Relationships between structural complexity, coral traits, and reef fish 1
assemblages 2
3
Emily S. Darling
1,2,*
, Nicholas A. J. Graham
3,4
, Fraser A. Januchowski-Hartley
5
, 4
Kirsty L. Nash
6,7
, Morgan S. Pratchett
4
and Shaun K. Wilson
8,9
5
6
1
Wildlife Conservation Society, Marine Program, Bronx, NY 10460, United States 7
2
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, M5S 8
3B2, Canada 9
3
Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, United Kingdom 10
4
ARC Centre for Excellence for Coral Reef Studies, James Cook University, Townsville, QLD, 11
4811, Australia 12
5
1 UMR 9190 MARBEC, IRD-CNRS-IFREMER-UM, Universite´ de Montpellier, Montpellier, 13
34095, France 14
6
Centre for Marine Socioecology, Hobart, Tasmania, 7000, Australia 15
7
Institute of Marine and Antarctic Studies, University of Tasmania, Hobart, Tasmania, 7000, 16
Australia 17
8
Science & Conservation, Department of Parks and Wildlife. Perth, 6983, Australia. 18
9
Oceans Institute, University of Western Australia, Crawley, Western Australia, 6009, 19
Australia 20
21
*Author for correspondence: edarling@wcs.org 22
Target journal: Coral Reefs 23
Article type: Report 24
2
Abstract 25
With the ongoing loss of coral cover and the associated flattening of reef 26
architecture, understanding the links between coral habitat and reef fishes is of 27
critical importance. Here, we investigate whether considering coral traits and 28
functional diversity provides new insights into the relationship between structural 29
complexity and reef fish communities, and whether coral traits and community 30
composition can predict structural complexity. Across 157 sites in Seychelles, 31
Maldives, the Chagos archipelago and Australia’s Great Barrier Reef, we find that 32
structural complexity and reef zone are the strongest and most consistent 33
predictors of reef fish abundance, biomass, species richness, and trophic structure. 34
However, coral traits, diversity and life histories provided additional predictive 35
power for models of reef fish assemblages, and were key drivers of structural 36
complexity. Our findings highlight that reef complexity relies on living corals – with 37
different traits and life histories – continuing to build carbonate skeletons, and that 38
these nuanced relationships between coral assemblages and habitat complexity can 39
affect the structure of reef fish assemblages. Seascape-level estimates of structural 40
complexity are rapid and cost-effective with important implications for the 41
structure and function of fish assemblages, and should be incorporated into 42
monitoring programs. 43
44
Keywords: Habitat diversity, species traits, functional ecology, reef architecture, 45
Scleractinian corals, coral reef fish 46
47
3
48
Introduction 49
Scleractinian corals – the foundation species of tropical reef ecosystems – have long 50
been recognized to provide essential habitat for reef associated organisms 51
(Luckhurst and Luckhurst 1978; Roberts and Ormond 1987; Stella et al. 2011). 52
Similarly, structural complexity, defined as the physical three-dimensional 53
configuration of a reef, can shape the abundance and diversity of reef fish 54
assemblages across both large and small spatial scales (McCormick 1994; Nash et al. 55
2012; Ferrari et al. 2016). Several ecological hypotheses are proposed to underlie 56
these relationships, notably that structural complexity and habitat diversity can 57
mediate competition and predation, and facilitate co-habitation of an increased 58
number of species (Hutchinson 1959; Hixon and Beets 1993; Beukers and Jones 59
1997). 60
Structural complexity is often positively associated with abundance and 61
diversity of fishes across both temperate and tropical ecosystems (Friedlander et al. 62
2003; Graham and Nash 2013). Moreover, reductions in structural complexity and 63
habitat diversity can result in reduced abundance, local extinctions, diversity loss 64
(Graham et al. 2006; Holbrook et al. 2015; Newman et al. 2015), and declining 65
fisheries productivity (Rogers et al. 2014); all outcomes with profound implications 66
for reef biodiversity and associated ecosystem services. 67
Despite important relationships between structural complexity and reef 68
fishes, coral reef monitoring programs typically focus on measuring total live cover 69
and composition of reef-building corals. While many relationships between coral 70
4
cover and reef fish assemblages have been weaker than structural complexity 71
(Holbrook et al. 2008; Wilson et al. 2012), field experiments suggest that 72
microhabitat (i.e., coral) diversity and some coral species can have a positive effect 73
on fish diversity and community structure (Messmer et al. 2011; Holbrook et al. 74
2015). Recently, trait-based approaches have outlined important characteristics of 75
coral assemblage beyond total coral cover or taxonomic composition (Darling et al. 76
2012; Madin et al. 2016a,b), which may provide insights for predicting the structure 77
and diversity of reef fish communities. Traits that describe coral morphology, 78
growth rate and colony size may be expected to predict structural complexity, and 79
thus the structure and composition of fish assemblages. As such, coral traits may 80
provide a means of quantifying structural complexity and predicting fish 81
assemblage properties from benthic surveys where direct measures of 82
macrocomplexity were not taken, particularly in combination with the availability of 83
open-access trait information (Madin et al. 2016a,b). For example, traits that 84
describe branching, corymbose or plating growth forms can provide keystone 85
structures for reef fishes, which can preferentially select specific structural traits of 86
corals for shelter (Noonan et al. 2012; Kerry and Bellwood 2012, 2015; Wilson et al. 87
2016). A range of other explicit links can be made for other coral traits (Table 1). 88
To the best of our knowledge, this study presents the first large-scale 89
empirical test of trait-based relationships among coral communities, structural 90
complexity and reef fish assemblages. We use surveys across a large gradient of fish 91
biomass in the Indian and Pacific Oceans ranging from exploited sites to those 92
within one of the world’s most pristine reef systems, the Chagos archipelago 93
5
(Graham and McClanahan 2013). Our objectives were to, 1) evaluate which aspects 94
of the physical and biological characteristics of benthic habitats best explain the 95
structure of reef fish assemblages, in particular how well do coral traits describe fish 96
assemblages relative to physical measures of reef structure, and 2) investigate the 97
relationships between hard coral cover, life histories and species traits with 98
structural complexity. 99
100
Methods 101
Study sites 102
We surveyed 157 sites in the Seychelles, Maldives, Chagos archipelago and the Great 103
Barrier Reef in Australia between 2010 and 2013 (Figure 1). Sites were 104
haphazardly sampled across three reef zones (reef crest, flat and slope; also referred 105
to as reef habitat) and include fished sites and sites within no-take marine reserves. 106
Depth was recorded for each site and ranged from 1.5 m to 10 m. At each site, 107
benthic and coral reef fish surveys were conducted using underwater visual census 108
methods to evaluate coral communities, habitat complexity and reef fish 109
assemblages. 110
111
Coral assemblages 112
Coral assemblages were surveyed using two methods: four x 50 m point intercept 113
transects in Chagos, Maldives and Australia, and eight x 10m line intercept transects 114
in the Seychelles. For point intercept transects, the substrate directly below the 115
transect tape was surveyed every 50 cm. For line intercept transects, the length of 116
