STATUS AND TRENDS FOR SHALLOW REEF ... - Parks Australia · 2008). In east Africa, south-east Asia,...

STATUS AND TRENDS FOR SHALLOW REEF HABITATS AND ASSEMBLAGES AT ELIZABETH AND MIDDLETON REEFS, LORD

HOWE MARINE PARK

Andrew S. Hoey, Morgan S. Pratchett, Katie Sambrook, Sallyann Gudge, and Deborah J. Pratchett

Produced for The Director of National Parks, June 2018

*Corresponding author – Professor Morgan Pratchett, ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville QLD 4811. E-mail: [email protected], Phone/ Fax: (07) 47815747 / 47816722

In responding to a tender from the Department of Environment, a team of researchers representing the ARC Centre of Excellence for Coral Reef Studies at James Cook University (JCU) completed surveys of the coral reef fauna at Elizabeth and Middleton Reef. The field team comprised Professor Morgan Pratchett, Dr Andrew Hoey, Ms Katie Sambrook and Mrs Sallyann Gudge. This report was prepared by Professor Morgan Pratchett, Dr Andrew Hoey, Ms Katie Sambrook, Mrs Sallyann Gudge and Mrs Deborah Pratchett

On the cover - Photograph taken by Scott Ling in Blue Holes, Middleton Reef on 27 February 2018

© Commonwealth of Australia 2018 This work is copyright. Apart from any use as permitted under the Copyright Act 1968, no part may be reproduced by any process without prior written permission from the Commonwealth. Requests and inquiries concerning reproduction and rights should be addressed to the Commonwealth Copyright Administration, Attorney General’s Department, Robert Garran Offices, National Circuit, Barton ACT 2600 or posted at http://www.ag.gov.au/cca

The views and opinions expressed in this publication are those of the authors and do not necessarily reflect those of the Australian Government.

This report has been produced for the sole use of the party who requested it. The application or use of this report and of any data or information (including results of experiments, conclusions, and recommendations) contained within it shall be at the sole risk and responsibility of that party. JCU does not provide any warranty or assurance as to the accuracy or suitability of the whole or any part of the report, for any particular purpose or application.

1 Executive Summary

Elizabeth and Middleton Reefs are the world’s southernmost open ocean platform

reefs, supporting a unique mix of tropical and subtropical species. In-water field

surveys were conducted in 2011, 2014 and 2018 using consistent methods at the

same locations, enabling rigorous assessment of trends in benthic habitats and

associated assemblages of reef fish and mobile macro-invertebrates.

The most recent surveys were conducted from February 25th to March 4th, 2018,

with 4 days (25-29 February) spent at Middleton Reef and 4 days (1-4 March) at

Elizabeth Reef. Surveys were conducted at a total of 17 sites across both

Middleton and Elizabeth reefs. Where possible, surveys were conducted in two

distinct habitats (shallow reef crest or top and deep reef slope or base) at each

site. Benthic composition and habitat structure, as well as coral health, densities

and biomass of functionally important reef fishes, densities of site attached and

endemic fishes, and densities of non-coral invertebrates were recorded along four

replicate 50 m transects in each habitat at each site.

Main findings include:

• Mean cover of hard (Scleractinian) corals was high in 2018 (Elizabeth Reef:

39.95% ±1.72 SE; Middleton Reef: 26.62% ±1.87 SE) and has increased

by >40% since 2014. There was however, low incidence of coral bleaching in

2018, which may have worsened after surveys were completed due to the

significant accumulation of heat stress that occurred in 2017/18.

• Aside from bleaching, there was very low incidence of coral predation, disease,

and or other unexplained coral injuries. Very few crown-of-thorns starfish or

Drupella spp. were recorded in 2018, though there is evidence of a persistent

low-density population of crown-of-thorns starfish at Elizabeth Reef. Given their

considerable reproductive potential and low visitation to these locations, it might

be prudent to remove these starfish so as to minimise the likelihood of future

population outbreaks.

• Cover of macroalgae (conspicuous seaweeds >5 mm in height) was high in

back reef and lagoonal habitats, but mostly very low in exposed reef habitats.

Both the cover and the predominant type of macroalgae found at each site was

largely unchanged since 2014. Similarly, the physical structure (topographic

complexity) of reef habitats was very consistent among sites and largely

unchanged from 2011 to 2018.

• The abundance of herbivorous fishes recorded at Elizabeth and Middleton

Reefs in 2018 were similar to those recorded in 2011 and 2014 (Elizabeth:

2011: 67.3 fishes/250m2, 2014: 54.8 fishes/250m2, 2018: 58.8 fishes/250m2;

Middleton: 2011: 72.8 fishes/250m2, 2014: 59.6 fishes/250m2, 2018: 60.0

fishes/250m2).

• The abundance of endemic fishes (Amphiprion mccullochi, Chaetodon

tricinctus, and Coris bulbifrons) varied greatly among study sites, but have

changed very little from 2011 to 2018. However, the abundance of C. tricinctus

at Elizabeth Reef has declined from 1.89 fish/100m2 in 2014 to 1.28 fish/100m2

in 2018, despite increases in coral cover during this period.

• The abundance of Galapagos sharks (Carcharinus galapagensis) at Elizabeth

Reef in 2018 (10.2 individuals/ha ± 4.0 SE) was higher than recorded in 2014

(6.58 individuals/ha ± 1.69 SE). In contrast, the abundance of C. galapagensis

at Middleton in 2018 (8.9 individuals/ha ± 2.4 SE) was lower than recorded in

2014 (17.11 individuals/ha ± 2.99 SE).

• The abundance of black cod (Epinephelus daemelii) at Elizabeth (1.50 fish/ha ±

0.35 SE) and Middleton Reefs (1.41 fish/ha ± 0.55 SE) in 2018, was lower than

recorded in 2014 (2.50 fish/ha ± 0.55 SE and 2.24 fish/ha ± 0.53 SE,

respectively).

2 Recommendations

1. Recurrent monitoring, using consistent and standardised protocols, is

fundamental in assessing the status and trends of coral reef habitats and

associated fish and non-coral invertebrate assemblages at Elizabeth and Middleton

Reefs. Nonetheless, it is very difficult to establish specific causes of any marked

changes in coral reef environments when the interval between recurrent surveys is

greater than a year, and up to 4-5 years. Importantly, if or when there are major

disturbances (e.g., outbreaks of crown-of-thorns starfish or climate-induced coral

bleaching) affecting these reefs, the current monitoring regime will be insufficient to

effectively assess the specific effects of these important and extremely influential

events.

2. Unpredictable and acute disturbances (e.g., outbreaks of crown-of-thorns

starfish or climate-induced coral bleaching) represent the greatest and most

immediate risk to the status and condition of shallow reef environments and

assemblages at Elizabeth and Middleton Reefs. It is critical therefore, that ongoing

monitoring is undertaken to assess these risks, and that there is effective capacity

to respond in a timely fashion to assess localised impacts and associated changes

in reef assemblages. For example, monitoring should be undertaken during, or

immediately following, periods of extreme temperatures and elevated bleaching

risk (NB. In compiling this report it has become apparent that the risk of bleaching

has increased since we undertook surveys in February/ March and the

accumulated heat stress this year is among the highest ever recorded for Elizabeth

and Middleton Reefs). In the absence of frequent or responsive surveys, the utility

of occasional visitors should be maximised, both at Elizabeth and Middleton Reefs.

At present there is an obligation for visitors to Elizabeth Reef to report on reef

condition (owing to the current management zoning), and this requirement should

should continue to be a requirement for all visitors to Elizabeth (proposed

TELHIRUZ03) whether undertaking fishing or not, as well as being extended to

include visitors to Middleton Reef. Visitor reports (however infrequent) are invaluable to potentially alert managers to any apparent concerns regarding threats

to coral and ecosystem health.

3. The black cod (Epinephelus daemelii) is listed as a vulnerable species

within NSW and is totally protected from any form of fishing. Recent surveys have

revealed declines in abundance of E. daemelii at both Elizabeth and Middleton

Reefs since 2014, with no E. daemelii being recorded at the lagoon sites on

Middleton Reef in 2018. Declines in the abundance of this species are concerning

given that there are very limited numbers of E. daemelii remaining elsewhere

throughout their geographic range. As such, much more information is needed on

the biology and ecology of this species, both at Elizabeth and Middleton Reefs and

at other nearby reefs (e.g., Lord Howe Island) to understand the population

dynamics, movement patterns and vulnerability of E. daemelii. Moreover, greater

efforts may be warranted to highlight the protected status of Black cod to visiting vessels and recreational fishers to assist in reducing incidental by-catch and any

fishing related mortality.

4. Recurrent surveys to assess the status and trends in coral health and reef

condition are conditional upon effective collaborations between coral biologists and

reef ecologists (not necessarily from James Cook University), with managers from

Commonwealth (the Director of National Parks) and state agencies (NSW

Department of Primary Industries). An important component of these collaborations

is to ensure all parties are present and represented during each and every

expedition (especially given limited connectivity whilst in the field), to facilitate

appropriate responses to emerging issues (e.g., re-directing survey effort to

document impacts of specific threats and disturbances). This is especially critical

for Elizabeth and Middleton Reefs given the limited frequency of surveys, and

potential for large changes to become apparent between successive surveys.

Table of Contents

1. Executive Summary 3

2. Recommendations 5

3. Introduction 8

3.1 Elizabeth and Middleton Reefs (Lord Howe Marine Park) 9

3.2 History of Coral Reef Surveys at Elizabeth and Middleton Reefs

12

3.3 Objectives and scope 14

4. Methods 15

4.1 Coral and reef habitats 15

4.2 Non-coral invertebrates 19

4.3 Coral reef fishes 20

4.4 Data analyses 21

5. Findings 22




6. Conclusions 51




7. Acknowledgements 57

8. References 58

3 Introduction

Coral reefs are among the most threatened natural ecosystems globally, owing to a

long-history of anthropogenic degradation and exploitation (Jackson et al. 2001;

Pandolfi et al. 2003), as well as their extreme vulnerability to global climate change

(Hughes et al. 2017a, 2018). Even before recent effects of global climate change

(which has caused successive years of severe coral bleaching in many coral reef

regions), one-fifth of the world’s coral reefs had been effectively destroyed,

meaning that coral cover had been reduced to such low levels (<5%) that these

systems were no longer effectively functioning as coral reefs, or that the reefs have

been completely removed and/ or buried by mining or land reclamation (Wilkinson

2008). In east Africa, south-east Asia, and the central and southern Caribbean, a

disproportionate number of coral reefs have been lost due high levels of sustained

human activities, including chronic pollution, eutrophication, sedimentation,

overfishing and/or destructive fishing practices (Pandolfi et al. 2003; Wilkinson

2008). Even isolated coral reefs that are well removed from effects of coastal

development are being increasingly affected by insidious effects of global fisheries

(Graham et al. 2010) and ongoing climate change (Hughes et al. 2003; Hoegh-

Guldberg et al. 2007).

Relatively isolated (Gilmour et al. 2013) and high latitude (Beger et al. 2014) coral

reef ecosystems are increasingly viewed as important refuges, and considered to

be relatively less susceptible to direct anthropogenic pressures and global climate

change, respectively. However, when isolated reefs are subject to major

disturbances recovery may be highly constrained compared to well-connected reef

ecosystems because there is less opportunity for larval replenishment from other

unaffected reef areas and populations (Graham et al. 2006; Smith et al. 2008,

Gilmour et al. 2013). High-latitude reefs systems may also be more (not less)

susceptible to global climate change because they are disproportionately affected

by changing seawater chemistry (specifically, ocean acidification and declining

aragonite saturation), which may impose increasing constraints on calcification and

reef accretion (Anderson et al. 2015), because there is a natural gradient of

declining aragonite saturation with increasing latitude. There is however, evidence

that corals subject to naturally higher fluctuations in temperature, are more

resistant to ocean warming (Oliver and Palumbi 2011), and potentially much less

susceptible to coral bleaching. Coral bleaching has been documented on high-

latitude reefs in Australia (e.g., Harrison et al. 2011) and Japan (Nishiguchi et al.

2018) though the relevant susceptibility and severity of bleaching (compared to

low-latitude reefs) is equivocal.

The foremost management strategy to address increasing anthropogenic

pressures on coral reefs (as for other marine and coastal ecosystems) is marine

protected areas (MPAs) or marine parks (Graham et al. 2011, Edgar et al. 2014),

which limit or prohibit extractive activities within specified areas. The effective

implementation (combining both designation and appropriate compliance) of

marine parks, and in particular no-take areas, can have significant benefits for

abundance and diversity of fisheries-target species, especially in large, long-

established and well-managed (well enforced) marine parks (e.g., Russ and Alcala

2010, Edgar et al. 2014). However, given the widespread and accelerating

degradation of coral reef ecosystems, marine parks are increasingly expected to

provide additional benefits beyond protection of major targeted species (Graham et

al. 2011), specifically related to preserving key ecological functions and maximising

ecosystem resilience. While there is increasing evidence that marine parks do

contribute to enhancing the ecological integrity and resilience of coral reef

ecosystems, it is also apparent that this alone may be insufficient to effectively

conserve these critically important habitats (Hughes et al. 2017b).

3.1 Elizabeth and Middleton Reefs (Lord Howe Marine Park)

Elizabeth and Middleton Reefs located within the Tasman Sea are the world’s

southernmost open ocean platform reefs, and supporting a unique mix of tropical

and subtropical species (Choat et al. 2006). These emergent reef systems are

contained within the Lord Howe Marine Park (Figure 1). The northernmost zone

encompassing Middleton Reef is a Sanctuary Zone, which allows “passive use by

the public”, but no fishing. Recreational fishing is permitted in the southern “Habitat

Protection Zone” that encompasses Elizabeth Reef, though fishing pressure is

presumed to be very low, owing to its isolation.

Figure 1: The spatial extent and location of specific management zones within the Lord Howe Marine Park. Notably, Middleton Reef is a Sanctuary Zone (IUCN Ia), while Elizabeth is classed as Habitat Protection Zone (IUCN II).

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Elizabeth and Middleton Reefs are critically important coral reef environments,

owing to their location and isolation. These reefs support a number endemic

species or species that are generally rare over most of their geographic range.

Most notably, Elizabeth and Middleton Reefs are renowned for being the last

remaining stronghold for the black cod (Epinephelus daemelii), which occurs

throughout southwestern Pacific, but has been overfished throughout much of its

range (Choat et al. 2006). Epinephelus daemelii is listed as vulnerable in New

South Wales, and is also listed as a ‘vulnerable’ species under the Environment

Protection and Biodiversity Conservation Act 1999.

3.2 History of Coral Reef Surveys at Elizabeth and Middleton Reefs

There have been at least 13 scientific surveys undertaken at Elizabeth and/ or

Middleton Reefs since 1979 (Table 1), including this survey and corresponding

assessments by Reef Life Survey. Collectively, these surveys represent the

longest running and most intensive temporal series of surveys of coral reef habitats

across Australian Marine Parks – the 58 marine parks managed by the Director of

National Parks and Parks Australia (Hoey and Pratchett 2017). Recurrent surveys

of the shallow reef environments have revealed very gradual, but sustained,

recovery of coral cover at Elizabeth and Middleton Reefs from 10% cover in 1994

up to 20-30% in 2014 (Hoey and Pratchett 2017). Low levels of coral cover

reported in the 1990s are widely attributed to coral depletion caused by a localised

outbreak of crown-of-thorns starfish in the 1980s, where high densities of these

corallivorous starfishes were documented by Harriot (1998). While the subsequent

recovery of coral assemblages is encouraging, it is apparent that rates of coral

recovery at these locations are slow, especially compared with isolated reefs at

lower latitudes (e.g., Scott Reef, Gilmour et al. 2013). Constraints on rates of

recovery are probably due to low levels of coral recruitment and population

replenishment (Pratchett et al. 2015), as well as environmental constraints on coral

calcification and growth (Anderson et al. 2015). It is possible, however, that

recruitment rates will increase in accordance with the size and abundance of adult

corals (Gilmour et al. 2013), leading to marked increases in rates of recovery once

local coral cover reaches certain thresholds.

Table 1. Marine surveys undertaken at Elizabeth and/ or Middleton Reef since

1979. For a comprehensive overview of surveys conducted prior to 1979 see

Australian Museum (1992).

No. Year Locations Purpose Reference

1 1979 Elizabeth & Middleton

Coral diversity Australian Museum 1992


Coral diversity Australian Museum 1992

3 1981 Middleton Assess impacts of COTS

Harriot 1998


Biodiversity assessment

Australian Museum 1992


Marine ecological survey

Choat et al. unpublished data

6 2003 Elizabeth Marine ecological survey

Oxley et al. 2004



Choat et al. 2006


Rapid assessment of reef health

Hobbs and Feary 2007



Pratchett et al. 2011


Reef Life Survey (RLS)

Stuart-Smith et al. 2017



Hoey et al. 2014



This report


Reef Life Survey (RLS)

3.2 Objectives and scope

The purpose of this study was to assess the status and trends of shallow coral reef

ecosystems and organisms at Elizabeth and Middleton Reefs, within the Lord

Howe Marine Park, using standardised methods and at fixed locations to allow

meaningful comparisons across 2011, 2014 and 2018. Replicate area-based

surveys (belt transects) were undertaken to quantify the contemporary abundance

of select fish species, as well as ecologically and economically important mobile

invertebrates (e.g., holothurians). Coral cover and composition, as well as overall

habitat structure, were also quantified along the same transects (n = 4) in two

distinct depth habitats in 2011, 2014 and 2018. In 2018, we re-visited and

successfully surveyed 16 sites that were surveyed in 2011 and 2014, and also

extended surveys to include three new sites at Elizabeth Reef, including additional

sites on the exposed reef front where adverse weather has prohibited prior

surveys.

These surveys provide rigorous quantitative information on:

i) benthic cover and composition, including estimates of percentage cover for hard

(Scleractinian) and soft (Alcyonarian) corals, macroalgae, and other sessile

organisms

ii) structural complexity of reef habitats

iii) coral health and injuries caused by coral disease, corallivorous invertebrates

(e.g., Acanthaster spp and Drupella spp), or reef fishes

iv) abundance of small/ juvenile corals (<5cm diameter), as a proxy of coral

recruitment and population replenishment,

v) size and abundance of large iconic species, including black cod (Epinephelus

daemelii) and Galapagos shark (Carcharinus galapagensis),

vi) abundances of other reef fishes including the endemic doubleheader wrasse

(Coris bulbifrons), rabbitfishes, drummers, damselfishes and butterflyfishes, and

vii) abundance of holothurians, urchins and other ecologically or economically

important reef-associated invertebrates.

4 Methods

This study was conducted at Elizabeth and Middleton Reefs from February 24th to

March 3rd, 2018. Sampling was undertaken at a total of 19 sites across both reefs

(Table 2; Figure 2). Three new sites were added at Elizabeth Reef (sites 8, 9, and

10) to provide better representation of exposed reef front habitats, and take

advantage of the relatively calm conditions. At each site, surveys were conducted

within each of two depth zones, i) the reef crest at 2-4m and ii) the reef slope at 6-

10m. In each depth zone at each site, four replicate 50-m transects were run

parallel to the depth contour, with up to 10 metres between successive transects (n

= 152 transects in total across both reefs). Along each transect (a) benthic cover

and composition, (b) reef topographic complexity, (c) juvenile coral densities (as a

proxy for coral replenishment), (d) coral condition/health, (e) herbivorous fish

assemblages, (f) endemic and site-attached fish densities, (g) apex predator

densities, and (h) mobile invertebrates were quantified using the same methods

used in 2011 and 2014.

4.1 Coral and reef habitats

Benthic cover and composition - Point-intercept transects (PIT) were used to

quantify benthic composition, recording the specific organisms or habitat types

underlying each of 100 uniformly spaced points (50cm apart) along each transect.

All corals and macroalgae were identified to genus. For survey points that did not

intersect corals or macroalgae, the underlying habitat was be categorised as either,

turf algae (< 5mm in height), crustose coralline algae (CCA), rubble or sand.

Topographic complexity - Topographic complexity was estimated visually at the

start of each transect, using the six-point scale formalised by Wilson et al. (2007),

where 0 = no vertical relief (essentially flat homogenous habitat), 1 = low and

sparse relief, 2 = low but widespread relief, 3 = moderately complex, 4 = very

complex with numerous fissures and caves, 5 = exceptionally complex with

numerous caves and overhangs.

Figure 2: Map showing the location of the study sites. (a) Geographic location of Elizabeth and Middleton reefs off Australia’s east coast. (b) Locations of the nine study sites on Middleton Reef. (c) Location of the seven existing study sites and three additional study sites at Elizabeth Reef. (d) Schematic diagram of reef cross-section showing the location of the three habitats and two depths sampled. 16 (out of 19) sites are explicitly matched to those surveyed in the 2011 (Pratchett et al. 2011) and 2014 (Hoey et al. 2014); Yellow circles = reef front locations, blue squares = back reef locations, and green stars = lagoon locations. “*” indicates new sites at Elizabeth Reef sampled in 2018.

Table 2. Sites surveyed at Elizabeth and Middleton Reefs during the 2018 marine survey (24th February – 4th March, 2018). GPS co-ordinates are given for each site, as well as brief site descriptions

Reef Habitat Site GPS Habitat description

Elizabeth Reef Front

1 29º 57.161’S; 159º 01.295’E

Marked step down at 6m, then gentle slope to >11m. Lots of deep holes and gutters at 4m.


2 29º 56.600’S; 159º 01.100’E

Gentle slope to 15m, then sandy gutters. Deep holes and gutters at 4m.


3 29º 55.970’S; 159º 01.390’E

Distinct spurs up to 50m wide separated by sand filled gutters. High relief at crest (3m) with wide gutters filled with coral boulders.


9 29o 57.423’S 159o 01.678’E

Gentle slope to 10m, then sharp drop-off and lots of holes. Lots of deep holes and gutters at 4m


10 29o 57.366’S; 159o 07.651’E

Very wide slope with rolling hills and wide valleys. Very flat at 3m with no distinct crest. Occasional deep gutters.

Elizabeth Back Reef

4 29º 55.616’S; 159º 02.406’E

Moderate slope to 8m then steps down to sand at 10-12m. Deep gutters at 3-4m, otherwise very flat.

Elizabeth Back Reef

5 29º 55.113’S; 159º 03.635’E

Gentle slope to 8m, then steps down to sand at 11m. Lots of patch reefs out over sand. Deep holes and gutters at 4m.

Elizabeth Back Reef

8 29o 54.613’S; 159o 04.132’E

Steep slope to sand/rubble at 12m. High relief at crest (2m) and lots of discontinuities in reef matrix.

Elizabeth Lagoon 6s 29º 56.148’S; 159º 05.346’E

Shallow lagoonal reef with very limited relief, though mostly contiguous carbonate structure

Elizabeth Lagoon 6d 29º 56.079’S; 159º 05.596’E

Distinct rock/rubble bank that drops down on to sand at ~7m, though deepens towards lagoon entrance

Elizabeth Lagoon 7 29º 56.170’S; 159º 03.097’E

Rubble reef flat with lots of arborescent Acropora, dropping to 8m on sand.

Middleton Reef Front

5 29º 26.880’S; 159º 03.310’E

Located due north of the bow of Runic. Gentle incline with lots debris.


6 29º 28.637’S; 159º 07.296’E

Relatively narrow reef slope compared to other reef front locations, and apparent drop off beyond deep transects.


7 29º 25.803’S; 159º 07.988’E

Very gentle incline (>100 m between slope and crest habitat). Lots of debris from wreck in grooves near crest.


8 29º 29.086’S; 159º 04.597’E

Reef front location with characteristic wide reef slope, and deep grooves extending to reef flat.


9 29º 27.262’S; 159º 08.532’E

Reef front location with characteristic wide reef slope, and deep grooves extending to reef flat.

Middleton Back Reef

1 29º 26.610’S; 159º 05.860’E

Located near wreck. Narrow reef slope which steps up sharply to reef crest.

Middleton Back Reef

2 29º 27.177’S; 159º 05.061’E

Wide reef slope with gentle incline, but steps down on to sand at 12m.

Middleton Lagoon 3 29º 27.223’S; 159º 03.940’E

Discrete reef with extensive reef top (1m depth) lactated among sand (3m depth).

Middleton Lagoon 4 29º2 6.574’S; 159º 06.901’E

Reef edge on northern margin of Blue Holes, just behind two large bommies.

Coral recruitment – Densities of juvenile corals (≤5 cm maximum diameter,

following Rylaarsdam 1983) were recorded within a 1m wide belt along the first

10m of continuous reef habitat on each transect. Densities of juvenile corals are

intended to provide a proxy for population replenishment (Trapon et al. 2013a),

incorporating variation in both settlement and early post-settlement mortality.

Coral health - To assess local impacts of the corallivorous crown-of-thorns starfish

(Acanthaster cf. solaris), pin-cushion starfish (Culcita novaeguineae) and the

corallivorous gastropod Drupella spp., as well as other large and potentially

destructive coral predators such as excavating parrotfishes (Choat et al. 2006,

Hoey and Bellwood 2008), any evidence of feeding scars were recorded 1m either

side of the 50m transect path (i.e., 100m2). In addition to signs of corallivory, any

evidence of adverse coral health, such as coral bleaching, and coral disease were

also recorded within these 100m2 belt transects.

4.2 Non-coral invertebrates

Non-coral invertebrates, including potential coral predators (e.g., crown-of-thorns

starfish, pin-cushion starfish, and coral snails) as well as ecologically and

economically important mobile invertebrates (mainly, urchins and holothurians)

were surveyed in a 2m wide belt along each transect, giving a sample area of

200m2. Coral predators are potentially important contributors to coral reef health

and habitat structure, especially during periods of elevated densities of coral

predation (Pratchett et al. 2014a). Importantly, outbreaks of crown-of-thorns

starfish have occurred previously (in the 1980s) at Elizabeth and Middleton Reefs

and caused extensive coral loss. The eastern Pacific crown-of-thorns starfish is

now recognised as being morphologically and genetically distinct from the

predominant Indian ocean species (Acanthaster planci) and is nominally referred to

as Acanthaster cf. solaris (Pratchett et al. 2017). Acanthaster cf. solaris has been

frequently sighted at Elizabeth and Middleton Reefs, as well as at Lord Howe

Island and Ball’s Pyramid, though densities are generally very low.

Aside from coral predators, we also surveyed other conspicuous (non-cryptic)

species of starfishes (asteroids), sea urchins (echinoids), sea cucumbers

(holothurians), clams (Tridacna spp.) and sea anemones. For all these organisms,

the number of individuals was counted within belt transects, providing density

estimates to compare among surveys. Sea urchins can have a major influence on

the habitat structure of coral reef environments (e.g., McClanahan and Shafir 1990;

Eakin 1996). Like herbivorous fishes, larger species such as Diadema spp. may be

important in removing algae that would otherwise inhibit coral growth and/or

settlement (Edmunds and Carpenter 2001). At high densities, however, intensive

grazing by sea urchins may have negative effects on habitat structure, causing

significant loss of corals, reducing topographic complexity of reef habitats

(McClanahan and Shafir 1990), can lead to a net erosion of the reef carbonates

(Glynn et al. 1979; Eakin 1996). Sea urchins can at times be particularly abundant

on high latitude reefs, and outbreaks of sea urchins have been recorded in this

region. For example, populations of the collector urchin Tripneustes gratilla

underwent an outbreak at Lord Howe Island in 2007-08, causing localized declines

in the abundance of many red and brown algae (Valentine and Edgar 2010).

4.3 Coral reef fishes

Herbivorous reef fishes – Functionally important coral reef fishes (mostly, roving

herbivores) were surveyed within a 5m wide path along replicate 50m transects

(i.e., 250m2). All surgeonfishes (Acanthuridae), parrotfishes (Labridae), drummers

(Kyphosidae), and rabbitfishes (Siganidae), were surveyed while deploying the

transect tape. Individual fishes were identified to species and placed into 5cm size

categories. Fish densities were converted to biomass using published length-

weight relationships for each species, following Hoey and Bellwood (2009).

Endemic and site-attached reef fishes – Smaller more site-attached species

from the families Chaetodontidae (butterflyfishes) and Pomacentridae

(damselfishes), and juvenile double-header wrasse (Coris bulbifrons) were counted

along a 2m wide path along each transect (i.e., 100m2) at every study site. Adult

double-header wrasse (C. bulbifrons) were surveyed in a 5m wide belt along each

transect (i.e., 250m2) at each study site. Mostly, we were interested in the local

abundance of endemic species (Table 3).

Table 3: Endemic fishes that were surveyed at Elizabeth and Middleton Reef, following

Hobbs and Feary (2007).

Species Common name Distribution

Coris bulbifrons Doubleheader wrasse

Lord Howe, Norfolk, Middleton, Elizabeth, NSW

Chaetodon tricinctus Three striped butterflyfish

Lord Howe, Norfolk, Middleton, Elizabeth

Amphiprion mccullochi McCulloch’s anemonefish

Lord Howe, Middleton, Elizabeth, NSW, Norfolk

Epinephelus daemelii Black cod, saddletail grouper

Lord Howe, Middleton, Elizabeth, SE Australia, Kermadec, Northern New Zealand

Apex predators - To effectively survey larger and highly mobile reef-associated

fishes (namely black cod and sharks) 250 - 500m long underwater visual transects

were conducted along the reef at each study site, following Robbins et al (2006).

Transects were run approximately parallel with the reef crest and covered a depth

range of approximately 4 – 20m. All black cod (E. daemelii) and sharks (primarily

the Galapagos shark, Carcharinus galapagensis) were recorded within 10-m of the

transect path, giving a total sample area of 10,000m2 (1 hectare) for a 500m

transect, and 5,000m2 (0.5 hectare) for a 250m transect. Two transects were

conducted at each site, one 500m in length and the other 250m in length.

4.4 Data analyses

Recurrent sampling at the same locations and using the same sampling protocols

to record a large number of variables (e.g., individual and combined cover of 85

categories of sessile organisms and substratum types, individual abundance of 37

genera of juvenile corals) is generating considerable and increasingly complex

data. For the purpose of this report we have extracted only the most salient

information necessary to assess current status and trends in a small number of key

summary variables (e.g., live coral cover). However, very preliminary analyses

were also conducted to assess the significance of temporal variation, relative to

spatial variation within and among reefs, for key summary variables. These

analyses were conducted using Generalised Linear Models (GLM) in R with

increasing complexity of models that include year, reef, zone, and site or habitat.

We then used model comparisons based on Akaike Information Criterion with

sample correction (AICc) to select the best model and assessed the relative

importance of the different predictor variables. Notably, these analyses show that

year is an important variable (reflecting variation among surveys conducted in

2011, 2014 and 2018) in accounting for overall variation in coral cover, showing

that the current sampling design is effective for assessing temporal trends in the

ecosystem state and condition of these systems.

5 Findings


Benthic cover and composition - In 2018, mean cover of hard (Scleractinian)

corals recorded at Elizabeth Reef was 39.95% (±1.72 SE), ranging from 22.75

(±3.24 SE) within lagoon habitats, up to 46.00% (±2.31 SE) at pre-existing reef

front locations (Figure 3a). Coral cover at Middleton Reef (26.62% ±1.87 SE) was

lower than at Elizabeth Reef, mainly due to low coral cover (14.5% ±1.89 SE) in

back reef locations (Figure 3a).

Overall coral cover at Elizabeth and Middleton Reefs has increased >40% since

2014 and is now higher (33.76% ±1.37 SE) than was recorded in 2011 (26.16%

±1.47 SE). The annual geometric rate of increase in coral cover from 2014 to 2018

equates to 9.2% for Elizabeth and 9.9% at Middleton Reef. Moreover, coral cover

has increased in all habitats since 2014 (Figure 3a). The greatest increase has

occurred within the lagoon at Middleton Reef, where recorded coral cover has

more than doubled from 15.08% (±3.50 SE) in 2014 up to 32.42% (±3.72 SE) in

2018.

Mean cover of macroalgae at Elizabeth and Middleton Reefs was 11.43% (±1.56

SE) and generally similar (<10% cover) across most habitats (Figure 3b). Both the

cover and the predominant type of macroalgae found at each site was largely

unchanged since 2014.

Figure 3. Temporal changes (2011 - 2018) in average cover (±SE) of (a) scleractinian (hard) corals, and (b) macroalgae across three different habitat types (see Figure 2 and Table 2 for details) at Elizabeth and Middleton Reefs.

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Topographic complexity - Topographic complexity is generally low (consistently

<3.0) across all sites at Elizabeth and Middleton Reefs. There was however

evidence of very moderate increases in topographic complexity within some

habitats (back reef and reef front) at Elizabeth Reef since 2014 (Figure 4). At

Middleton Reef, however, structural complexity was largely unchanged relative to

2014, and was actually lower for Reef Front habitats in 2018 compared to 2014.

Figure 4. Temporal changes in the topographic complexity (±SE) of reef substratum across three different habitat types (see Figure 2 and Table 2 for details) at Elizabeth and Middleton Reefs. Topographic complexity was assessed visually using a 6-point scale (following Wilson et al. 2007). 0 = flat homogenous habitat, 5 = exceptionally complex.

Statistical analyses, using GLM and model selection, show that coral cover,

macroalgal cover, topographic complexity, and densities of juvenile corals (which is

discussed later) all vary with year of sampling (2011, 2014, and 2018), with Year

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included in the best models for all variables (Figure 5). Moreover, Year was most

important variable for explaining variation in coral cover and topographic

complexity. The most important variables for explaining variation in cover of

macroalgae were Reef, Depth and Habitat, whereas variation in densities of

juvenile corals were explained mostly by Site, and then Depth (or zonation).

Year Reef Depth Habitat Site

Live cover (%) of Scleractinian coral

Overall densities of juvenile corals

Live cover (%) of macroalgae

Topographic complexity

Figure 5. Variable selection and importance for alternative measures of coral habitat structure. All variables included in the selected model are coloured from yellow to red in terms of relative importance. Where there is no colour (i.e., Grey or white background colours) the factors was excluded from the best model.

Coral recruitment – The average density of juvenile corals in 2018 was 12.51

colonies per 10m2 (± 0.56 SE), which is slightly higher than was recorded in 2014

(11.26 ± 0.71 SE). However, temporal trends in the abundance of juvenile corals

are variable among reefs and habitats (Figure 6). The highest densities of juvenile

corals are generally recorded in reef front habitats at Elizabeth Reef, though the

densities of juvenile corals in these habitats (14.79 ± 1.31 SE) were much lower in

2018 than had been recorded previously (Figure 6). At Middleton Reef, densities of

juvenile corals in back reef habitats (13.37 ± 2.24 SE) were higher than have been

recorded previously, but these increases were offset by a decline in the densities of

juvenile corals on the Reef Front since 2014 (Figure 6).

Figure 6. Changes in (A) overall densities and (B) composition of juvenile corals (<5cm maximum diameter) three different habitat types (see Figure 2 and Table 2 for details) at Elizabeth and Middleton Reefs. Densities of juvenile corals (hard corals only) were recorded using replicate 10 x 1m belt transects.

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Juvenile coral assemblages at Elizabeth and Middleton Reefs are dominated by

Acropora, Pocillopora, Isopora and Porites. The relative abundance of these taxa

has been relatively consistent from 2011 to 2018, though there was an apparent

decline in abundance of juvenile Acropora in 2014 (Figure 6). It should be noted

that densities of juvenile Acropora recorded in 2018 (2.24 ± 0.07 SE) were

equivalent to those recorded in 2011 (2.39 ± 0.08 SE). Also, densities of juvenile

Porites increased from 2011 (0.75 ± 0.13 SE) to 2014 (1.94 ± 0.33 SE), and

remained high in 2018 (Figure 6). Local variation in the abundance of Isopora is

much more pronounced than for other dominant taxa (as evident by the very large

SE), reflecting patchiness in their distribution and abundance, but also their

disproportionate abundance in specific habitats, shallow reef fronts. Overall

densities of juveniles for other less common genera (e.g., Seriatopora, Stylophora

and Acanthastrea) have remained fairly constant across the three survey periods

(2011, 2014 and 2018).

Coral health - There were no definitive or confirmed incidences of coral disease

recorded at Elizabeth and Middleton Reefs in 2018, though recent and extensive

mortality of several distinct colonies of Acropora and Isopora corals in the lagoon

(Site 3) at Middleton Reef, may have resulted from disease (most likely White

Syndrome). The problem with white syndrome is that rapid tissue loss may occur in

absence of any clear signs of disease (Sussman et a. 2008, Sweet and Bythell

2012) and are indistinguishable from tissue removal caused by coral predators

when observed only after whole coral mortality. We could not clearly establish the

cause of this recent coral mortality, but given the apparent lack of coral predators

(e.g., crown-of-thorns starfish) at this site, the most likely causes are coral disease

and/ or coral bleaching (see below).

Bleached corals were prevalent and conspicuous, especially in the back reef (Site

3) and lagoon (Site 7) at Elizabeth Reef, when surveyed on February 19th, 2018.

Bleaching was severe, but restricted to select coral species, mainly Stylophora cf.

subseriata (Figure 7), which is among those corals that are known to be particularly

prone to bleaching (McClanahan et al. 2004). This is concerning given that it there

was significant potential for further accumulation of heat stress prior to seasonal

cooling of ocean temperature in April/May. Accordingly, we compiled NOAA

satellite sea-surface temperature (SST) data to explicitly consider the accumulated

heat stress (measured as degree heating weeks; Liu et al. 2003) in 2018 compared

to other recent years. We find that heat stress continued to accumulate well

beyond the timing of our surveys (late February/ early March), when bleaching was

already apparent (Figure 7), and the risk of bleaching is higher in 2018 than it has

been in recent years.

Figure 7. Bleaching risk for Elizabeth Reef; Severe, but selective, coral bleaching was observed within the lagoon (Site 7) at Elizabeth Reef on February 19th. 2018. Virtually all colonies of Stylophora (shown here) were completely bleached at this location, along with a proportion of colonies of Montipora and Acropora. Accumulated heat stress (in Degree Heating Weeks) for Elizabeth Reef in 2018 (DHW>3) is the higher than recorded in previous years (2016-17).


Coral predators - Densities of coral-feeding invertebrates, specifically crown-of-

thorns starfish (Acanthaster cf. solaris), the pin cushion starfish (Culcita

novaeguineae) and coral snails (Drupella spp.) were very negligible at Elizabeth

and Middleton Reefs. In 2018, only one crown-of-thorn starfish, one pin cushion

starfish, and two individual coral snails were recorded across all 155 transects.

Despite increased search area (owing to the addition of three new sites at

Elizabeth Reef), these numbers are lower than were recorded in 2011 and 2014,

though abundances of corallivorous species have been very low throughout (Table

4). The single crown-of-thorns starfish that was recorded in 2018 (as well as one

additional individual that was found just off the transect) was located in the back

reef (Site 4) at Elizabeth Reef. Notably, this is the same site where crown-of-thorns

starfish have been sighted during previous surveys. This suggests that there is a

small persistent remnant population restricted to this area that are being re-

surveyed each year.

In accordance with the low densities of A. cf. solaris, Drupella spp. and C.

novaeguineae, the incidence of feeding scars on live coral colonies across all 155

transects was negligible. Recent coral injuries that were detected, were not

consistent with feeding scars caused by the above mentioned coral-feeding

invertebrates, but represent physical removal of many (if not all) branches,

presumably caused by feeding activities (i.e., ‘cropping’) by fishes, most likely

caused by the excavating parrotfish, Chlorurus microrhinos and C. frontalis (Hoey

et al. 2014). The overall incidence of this cropping in 2018 (29 colonies, 0.23

colonies per transect) was substantially lower than recorded in 2014 (100 colonies,

0.81 colonies per transect), and largely restricted to exposed reef front locations at

Middleton Reef. Moreover, affected corals were almost exclusively Acropora. This

damage is not cause for concern and is likely to reflect the normal background

levels of coral predation by excavating parrotfishes.

Table 4: Total abundance of coral-feeding invertebrates recorded at Elizabeth and Middleton Reefs, from 2011-2018.

Species 2011 2014 2018 Total

No. transects 124 124 155 403

Crown-of-thorns starfish (Acanthaster cf. solaris)

1 4 1 6

Pin cushion starfish (Culcita novaeguineae)

3 6 1 10

Coral snails (Drupella spp.)

5 3 2 10

Sea cucumbers (Holothurians) - A total of 839 sea cucumbers were recorded

across all transects (n = 155) in 2018, corresponding with a mean density of 5.41

(± 0.95 SE) individuals per 200m2, which is higher than recorded in 2011 (3.29 ±

0.77 SE) and 2014 (5.06 ± 0.93 SE). The dominant species were Holothuria edulis

(437/ 839 individuals) and Holothuria atra (319/ 839), both of which exhibit

increasing trends in abundance (Figure 8). Overall densities of sea cucumbers

were highest in the lagoon, coinciding with the availability of sand, as opposed to

consolidated reef matrix. Densities of sea cucumbers were also higher at Middleton

Reef than at Elizabeth Reef (Figure 8).

Sea urchins (Echinoids) - >10,000 sea urchins (mostly Echinostrephus sp. and

Diadema savignyi) were counted across 155 transects at Elizabeth and Middleton

Reefs in 2018. Diadema savignyi (which was previously misidentified as D.

setosum) is a large, mobile and nocturnally active herbivore that is most abundant

in the Back Reef at Middleton Reef (Figure 10a). Densities of D. savignyi recorded

in 2018 within this habitat (17.5 ± 6.63 SE urchins per 200m2) are a fraction of

maximum densities (171.0 ± 47.7 SE) recorded in 2014. Densities of

Echinostrephus sp., which is a small burrowing urchin with long thin spines are

found predominantly outside of the lagoon, and are common in both Back Reef and

Reef Front habitats (Figure 9). Overall densities of Echinostrephus sp. were higher

in 2018 than recorded previously, largely due to high densities in the Back Reef at

Middleton Reef (Figure 10).

Figure 8. Changes in (A) overall densities and (B) composition of sea cucumbers at three different habitat types (see Figure 2 and Table 2 for details) at Elizabeth and Middleton Reefs. Densities of sea cucumbers are recorded along replicate 50 x 2m belt transects.

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5.3 Coral reef fishes

Roving herbivores - The overall abundance of herbivorous fishes was very similar

between reefs in 2018, averaging 58.8 (± 6.1 SE) fishes/250m2 on Elizabeth and

60.0 (± 5.3 SE) fishes/250m2 on Middleton Reef (Figure 11a). The abundance of

roving herbivorous fishes did differ between habitats and depths (Figure 11a),

being consistently higher on the reef crest than the reef slope at exposed reef front

sites on both Elizabeth and Middleton Reefs, but displayed limited difference

among depths at either the lagoon or back reef (Figure 11a). These patterns are

consistent with numerous studies on tropical and subtropical reefs that have

demonstrated the abundance and biomass of herbivorous fishes is generally

greatest on shallow habitats on exposed reef fronts and decreases with both depth

and decreasing wave exposure (e.g., Russ 1984, 2003; Hoey and Bellwood 2008;

Hoey et al. 2013, 2018).

In contrast to abundance, the biomass of herbivorous fishes differed between

reefs, averaging 17.4 (± 2.0 SE) kg/250m2 on Elizabeth and 24.4 (± 3.8 SE)

kg/250m2 on Middleton Reef (Figure 11b). In addition to these differences in

biomass between the two reefs, herbivore biomass differed among habitats and

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reef zones, with biomass on the reef crest within the exposed reef front and back

reef habitats being 2- to 5-fold greater than the biomass of the shallow (i.e., reef

crest) habitat within the lagoons at both reefs (Figure 11b). Herbivore biomass was

more consistent among habitats on the reef slope. The different patterns in

abundance and biomass reflect differences in the body size among habitats. This

distinction is important as herbivore biomass has been shown to be a better

predictor of ecological impact than abundance (e.g., Bonaldo and Bellwood 2008;

Lokrantz et al. 2008; Hoey and Bellwood 2009). In contrast, comparable

abundances but lower biomass of herbivorous fishes within the lagoonal habitats is

reflective of the generally smaller bodied fishes, notably juvenile fishes, and

highlights the importance of the lagoons on these reefs as nursery habitats.

Figure 11. Spatial variation in (a) the abundance, and (b) the biomass of roving herbivorous fishes among reefs (Elizabeth and Middleton), habitat zones (Back reef, lagoon, reef front), and depths (crest, slope) in February-March 2018 (see Figure 2 and Table 2 for details). Data are means ± SE. The dashed lines represent overall reef means.

Overall, the abundance of herbivorous fishes recorded at Elizabeth and Middleton

Reefs in 2018 were remarkably similar to those recorded in both 2011 and 2014

(Figure 11a; Elizabeth: 2011: 67.3 fishes/250m2, 2014: 54.8 fishes/250m2, 2018:

58.8 fishes/250m2; Middleton: 2011: 72.8 fishes/250m2, 2014: 59.6 fishes/250m2,

2018: 60.0 fishes/250m2). Similarly, the abundance of herbivores within the back

reef and exposed reef front sites were relatively stable among surveys (2011, 2014

and 2018), whereas abundances of herbivorous fishes in the lagoon sites declined

from 2011 to 2014, and then increased again in 2018 (Figure 12a). The observed

changes in the lagoon sites was primarily attributable to changes in the abundance

of small-bodied grazing fishes, primarily juvenile parrotfishes, in these habitats

(Figure 12b), and may reflect temporal variation in the recruitment of these

species. Interestingly, previous declines in the abundance of grazing fishes at both

Elizabeth and Middleton Reefs from 2011 to 2014, have largely been reversed with

our abundance estimates for 2018 being broadly similar to those recorded in 2011

(Figure 12b). There have been some declines in the abundance of browsing fishes

at both Elizabeth and Middleton Reefs since 2014, however the abundances of

browsing fishes in 2018 are as high or higher than those from 2011 (Figure 12c).

The biomass of herbivorous fishes was relatively consistent at Middleton Reef over

the three surveys (2011: 31.4 kg/250m2; 2014: 25.2 kg/250m2; 2018: 24.5

kg/250m2; Figure 13a). In contrast, the biomass of herbivorous fishes at Elizabeth

reef declined by 43%, from 30.7 kg/250m2 in 2014 to 17.5 kg/250m2 in 2018

(Figure 12a). Despite this decline the biomass of herbivorous fishes on Elizabeth

Reef in 2018 was still greater than the herbivore biomass recorded in 2011 (13.2

kg/250m2). This temporal variation in total herbivore biomass was almost solely

attributable to changes in the biomass of browsing fishes (primarily the Pacific

Chub Kyphosus sectatris (formerly Kyphosus pacificus) and the Spotted Sawtail

Prionurus maculatus) (Figure 13c). In contrast, there was limited temporal variation

in the biomass of grazing fishes between 2014 and 2018 (Figure 13b).

Figure 12. Temporal variation (2011 - 2018) in the mean abundance of roving herbivorous fishes across three habitat types (see Figure 2 and Table 2 for details) at Elizabeth and Middleton Reefs. (a) Total herbivorous fishes, (b) Grazing fishes, (c) Browsing fishes. Error bars represent 1 SE.

Figure 13. Temporal variation (2011-2018) in the mean biomass of roving herbivorous fishes across three habitat types (see Figure 2 and Table 2 for details) at Elizabeth and Middleton Reefs. (a) Total herbivorous fish biomass, (b) Grazing fish biomass, (c) Browsing fish biomass. Error bars represent 1 SE.

A principal component analysis (PCA) revealed strong spatial structuring, but

limited temporal change, in the taxonomic composition of the herbivorous fish

assemblages on Elizabeth and Middleton reefs (Figure 14). The first two axes of

the PCA explained 39.4 % of the total variation in composition of herbivore

assemblages, with the exposed reef (or reef front) crest sites clearly separated

from all lagoonal sites along the first principal component. The reef front crest sites

were characterised by a high biomass of the macroalgal browsing Kyphosus spp,

large excavating parrotfishes (Chlorurus frontalis, C. microrhinos) and to a lesser

extent the browsing Prionurus maculatus and scraping parrotfish Scarus altipinnis.

In contrast, the lagoonal sites were characterised by the smaller excavating

parrotfish (Chlorurus spilurus, formerly Chlorurus sordidus), and a diversity of

smaller scraping parrotfishes (Scarus chameleon, S. globiceps, S. psitticus; Figure

14).

Interestingly, there was no relationship between the biomass of roving herbivorous

fishes and either the cover of macroalgae, the cover of live scleractinian (hard)

coral, or the cover of bare space (i.e., turf algae and crustose coralline algae)

(Figure 15). While numerous studies have linked the abundance and/or biomass of

herbivorous fishes to the cover of live coral and/or the structural complexity of the

habitat, and others have reported negative correlations between the cover of

macroalgae and the biomass of herbivorous fishes across a range of spatial scales

(e.g., Williams et al. 2001; Wismer et al. 2009), we found no evidence for such

relationships at Elizabeth and Middleton Reefs. This is largely consistent with

previous surveys at these reefs (Hoey et al. 2014), and may reflect the limited

variation in the cover of these benthic variables, or that other factors (such as wave

action and larval supply) that may be influencing these relationships. The lack of

relationship with either macroalgae or live coral while unexpected, does not mean

that herbivorous fishes are unimportant in the ecology and resilience of coral reefs

at Elizabeth and Middleton Reefs. Clearly, further research is required to

understand the ecological functioning of these high latitude reefs, especially what

are the determinants of macroalgal abundance and biomass (Choat et al 2006,

Pratchett et al. 2011, Hoey et al. 2011, 2018).

Figure 14. Principal component analysis (PCA) showing variation in the composition of roving herbivorous fish assemblages between years, habitats and depths. Symbols indicate sampling year; triangles - 2011, circles – 2014, squares - 2018. Colours indicate habitat; dark green – lagoon slope, light green – lagoon crest, dark blue – back reef slope, light blue – back reef crest, bright yellow – exposed reef crest, dull yellow – exposed reef slope. Analysis was based on the covariance matrix of the mean biomass (log-transformed) of each species at each site.

Figure 15. Relationships between the herbivore biomass and the cover of (a) macroalgae, (b) live coral, and (c) bare space (the sum of algal turfs and CCA). Each point represents the mean of 4 transects at each depth at each of 19 sites. triangles: Elizabeth Reef, circles: Middleton Reef. Colours represent the three habitats shown in Figure 2. Yellow: exposed reef front; Blue: back reef; Green: lagoon.

Endemic and site-associated fishes - The endemic anemone fish Amphiprion

mccullochi is a relatively minor component of the total pomacentrid community on

Elizabeth and Middleton Reefs, with an average density of 0.31 fish/100m2 on

Elizabeth Reef and 0.03 fish/100m2 on Middleton Reef (Figure 16). In contrast, the

endemic three-striped butterflyfish Chaetodon tricinctus was the most abundant of

22 butterflyfish species recorded on these reefs with a mean density of 1.28

fish/100m2 on Elizabeth Reef and 1.15 fish/100m2 on Middleton Reef (Figure 16).

A. mccullochii is a habitat specialist, being only found in close association with the

anemone Entacmaea quadricolor. The distribution of the A. mccullochi is,

therefore, restricted by the availability of its host anemone. At Elizabeth and

Middleton Reefs this anemone is restricted primarily to lagoonal areas and is

reflected in the distribution on A. mccullochi (Figure 17a). The low and variable

abundance of A. mccullochi precluded any meaningful analyses. In contrast, the

three-striped butterflyfish C. tricinctus was more widely distributed among habitats,

being recorded across all habitats on both reefs (Figure 17b). Although there is

some debate over the diet of C. tricinctus (Pratchett et al. 2014b), the abundance

of this species was positively related to live coral cover suggesting it relies on live

coral for food and/shelter. Like many other butterflyfishes, such reliance on live

coral likely make populations of this species will be susceptible to changes in live

coral cover.

The overall abundances of both A. mccullochi and C. tricinctus have remained

relatively stable from 2011 to 2018 (Figure 18). The abundance of A. mccullochi

was relatively stable on Elizabeth Reef, but showed a sharp decline on Middleton

Reef from 2014 to 2018 (Figure 18a). This decrease is no cause for alarm as the

abundances are now back to 2011 levels, and several individuals were seen

outside the transect boundaries in the lagoon sites at Middleton reef. The densities

of C. tricinctus were relatively consistent from 2014 to 2018 on both Elizabeth and

Middleton Reefs, and remained above the 2011 abundances (Figure 18b). There

was a relatively small decline in abundances of C. tricinctus on Elizabeth Reef from

1.89 ind/100m2 in 2014 to 1.28 ind/100m2 in 2018, that was driven by a decline in

abundances on exposed reef front sites (Figure 18b), despite increases in live

coral cover over the same period (Figure 3).

Figure 16. Relative abundances of members of the (a) Pomacentridae (damselfishes), and (b) Chaetodontidae (butterflyfishes) recorded across all transects on Elizabeth and Middleton Reefs in February/March 2018. Arrows indicate the relative abundances of the endemic species Amphiprion mccullochi and Chaetodon tricinctus. Data are means ± SE.

Figure 17. Spatial variation in the abundance of (a) Amphiprion mccullochi, and (b) Chaetodon tricinctus among reefs (Elizabeth and Middleton), habitat zones (back reef, lagoon, reef front), and depths (crest, slope) in February/March 2018 (see Figure 2 and Table 2 for details). Data are means ± SE.

Figure 18. Temporal variation (2011 - 2018) in the mean abundance of (a) Amphiprion mccullochi, and (b) Chaetodon tricinctus across three habitat types (see Figure 2 and Table 2 for details) at Elizabeth and Middleton Reefs. Error bars represent 1 SE.

The endemic double-header wrasse Coris bulbifrons was relatively abundant

across both Elizabeth and Middleton Reefs in 2018, with 206 adults and 39

juveniles (<10cm Total Length) being recorded across all transects, compared to

232 adults and 14 juveniles in 2014. Juvenile C. bulbifrons were largely restricted

to the back reef and lagoon habitats (Figure 18a), while adult C. bulbifrons were

recorded across all habitats and depths at both reefs (Figure9).

The mean densities of both juvenile and adult C. bulbifrons were relatively stable at

Elizabeth and Middleton reefs over the past 4-years. The overall densities of

juvenile C. bulbifons changed little at Elizabeth Reef from 2014 to 2018, although

there was a decline in abundance from 0.09 ind/100m2 in 2014 to 0.03 ind/100m2

to 2018 on Middleton Reef (Figure 20a). This decline likely represents variation in

recruitment success among years. The densities of adult C. bulbifons remained

unchanged on Middleton Reef from 2014 to 2018, but showed a small decline on

Elizabeth Reef over the same period (2014: 0.78 ind/100m2; 2018: 0.44 ind/100m2;

Figure 20b). This decrease in adult C. bulbifrons was solely attributable to a

decline in abundances within the lagoon sites.

Figure 19. Spatial variation in the abundance of (a) juvenile, and (b) adult Coris bulbifrons among reefs (Elizabeth and Middleton), habitat zones (back reef, lagoon, reef front), and depths (crest, slope) in February-March 2018 (see Figure 2 and Table 2 for details). Data are means ± SE.

Figure 20. Temporal variation (2011 - 2018) in the mean abundance of (a) juvenile, and (b) adult Coris bulbifrons across three habitat types (see Figure 2 and Table 2 for details) at Elizabeth and Middleton Reefs. Error bars represent 1 SE.

Apex predators - High densities of Galapagos reef sharks (Carcharhinus

galapagensis) were again recorded at Elizabeth and Middleton Reefs in 2018. The

average abundance of C. galapagensis across all habitats was 10.2 individuals per

hectare (± 4.0 SE) on Elizabeth Reef and 8.9 individuals/ha (± 2.4 SE) on

Middleton Reef (Figure 21a). These abundances represent an increase at

Elizabeth Reef (2014: 6.58 individuals/ha ± 1.69 SE) and a decrease at Middleton

Reef (2014: 17.11 individuals/ha ± 2.99 SE). The most pronounced increases were

recorded within the lagoon sites on Elizabeth Reef, while moderate declines were

recorded in the back reef sites on both reefs and the reef front on Middleton reef

(Figure 21a). The vast majority of C. galapagensis recorded were relatively small

(< 120cm; Figure 21) with the largest individual recorded being 200cm total length.

These size distributions largely reflected those from 2014 (Figure 22). Given that

C. galapagensis reaches up to 300 cm in length, does not mature until 210-250

cm, and is born at 60-80 cm (Last and Stevens 1994), these data indicate that the

large populations at Elizabeth and Middleton Reefs comprise mostly immature

individuals, and that these reefs are likely to represent an important nursery area

for this species.

Figure 21. Temporal variation (2011 - 2018) in the mean abundance of (a) the Galapagos Reef Shark and (b) the Black Cod across three habitat types (see Figure 2 and Table 2 for details) at Elizabeth and Middleton Reefs. Error bars represent 1 SE.

Figure 22. Comparison of the size structure of Galapagos Shark (Carcharhinus galapagensis) populations between Elizabeth and Middleton Reefs in (A) 2014, and (B) 2018. Size at birth is 60-80cm, size at maturity is 210-230cm (males) and 250cm (females).

Black cod (Epinephelus daemelii) were recorded across most sites at Elizabeth

and Middleton Reefs (Figure 21b). The average abundance of E. daemelii across

all habitats in 2018 was 1.50 individuals per hectare (± 0.35 SE) at Elizabeth Reef,

and 1.41 individuals per hectare (± 0.55 SE) at Middleton Reef. These represent

declines of approximately 40% from 2014 levels (Elizabeth: 2.50 (± 0.44 SE)

individuals per hectare; Middleton: 2.24 (± 0.53 SE) individuals per hectare).

Concerningly, theses declines were were widespread with abundances of E.

daemelii decreasing in all three habitat zones on both reefs, with no E. daemelii

being recorded at the lagoon sites on Middleton Reef in 2018. The reasons for

these declines are not apparent but clearly warrant further investigation.

6 Conclusions

Elizabeth and Middleton Reefs are important examples of sub-tropical reefs,

supporting unique assemblages of both tropical and temperate species (Hobbs et

al. 2008, Hoey et al. 2011). While not exposed to the frequency or intensity of

disturbances affecting tropical reefs, subtropical reefs are extremely vulnerable to

acute disturbances, such as coral bleaching and disease, storms, and crown-of-

thorns starfish outbreaks (e.g., Harriott 1995; Riegl 2003; Harrison et al. 2011)

because their capacity for recovery and resilience is likely to be limited both by

isolation (e.g., Gilmour et al. 2013) and environmental constraints on population

dynamics (Anderson et al. 2015). Current rates of increasing coral cover at

Elizabeth and Middleton Reefs (9-10% per year) are comparable to rates of coral

recovery recorded on the Great Barrier Reef (e.g., Lourey et al. 2000), though it is

clear that coral recovery since outbreaks of crown-of-thorns starfish in this region in

the 1980s has been extremely protracted.


Coral cover at Elizabeth and Middleton Reef is currently high (33.76% ±1.37 SE),

especially compared to highly depressed mean coral cover across the Great

Barrier Reef in the aftermath of the recent back-to-back coral bleaching events

(Hughes et al. 2017a, 2017b, 2018). Even more importantly, coral cover at

Elizabeth and Middleton Reefs is increasing, whereas coral cover is generally

declining across most major coral reef regions (e.g., Bellwood et al. 2004; Bruno

and Selig 2007), and declined further due to recent, unprecedented, severe and

recurrent bleaching at many locations (Hughes et al. 2018).

Densities of juvenile corals at Elizabeth and Middleton Reefs are very low

compared to low latitude reef systems, but similar to those from Lord Howe Island.

These low rates of replenishment appear to be characteristic of high latitude reefs

(Harriott 1992; Hoey et al. 2011; Bauman et al. 2014), and coupled with the lower

coral growth rates on subtropical reefs (Harriott 1999; Anderson et al. 2012) and

isolation (Gilmour et al. 2013) are likely to limit the recovery potential of these reefs

following disturbance. Collectively these factors are likely to have contributed to the

protracted recovery of coral communities following the crown-of-thorns starfish

outbreak in the late 1980’s and early 1990’s.

Given the high and increasing coral cover at Elizabeth and Middleton Reefs, it

appears that these locations were largely unaffected by recent spikes in global

ocean temperatures that caused wide-spread and severe coral bleaching (Hughes

et al. 2017b). However, severe bleaching of select corals was conspicuous in some

locations during recent surveys. Moreover, the temperature stress that occurred in

2018 (>3 DHW) was higher than recorded at these locations in 2016 and 2017. For

context, there is a 40% probability of severe mass bleaching on the GBR at 3DHW

(Hughes et al. 2017a). This might provide significant imperative to re-visit these

locations and establish vulnerability to temperature stress and coral bleaching.

These locations are particularly vulnerable to coral bleaching or any other acute

disturbances, given low rates of population replenishment, which will greatly

constrain recovery.


Coral predators – While there have been previous outbreaks of crown-of-thorns

starfish at Elizabeth and Middleton Reefs (Australian Museum 1992; Harriot 1998),

which devastated local coral assemblages with very protracted recovery, current

densities of A. cf. solaris (as well as other invertebrate corallivores) are very low.

There is, however, a persistent low-density population of A. cf. solaris at Elizabeth

Reef. Given that outbreaks of crown-of-thorns starfish may arise through the

gradual accumulation of individuals over several successive cohorts (Pratchett

2005), culling these low-density populations may greatly reduce the risk of future

outbreaks (Pratchett et al. 2014a). Conversely, there is little to no evidence that

low-density populations of crown-of-thorns starfish have beneficial effects on the

structure or diversity of coral assemblages (Pratchett 2010).

Sea cucumbers - The management and isolation of Elizabeth and Middleton

Reefs appears to be having positive effects on sea cucumber populations, which

are overexploited in most other locations (Purcell 2014, Purcell et al. 2014).

Densities of H. whitmaei (listed as endangered on IUCN Redlist) recorded in 2018

were lower than recorded in 2014 (Figure 9), but it is unknown whether this is

reflective of reef-wide population declines and other predominant species were

more abundant in 2018 than recorded in 2011 or 2014. It is also important to

realise that these surveys are designed to assess fish and benthic communities

within consolidated reef, or coral-dominated, habitats, whereas accurate

assessment of sea cucumber populations would require dedicated sampling of

shallow reef flat areas and sand-dominated habitats.

Urchins - Although they are considered functionally important in some locations

(e.g., Diadema on Caribbean reefs), high densities of urchins on Indo-Pacific reefs

are often viewed as evidence of reef degradation (Bellwood et al. 2004). Densities

of D. savignyi within the back reef at Middleton reef have actually declined since

2014, though there have been corresponding increases in the abundance of

Echinostrephus spp. within this habitat. Notably, these habitats are already

characterized by high levels of bioerosion, potentially attributable to sustained high

densities of Diadema, and Echinostrephus spp. may further exacerbate erosion

and destabilise reef structures. Echinoids, and echinoderms in general, are

renowned for their marked population fluctuations (Uthicke et al. 2009), but the

ecological importance and consequence of these population fluctuations does

warrant increased attention.

6.2 Reef fishes

Fishes on coral reefs are being increasingly viewed in terms of their ecological

roles, or functions, irrespective of their taxonomic affinities (e.g., Richardson et al.

2018). This shift in focus has been driven by the realisation that the removal of key

functional groups of fishes through fishing activities has underpinned the

degradation of coral reef systems worldwide (e.g., Hughes 1994; Rasher et al.

2013). Reductions in predatory fishes have been suggested to cause meso-

predator release and potentially drive trophic cascades, although evidence for such

effects is limited (e.g., Casey et al. 2017). Reductions in predators have, however,

been related to increased incidence of outbreaks of crown-of-thorns starfish in the

tropical Pacific, and the subsequent loss of live coral cover (Sweatman 2008; Dulvy

et al. 2004), as well as changes in the foraging behaviour of herbivorous fishes

(Rizzari et al. 2014, Rasher et al. 2017). Perhaps the most pervasive effect of

fishing on the functioning of coral reefs is the reduction in herbivorous fish

populations that have underpinned shifts from coral- to macroalgal-dominated reefs

in many regions (Hughes 1994; Rasher et al. 2013; Graham et al. 2015). Coral reef

fish communities appear to be relatively stable at Elizabeth and Middleton Reefs

with similar abundances recorded from 2011 to 2018 (Pratchett et al. 2011; Hoey

et al. 2014). The only exception to this was the black cod (E. daemelii) which

exhibited small but consistent declines across all habitats at both Elizabeth and

Middleton Reefs from 2014 to 2018.

The Black cod (E. daemelii) has declined throughout much of its geographic range,

largely due to overfishing. At Elizabeth and Middleton Reefs, the overall

abundance of black cod (across all sites) averaged 1.50 and 1.44 individuals per

hectare respectively, and there has been a small but consistent decline in densities

recorded at the same sites in 2011 and 2014 (Pratchett et al. 2011; Hoey et al.

2014). Although the current densities of Black cod are within the range of densities

recorded by Oxley et al. (2004) and Choat et al (2006), the consistency of the

declines across all habitats is cause for concern. It appears unlikely that these

declines are a direct result of fishing activities as other species that are likely to be

affected by line fishing (e.g. Galapagos shark, double-header wrasse) did not

decline in abundance. The smallest Black cod observed during the present surveys

was 40cm in length, suggesting that recruitment to the population may be limited,

or that recruitment habitats were not adequately captured by our surveys (e.g.,

they may recruit to deeper water). Continued and extensive long-term monitoring is

critical to assess the fate of Black cod at Elizabeth and Middleton Reefs,

considered one of the last strongholds for this species. Importantly, more intensive

research is also required to assess the natural dynamics of local populations (e.g.,

recruitment rates, recruitment/nursery habitats, growth and longevity), which will be

critical for assessing the overall vulnerability of these populations. Any future

declines, no matter how slight, could threaten the sustainability of this population.

The structure and resilience of coral reef ecosystems are fundamentally dependent

on the actions of herbivorous fishes. Through their grazing activities, herbivorous

fishes have been estimated to remove up to 90 percent of the net algal production

from shallow coral reefs (Polunin and Klumpp 1992; Ferreira et al. 1998). In doing

so herbivorous fishes inhibit the proliferation of algal biomass (Lewis 1986),

minimize algal-coral competition (Hughes et al. 2007; Rasher and Hay 2010) and

facilitate coral settlement through the provision of suitable settlement substrata

(Hughes et al. 2007; Hoey et al. 2011). On reefs with relatively intact herbivorous

fish assemblages, populations of herbivores have been shown to increase in

response to large-scale coral loss and consequent increases in algal cover (Adam

et al. 2011, Gilmour et al. 2013) thereby compensating the increased algal

production and promoting the recovery of coral assemblages following disturbance

(Bellwood et al. 2004; Mumby and Steneck 2008).

The herbivorous fish assemblages of Elizabeth and Middleton Reefs represent a

unique mix of both tropical and temperate species, and appear to have changed

little over the past 7 years (Pratchett et al. 2011; Hoey et al. 2014). Collectively, the

densities of all herbivorous fishes on Elizabeth and Middleton Reefs were broadly

comparable to lower latitude reefs of the central and northern Great Barrier Reef

(Wismer et al. 2009) and substantially greater than those of Lord Howe Island, 260

km to the south (e.g., Hoey et al. 2011). There were, however, marked differences

in the functional composition of herbivorous fish assemblages between these

different reef systems. Herbivorous fish assemblages on Elizabeth and Middleton

Reefs were dominated by macroalgal browsing species, in particular Kyphosus

sectatris. On lower latitude, or tropical, reefs macroalgal browsing species typically

account for < 10% of the herbivorous fish biomass (e.g., Hoey and Bellwood

2010a, b). While these fishes have been suggested to play a critical role in

removing macroalgal biomass and potentially reversing phase-shifts on low latitude

reefs (Hoey and Bellwood 2011; Rasher et al. 2013), their role limiting the cover

and biomass of macroalgae on higher latitude reefs, such as Elizabeth and

Middleton Reefs, is largely unknown. For example, the two browsing species

Kyphosus sectatris and Prionurus maculatus accounted for >70 % of the total

herbivorous fish biomass on Elizabeth and Middleton reefs, but we currently know

very little of their diet, feeding behaviour, functional impact. The role these fishes

play in limiting the abundance and biomass of macroalgae on high latitude reefs is

currently unknown and is an area that requires specific targeted research if we are

to understand the process that structure these unique reef systems.

Together with the high biomass of browsing fishes, the biomass of grazing fishes

on Elizabeth and Middleton Reefs has been stable over the past 7 years at a level

that is approximately 25% of that on low latitude reefs. Grazing fishes, and in

particular scraping and excavating parrotfishes, perform a key role in clearing

space for the settlement of benthic organisms such as corals (Mumby 2006; Hoey

and Bellwood 2008, Trapon et al. 2013a,b). Although there has been some debate

regarding the nutritional target of parrotfishes, a recent synthesis indicates they are

targeting protein-rich epiphytic and endolithic phototrophs (primarily cyanobacteria,

Clements et al. 2017). Irrespective of their nutritional target, intensive feeding by

parrotfishes and other grazing fishes is critical to maintaining algal communities in

a cropped state (e.g., Bellwood et al. 2006, Hughes et al. 2007). Interestingly, we

found no relationship between the biomass herbivorous fishes and the cover of

macroalgae, live coral, or bare space (i.e., algal turfs and crustose coralline algae).

Focused and intensive research will be required to disentangle the complexities of

the relationships between herbivorous fishes and the condition and composition of

benthic assemblages on these unique reefs.

7 Acknowledgements

The latest surveys (February-March 2018) at Elizabeth and Middleton

Reefs were conducted using M.V. Iron Joy, alongside parallel surveys undertaken

by Reef Life Survey. We are grateful to the entire crew, especially skipper Rob

Benn.

Field surveys were commissioned by the Director of National Parks, with

additional in-kind support from the Australian Centre of Excellence for Coral Reef

Studies. We also gratefully acknowledge the guidance and contributions of Cath

Samson, who would have been a very valuable person to accompany us during

this expedition.

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