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Boom and bust of keystone structure on coral reefs 1
2
Shaun K Wilson
1,2*
, James PW Robinson
3
, Karen Chong-Seng
4
, Jan Robinson
5
, 3
Nicholas AJ Graham
3
4
5
1 Department of Biodiversity, Conservation and Attractions: Marine Science Program, 6
Kensington, WA 6151, Australia 7
2 Oceans Institute, University of Western Australia, Crawley, WA 6009, Australia 8
3 Lancaster Environment Centre, Lancaster University, Lancaster, LA1 4YQ, UK 9
4 ARC Centre of Excellence for Coral Reef Studies, James Cook University, 10
Townsville, QLD 4811, Australia 11
5 Ministry of Finance, Trade, Investment and Economic Planning, Victoria, Mahe, 12
Seychelles 13
14
*Communicating author. Email: shaun.wilson@dbca.wa.gov.au 15
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Keywords: reef resilience, coral reef ecology, disturbance ecology, structural complexity 17
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Abstract 19
Repeated bouts of coral bleaching threaten the long-term persistence of coral reefs and 20
associated communities. Here we document the short- and long-term impacts of heatwave 21
events on coral and fish assemblages, based on regular surveys of 18 reefs of the granitic 22
islands of Seychelles over 23 years. Extreme heat events in 1998 and 2016 led to bleaching 23
associated declines in coral cover, whilst between these years there was an interim period of 24
coral recovery on some reefs. Coral decline and recovery were primarily due to changes in 25
the cover of branching coral, particularly those from the families Acroporidae and 26
Pocilloporidae. Surveys during the 2016 bleaching, found that 95% of the 484 Acropora and 27
Pocillopora colonies observed were either bleached or recently dead. The extent of bleaching 28
and subsequent mortality were best explained by a priori assessments of community 29
susceptibility to heat stress. One year later (2017) coral cover had fallen by 70% and average 30
coverage across the 18 reefs was at 6%, similar to levels recorded in 2005, seven years after 31
the 1998 bleaching. Decline in coral following the 2016 bleaching coincided with reduced 32
abundance of fish <11cm TL, particularly corallivores, invertivores and mixed diet feeders. 33
These changes are likely to foreshadow more widespread loss once the habitat structure 34
erodes. Accordingly, seven years after the 1998 bleaching, when coral skeletons and reef 35
structure had collapsed on some reefs, abundance of both large and small bodied fish had 36
declined. We show that fluctuation in the cover of branching coral is positively associated 37
with changes in the abundance of small-bodied fish which contribute to ecological processes 38
and high diversity, suggesting branching corals are a keystone structure. Increased frequency 39
of bleaching threatens the capacity of branching corals to fully recover after disturbances, 40
reducing the amplitude of boom bust cycles of these corals and the keystone habitat structure 41
they provide reef fish. 42
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Introduction 44
Like many high diversity ecosystems in the tropics, coral reefs are threatened by a range of 45
anthropogenic disturbances (Barlow et al. 2018). Of particular concern is the increasing 46
frequency of marine heat waves that cause extensive mass bleaching and mortality of corals 47
(Hughes et al. 2018a). These corals create the reef framework, underpinning ecological 48
processes and services. For example, corals provide food and habitat for many of the reef 49
associated species including highly diverse assemblages of fish (Wilson et al. 2006). These 50
fish have crucial functional roles in terms of herbivory and bioerosion, and multispecies 51
fisheries provide food and livelihoods for coastal communities around the world (Moberg and 52
Folke 1999; Bellwood et al. 2004). 53
The physical structure, occurrence and life history traits of corals are variable, which may 54
make some components of the coral assemblage of greater importance to reef associated 55
fauna than others. For example, the types of corals with which fish associate varies among 56
fish species and life history stages. Some fish feed or dwell with specific coral taxa, whilst 57
others may associate with a broader group of corals (Cole et al. 2008; Coker et al. 2014). 58
Branching corals appear especially important for fish as the structural complexity provided 59
by this diverse group of corals provides refuges of numerous dimensions (Komyakova et al. 60
2018). 61
When a group of habitat forming taxa have a disproportionate contribution to ecological 62
diversity and processes relative to their abundance, they may be considered keystone 63
structures (Tews et al. 2004). This terminology has been used to highlight the ecological 64
importance of large trees in terrestrial landscapes (Manning et al. 2006), and has recently 65
been used to describe corals with specific growth forms (Kerry and Bellwood 2015). It is 66
however difficult to definitively identify keystones as their influence may vary in different 67
ecological settings (Menge et al. 1994). Large scale perturbations that remove candidate 68
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keystones, combined with temporal assessments of changes in the community, provide an 69
opportunity to identify keystone structures. Coral reefs regularly experience disturbances, and 70
fast-growing coral taxa may represent a ‘boom’ growth form that can recover habitat 71
structure relatively quickly. 72
Since the 1980s there have been several global scale marine heatwaves that have caused 73
widespread bleaching and mortality of corals. The granitic islands of Seychelles, in the Indian 74
Ocean, have a history of exposure to severe bleaching over this time. Previous research has 75
described the impact of mass bleaching on coral and fish assemblages on reefs in Seychelles 76
following the 1998 heatwave (Graham et al. 2006). Subsequent surveys of the same reefs 77
identified environmental and ecological factors that promote coral recovery and prevent reefs 78
undergoing regime shifts (Graham et al. 2015). Here we provide detailed assessments of how 79
the 2016 El Niño associated heatwave affected corals and associated fish on reefs in 80
Seychelles. Based on long-term assessments of reef communities that span the major 81
bleaching events in 1998 and 2016, and an intervening period of recovery, we identify the 82
change in abundance of branching corals as the major cause of temporal change in coral 83
cover and habitat structure. We then assess how periods of decline and increase in branching 84
coral cover have influenced fish assemblages to investigate whether these corals are keystone 85
structures on coral reefs. 86
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Methods 88
Benthic and fish surveys of 18 Seychelles reefs were initially undertaken in 1994, with 89
subsequent surveys in 2005, 2008, 2011, 2014 and 2017. The 18 reefs were founded on 90
habitats of either granitic, contiguous carbonate or patches surrounded by sand or rubble. Six 91
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of the reefs were within no-take marine reserves, that have been in place since the 1970s and 92
are managed by the government in Seychelles (Jennings et al. 1996). 93
At each of the 18 reefs the abundance and size (total length, TL) of fish >7cm was recorded 94
from 134 non-cryptic, diurnally active species observed within 154m
2
replicate areas (7m 95
radius). The diver conducting fish surveys calibrated size estimates of fish by estimating and 96
confirming the size of plastic pipes at the start of each survey day, with mean error within 97
~3% (Graham et al. 2007). All large mobile fish were recorded first, before a systematic 98
search of smaller site attached species. Count areas were located at the base of reef slopes at 99
2-9m depth. In 1994, 2005 and 2008 there were 16 replicate areas surveyed at each of the 18 100
reefs and in 2011, 2014 and 2017 eight replicate areas per reef. Average values were 101
calculated from the number of areas surveyed at each reef to account for differences in 102
sampling intensity over time. 103
The structural complexity of each replicate area was scored on a scale between 0 and 5, 104
where areas with 0 structure were sandy or rubble substrate with no vertical relief and areas 105
that scored 5 were exceptionally complex, with numerous caves and overhangs (Polunin and 106
Roberts 1993). The percent cover of coral and coral growth forms (branching, massive, 107
encrusting, tabular) within each replicate area was estimated from a plan view of the area, the 108
coral forms being based on broad growth forms described by Veron (1986). In addition to 109
plan view surveys, 10m line intercept transects were carried out in each area from 2008. Line 110
intercept transects recorded percent cover of coral to the genera level and comparisons 111
between this technique with plan view surveys found estimates of coral cover from the two 112
techniques were very similar (Wilson et al. 2007, 2012). 113
Reefs were also categorised as either recovering or regime shifted based on temporal trends 114
in coral and macroalgal cover (Graham et al. 2015). Recovering reefs had higher coral than 115
