closed to commercial crabbing in September and October. When P. armatus catches were excluded from the total monthly catches, the total catch was highest in September with over (800,000 kg), and lowest in May (~ 400,000 kg, Figure 3.17b). The proportion of M. cephalus in the total catch over the five-year period peaked in September, accounting for more than 600,000 kg (Figure 3.17). The proportion of S. schomburgkii was greatest between May and October while A. forsteri was greatest between November and April (Figure 3.17).

Table 3.13. Mean (± 1 SD) annual total catch (kg), the proportion of catch (%) and catch effort (mean vessels/month) for 11 commercially-caught species on Peel-Harvey Estuary over a five-year period (2013-2018) (data: Department of Primary Industries and Regional Development, 2019).

Species Mean total catch (kg) % Catch Mean vessels / month Mugil cephalus 420,416 (± 13,004) 40.0 7.8 Portunus armatus 414,193 (± 25,566) 39.4 8.4 Sillago schomburgkii 98,061 (± 6,701) 9.3 4.4 Aldrichetta forsteri 62,740 (± 4,490) 6.0 5.0 Pomatomus saltatrix 27,213 (± 4,959) 2.6 4.4 Arripis georgianus 14,959 (± 542) 1.4 4.1 Nematalosa vlaminghi 5,795 (± 709) 0.6 3.8 Cnidoglanis macrocephalus 3,911 (± 917) 0.4 3.5 Trevallies (Pseudocaranx spp.) 2,340 (± 255) 0.2 3.4 Whitings (Sillaginidae) 479 (± 214) 0.0 3.0 Acanthopagrus butcheri 62 (± 28) 0.0 3.5 Total 1,050,169 (± 25,367) 100.0

(a) Mugil cephalus 120000 Portunus armatus Sillago schomburgkii Aldrichetta forsteri 100000 Other

80000

60000 Catch (kg) Catch 40000

20000

0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Month (b) 90000 80000 70000 60000 50000 40000

Catch (kg) Catch 30000 20000 10000 0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Month

Figure 3.17. Accumulative monthly catch (kg) of (a) all commercially caught species, and (b) all fish species excluding Blue Swimmer Crab (Portunus armatus) over a five-year period between 2013-18 (data source: Department of Primary Industries and Regional Development, 2019).

3.4 Discussion

This study used tern counts, focal sampling, and dietary analysis of bill-loaded images and regurgitation pellets to investigate the abundance, distribution and foraging ecology of Caspian

Terns, Hydroprogne caspia, on the Peel-Harvey Estuary during five months of the non- breeding season (October 2018 to February 2019). Patterns in abundance and distribution across the system are described. Differences in their foraging activity between areas and time of day are examined, and spatial differences in the composition of prey species are also identified. A single overnight roosting site for H. caspia was identified on the Peel-Harvey

Estuary during this period, which is a significant finding for the monitoring and conservation of this population (see below).

The total numbers of terns and foragers, and the proportion of time spent foraging by terns differed with area of the Estuary, and the counts of foragers and proportion of time spent foraging also differed significantly with time of day. Overall, 16 fish species and one crustacean were recorded on the Estuary, the most common being whitings (Sillaginidae,

35.0%), mullets (Mugilidae, 33.9%) and Eight-lined Trumpeter (Pelates octolineatus, 14.4%;

Table 3.9). All the information gained from this study was collated to develop an understanding of the potential to use H. caspia as a biological indicator for ecological monitoring across the

Peel-Harvey Estuary and to develop a potential monitoring program based on H. caspia for this

Ramsar-listed site (Chapter 4; Appendix 4).

3.4.1. Abundance and distribution

The highest abundance of H. caspia was found across six main areas of the Peel-Harvey

Estuary. These sites are characterised by exposed sandy spits and large expanses of shallow water adjacent to the mouths of tributary rivers such as the Serpentine, Murray and Harvey; drains such as from Lake Mealup; and oceanic channels such as Mandurah Channel and

Dawesville Cut (Figure 3.3). Areas with higher abundance of H. caspia reflected areas with consistently high tern abundance throughout more intensive focal sampling. Similarly, the total numbers of H. caspia at the roost site followed a similar pattern of change to those summed across sites during the fortnightly estuary census. Any variation between these counts could be attributed to several factors. Initially, the duration of the census was longer (due to less familiarity of the observer in the area), and consequently, there was potential for birds moving between sites to be double counted. The range expansion of foraging H. caspia to nearby wetlands in January and February 2019 could account for reduced tern counts in the census but higher roost counts at night.

Studies on the abundance and distribution of H. caspia throughout the non-breeding period in other locations are difficult to find in the published literature. Therefore, direct comparisons with the results from the current study cannot be made. Despite the cosmopolitan distribution and increasing global population of H. caspia (Burger et al. 1996; Menkhorst et al.

2017; IUCN 2019), very few studies have investigated the abundance, distribution or foraging ecology of the species during the non-breeding periods. Most published studies of H. caspia are focussed on the foraging activity and energetic requirements of a large colony

(approximately 9,700 pairs) on the Columbia River Estuary, USA during the breeding season

(Roby et al. 2002; Antolos et al. 2004; Anderson et al. 2005; Lyons et al. 2005; Anderson et al.

2007; Lyons et al. 2007). Birds from this population, tracked using GPS tags, foraged further from their breeding colony as the breeding season progressed, travelling further for fish in the late chick-rearing period than the early chick-rearing period (Lyons et al. 2005). From these results, Lyons et al. (2006) suggested that H. caspia were generalist foragers, capitalising on proximate, abundant forage fish, especially whilst breeding. Recently, GPS technology have also been used to understand the habitat usage of H. caspia during their migration stopover on the Salton Sea, USA (Lyons et al. 2018). Both these areas support a high abundance of terns at

81 critical stages in their life history; as a breeding colony and migration stopover (Lyons et al.

2005; Lyons et al. 2018). Consequently, they are of high value for the conservation of this species, as are areas of the Peel-Harvey Estuary, Western Australia.

Foraging sites

Six main foraging areas were identified on the Peel-Harvey Estuary where most birds were observed foraging. All foraging areas were characterised by their close proximity to channels/drains/rivers and the presence of one or more sand spits upon which terns could loaf between foraging bouts. For example, H. caspia were frequently sighted in high numbers at the mouths of the Murray and Serpentine rivers with multiple, exposed sand spits at the mouth of tributaries and with consistently shallow waters, less than 1 m depth on average (Department of Transport 2006; Hale & Butcher 2007). In comparison, Boodalan Island, approximately

500 m from the mouth of the Murray River, was frequently submerged at higher tides and therefore, tern occupancy and abundance was more sporadic; restricted to periods of low tide

(Department of Transport 2006; pers. obs.).

Opportunistic observations of H. caspia showed that low numbers of birds occasionally moved along the adjacent coastline (i.e. Falcon Bay Beach). Although, no large aggregations of H. caspia or foraging events were observed at this location. In January and February of 2019,

H. caspia were observed on the network of wetlands and lakes (i.e. Lake McLarty and Lake

Goegrup) within the greater Peel-Yalgorup system – they were first sighted on Lake McLarty on 28 January 2019, and consistently in small numbers from then on. The appearance of terns at these lakes later in summer may be a result of the lower water levels in these wetlands following periods of high evaporation and little rainfall, which in turn exposes sand spits and concentrates forage fish in the reduced volume of water (pers. obs.).

Roost counts

A night roost site location was identified during this study which appears to be the area where all birds using the Peel-Harvey Estuary assembled during the evenings for much of the study. This appears to be the first report of a night roost for H. caspia during the non-breeding season. A maximum of 147 birds were recorded at the night roost in mid-February, matching estimates of the total number of adult birds at their Penguin Island breeding colony combined with an approximation for the number of fledged chicks (Dunlop & McNeill 2017). Tern numbers counted at the roost site may provide an insight into recruitment rates over time as chicks fledging from the colony on Penguin Island appear to forage with their parents on the

Estuary during the non-breeding season (pers. obs.).

Roost site counts probably provide a reliable population estimate of H. caspia on Peel-

Harvey Estuary, as no other night aggregations of birds were discovered within the area, and this number is consistent with the estimate of 60 pairs (120 birds) breeding on Penguin Island in 2017 and 2018 (Dunlop & McNeill 2017; pers. comm. J.N. Dunlop) combined with their chicks from that season (pers. obs.). The dramatic reduction in birds at the night roost site in late February could be due to a disturbance of the colony (e.g. a fishing event) or a natural response to a change in fish abundance or abiotic conditions. Although their new roost site was not discovered before the end of the study period, similar numbers of H. caspia were observed at regular foraging sites during the day. Therefore, the decline in night roost attendance did not appear to be reflective of a change in population abundance in the region. The capacity of H. caspia to shift night roost locations on the Peel-Harvey Estuary may be an important indicator of the species’ resilience.

The identification of the night roost site is very significant for the management, conservation and monitoring of H. caspia in the Peel-Harvey Estuary. The area can now be characterised and risks to the terns assessed. If they are considered significant, mitigation

83 strategies could be developed by the City of Mandurah in consultation with the Department of

Biodiversity, Conservation and Attractions, Peel Harvey Catchment Council and BirdLife

Australia.

Individual foraging patterns

Initially, attempts were made to follow individual terns i.e. a focal follow, to better understand their daily foraging patterns and energetic requirements. Following individual terns proved too difficult for collecting reliable data on individual foraging behaviour, mainly because H. caspia are both superficially indistinct and can move quickly over long distances within and between foraging sites. Many terns were observed moving between multiple foraging sites within a day. Additionally, H. caspia often forage in larger groups when prey is locally abundant and in association with other foraging marine predators such as dolphins.

Focal following of individuals could not be used under these conditions, especially when they foraged at locations further away from the observer. As most focal follow attempts were unsuccessful, this method of data collection was abandoned in favour of focal sampling.

Frequent resights of nine colour-banded individuals from research on the breeding colony of Penguin Island (refer to: J.N Dunlop, Conservation Council of Western Australia) provide some insight into individual foraging patterns. These observations show large variation between individual foraging patterns as some birds indicate a preference for specific forage sites. For example, one bird was sighted frequently at Wannanup spit and nowhere else, while two others were sighted on spits across foraging areas in the northern and southern reaches of the estuary (Figure 3.9). The most frequently-sighted tern was observed on sandspits throughout the Peel-Inlet but never on Harvey Estuary. This suggests that there could be some

‘forage site fidelity’ amongst individual H. caspia, whereby some birds make foraging decisions based on territoriality or learnt habitual behaviours (pers. obs.). No other studies of

H. caspia populations from other parts of the world were found that document variation

84 between individual foraging patterns or interactions between birds within a population.

However, social-learning is thought to play a critical role in maximising feeding efficiency and the identification of productive foraging sites among gregarious birds such as terns (Turner

1964; Emlen & Demong 1975).

GPS tracking studies of H. caspia would be very valuable for gaining more detailed knowledge of its individual foraging patterns and energetic requirements (Brisson-Curadeau et al. 2017). This approach provides useful information on seabird foraging ecology that might otherwise be largely inaccessible (Fijn et al. 2017) and in doing so, enhance conservation of seabirds and management of their ecosystem (Montevecchi et al. 2012). GPS trackers were used to uncover the foraging ecology of breeding Sandwich Terns (Thalasseus sandvicensis) in Scheelhoek Nature Reserve, the Netherlands. A total of 34 individuals were followed, representing 0.1-2% of the estimated colony size in the nature reserve (1500-3000 birds; Fijn et al. 2017). The authors concluded that combining observation with GPS technology could provide a near-complete insight into the foraging ecology of terns throughout their breeding season (Fijn et al. 2017). Trackers provided information on home range and foraging range, trip duration, and time-activity budgets, which offered insight into food availability, chick ages, and environmental conditions (Fijn et al. 2017). Another study tracked 29 Brown Skuas

(Stercorarius antarcticus lonnbergi) from their breeding colony on the Shetland Islands to their foraging grounds in this region (Carneiro et al. 2015). They found high variability in foraging patterns that were uncorrelated with sexual dimorphism or breeding success (Carneiro et al.

2015). Foraging ecology can vary between individual birds based on differences in sex, age, breeding stage and other factors such as dominance, and GPS tracking can provide insight into these patterns at individual and population-levels (Carneiro et al. 2015).

Re-sightings of colour-banded birds coupled with known differences in H. caspia diet, based on foraging area, suggest there is considerable variation in the foraging ecology of

85 individual H. caspia on the Peel-Harvey Estuary. GPS-tracking could be used to fill a remaining knowledge gap identified by this study and uncover the diversity in individual foraging patterns. In addition, the relatively small population of terns (~ 150 birds) using the

Peel-Harvey means a higher proportion of birds could be fitted with trackers. For example, if a similar number of terns to Fijn et al. 2017 (34 birds) were GPS-tracked, this would represent

~20 to 25% of the H. caspia known to use Peel-Harvey Estuary, compared to 0.1-2% of

T. sandvicensis. Even a small sample of GPS-tagged H. caspia (e.g. 5-15 individuals would represent approximately 3-10% of the birds using the Estuary) would enhance our knowledge of H. caspia foraging ecology across the Peel-Harvey Estuary. However, GPS-tracking technology can be expensive, especially if the recovery rates of trackers are low and the results from a small sample of birds may not represent patterns in the foraging ecology of birds at a population-level.

3.4.2 Foraging activity

Studies of H. caspia foraging activity throughout non-breeding periods in other locations are difficult to find in the published literature. Therefore, direct comparisons with the results from the current study cannot be made. Focal sampling from this study revealed significant variation in the counts of total terns and foragers, as well as the proportion of time spent foraging across six main foraging areas of the Peel-Harvey Estuary. Similar to the mean number of terns, Mealup Drain had the greatest mean number of foraging terns, while

Dawesville had the lowest mean value between October 2018 and February 2019. The highest mean proportion of time spent foraging was in Serpentine while Mandurah Channel recorded the lowest proportion of foraging time throughout the study period. Additionally, H. caspia foraging activity varied significantly with time of day, with the mean values of both forager counts and time spent foraging higher in the morning than at other times.

Preliminary correlation analysis of data from the whole estuary found that tidal height did not have a significant influence over these results while the influence of wind speed accounted for approximately 5% of the total tern counts and time spent foraging. Further analyses of the environmental data, taking into account each area in the Peel-Harvey Estuary, using Generalised Liner Models would be valuable to better understand whether tide height and wind speed influence tern numbers and foraging time. Other factors may also be important in influencing H. caspia foraging activity on Peel-Harvey Estuary such as chlorophyll-a.

Chlorophyll-a can be useful as an indicator of productivity and conditions for young fish within marine and estuarine ecosystems (Henson et al. 2010). Peaks in chlorophyll-a on the Peel-

Harvey Estuary coincided with the end of the tern’s annual breeding season in August (Dunlop

& McNeill 2017).

Estuaries are productive environments, which create ideal conditions for rapid growth of fish species (Lenanton et al. 1984). Marine fish species, such as A. forsteri, M. cephalus,

P. octolineatus and S. schomburgkii enter the Peel-Harvey Estuary at various time periods to coincide with important foraging and breeding times (Potter, Loneragan, et al. 1983). Many of these marine species are more abundant in the Estuary in November or December (Potter,

Loneragan, et al. 1983). In contrast, P. octolineatus enter the Estuary as young fish where they can remain for 15 months, migrating away from the banks as they increase in size (Potter,

Loneragan, et al. 1983). Estuarine species such as Cnidoglanis macrocephalus are resident year-round (Potter, Loneragan, et al. 1983; Nel et al. 1985) providing a reliable food source year-round for piscivorous predators such as H. caspia. Both mullet species, A. forsteri and

M. cephalus enter estuaries at very small sizes and remain in them for several years before returning to the sea to spawn (Chubb et al. 1981; Lenanton et al. 1984). These species, and estuarine species like C. macrocephalus, grow rapidly in the Peel-Harvey Estuary, reaching an adult length within two years (Lenanton et al. 1984). Specifically, M. cephalus can attain this

87 length within one year and consequently, the M. cephalus composition on Peel-Harvey represents fish of two or more age classes (Lenanton et al. 1984). Based on the mean length of forage fish caught by H. caspia, the birds appear to target one-year-old fish in the transitional areas between shallow and deep water.

Other studies of fish abundance and distribution across Peel-Harvey Estuary show some similarity between diet composition of H. caspia across their six main foraging areas. Marine species such as P. octolineatus were frequently caught in fish studies at Dawesville and comprised a significant proportion of forage fish caught by H. caspia in this area (Loneragan et al. 1986; Loneragan et al. 1987; Potter et al. 2016). Similarly A. forsteri and S. schomburgkii have been found to penetrate throughout the Estuary and its tributaries, and comprised a significant proportion of the H. caspia diet in both the Murray and Serpentine areas (Loneragan et al. 1986; Loneragan et al. 1987; Potter et al. 2016).

Commercial fisheries catch and effort data from a more recent five-year period (between

2013 and 2017 inclusive) indicated that Sea Mullet (Mugil cephalus) was caught year-round, with peak catches in September and October, coinciding with end of the terns annual breeding season (Dunlop & McNeill 2017). The proportion of M. cephalus taken by H. caspia followed a similar trend, comprising 47.8 and 53.3% of all prey species caught in October and November

2018. Commercial fisheries data also show that the catch of Yellow-eye Mullet, Aldrichetta forsteri, was greatest between November and April, while the catches of Yellow-fin Whiting,

Sillago schomburgkii, were greatest between May and October. These trends were not mirrored in the proportion of prey species taken by H. caspia. Although, samples were not collected between March and September, which could account for this disparity. All three species are both commercially significant for estuarine fisheries and ecologically significant as important forage fish for H. caspia. Their prevalence within the Peel Harvey Estuary provides a reliable food source for H. caspia and year-round.

3.4.3 Diet

Of the 21 prey taxa recorded on the Peel-Harvey Estuary and at the Penguin Island breeding colony between October 2018 and February 2019, 16 fish species and one crustacean were recorded on the Estuary only using bill-loaded images and otoliths in regurgitation pellets

(Table 3.9). Most prey items were between 117 and 195 mm in length or 1 ½ to 2 ½ bill-lengths long. Overall, the most common prey species were whitings (Sillaginidae, 35.0%), mullets

(Mugilidae, 33.9%) and Eight-lined Trumpeter (Pelates octolineatus, 14.4%; Table 3.9).

Interestingly, the results of dietary composition from otoliths in regurgitation pellets reflected the main prey species identified from bill-loaded images. This suggests that both methods could be used to capture accurate data on H. caspia diet, although, less resolution of prey items was captured using pellet analysis.

The relative prey abundance from images varied temporally between months as well as spatially between foraging areas. Ordination and shade plots using bootstrapped average nMDS of the photo-images clearly identified distinct prey compositions between foraging sites within the Peel-Harvey Estuary (Serpentine and Dawesville) and the Penguin Island breeding site

(Dunlop & McNeill 2017). Variation in individual foraging patterns (observed from re- sightings of colour-banded birds) could be linked to this distinction between prey taken from various foraging sites. Alternatively, forage-site fidelity in some birds or territorial behaviour observed in others could also influence these foraging patterns (Appendix 3).

This study is the first in which the diet of H. caspia was investigated throughout the non- breeding season. Hydroprogne caspia were previously perceived to be generally opportunistic, taking the most abundant medium-sized benthic forage fish throughout the year (Serventy et al. 1971; Dunlop & McNeill 2017). In the present study, the diet of H. caspia on Peel-Harvey

Estuary was dominated by several abundant species of small- to medium-sized benthic forage fish recorded in the Estuary (Potter, Loneragan, et al. 1983; Lenanton et al. 1985; Loneragan

89 et al. 1986; Loneragan et al. 1987; Potter et al. 2016) where birds appeared to exercise a preference, selecting whitings (Sillaginidae), mullets (Mugilidae) and Striped Trumpeter

(Pelates octolineatus) over other prevalent species. Re-sightings of colour-banded terns in this study suggest birds may exhibit preference for specific species or target different forage fish species in different foraging areas, in accordance with optimal foraging theory which suggests that predators select prey to maximise their fitness and optimise their net energy intake (Figure

3.12; Hughes 1980). Additionally, based on the average length of forage fish, foraging terns appear to be targeting larger fishes. Again, this matches the ideologies of optimal foraging theory, which state that prey selection is based on a balance between net energy expenditure in the foraging process and nutritional gain from successful capture and consumption of prey

(Hughes 1980; Greenwell 2017).

This study found significant differences in the diet of H. caspia in the Peel-Harvey Estuary

(non-breeding site) compared to Penguin Island (breeding site), 30 km north of the Estuary mouth from the non-breeding to the breeding season. Although a greater diversity of fish were recorded in images from the Peel-Harvey Estuary (16 forage fish and one crustacean compared to 13 forage fish species recorded on Penguin Island; Table 3.9; Dunlop & McNeill 2017), more images were recorded in the Peel-Harvey Estuary and more photographs from Penguin

Island would be invaluable for understanding the diet during the breeding season in greater detail. Dunlop & McNeil (2017) studied the diet of birds in this population during the breeding seasons of 2012, 2013 and 2016 using similar methodologies. The relative contribution of prey species differed between breeding (Penguin Island) and non-breeding sites (Peel-Harvey

Estuary) although the size of each prey species taken by H. caspia was similar at these two locations (Dunlop & McNeill 2017). Sea Mullet (M. cephalus) and Perth Herring (Nematalosa vlaminghi) were the most frequently caught species, comprising 49.6 and 12.6 % of their diet, respectively, on Penguin Island (Dunlop & McNeill 2017). In contrast, M. cephalus comprised

90 a much smaller proportion of H. caspia’s diet on Peel-Harvey Estuary and N. vlaminghi was not recorded as a prey item there. Despite this, there was significant overlap in most species comprising H. caspia diet at their breeding and non-breeding sites, with forage fish such as A. forsteri, P. octolineatus, S. schomburgkii, and S. punctatus as well as M. cephalus recorded frequently at both Peel-Harvey Estuary and Penguin Island (Dunlop & McNeill 2017). Several of these forage fish species taken by terns (e.g., A. forsteri, M. cephalus, and S. schomburgkii) are also commercially- and recreationally-significant species, especially on Peel-Harvey

Estuary (Department of Primary Industries and Regional Development, 2019). When testing tail feather samples, Dunlop & McNeill (2017) found that one third of adult birds at the breeding site (most birds tested) had elevated levels of methyl-mercury, ranging between 0.9 and 5.9 mg/kg (mean 2.27 mg/kg, ± 1.44) but the source of this contamination was unknown.

The results from this dietary analysis have identified species of fish that merit further investigation of the prevalence of mercury contamination in the Peel-Harvey where this population spend approximately 7 months of each year.

3.4.4 Energetic requirements of non-breeding terns

The daily energetic requirement of adult H. caspia during the non-breeding season were estimated with an online calculator (https://ruthedunn.shinyapps.io/seabird_fmr_calculator/;

2018) developed by Dunn et al. to estimate field metabolic rates in the breeding season, using the latitude of the Peel-Harvey Estuary and the average size of adult birds as input data.

Empirical estimates of another seabird, the Great Cormorant, were used to gain an understanding of the possible difference in metabolism between the breeding and non-breeding periods (Gremillet et al. 2003). The input parameters for H. caspia included a colony latitude of 32°S and an average bird mass of 747.83 g, based on measurements weights of H. caspia recorded whilst banding individuals from Penguin Island (Table 3.14; J.N. Dunlop,

Conservation Council WA, unpublished data). Estimates were generated for the south-western

Australian H. caspia population at three breeding stages; “incubation,” “brood” and “creche.”

The daily energetic requirements of adult H. caspia on the Peel-Harvey Estuary, during three key phases of their breeding season, were estimated at 738.9 kJ day-1, 794.3 kJ day-1 and 984.1 kJ day-1 for the incubation, brood and creche phases, respectively (Table 3.14; Dunn et al.

2018).

Table 3.14. Input values used in energetic estimate calculations (Gremillet et al. 2003; Dunn et al. 2018) and calculated values (bolded). Caspian Tern Great Cormorant

Mean mass (g) 747.8 3,200 Colony Latitude (o) 32 56 Energetic Estimates Dunn et al. 2018 Dunn et al. 2018 Gremillet et al. 2003 Non-breeding (kJ day-1) 945.3 1,719 3,582 Incubation (kJ day-1) 738.9 1,419 2,800 Brood (small chick; kJ day-1) 794.3 1,685 3,500 Creche (large chick; kJ day-1) 984.1 1,685 5,500

The estimates from a study of Great Cormorant (Phalacrocorax carbo) at Loch Levan,

Scotland during the non-breeding season were used to gain an understanding of the potential difference in energetic requirements between the breeding and non-breeding season and between empirical estimates and those from Dunn et al. (2018). The daily energetic requirements of P. carbo were estimated using a combination of radio-tracking behavioural data of free-ranging birds, metabolic measurements of captive birds, and published data

(Gremillet et al. 2003). This approach gave estimates of 3,582 kJ day-1 during the non-breeding season compared with 2,800 (incubation) to 5,500 kJ day-1 (crèche) during the breeding season

(Table 3.14), all much higher during the breeding season than those obtained from Dunn et al.

(2018) (Table 3.14). The reason for this discrepancy is not known. However, if H. caspia follows a similar pattern of metabolism to P. carbo between non-breeding and breeding phases,

92 the non-breeding metabolism would be ~28% higher than during incubation - ~ 945.3 kJ day-

1. In view of the large disparity (up to ~50%) between the estimates for Great Cormorants between methods, further research on H. caspia field metabolic rates is needed.

Fish species have different nutritional values based on their mass and calorific content.

The mean energy value per fish has been determined for a number of species in the Leschenault

Estuary, approximately 80 km south of the Peel-Harvey system (Table 3.15; McCluskey et al.

2016). Species such as P. octolineatus, whiting species and A. forsteri have high nutritional values of 327.0, 317 & 288 kJ/fish respectively (Table 3.15; McCluskey et al. 2016). To meet their daily energy requirements, H. caspia could take 2.89 P. octolineatus, 2.98 whiting species or 3.27 A. forsteri per day, or any other combination of these prey species. McCluskey et al.

(2016) recorded M. cephalus on the Leschenault Estuary as having a smaller mean size than fish selected by foraging H. caspia on Peel-Harvey Estuary and consequently calculated a lower calorific content (81.3 kJ/fish; Table 3.15; McCluskey et al. 2016). The nutritional value of M. cephalus is likely to be closer to that of A. forsteri for the size of Sea Mullet taken by H. caspia on the Peel-Harvey.

Table 3.15. Summary of mean mass (g), mean energy value by fish weight (kJg-1) and mean energy value (kJ) or nutritional content of some H. caspia prey species, using data from McCluskey et al. 2016. Mean energy value Mean energy value Species Mean wet mass (g) by weight (kJg-1) (kJ/fish) Arripis georgianus 58.03 6.62 384.55 Aldrichetta forsteri 62.60 4.58 288.33 Mugil cephalus 15.04 5.30 81.34 Sillago bassensis 48.82 5.88 315.84 Sillaginodes punctatus 65.09 4.90 316.77 Sillago schomburgkii 57.62 5.60 311.27 Pelates octolineatus 31.51 12.83 326.97 Portunus armatus 129.73 2.63 854.38

3.4.5 Conclusion

This study investigated patterns in abundance, distribution and foraging ecology, and dietary composition of H. caspia on the Peel-Harvey Estuary throughout their non-breeding

93 season. It found that most H. caspia within this population in south-western Australia spend at least five months of the non-breeding season on Peel-Harvey Estuary, where they foraged across six main areas. It also identified one location where all birds appeared to roost. This has significant conservation implications as the threats to Caspian Terns at the night roost can be evaluated and management measures implemented to reduce any threats to the birds. At a population-level, tern-based indices of foraging (i.e., number of foragers and time spent foraging) varied between these sites over time, suggesting there were environmental cues that influence H. caspia foraging activity. Neither wind speed nor tide height explained the variation in tern foraging activity. Instead, spatial and temporal variation in forage fish availability is more likely to be a driving factor in H. caspia foraging patterns. If the daily energetic requirements of H. caspia on the Estuary throughout the non-breeding season is estimated at 945.3 kJ day-1 which could be attained by catching and consuming approximately

3 forage fish species on average each day. The results of this study have offered a unique insight into the foraging ecology of a ubiquitous coastal seabird, using multiple, repeatable methods and in doing so, has filled an important knowledge gap in understanding the distribution, abundance, foraging ecology and diet of H. caspia in south-western Australia. Further studies are required to explore patterns in H. caspia foraging ecology in the second half of the non- breeding season as well as the link between mercury contamination and H. caspia foraging on

Peel-Harvey Estuary. The results from the dietary analyses have identified species of fish for further investigating the prevalence of mercury contamination in the Peel-Harvey.

Additionally, the study has facilitated the development of a potential monitoring plan based on

H. caspia to contribute towards the conservation and ongoing management of both the birds and this Ramsar-listed site (Chapter 4).

Chapter 4. Conclusions and recommendations

4.1. Conclusions

This study on the patterns of distribution and abundance, and foraging ecology of Caspian

Terns (Hydroprogne caspia) on the Peel-Harvey Estuary, south-western Australia demonstrated that H. caspia utilise the estuary during at least five months of the non-breeding season, which spans about 75% of the year. It also identified an area at Creery Wetlands

(Figure 3.1) where all terns in the region appear to gather at night (night roost), indicating great potential for being able to census the population on a regular basis. The number of birds counted at the night roost increased with time since the end of the breeding season (October) to a maximum of 147 terns five months later in early February. While large colonies with thousands of breeding H. caspia pairs are found in other parts of the world, e.g. the Columbia

River Estuary, the United States, most populations in south-western Australia typically comprise two or three pairs only (Lyons et al. 2005; Dunlop & McNeill 2017). Consequently, counts at this night roost represent a significant aggregation of H. caspia in this area and are, possibly, close to a population estimate of adult birds that breed on Penguin Island, Shoalwater

Bay, their surviving young of the year and immature birds.

This night roost location is close to the centre of the City of Mandurah, and consequently there are an increased set of risks to H. caspia including human disturbance (especially from fishing and recreational activities nearby on the Estuary), feral predation by Cats (Felis catus),

European Foxes (Vulpes vulpes) and Black Rats (Rattus rattus) as well as habitat loss due to urbanisation, pollution or development on the Estuary. The night roost location for H. caspia is shared by other species of waterbird and consequently, this is an area of conservation significance. Management to protect this area and others of significance for H. caspia, such as the alternative location used by terns following their disappearance from Creery Wetlands on

22 February 2019, should be a priority for the conservation of H. caspia within this region.

Tern foraging activity varied temporally and spatially between six main foraging areas identified across the Peel-Harvey Estuary, and their breeding colony on Penguin Island between October 2018 and February 2019. The terns forage over expansive areas, taking mostly whiting species (Sillaginidae), mullet species (Mugilidae) and Eight-lined Trumpeter

(Pelates octolineatus) throughout this period. In accordance with optimal foraging theory, it is likely that H. caspia exhibits a preference for specific prey species, when available, rather than targeting the most available fish in the Estuary. In doing so, they appear to target specific forage fish in different foraging areas as the diet of birds on the western Peel was dominated by different species (P. octolineatus) compared with that on the eastern Peel Inlet at the mouth of the Serpentine River (mullets and whiting). This study also found that the diet of H. caspia differed significantly between the Peel-Harvey Estuary in the non-breeding season and Penguin

Island during the breeding season (Dunlop & McNeill 2017). The major differences were in the marine reef-associated fish species that were found as prey of H. caspia at Penguin Island that were not present in estuary birds.

This study successfully developed and implemented a range of repeatable, low-impact sampling methods suitable for monitoring the foraging ecology of H. caspia. These methods require minimal equipment and thus, are of low cost, they are easily replicated and have the potential to be used in a citizen science monitoring program. Such a program would be enhanced by the establishment of a network to link researchers, interested community members and managers, like the Fairy Tern (Sternula nereis nereis) networks

(http://www.ccwa.org.au/fairyterns). This network has over 200 citizen science members within south-western Australia and has made a significant contribution to S. nereis nereis research, monitoring, and conservation of terns utilising the region.

The current study also establishes a comprehensive insight into H. caspia foraging activity and diet over the first five months of the non-breeding season (between October 2018

96 and February 2019), which can act as a baseline for comparison in future years. Over time, an abridged methodology could be used to monitor changes in diet and foraging grounds. For example, parameters, such as the diversity, abundance, and location of prey species taken by

H. caspia can be indicative of ecosystem productivity, habitat quality, trophic structure, or pollutant or nutrient imbalances amongst other factors. Over time, these relationships and patterns can be fine-tuned to provide more direct correlations between tern-based indices (i.e., counts of terns, foragers, and time spent foraging) and other factors of ecosystem condition.

Consequently, long-term observations could reflect shifts in ecosystem health and productivity and help to distinguish between natural or seasonal variatio and the effects of disturbance or pollution. As piscivorous meso-predators, seabirds are currently used to indicate a range of metrics of ecosystem health including localised forage fish availability (Sydeman, Piatt, et al.

2017; Piatt et al. 2018), plastic pollution (Donnelly-Greenan et al. 2014), heavy metal contamination (Furness & Camphuysen 1997; Bond & Diamond 2009) as well as broader-scale changes in climate (Mallory et al. 2010; Boyd et al. 2014) and fisheries productivity (Einoder

2009).

This study has filled a knowledge gap by uncovering new information on the foraging ecology of H. caspia in the Peel-Harvey Estuary at a population-scale during the non-breeding season. This facilitates the establishment of a monitoring program to look at the change in tern abundance, distribution and foraging activity over time (directly) as well as developing their use as effective indicators of ecosystem condition and other primary abiotic components as well as habitat quality, forage fish availability, pollution, and contamination (indirectly).

4.2. Recommendations: the use of Caspian Terns as bio-indicators on the Ramsar-listed

Peel-Harvey Estuary, south-western Australia

4.2.1 Caspian Terns as bio-indicators on Peel-Harvey Estuary

Caspian Terns (Hydroprogne caspia) embody several life-history and behavioural traits that make them ideal candidates for use as bio-indicators of their ecosystem health. Firstly, they are the largest tern species worldwide at 54 cm tall (mean mass ~ 750 g), and are active during the day across coastal and estuarine ecosystems worldwide, with a unique appearance and call (Serventy et al. 1971; Burger et al. 1996). This makes them easy to identify and accessible for regular observations in near-shore environments. Secondly, like other seabirds, they are top, piscivorous predators and, consequently, provide an insight into the composition of lower trophic levels and condition of their ecosystem (Cairns 1988; Einoder 2009; Mallory et al. 2010). Thirdly, they have high nest site fidelity and return annually to previously occupied breeding colonies, often in coastal and estuarine environments (Burger et al. 1996; Lyons et al.

2005) providing opportunities for regular monitoring of these marine birds in a terrestrial environment. The results of the current study and previous observations of Dunlop and McNeill

(2017) also demonstrate that H. caspia show strong fidelity to returning to the Peel-Harvey

Estuary each non-breeding season.

The Peel-Yalgorup Ramsar wetlands have traditionally been monitored using a hierarchical framework for setting limits of acceptable change in ecological parameters

(Table 4.1; Hale and Butcher, 2007). Abiotic components such as water quality (salinity, nutrients, pH, etc.) and hydrology (groundwater, flows, etc.) are primary determinants of ecological character and health, with the primary response to these components manifesting in habitats and supporting biological communities such as phytoplankton and invertebrates (Hale

& Butcher 2007; Hale 2008). Target species and communities such as thrombolites, fish

98 assemblages, and waterbird populations are dependent upon the abiotic and habitat components, and limits of acceptable change in these components are determined from monitoring target species and communities (Hale 2008). Existing monitoring frameworks for the Estuary correlate values within these limits of acceptable change to indicate ecosystem health (Hale 2008).

Long-term monitoring of waterbird populations on wetlands is inherently challenging because of the natural fluctuation in numbers as birds move from area to area for feeding, breeding, and roosting purposes (Hale 2008). In addition, the size and diversity of the Peel-

Yalgorup system delivers an additional challenge (Hale 2008). As such, the use of target species and a strategic program to monitor feeding, breeding and roosting activities is ideal to represent the broader context of waterbird activity on the Peel-Yalgorup system. Historically, two cormorant species (Pied Cormorants, Phalacrocorax varius and Little Black Cormorants,

Phalacrocorax sulcirostris) breeding at Carrabungup (Robert Bay Swamp), were selected as a target species for waterbird monitoring (Hale 2008). However, large parts of their life history and population structure in this region remain unknown (Hale 2008). The results from this study suggest that H. caspia would be an ideal target species for waterbird monitoring on Peel-

Yalgorup as they rely upon key services provided by the Ramsar system: they appear to forage and roost on the Peel-Harvey Estuary for much of their non-breeding season (at least seven months) and feed on fish using the estuary that are of commercial and recreational significance.

Recent research has shown that H. caspia can be used to indicate the presence or absence of heavy metals such as mercury in forage fish (Dunlop & McNeill 2017). Further research could facilitate their use as indicators of bio-accumulation of heavy metals in their main forage fish species and ecosystem. By extension, H. caspia could be used to quantify chemical contamination, the presence of microplastics and other pollutants (Burger & Gochfeld

2004; Mallory et al. 2010). Although the preliminary results from Chapter 3 found that H.

99 caspia foraging activity was not significantly influenced by abiotic factors such as tide height and wind speed, they require further investigation. Hydroprogne caspia foraging activity could be linked to forage fish availability, and, if so, patterns in H. caspia foraging activity could be used to indicate the abundance and distribution of forage fish across the Peel-Yalgorup system

(Einoder 2009). Further research to investigate these links and long-term monitoring of

H. caspia would help confirm the significance of these relationships, as well as to compare these values to baseline levels of H. caspia foraging activity across the Estuary generated from this study. With this information, limits of acceptable change in H. caspia foraging activity that reflect forage fish availability could be used to enhance ecosystem and fisheries management at Ramsar site 482.

Logistically, the population of H. caspia on the Peel-Yalgorup system present a unique opportunity for use as indicators of estuary condition, and as subjects for an ongoing monitoring program. Both the breeding colony (Penguin Island, Shoalwater Bay) and non- breeding season foraging grounds (Peel-Harvey Estuary) are readily accessible for regular monitoring. The population size of approximately 150 birds (including ~ 60 breeding pairs) is large enough to reveal patterns in their life history and group behaviour and to buffer against individual variation or anomalies. Owing to its ecological and cultural significance, as well as its proximity to the City of Mandurah, the Peel-Harvey Estuary has an ongoing history of science, monitoring and community engagement through a number of different organisations including the Peel-Harvey Catchment Council, City of Mandurah, state universities, and government agencies. Several bird watching and citizen science groups are already established in the area (e.g., Mandurah Bird Observation Group and Peel Birds branch of BirdLife

Australia), and photographs and opportunistic observations of H. caspia could be used for ongoing estuary monitoring. A network similar to that established for Fairy Terns, Sternula nereis nereis could promote information flow between groups and the involvement of people

100 in research through submitting photos of Caspian Terns and their prey (Dunlop 2018) to enhance the awareness and increase stewardship of the broader Peel-Harvey Estuary.

4.2.2 Proposed monitoring program

The key ecological characteristics of the Ramsar site and their respective limits of acceptable change in Monitoring and Evaluation Guide for the Peel-Yalgorup Ramsar Site

(Hale & Butcher 2007; Hale 2008) provide a foundation for the development of this monitoring program. Currently, there are four waterbird metrics outlined in the monitoring plan (Hale

2008), and H. caspia could be a valuable addition as “Waterbirds E: Caspian Terns” (Appendix

4). The ecological characteristics of the Estuary that could be monitored using H. caspia are high diversity and abundance of waterbirds, important source of food, spawning, migration route and habitat for fish, high water quality and low levels of pollution (Table 4.1).

Table 4.1. Ecological characteristics of the Peel-Harvey Ramsar wetlands (Ramsar site 482) identified for monitoring, limits of acceptable change, and possible use of Caspian Terns, Hydroprogne caspia, to monitor performance of the ecological characteristic. Limits of acceptable change are shown when guidelines are available.

Ecological characteristic Proposed Limit of Application (H. caspia) Monitoring Parameter of RAMSAR site 482 Acceptable Change The largest H. caspia Roost counts of H. caspia population in south- High diversity and on the Estuary can show western Australia spend abundance of waterbirds recruitment and change in their non-breeding season numbers over time. on site 482. H. caspia catch medium- Identification of forage size, benthic forage fish: fish from bill-loaded whitings (Sillaginidae), H. caspia images. Images

Important source of food, mullets (Mugilidae) and taken at main foraging spawning, migration route Striped Trumpeter (P. areas and submitted by the and habitat for fish octolineatus) community. H. caspia forage in areas Abridged Estuary Census with high abundance of to monitor foraging forage fish activity by area over time. H. caspia feathers show Heavy metals and other mercury concentrations Mercury threshold 5 Aim for high water quality contaminant 0.9-5.9 mgkg-1 (mean 2.27 mg.kg-1 (Burger & and low levels of pollution concentrations can be mgkg-1; Dunlop and Gochfeld 2004) detected in feathers McNeill, 2017)

101

The overarching aim of this monitoring program is to develop the use of H. caspia as a bio- indicator of the Peel-Harvey Estuary by identifying changes in tern counts, foraging activity and diet, over time, to indicate ecosystem condition. The program seeks to contribute towards setting thresholds for limits of acceptable change (LACs) in H. caspia parameters associated with ecosystem condition on the estuary.

The objectives for the “Waterbirds E: Caspian Terns” monitoring program are:

• to understand how changes in tern counts (between October and December) may

reflect recruitment, and indicate health and suitability of the Estuary for foraging

H. caspia;

• to understand how fluctuation in forage-fish availability affect H. caspia foraging

activity across the Estuary; and

• to understand long-term dietary trends of H. caspia using bill-loaded images of

forage fish.

Regular monitoring over a two-day period would take place on a monthly basis involving two key components to determine spatial and temporal patterns in H. caspia abundance, distribution, and foraging activity. This includes counts at the night roost and an estuary census across six sites (Appendix 4). In the nine-week period between mid-October to mid-December, an additional dietary study using digiscoping across all six foraging areas would be used to uncover the composition of prey species across the Estuary (Appendix 4).

Opportunistic observations and bill-loaded images submitted by community members as part of a citizen science network would also be collated and any prey species identified to contribute to the monitoring plan.

Visual counts of terns and their foraging activity should be undertaken by a trained bird-observers (to limit observer bias), and photographs of bill-loaded birds by trained digiscopers or community-submitted images. All records of tern counts, foraging activity, and

102 bill-loaded image data should be analysed and interpreted to determine trends over time and inform limits of acceptable change.

Data collated should be stored in a dedicated Peel-Yalgorup Ramsar Site Waterbird

Database (similar to that described in Waterbird Program D, Hale 2008), managed by an overseeing body such as Peel-Harvey Catchment Council (PHCC), Conservation Council of

Western Australia (CCWA) or a newly established group for this purpose. In addition, data should be forwarded to Birdlife Australia and the Department of Biodiversity, Conservation and Attractions for inclusion in their databases. When one of the LAC indicators is exceeded, a management process should be triggered, and relevant technical experts on the Peel-Yalgorup

Technical Advisory Panel consulted where necessary. An annual report describing the results of the monitoring program, against LAC and describing trends should be produced and made available to all stakeholders and the wider community. In addition to the details of a potential monitoring program, estimated costs have been shown in Appendix 4. This monitoring is of medium to high priority in developing H. caspia as a bio-indicator to contribute towards conservation and management of the Ramsar site 482.

103

References

Anderson SK, Roby DD, Lyons DE, Collis K. 2005. Factors affecting chick provisioning by Caspian Terns nesting in the Columbia River Estuary. Waterbirds. 28:95–105. Anderson SK, Roby DD, Lyons DE, Collis K. 2007. Relationship of Caspian Tern foraging ecology to nesting success in the Columbia River Estuary, Oregon, USA. Estuarine, Coastal and Shelf Science. 73:447–456. Antolos M, Roby DD, Collis K. 2004. Breeding ecology of Caspian Terns at colonies on the Columbia plateau. Northwest Science. 78:303–312. Ashmole NP. 1971. Seabird ecology and the marine environment. In: Farner DS, King JR, editors. Avian Biology. 1st ed. New York: Academic Press; p. 223–286. Ashmole NP, Ashmole MJ. 1967. Comparative feeding ecology of seabirds of a tropical oceanic island. 24th ed. New Haven Connecticut: Peabody Museum of Natural History, Yale University. Australian Bureau of Statistics 2018. City of Mandurah: Population. [cited 2018 Apr 17]:1. Available from: https://economy.id.com.au/mandurah/population Balance LT, Ainley DG, Hunt GL. 2008. Seabird Foraging Ecology. In: Steele J., Thorpe SA, Turekian KK, editors. Encyclopedia of Ocean Science. 2nd ed. [place unknown]: Elsevier Ltd.; p. 2636–2644. Baltz, D.M. & Morejohn, G.V. 1977. Food habits and niche overlap of seabirds wintering on Monterey Bay, California. The Auk. 94:526-543. Barrett RT, Camphuysen K, Anker-Nilssen T, Chardine JW, Furness RW, Garthe S, Hüppop O, Leopold MF, Montevecchi WA, Veit RR. 2007. Diet studies of seabirds: A review and recommendations. ICES Journal of Marine Science. 64:1675-1691. Berg MP, Kiers TE, Driessen G, Heijden MVD, Kooi BW, Kuenen F, Liefting M, Verhoef HA, Ellers J, Berg MP, et al. 2010. Adapt or disperse: understanding species persistence in a changing world. Global Change Biology. 16:587-598. Bond AL, Diamond AW. 2009. Mercury concentrations in seabird tissues from Machias Seal Island, New Brunswick, Canada. Science of the Total Environment. 407:4340-4347. Bornatowski H, Angelini R, Coll M, Barreto RRP, Amorim AF. 2018. Ecological role and historical trends of large pelagic predators in a subtropical marine ecosystem of the South Atlantic. Reviews in Fish Biology and Fisheries. 28:241-259. Boyd C, Punt AE, Weimerskirch H, Bertrand S. 2014. Movement models provide insights into variation in the foraging effort of central place foragers. Ecological Modelling. 286:13-25. Bradshaw CJA, Hindell MA, Sumner MD, Michael KJ. 2004. Loyalty pays: Potential life history consequences of fidelity to marine foraging regions by southern elephant seals. Animal Behaviour. 68:1349-1360. Brisson-Curadeau E, Patterson A, Whelan S, Lazarus T, Elliott KH. 2017. Tracking Cairns: Biologging Improves the Use of Seabirds as Sentinels of the Sea. Frontiers in Marine Science. 4:1-7 Brooke M. 2004. The food consumption of the world’s seabirds. Proceedings of the Royal Society of London. Series B: Biological Sciences. 271:246-248. Burger J. 2008. Social Attraction in Nesting Least Terns: Effects of Numbers, Spacing, and Pair Bonds. The Condor. 90:575-582. Burger J, Gochfeld M. 2004. Marine Birds as Sentinels of Environmental Pollution. Ecohealth Journal Consortium. 1:263-274. Burger J, Gochfeld M, Bonan A. 1996. Gulls, Terns, Skimmers (Laridae). In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E, editors. Handbook of the Birds of the World Alive Vol 3. Barcelona: Lynx Edicions. Cairns DK. 1988. Seabirds as indicators of marine food supplies. Biological Oceanography. 5:261-271. Campana SE. 1999. Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Marine Ecology Progress Series. 188:263-297. Campos LFAS, Andrade AB, Bertrand S, Efe MA. 2017. Foraging behavior and at-sea distribution of White- Tailed Tropicbirds in tropical oceans. Brazilian Journal of Biology. 78:556-563. Carneiro APB, Manica A, Trivelpiece WZ, Phillips RA. 2015. Flexibility in foraging strategies of Brown Skuas in response to local and seasonal dietary constraints. Journal of Ornithology. 156:625-633. Catry T, Ramos JA, Jaquemet S, Faulquier L, Berlincourt M, Hauselmann A, Pinet P, Corre M Le. 2009. Comparative foraging ecology of a tropical seabird community of the Seychelles, western Indian Ocean. Marine Ecology Progress Series. 374:259-272. Chang CW, Iizuka Y, Tzeng WN. 2004. Migratory environmental history of the grey mullet Mugil cephalus as revealed by otolith Sr:Ca ratios. Marine Ecology Progress Series. 269:277-288. Chubb CF, Potter IC, Grant CJ, Lenanton RCJ, Wallace J. 1981. Age, stucture, growth rates and movements of Sea Mullet, Mugil cephalus L. and Yellow-eye Mullet, Aldrichetta forsteri (valenciennes), in the Swan-Avon River system, Western Australia. Marine and Freshwater Reserves. 32:605-628. Clarke KR, Gorley RN. 2015. Getting started with PRIMER V7. Plymouth PRIMER-E. Clarke KR, Tweedley JR, Valesini FJ. 2014. Simple shade plots aid better long-term choices of data pre-treatment

104

in multivariate assemblage studies. Journal of Marine Biology Assocociation of the United Kingdom. 94:1- 16. Collar S, Roby DD, Lyons DE. 2017. Top-down and bottom-up interactions influence fledging success at North America’s largest colony of Caspian Terns (Hydroprogne caspia). Estuaries and Coasts. 40:1808-1818. Collins PM, Halsey LG, Arnould JPY, Shaw PJA, Dodd S, Green JA. 2016. Energetic consequences of time- activity budgets for a breeding seabird. Journal of Zoology. 300:153-162. Crawford RJM, Barham PJ, Underhill LG, Shannon LJ, Coetzee JC, Dyer BM, Leshoro TM, Upfold L. 2006. The influence of food availability on breeding success of African Penguins Spheniscus demersus at Robben Island, South Africa. Biological Conservation. 132:119-125. Crawford RJM, Makhado AB, Waller LJ, Whittington PA. 2014. Winners and losers – responses to recent environmental change by South African seabirds that compete with purse-seine fisheries for food. Ostrich. 85:111-117. Croxall JP. 1987. Seabirds: Feeding Ecology and Role in Marine Ecosystems. Cambridge University Press, Cambridge, United Kingdom. Croxall JP, Butchart SHM, Lascelles B, Stattersfield AJ, Sullivan B, Symes A, Taylor P. 2012. Seabird conservation status, threats and priority actions: A global assessment. Bird Conservation International. 22:1- 34. Delany S, Scott D. 2006. Waterbirds Populations Estimates - fourth edition. Mandurah, Western Australia. Department of Primary Industries and Regional Development. 2019. Data for the annual total catch (kg), the proportion of catch (%) and catch effort (mean vessels/month) for 11 commercially-caught species on Peel- Harvey Estuary, Western Australia over a five-year period (2013-2018). [Unpublished data] Perth, Western Australia. Department of Transport 2006. Map 842: Peel Inlet and Harvey Estuary. Perth, Western Australia. Department of Water and Environmental Regulation, 2019. Water Quality Data on Peel-Harvey Estuary from 2017-2019. Government of Western Australia. [Unpublished data] Perth, Western Australia. [cited 2019 Apr 1]. Available from: http://wir.water.wa.gov.au/Pages/Water-Information-Reporting.aspx Dies JI, Marín J, Pérez C. 2006. Diet of Nesting Gull-billed Terns in Eastern Spain. Waterbirds. 28:106-109. Donnelly-Greenan EL, Harvey JT, Nevins HM, Hester MM, Walker WA. 2014. Prey and plastic ingestion of Pacific Northern Fulmars (Fulmarus glacialis rogersii) from Monterey Bay, California. Marine Pollution Bulletin. 85:214-224 Donovan T., Welden CW. 2002. Niche breadth and resource partitioning. In: Spreadsheet Exercises in Ecology and Evolution. Sunderland, Massachusets, USA: Sinauer Associates, Inc. pp. 289–297. Dowling C, Brown J, Lek E. No date. Fish otoliths of south-western Australia: a photographic catalogue. [place unknown]. 1-258. Duffy DC. 1983. The Foraging Ecology of Peruvian Seabirds. The Auk.100: 800-810. Dunlop JN. 2017. Sentinel seabirds: A guide to using marine birds to monitor marine ecosystems in Western Australia. Perth, Western Australia. Conservation Council of Western Australia. Dunlop JN. 2018. Fairy Tern (Sternula nereis) conservation in south-western Australia. Second Edition. Perth, Western Australia. Conservation Council of Western Australia. Dunlop JN, McNeill S. 2017. Local movements, foraging patterns, and heavy metals exposure in Caspian Terns Hydroprogne caspia breeding on Penguin Island, Western Australia. Marine Ornithology. 45:115-120. Dunlop JN, Surman CA, Wooller RD. 2001. The marine distribution of seabirds from Christmas Island, Indian Ocean. Emu. Dunn RE, White CR, Green JA. 2018. A model to estimate seabird field metabolic rates. Biology Letters. 14:1-4. Einoder LD. 2009. A review of the use of seabirds as indicators in fisheries and ecosystem management. Fisheries Research. 95:6-13. Ellis HI, Gabrielsen GW. 2002. Energetics in Free-ranging Seabirds. In: Schreiber EA, Burger J, editors. Biology of Marine Birds. Boca Raton: CRC Press; pp. 359–407. Emlen S, Demong N. 1975. Adaptive significance of synchronized breeding in a colonial bird: a new hypothesis. Science 188:1029-1031. "EPBC 1999". Department of the Environment and Energy. 1999. Environmental Protection and Biodiversity Conservation Act, Australian Government. Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ, Carpenter SR, Essington TE, Holt RD, Jackson JBC, et al. 2011. Trophic downgrading of planet earth. Science. 333:301-306. Fasola, M.., Bogliani, G., Saino, N. & Canova, L. 2009. Foraging, feeding and time-activity niches of eight species of breeding seabirds in the coastal wetlands of the Adriatic Sea. Italian Journal of Zoology. 56: 61-72. Fayet AL, Freeman R, Shoji A, Padget O, Perrins CM, Guilford T. 2015. Lower foraging efficiency in immatures drives spatial segregation with breeding adults in a long-lived pelagic seabird. Animal Behaviour. 110:79- 89. Ferreira LC, Thums M, Heithaus MR, Barnett A, Abrantes KG, Holmes BJ, Zamora LM, Frisch AJ, Pepperell

105

JG, Burkholder D, et al. 2017. The trophic role of a large marine predator, the Tiger Shark Galeocerdo cuvier. Scientific Reports. 7: 1-14. Fijn RC, de Jong J, Courtens W, Verstraete H, Stienen EWM, Poot MJM. 2017. GPS-tracking and colony observations reveal variation in offshore habitat use and foraging ecology of breeding Sandwich Terns. Journal of Sea Research. 127:203-211. Fort J, Porter WP, Grémillet D. 2011. Energetic modelling: A comparison of the different approaches used in seabirds. Comparative Biochemistry and Physiology, Part A (Molecular and Integrative Physiology). 158:358-365. Furlani D, Gales R, Pemberton D. 2007. Otoliths of Common Australian Temperate Fish: A Photographic Guide. Collingwood, Victoria, Australia: CSIRO Publishing. Furness RW, Camphuysen K. 1997. Seabirds as monitors of the marine environment. ICES Journal of Marine Science. 54:726-737. Furness RW, Monaghan P. 1987. Seabird Ecology. Blackie, Glasgow, Scotland. 164 pp. Gaglio D. 2017. Investigating the foraging ecology and energy requirements of a seabird population increasing in an intensely exploited marine environment. Cape Town: University of Cape Town, South Africa. 173 pp. Gaglio D, Cook TR, Connan M, Ryan PG, Sherley RB. 2017. Dietary studies in birds: testing a non-invasive method using digital photography in seabirds. Methods in Ecology and Evolution. 8:214-222. Gaglio D, Cook TR, McInnes A, Sherley RB, Ryan PG. 2018. Foraging plasticity in seabirds: A non-invasive study of the diet of Greater Crested Terns breeding in the Benguela region. PLoS ONE. 13:1-20. Gochfeld M, Burger J. 1992. Family Sternidae (Terns). In: Hoyo J del, Elliott A, Sargatal J, Cabot J, editors. Handbook of the Birds of the World Alive. Lynx Edicion. Barcelona: Lynx Edicions. 624–667. Gould J. 1848. The Birds of Australia. London, United Kingdom. 392-393. Green DB, Klages NTW, Crawford RJM, Coetzee JC, Dyer BM, Rishworth GM, Pistorius PA. 2015. Dietary change in Cape Gannets reflects distributional and demographic shifts in two South African commercial fish stocks. ICES Journal of Marine Science. 72:771-781. Greenwell C.N. 2017. Octopus as predators of Haliotis laevigata on an abalone sea ranch of south-western Australia. Perth, Western Australia: Murdoch University. Greenwell, C.N., Loneragan, N.R., Tweedley, J. & Wall, M. 2019. Diet and trophic role of octopus on an abalone sea ranch. Fisheries Management and Ecology. 26: 1-10. Gremillet D, Wright G, Lauder AN, Carss DN, Wanless S. 2003. Modelling the daily food requirements of wintering Great Cormorants: a bioenergetics tool for wildlife management. Journal of Applied Ecology. 40:266-277. Hale J. 2008. Monitoring and Evaluation Guide for the Peel-Yalgorup Ramsar Site, A report to the Peel-Harvey Catchment Council and the Department of Environment and Conservation. Mandurah, Western Australia. Hale J, Butcher R. 2007. Ecological Character Description of the Peel-Yalgorup Ramsar Site, Report to the Department of Environment and Conservation and the Peel-Harvey Catchment Council. Perth, Western Australia. Henson SA, Sarmiento JL, Dunne JP, Bopp L, Lima I, Doney SC, John J, Beaulieu C. 2010. Detection of anthropogenic climate change in satellite records of ocean chlorophyll and productivity. Biogeosciences. 7:621-640. Heupel MR, Knip DM, Simpfendorfer CA, Dulvy NK. 2014. Sizing up the ecological role of sharks as predators. Marine Ecology Progress Series.495:291-298. Holm KJ, Burger AE. 2002. Foraging Behavior and Resource Partitioning by Diving Birds During Winter in Areas of Strong Tidal Currents. Waterbirds. 25:312-325. Hughes RN. 1980. Optimal foraging theory in the marine context. Annual Review of Marine Biology and Oceanography. 18:423-481. Ismar SMH, Trnski T, Beauchamp T, Bury SJ, Wilson D, Kannemeyer R, Bellingham M, Baird K. 2014. Foraging ecology and choice of feeding habitat in the New Zealand Fairy Tern Sternula nereis davisae. Bird Conservation International. 24:72-87. Jakubas D, Iliszko LM, Strøm H, Helgason HH, Stempniewicz L. 2018. Flexibility of foraging strategies of the Great Skua Stercorarius skua breeding in the largest colony in the Barents Sea region. Frontiers in Zoology. 15:1-14. Jetz W, Thomas GH, Joy JB, Hartmann K, Mooers AO. 2012. The global diversity of birds in space and time. Nature. 491:444-448. Jordan MJR. 2005. Dietary analysis for mammals and birds: A review of field techniques and animal-management applications. International Zoo Yearbook. 39:108-116. Klages NTW, Cooper J. 1992. Bill morphology and diet of a filter‐feeding seabird: the Broad‐billed Prion Pachyptila vittata at South Atlantic Gough Island. Journal of Zoology. 227:385-396. Kokubun N, Lee WY, Kim JH, Takahashi A. 2015. Chinstrap Penguin foraging area associated with a seamount in Bransfield Strait, Antarctica. Polar Science. 9:393-400.

106

Larson, K. & Craig, D. (2006). Digiscoping vouchers for diet studies of bill-load holding birds. Waterbirds: The International Journal of Waterbird Biology 29: 198-202. Leal GR, Furness RW, McGill RAR, Santos RA, Bugoni L. 2017. Feeding and foraging ecology of Trindade Petrels Pterodroma arminjoniana during the breeding period in the South Atlantic Ocean. Marine Biology. 164:1-17 Lenanton RCJ, Loneragan NR, Potter IC. 1985. Blue-green algal blooms and the commercial fishery of a large Australian estuary. Marine Pollution Bulletin. 16:477-482. Lenanton RCJ, Potter IC, Loneragan NR, Chrystal PJ. 1984. Age structure and changes in abundance of three important species of teleost in a eutrophic estuary (Pisces: Teleostei). Journal of Zoology. 203:311-327. Loneragan NR, Potter IC, Lenanton RCJ, Caputi N. 1986. Spatial and seasonal differences in the fish fauna in the shallows of a large Australian estuary. Marine Biology: International Journal on Life in Oceans and Coastal Waters. 92:575-586. Loneragan NR, Potter IC, Lenanton RCJ, Caputi N. 1987. Influence of environmental variables on the fish fauna of the deeper waters of a large Australian estuary. Marine Biology. 94:631-641. Lyons DE, Patterson AGL, Tennyson J, Lawes TJ, Roby DD. 2018. The Salton Sea: Critical Migratory Stopover Habitat for Caspian Terns (Hydroprogne caspia) in the North American Pacific Flyway. Waterbirds. 41:154- 165. Lyons DE, Roby DD, Collis K. 2005. Foraging Ecology of Caspian Terns in the Columbia River Estuary, USA. Waterbirds. 28:280-291. Lyons DE, Roby DD, Craig DP, Myers AM, Suryan RM, Adkins JY, Collis K. 2007. Effects of Colony Relocation on Diet and Productivity of Caspian Terns. The Journal of Wildlife Management. 66:662-673. Mallory ML, Boadway KA, Davis SE, Maftei M, Diamond AW. 2017. Breeding biology of Arctic Terns (Sterna paradisaea) in the Canadian High Arctic. Polar Biology. 40:1515-1525. Mallory ML, Robinson SA, Hebert CE, Forbes MR. 2010. Seabirds as indicators of aquatic ecosystem conditions: A case for gathering multiple proxies of seabird health. Marine Pollution Bulletin. 60:7-12. Del Marco A, Willmott A. 2017. Wetlands and People plan Peel Yalgorup system – a CEPA action plan for Ramsar site 482: A report by Andrew Del Marco & Amanda Willmott to the Peel-Harvey Catchment Council. Mandurah, Western Australia. Mazloumi N, Doubleday ZA, Gillanders BM. 2017b. The effects of temperature and salinity on otolith chemistry of King George Whiting. Fisheries Research. 196:66-74. McCluskey SM, Bejder L, Loneragan NR. 2016. Dolphin Prey Availability and Calorific Value in an Estuarine and Coastal Environment. Frontiers in Marine Science. 3:1-23 McKinney, RA & Paton, PWC. 2009. Breeding birds associated with seasonal pools in the northeastern United States. Journal of Field Ornithology. 80: 380-386. Menkhorst P, Rogers D, Clarke R, Davies J, Marsack P, Franklin K. 2017. The Australian Bird Guide. 1st ed. Victoria, Australia: CSIRO Publishing. Meteorology B of. 2019. Mandurah (station 009977) Daily Weather Observations [Internet]. [cited 2019 Mar 18]. Available from: www.bom.gov.au/climate/dwo/ Monaghan AP, Uttley JD, Burns MD, Thaine C, Blackwood J. 1989. The relationship between food supply, reproductive effort and breeding success in Arctic Terns Sterna paradisaea. Journal of Animal Ecology. 58:261-274. Montevecchi WA, Hedd A, McFarlane Tranquilla L, Fifield DA, Burke CM, Regular PM, Davoren GK, Garthe S, Robertson GJ, Phillips RA. 2012. Tracking seabirds to identify ecologically important and high risk marine areas in the western North Atlantic. Biological Conservation. 156:62-71. Monticelli D, Ramos JA, Tavares PC, Bataille B, Lepoint G, Devillers P. 2008. Diet and Foraging Ecology of Roseate Terns and Lesser Noddies Breeding Sympatrically on Aride Island, Seychelles. Waterbirds. 31:231- 240. Morcombe M, Stewart D. 2010. The Morcombe & Stewart Guide to Birds of Australia. [place unknown]. Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH. 2007. Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science. 315:1846-1850. Nagy KA. 2005. Field metabolic rate and body size. Journal of Experimental Biology. 208:1621-1625. Nel SA, Potter IC, Loneragan NR. 1985. The biology of the Catfish Cnidoglanis macrocephalus (Plotosidae) in an Australian estuary. Estuarine, Coastal and Shelf Science. 21:895-909. Nye ER, Dickman CR. 2005. Activity budgets and habitat use of the Green Pygmy-goose (Nettapus pulchellus) on dry-season refuges in Kakadu National Park, Northern Territory. Emu. 105:217-222. O’Malley J, Willmott A. 2015. Binjareb Boodja Landscapes 2025, A Strategy for Natural Resource Management in the Peel-Harvey Region, A report to the Peel-Harvey Catchment Council, Jane O’Malley & Andrew Del Marco. Mandurah, Western Australia. Parsons M, Mitchell I, Butler A, Ratcliffe N, Frederiksen M, Foster S, Reid JB. 2008. Seabirds as indicators of the marine environment. ICES Journal of Marine Science. 65:1520-1526.

107

Paterson JT, Rotella JJ, Link WA, Garrott R. 2018. Variation in the vital rates of an Antarctic marine predator: the role of individual heterogeneity. Ecology. 99:2385-2396. Phillips RA, Gales R, Baker GB, Double MC, Favero M, Quintana F, Tasker ML, Weimerskirch H, Uhart M, Wolfaardt A. 2016. The conservation status and priorities for albatrosses and large petrels. Biological Conservation. 201:169-183. Piatt JF, Arimitsu ML, Sydeman WJ, Thompson SA, Renner H, Zador S, Douglas D, Hatch S, Kettle A, Williams J. 2018. Biogeography of pelagic food webs in the North Pacific. Fisheries Oceanography. 27:366-380. Pinet P, Jaquemet S, Phillips RA, Le Corre M. 2012. Sex-specific foraging strategies throughout the breeding season in a tropical, sexually monomorphic small petrel. Animal Behaviour. 83:979-989. Popper AN, Lu Z. 2000. Structure-function relationships in fish otolith organs. Fisheries Research. 46:15-25. Potter IC, Chrystal PJ, Loneragan NR. 1983. The biology of the Blue Manna Crab Portunus pelagicus in an Australian estuary. Marine Biology. 78:75-85. Potter IC, Loneragan NR, Lenanton RCJ, Chrystal PJ, Grant CJ. 1983. Abundance, distribution and age structure of fish populations in a Western Australian estuary. Journal of Zoology. 200:21-50. Potter IC, Tweedley JR, Elliott M, Whitfield AK. 2015. The ways in which fish use estuaries: A refinement and expansion of the guild approach. Fish and Fisheries. 16:230-239. Potter IC, Veale L, Tweedley JR, Clarke KR. 2016. Decadal changes in the ichthyofauna of a eutrophic estuary following a remedial engineering modification and subsequent environmental shifts. Estuarine, Coastal and Shelf Science. 181:345-363. Prum RO, Berv JS, Dornburg A, Field DJ, Townsend JP, Lemmon EM, Lemmon AR. 2015. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature. 526:569-573. Raeside JB. 2012. The ecology of the bottlenose dolphin (Tursiops aduncus) in the Peel-Harvey Estuary. Perth, Western Australia: Murdoch University. "RAMSAR 1971". RAMSAR Convention on Wetlands: site criteria for identifying wetlands of international importance. 1971. Iran. Rishworth GM, Tremblay Y, Green DB, Pistorius PA. 2014. An automated approach towards measuring time- activity budgets in colonial seabirds. Methods in Ecology and Evolution. 5:854-863. Robertson GS, Bolton M, Grecian WJ, Wilson LJ, Davies W, Monaghan P. 2014. Resource partitioning in three congeneric sympatrically breeding seabirds: Foraging areas and prey utilization. The Auk. 131:434-446. Roby DD, Collis K, Lyons DE, Craig DP, Adkins JY, Myers M, Suryan RM. 2002. Effects of colony relocation on diet and productivity of Caspian Terns. The Journal of Wildife Management. 66:662-673. Rock JC, Leonard ML, Boyne AW. 2008. Do co-nesting Arctic and Common Terns partition foraging habitat and chick diets? Waterbirds. 30:579-587. Rogers TA, Fowler AJ, Steer MA, Gillanders BM. 2019. Resolving the early life history of King George Whiting (Sillaginodes punctatus: Perciformes) using otolith microstructure and trace element chemistry. Marine and Freshwater Research. (Special Issue). [published online]. Rojas LM, McNeil R, Cabana T, Lachapelle P. 1997. Diurnal and nocturnal visual function in two tactile foraging waterbirds: the American Ibis and the Black Skimmer. The Condor. 99:191-200. Serventy DL, Serventy V, Warham J. 1971. The Handbook of Australian Seabirds. Reed AH, Reed AW, editors. [place unknown]: A.H. & A.W. Reed Ltd. Shephard JM, Dunlop JN, Bouten W. 2018. Foraging movements of common noddies in the East Indian Ocean are dependent on breeding stage: Implications for marine reserve design. Pacific Conservation Biology. 25:164-173. Sommerfeld J, Hennicke JC. 2010. Comparison of trip duration, activity pattern and diving behaviour by Red- tailed Tropicbirds (Phaethon rubricauda) during incubation and chick-rearing. Emu.110:78-86. Spatz DR, Holmes ND, Reguero BG, Butchart SHM, Tershy BR, Croll DA. 2017. Managing Invasive Mammals to Conserve Globally Threatened Seabirds in a Changing Climate. Conservation Letters. 10:736-747. Spatz DR, Newton KM, Heinz R, Tershy B, Holmes ND, Butchart SHM, Croll DA. 2014. The biogeography of globally threatened seabirds and island conservation opportunities. Conservation Biology. 28:1282-1290. Steen VA, Powell AN. 2012. Wetland Selection by Breeding and Foraging Black Terns in the Prairie Pothole Region of the United States. The Condor. 114:155-165. Surman CA, Wooller RD. 2003. Comparative foraging ecology of five sympatric terns at a sub-tropical island in the eastern Indian Ocean. Journal of Zoology. 259:219-230. Sydeman WJ, Piatt JF, Thompson SA, García-Reyes M, Hatch SA, Arimitsu ML, Slater L, Williams JC, Rojek NA, Zador SG, Renner HM. 2017. Puffins reveal contrasting relationships between forage fish and ocean climate in the North Pacific. Fisheries Oceanography. 26:379-395. Sydeman WJ, Thompson SA, Piatt JF, García-Reyes M, Zador S, Williams JC, Romano M, Renner HM. 2017. Regionalizing indicators for marine ecosystems: Bering Sea–Aleutian Island seabirds, climate, and competitors. Ecological Indicators. 78:458-469. Szabo JK, Khwaja N, Garnett ST, Butchart SHM. 2012. Global Patterns and Drivers of Avian Extinctions at the

108

Species and Subspecies Level. PLoS ONE. 7:1-9. Team RCD. 2011. R: A Language and environment for statistical computing ’. (The R Foundation for Statistical Computing: Vienna, Austria.) [Internet]. Available from: http://www.r-project.org/ Thiel M, Macaya E, Acuna E. 2007. The Humboldt Current System of northern and central Chile: oceanographic processes, ecological interactions and socioeconomic feedback. Oceanography and Marine Biology. 45:195- 345. Turner ERA. 1964. Social Feeding in Birds. Behaviour. 24:1-44. Ugland KI, Gray JS, Ellingsen KE. 2003. The species accumulation curve and estimation of species richness. Journal of Animal Ecology. 72:888–897. Velando A, Lessells CM, Márquez JC. 2001. The function of female and male ornaments in the inca tern: Evidence for links between ornament expression and both adult condition and reproductive performance. Journal of Avian Biology. 32:311-318. Washburn BE, Chipman RB, Bernhardt GE, Francoeur LC, Kutschbach-Brohl L. 2013. Foraging Ecology of Four Gull Species at a Coastal–Urban Interface. The Condor. 115:67-76. Watanabe S, Sato K, Ponganis PJ. 2012. Activity Time Budget during Foraging Trips of Emperor Penguins. PLoS ONE. 7:1-11. Weimerskirch H, Le Corre M, Jaquemet S, Potier M, Marsac F. 2004. Foraging strategy of a top predator in tropical waters: Great Frigatebirds in the Mozambique Channel. Marine Ecology Progress Series. 275:297- 308. Weimerskirch H, Le Corre M, Ropert-Coudert Y, Kato A, Marsac F. 2005. The three-dimensional flight of red- footed boobies: Adaptations to foraging in a tropical environment? The Royal Society Publishing, Proceedings: Biological Sciences. 272:53-61. Whittow GC, Rahn H. 1984. Seabird Energetics. New York: Plenum Press, New York. Wood KA, Stillman RA, Goss-Custard JD. 2015. The effect of kleptoparasite and host numbers on the risk of food-stealing in an avian assemblage. Journal of Avian Biology. 46:589-596. Zarza R, Cintra R, Anciäes M. 2013. Distribution, abundance and habitat selection by breeding Yellow-billed Terns (Sternula superciliaris), Large-Billed Terns (Phaetusa simplex) and Black Skimmers (Rynchops niger) in the Brazilian Amazon. Waterbirds. 36:470-481. Zimmer I, Wilson RP, Beaulieu M, Ropert-Coudert Y, Kato A, Ancel A, Plötz J. 2010. Dive efficiency versus depth in foraging emperor penguins. Aquatic Biology. 8:269-277. Zimmer I, Wilson RP, Gilbert C, Beaulieu M, Ancel A, Plötz J. 2008. Foraging movements of emperor penguins at Pointe Géologie, Antarctica. Polar Biology. 31:229-243 Zuur F. A, Ieno N. E, Elphick S. C. 2010. A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution. 1:3-14.

109

Appendix 1. Summary of representative species from each genus of larger tern featured in this literature review and their foraging ecology.

Foraging Ecology Species Size Distribution Foraging Range Strategy Prey

Common Noddy Tropical and sub-tropical pelagic Larger post-larval forage fish; beaked 40-45cm Worldwide Anous stolidus waters, up to 180km from breeding Surface salmon, anchovies and squid, often in (Serventy et (Serventy et colonies (Catry et al. 2009; feeders association with surface-feeding tuna al. 1971). al. 1971). (IOC 2018) Surman & Wooller 2003). (Dunlop 2017).

Lesser Noddy Confined to Tropical and sub-tropical pelagic Smaller post-larval forage fish; black-spot Anous tenuirostris 30-34cm the Indian waters (Catry et al. 2009; Surface goatfish and beaked salmon, often in (Serventy et Ocean Monticelli et al. 2008) up to feeders association with surface-feeding tuna (IOC 2018) al. 1971). (Serventy et 180km from breeding colonies (Dunlop 2017). al. 1971). (Surman & Wooller 2003).

Gull-billed Tern Shallow coastal marine and inland, 36-42cm Worldwide Gelochelidon nilotica freshwater systems including Surface Generalists, especially crustaceans (Dies (Serventy et (Serventy et wetlands, tidal mudflats and rice feeders et al. 2018; Menkhorst et al. 2017) al. 1971). al. 1971). (IOC 2018) paddies (Dies et al. 2005).

Caspian Tern Coastal marine systems in 48-54 cm Worldwide Benthic forage fish, such as juvenile Hydroprogne caspia sheltered, shallow water with Plunge (Serventy et (Serventy et salmonids (Lyons et al. 2005), sea mullet, seagrass cover (Dunlop & McNeil divers al. 1971). al. 1971). herring and whiting (Dunlop 2017). (IOC 2018) 2017).

Inca Tern South Restricted to coastal areas off Peru Larosterna inca America and Chile (Velando et al. 2001) Plunge Mostly anchovies (Engraulis ringens) 40cm (Velando et Humboldt current (Duffy 1983; divers (Duffy 1983). (IOC 2018) al. 2001). Thiel et al. 2007)

Bridled Tern 30-32cm Equatorial Small forage and larval fish, associated Tropical and sub-tropical Surface Onychoprion anaethetus (Serventy et (Serventy et with sargassum (seaweed) rafts (Dunlop pelagic waters (Dunlop 2017) feeders (IOC 2018) al. 1971) al. 1971). 2017).

Sooty Tern 33-36cm Equatorial Tropical and sub-tropical pelagic Onychoprion Surface Target forage fish (including lanternfish) (Serventy et (Serventy et waters, 480-600km from colony fuscatus feeders and squid (Surman & Wooller 2003). al. 1971) al. 1971). (Surman & Wooller 2003) (IOC 2018)

Large-billed Tern South Phaetusa simplex America Freshwater rivers (Zarza et al. Plunge Medium-sized surface forage fish (Zarza 38-42cm (IOC 2018) (Zarza et al. 2013). divers et al. 2013). 2013).

Roseate Tern Tropical, sub-tropical (Surman & Sterna dougallii 31-38cm Worldwide Wooller 2003) and temperate Small and larval forage fish (Catry et al. Plunge (IOC 2018) (Serventy et (Serventy et (Robertson 2004) pelagic waters; 2009; Dunlop 2017; Robertson et al. divers al. 1971). al. 1971). wider-ranging to deeper areas 2014; Surman & Wooller 2003). (Monticelli et al. 2008)

Common Tern 32-37cm Worldwide Forage in deeper waters Sterna hirundo Plunge Mostly hake (Urophycis spp.) and sand (Serventy et (Serventy et (Robertson et al. 2014; Rock et al. divers lance (Ammodytes spp.) (Rock et al. 2007) al. 1971). al. 1971). 2007) (IOC 2018)

Arctic Tern 32-37cm Worldwide Forage in shallower, sheltered Sterna paradisaea Plunge Mostly hake (Urophycis spp.) and sand (Serventy et (Serventy et waters (Robertson et al. 2014; divers lance (Ammodytes spp.) (Rock et al. 2007) al. 1971). al. 1971). Rock et al. 2007) (IOC 2018)

Crested Tern Adults: schooling forage fish including 43-48cm Worldwide Coastal waters (Gaglio et al. 2017) Thalasseus bergii Plunge sardines, mackerel, scad (Gaglio et al. (Serventy et (Serventy et in shallower reef habitats (Surman divers 2017); Chicks: fed smaller seagrass- and al. 1971). al. 1971). & Wooller 2003). (IOC 2018) reef-associated fish (Dunlop 2017)

Appendix 2. Identification guide to prey species in Caspian Tern (Hydroprogne caspia) diet, as recorded between October 2018 and February 2019 across Peel-Harvey Estuary from (a) bill-loaded images and (b) otoliths in regurgitation pellets, with reference images.

NB: All fish images are sourced from Fishes of Australia (http://fishesofaustralia.net.au/, 2019) and all otolith images are sources from Dowling, Brown and Lek (unpublished report). All images of bill-loaded terns, and otoliths taken by S. Stockwell unless otherwise stated.

a) Bill-loaded Images Hemiramphidae Southern Garfish (Hyporhamphus melanochir)

Gobiidae Goby sp. (possibly: Favonigobius lateralis)

Mugilidae Yellow-eyed Mullet (Aldrichetta forsteri)

Sea Mullet (Mugil cephalus)

112

Arripidae Tommy Rough or Australian Herring (Arripis georgianus)

Gerreidae Common Silverbiddy or Roach (Gerres subfasciatus)

Sillaginidae King George Whiting (Sillaginodes punctatus)

Southern School Whiting (Sillago bassensis)

Trumpeter Whiting (Sillago maculata)

113

Yellowfin Whiting (Sillago schomburgkii)

Terrapontidae Yellowtail Grunter (Amniataba caudavittata)

Striped Trumpeter (Pelates octolineatus)

Paralichthyidae Smalltooth Flounder (Pseudorhombus jenynsii)

Plotosidae Estuarine Catfish or Cobbler (Cnidoglanis macrocephalus)

114

Tetradontidae Weeping Toadfish or Common Blowfish (Torquigener pleurogrammai)

Portunidae Blue Swimmer Crab (Portunus armatus)

Image: Cherilyn Corker, 2019

115

b) Otoliths Mugilidae Yellow-eyed Mullet (Aldrichetta forsteri)

Sea Mullet (Mugil cephalus)

Sillaginidae Whiting spp.

Terapontidae Striped Trumpeter (Pelates octolineatus)

116

Appendix 3. Observations of foraging behaviour of Caspian Terns (Hydroprogne caspia) on Peel-Harvey Estuary during their non-breeding period.

This appendix provides a compilation of observations of foraging behaviour in Caspian Tens

(Hydroprogne caspia) on the Peel-Harvey Estuary, south-western Australia between October

2018 and February 2019, immediately following the breeding season.

Plunge-diving and foraging behaviour Throughout the study period, H. caspia foraged on Peel-Harvey Estuary by flying parallel to the water, 10 to 20m above the surface (scanning) before hovering and characteristically plunge-diving (a rapid, direct plummet) for prey species (Figure 1; pers. obs. S. Stockwell).

During the plunge-dive, their bodies can submerge completely upon impact with the water, allowing them to maximise the depth they were able to penetrate to take prey species, at depths estimated between 0 and 0.75m below the surface (Figure 1). Many terns foraged along the shorelines of the estuary, small islands, tributary rivers or channels, as well as the edges of boating channels or areas of sediment build-up (Pers. obs. S. Stockwell). Between foraging bouts, most H. caspia returned to sandspits to loaf, either on their own, or with birds of the same or different species. The largest numbers of H. caspia observed together on a single spit within the study period was 53 at Chimneys site (in area three) on 13 February 2019, and before this, 49 in early January 2019 and 47 in early December at Nairns site (in area two).

Figure 1. Sequences of shallow (a) and fully-submerged (b) plunge-dives of foraging H. caspia. Image source: Bob Patterson, 2018. 117

Monthly variation in foraging activity

Numbers of H. caspia increased on Peel-Harvey Estuary with time since their breeding season. The first juvenile birds were observed on the Estuary in mid-October where they were fed by their parents as they grew (increased in size and moulted their juvenile plumage) and learnt to fish for themselves. Observations of terns found they returned consistently to the night roost in the north-western part of the estuary for most of the study period, arriving just before twilight (pers obs.). Each morning, the terns left after first light and travelled out to foraging areas (pers obs.).

Hourly variation in foraging activity

Foraging activity and tern numbers at foraging sites varied with time of day. On average,

5.4 terns foraged for 37.1% of every hour of the day of the 14.9 birds present at foraging sites on average (Figure 2). The mean proportion of time spent foraging peaked in the first hour block and decreased gradually at a non-linear rate throughout the day (Figure 2) while the number of foragers was significantly higher in that same block then decreased to a steady average of 3 to 6 foragers every hour (Figure 2). In contrast, counts of total terns peaked in the mid-morning and mid-afternoon periods and were lowest in blocks either side of dawn and dusk (Figure 2).

Figure 2. The average count of total (red) and foraging terns (black), and time spent foraging in each hour of the day across all foraging sites from October 2018 to February 2019.

118

Territoriality

Observations whilst focal sampling revealed some territorial behaviour amongst some foraging H. caspia at sites in Murray, Serpentine, Dawesville and Mealup Drain. Foraging behaviour was perceived to be ‘territorial’ when terns patrolled a specific, often small area by circling above it, and engaged in conflict with waterbirds upon approach. Some birds were observed chasing and squawking at other birds who fished within an area they patrolled in place of fishing themselves (pers. obs.). Colour-banded birds also provided insight into potential ‘territorial’ birds. For example, orange-grey-white was reliably present at Wannanup spit with its chick and wasn’t sighted elsewhere. In addition, this bird was observed chasing other birds from this area (Figure 3)

Figure 3. Colour-banded bird orange-grey-white exhibiting “territorial behaviour” (squawking and advancing on other birds).

119

Meso-predator interactions

Observations of foraging H. caspia indicated a relationship with meso-predators, especially Indo-Pacific Bottlenose Dolphins (Tursiops aduncus). Terns interacted with dolphins in 78.4% of events when they were presence, mostly for foraging purposes (Figure

4). Between 1 and 15 terns were observed joining a fishing event, with an average of 2.8 birds per dolphin foraging event. While H. caspia showed preference for interaction with T. aduncus whilst feeding, they did not appear to make foraging decisions based on dolphin presence or absence, nor did they appear to follow dolphins between foraging sites. This suggests the interaction between these meso-predators is purely an opportunistic one, whereby H. caspia join foraging events because of learnt associations between dolphin foraging and enhanced foraging success, possibly due to the concentration of forage fish. Other piscivorous bird species, including Australasian Darter (Anhinga novaehollandiae), Little Black Cormorant

(Phalacrocorax sulcirostris) and Australian Pelican (Pelecanus conspicillatus) also joined dolphin fishing events.

Figure 4. Caspian Terns and other piscivorous waterbirds join foraging dolphins in ‘feeding event’.

120

Kleptoparasitism

Throughout the study period, opportunistic observations of inter and intraspecific piracy were recorded whereby H. caspia were both the pirates and the victims of this kleptoparasitism on separate occasions. H. caspia were observed chasing fish-bearing Crested Terns (Sterna bergii), A. novaehollandiae, Silver Gulls (Croicocephalus novaehollandiae), Whistling Kite

(Haliastur spenurus) and Eastern Osprey (Pandion cristatus) as well as other H. caspia, especially when returning to sandspits to feed chicks. Piracy by S. bergii, C. novaehollandiae,

P. conspicillatus, Great Egret (Ardea modestus), A. novaehollandiae, H. sphenurus and P. sulcirostris on bill-loaded H. caspia was also observed whilst birds were in the air, on sandspits and in the water whilst plunge-diving (Figure 5). Kleptoparasitism by gulls and raptors has been observed at H. caspia breeding colonies in other studies with associated negative impacts to the terns (Collar et al. 2017). Observations of kleptoparasitism on Peel-Harvey Estuary appeared to be opportunistic and infrequent suggesting no long-term impact on H. caspia fitness.

Figure 5. Inter- and intra-specific kleptoparasitism on bill-loaded H. caspia whilst (a) in air (b) mid plunge-dive and (c) on sandspits.

121

Appendix 4. Proposed monitoring plan for Caspian Terns (Hydroprogne caspia) as a biological indicator of ecosystem health on Peel-Yalgorup Ramsar site 482.

This proposed monitoring plan is written in the style of the current Monitoring and Evaluation

Guide for the Peel-Yalgorup Ramsar Site for consideration by the Technical Advisory Group for Ramsar site 482 (Hale 2008).

Waterbirds E: Caspian Terns

Rationale

Seabirds have high value as indicators of their ecosystem health and for monitoring changes within and between marine environments over time (Cairns 1988) as a result of many aspects of their behaviour and life history (Burger & Gochfeld 2004). Caspian Terns

(Hydroprogne caspia) are conspicuous birds (large, diurnally-active, with unique appearance and distinctive calls) and are top piscivorous predators across Peel-Yalgorup throughout the non-breeding season annually (between October and May, approximately 75% of the year). In this way, patterns in their behaviour and life history are indicative of the health and productivity of the Peel-Yalgorup ecosystem.

Objectives/hypothesis:

The key ecological characteristics of the Ramsar site and their respective limits of acceptable change in Monitoring and Evaluation Guide for the Peel-Yalgorup Ramsar Site

(Hale & Butcher 2007; Hale 2008) provide a foundation for the development of this monitoring program. The ecological characteristics of the Estuary that could be monitored using H. caspia are high diversity and abundance of waterbirds, important source of food, spawning, migration route and habitat for fish, high water quality and low levels of pollution (Table 1).

The overarching aim of this program is to develop the use of H. caspia as a bio-indicator of the Peel-Harvey Estuary by monitoring changes in tern counts, foraging activity and diet, over time, to indicate ecosystem condition. The program seeks to contribute towards setting

122 thresholds for limits of acceptable change (LACs) in H. caspia parameters associated with ecosystem condition on the estuary. Objectives for the Waterbirds E monitoring program are:

• To understand how changes in tern counts (October to December) may reflect

recruitment, and indicate health/suitability of the Estuary for foraging H. caspia;

• To understand how fluctuation in forage-fish availability affect H. caspia foraging

activity across the Estuary; and

• To understand long-term dietary trends of H. caspia using bill-loaded images of

forage fish.

Table 1. Ecological characteristics of the Peel-Harvey Ramsar wetlands (Ramsar site 482) identified for monitoring, limits of acceptable change, and possible use of Caspian Terns, Hyrdropogne caspia, to monitor performance of the ecological characteristic. Limits of acceptable change are shown when guidelines are available. Ecological Limit of Monitoring characteristic of Application (H. caspia) Acceptable Parameter RAMSAR site 482 Change The largest H. caspia Roost counts of population in H. caspia on the High diversity and southwestern Australia Estuary can show abundance of waterbirds spend their non- recruitment and breeding season on site change in numbers 482. over time. H. caspia catch Identification of forage medium-size, benthic fish from bill-loaded forage fish: whitings H. caspia images. (Sillaginidae), mullets Images taken at main Important source of (Mugilidae) and Striped foraging areas and food, spawning, Trumpeter (P. submitted by the migration route and octolineatus) community. habitat for fish Abridged Estuary H. caspia forage in areas Census to monitor with high abundance of foraging activity by forage fish area over time. H. caspia feathers Heavy metals and other show mercury Aim for high water Mercury threshold contaminant concentrations 0.9-5.9 quality and low levels of 5 mg.kg-1 (Burger concentrations can be mgkg-1 (mean 2.27 pollution & Gochfeld 2004) detected in feathers mgkg-1; Dunlop and McNeill, 2017) Current and historical programs:

123

H caspia are included in most general bird counts across the Ramsar site. In 1990, H. caspia were one of six bird species included under criterion six that contributed towards the site’s initial RAMSAR listing (Hale & Butcher 2007) although the species was later removed as it did not meet the 1% threshold (1,000 birds supported) with revised Waterbird Population

Estimates of the Australia-wide population (Delany & Scott 2006). A 2017 study offered insight into the foraging and reproductive ecology of this population throughout the breeding season. It also found all breeding adults (39 birds, approximately 25% of population) tested had elevated levels of mercury (mean 2.27 mgkg-1; range 0.9 – 5.9 mgkg-1) in tail feather samples taken (Dunlop & McNeill 2017). In response, this study uncovered their foraging ecology through the non-breeding season, which was primarily on the Ramsar site (Chapter 3).

Monitoring method

Population fluctuation: night roost counts

Counts at the night roost require an experienced bird-observer to find the site and count all birds assembled, using binoculars or a scope. Each count is done by a concealed observer in the ten-minute period before twilight falls, where the flock is counted three times on each occasion, and the average number of birds recorded. The number of juveniles, adults and year- old birds can be distinguished if light and skill permit.

In order to locate the night roost, the observer(s) should watch and listen for terns as they leave popular foraging areas (such as Nairns) in the late afternoon, and follow them to roost sites. Night roost sites are characterised as large, flat sandy areas without tidal inundation, such as historical roost sites like Creery Wetlands (Figure 3.3).

Estuary surveys

In order to monitor foraging activity (total terns, foragers, % time foraging) across Peel-

Harvey Estuary, six key sites were established around the Estuary perimeter, for surveys following methods set out in Section 3.2.2 (Table 2).

124

Table 2. Location and access description for the six main Estuary Census sites for monitoring H. caspia across Peel-Harvey Estuary. Area Site Latitude Longitude Description on access Take Batavia Quays Rd off South 1 Yunderup -32.5912 115.7628 Yunderup Rd and walk from the boat ramp on track to Little Yunderup Is. spit Walk east from John Street Carpark at 2 Nairns -32.5723 115.7620 Coodanup Foreshore. Count birds on this side and far spit of Serpentine river mouth. Check dredge spoil across from Mandurah 3 Chimneys -32.5609 115.7128 Quay opening. Walk in from Pleasant Grove Circle and 4 Pt Ward -32.5939 115.6726 check far sand spit Park at boat ramp and look to two exposed 5 Heron Pt -32.7432 115.7110 sandspits and beach on Brunswick Island. Walk up from Mills/Mealup Rd carpark, 6 Mealup 1 -32.7020 115.7005 wide spit near large fallen tree.

Diet study

Digiscoping between mid-October and end-December is an efficient way to determine change in H. caspia diet over time. Following an abridged method from Section 3.2.4, monitoring periods are two-hours in duration, best achieved at first light, midday or mid- afternoon when foraging activity is higher (Figure 3.11). A quiet, still photographer sits in close proximity to birds on a spit (20-50m from birds) with a camera or digiscope to capture as many bill-loaded events as possible. A record is kept of the number of all bill-loaded events observed, and the number of these captured on camera, as well as the date, time and location of the monitoring period. These images are later collated, the prey species identified to lowest taxonomic order possible and the length estimated in comparison to average tern bill length

(see Section 3.2.4). The most effective digiscoping sites include sand spits at Nairns and Pt

Ward as well as Yunderup and Chimneys. Monitoring could rotate around spits across all six areas (Table 2) or focus on Nairns as a consistent diet monitoring site as it has reliable high frequencies of bill-loaded events within this period.

125

Opportunistic observations

Opportunistic observations of Caspian Tern presence (or absence), counts and activity, band numbers or colour combinations, or bill-loaded birds can all be submitted to the overseeing body for entry into an overarching database. Opportunistic H. caspia data recorded from locations within the RAMSAR site that are entered into BirdData by community members can also be acquired and recorded in this database.

Location

Six sites established across Peel-Harvey Estuary for estuary census and digiscoping

(Table 2) as well as the night roost site (Figure 3.3).

Frequency

Monthly (estuary census and roost counts)

Nine-week diet sampling period (digiscoping) mid-October to mid-December

Parameters and methods

Visual counts of terns and their foraging activity by trained bird-observers, and photographs of bill-loaded birds by trained digiscopers or community-submitted images.

Data analysis and interpretation

Records of tern counts, foraging activity and bill-loaded image data should be analysed to determine trends over time and inform refinement of limits of acceptable change.

126

Quality assurance and quality control

In order to maintain consistency in monitoring and minimise disturbance to terns, all observers should be trained prior to their involvement in the monitoring program.

Reporting information

Data collated should be stored in a dedicated Peel-Yalgorup Ramsar Site Waterbird

Database (see Waterbird Program D: Cormorants), managed by an overseeing body. In addition, data should be forwarded to Birdlife Australia for inclusion in their database.

Exceedances of the LAC should trigger the management process, and relevant technical experts on the Peel-Yalgorup Technical Advisory Panel consulted where necessary.

An annual report describing the results of the monitoring program, against LAC and describing trends should be produced and made available to stakeholders and the wider community.

Links to other programs

Although there is no Western Australian or national program for monitoring foraging activity or bird populations, data could be copied to Peel-Harvey Catchment Council, Birdlife

WA and Wetlands International – Oceania or other relevant bodies.

Roles and responsibility

Currently, waterbird monitoring is undertaken by a pool of volunteers with varying experience, coordinated by BirdLife and Peel-Harvey Catchment Council. The body established to administer the management plan for the Peel-Yalgorup Ramsar site should be responsible coordination of monitoring as well as for annual reporting and informing the

Technical Advisory Panel. The foraging activity monitoring (monthly estuary census and night roost counts) and dietary studies (including the digiscoping fieldwork and identification of bill- loaded images) should be conducted by an ornithologist on a casual contract, preferably the

127 same observer or from the same consultancy for consistency. Additional administration and coordination of the data base and citizen science team could be a volunteer role or included in an existing science/administration role as part of a co-ordinating body (for example, the Peel-

Harvey Catchment Council or an environmental consultant or consulting company with which the ornithologist is aligned).

Estimated costs

The estimated cost for the project would cover initial capital costs of equipment (access to an appropriate vehicle, spotting scope and tripod, binoculars and a camera with sufficient capacity) as well as the ongoing cost of conducting the monitoring. Ongoing costs include the casual wage of an ornithologist for two days each month (24 days work annually) as well as the reimbursement of all petrol and vehicle maintenance costs.

Each month, two days of monitoring would follow this timeframe:

o Day 1: estuary census and roost count

o Day 2: digiscoping and data entry/analysis

Dietary studies using a digiscope would accrue an additional two or three days of work each week for an ornithologist over a nine-week period (2.5 months) mid-October to end-

December.

Priority

Medium to high priority

128