Effects of habitat structure on tropical fish assemblages Kajsa Garpe

Effects of habitat structure on
tropical fish assemblages
Kajsa Garpe
Doctoral dissertation
Department of Zoology
Stockholm University
2007
© Kajsa Garpe, Stockholm 2007
Zoologiska Institutionen
Stockholms universitet
SE-106 91 Stockholm
Cover by Danika Williams
Printed in Sweden by US-AB, Stockholm 2007
ISBN 91-7155-361-4
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To our precious little ones,
Silas, Milla & Lola
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“So long as water moves, so long as fins press against it, as
long as weather changes and man is fallible, fish will remain in
some measure unpredictable”
Roderick Haig-Brown
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ABSTRACT
Rates of habitat alteration and degradation are increasing worldwide due to
anthropogenic influence. On coral reefs, the loss of live coral reduces structural
complexity while facilitating algal increase. In many coastal lagoons seagrass and
corals are cleared to make room for cultivated macroalgae. This thesis deals with
reef and lagoon habitat structure and how fish assemblage patterns may be related to
physical and biological features of the habitat. It further examines assemblage
change following habitat disturbance. Four studies on East African coral reefs
concluded that both the abundance and species richness of recruit and adult coral
reef fish were largely predicted by the presence of live coral cover and structural
complexity (Papers I-III, VI). Typically, recruits were more selective than adults,
as manifested by limited distributions to degraded sites. Paper VI compared shortand long-term responses of fish assemblages to the 1997-1998 bleaching event. The
short-term response to coral mortality included the loss of coral dwelling species in
favour of species which feed on algae or associated detrital resources.
Counterintuitively, fish abundance and taxonomic richness increased significantly at
one of two sites shortly after the bleaching. However, the initial increase was later
reversed and six years after the death of the coral, only a limited number of fish
remained. The influence of fleshy algae on fish assemblages was studied in algal
farms (Paper IV), and examined experimentally (Paper V). The effects of algal
farming in Zanzibar were significant. Meanwhile, manually clearing algaldominated patch reefs in Belize from macroalgae resulted in short-term increases of
abundance, biomass and activity of a few species, including major herbivores. The
findings of this thesis demonstrate the significance of habitat as a structuring factor
for tropical fish assemblages and predicts that coral death, subsequent erosion and
algal overgrowth may have substantial deleterious impacts on fish assemblage
composition, abundance and taxonomic richness, with recovery being slow and
related to the recovery of the reef framework.
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LIST OF PAPERS
This thesis is based on the following papers, which will be referred to in the text by
their Roman numerals. The published papers are reprinted with the kind permission
of the publishers.
I
Bergman* KC, Öhman MC, Svensson S (2000) The influence of habitat
structure on the abundance of Pomacentrus sulfureus, a western Indian Ocean
reef fish. Environ Biol Fish 59:243-252
II
Garpe KC, Öhman MC (2003) Coral and fish distribution patterns in Mafia
Island Marine Park, Tanzania. Fish-habitat interactions. Hydrobiologia
498:191-211
III
Garpe KC, Öhman MC Non-random habitat use by coral reef fish recruits in
Mafia Island Marine Park. Afr J Mar Sci (in press)
IV
Bergman* KC, Svensson S, Öhman MC (2001) Influences of algal farming
on fish communities. Mar Poll Bull 42:1379-1389
V
McClanahan TR, Bergman* K, Huitric M, McField M, Elfwing T, Nyström
M, Nordemar I (2000) Response of fishes to whole patch reef algal
reductions on Glovers Reef, Belize. Mar Ecol Prog Ser 206:273-282
VI
Garpe KC, Yahaya SAS, Lindahl U, Öhman MC (2006) Long-term effects of
the 1998 coral bleaching event on reef fish assemblages. Mar Ecol Prog Ser
315:237-247
* The author has since changed her surname to Garpe
My contribution to the papers in the thesis is as follows:
I-III Responsible for project design, field work, data analyses and writing
IV
Participated in field work, responsible for analyses and writing
V
Participated in field work, responsible for fish counts and behaviour study,
assisted with fish data analyses and all fish-related parts of the paper
VI
Responsible for data analyses and writing
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CONTENTS
ABSTRACT .............................................................................................................7
LIST OF PAPERS....................................................................................................8
INTRODUCTION.........................................................................................................11
Habitat structure – the arrangement of objects in space ........................................11
The tropical coral reef ............................................................................................12
Habitat alteration and disturbance in the reef environment ....................................13
The impacts of coral degradation on reef fish assemblages ..................................14
The algal habitat ....................................................................................................15
Objectives in brief ..................................................................................................15
PAPERS IN BRIEF .....................................................................................................16
Paper I ...................................................................................................................16
Paper II ..................................................................................................................16
Paper III .................................................................................................................17
Paper IV ................................................................................................................18
Paper V .................................................................................................................18
Paper VI ................................................................................................................19
GENERAL METHODS ................................................................................................20
Study sites .............................................................................................................20
Field methods ........................................................................................................21
Data analysis .........................................................................................................23
GENERAL DISCUSSION............................................................................................25
Evidence of non-random habitat use .....................................................................25
The influence of structural complexity....................................................................26
Alteration in algal abundance.................................................................................27
Reef fish communities facing habitat degradation..................................................29
REFERENCES ...........................................................................................................31
TO ALL OF YOU WHO CONTRIBUTED… .................................................................40
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INTRODUCTION
Habitat structure – the arrangement of objects in space
Habitat provides functional space for associated organisms and constitutes a
fundamental concept in ecology, affecting community structure in a variety of
organisms and environments. In a broad sense, habitat is defined as an area of the
physical environment more or less distinct from others in a range of abiotic and
biotic variables (Kramer et al. 1997). Habitats may be continuous, patchy or isolated
and they may be stable, seasonal, unpredictable or temporary (Southwood 1977).
Habitat has a particular structure in which resources are arranged in space and time
according to changes in the physical environment and according to a range of
ecological processes. The essential aspects of habitat structure have been defined as
heterogeneity, complexity and scale (McCoy & Bell 1991). Heterogeneity is the
relative abundance of different structural components per unit area (e.g. the
proportions of coral, algae and bare rock on a coral reef). Complexity is defined as
the absolute abundance of individual structural components per unit area (e.g. the
degree of branching in corals or the density of macroalgae). Finally, scale is defined
as the size of the area used to measure heterogeneity or complexity (e.g. size of
sampling area, transect, quadrate). Microhabitat is used at higher resolution to
address subdivisions of the habitat that are relatively homogenous and differ only in
limited number of variables.
Most organisms exhibit non-random and predictable spatial distributions associated
with the biotic and physical structure of their habitat (Bell et al. 1991). The use of
any resource in disproportion to availability is described as selective resource use,
while selection is the process in which an animal chooses a resource (Johnson 1980).
Typical for the study of habitat selection is that the actual behaviour is rarely
observed; rather it is inferred from observed patterns of non-random distributions.
Species-specific habitat selection is typically related to the quality of the habitat for
a particular species, in terms of e.g. prospective availability of food resources and
predator shelter. The expectancy of finding a suitable habitat in which to hide, feed
and breed is foremost governed by spatial habitat features such as the degree of
isolation, the distance between and the size of habitat patches as well as by the
dispersal or migratory range of the organism (Southwood 1977). Remaining in
suboptimal habitat may affect condition and survival (Berumen et al. 2005). The
degree of habitat selection and, as a consequence, habitat dependency, typically
varies among taxa as well as among life stages within taxa.
This thesis pays special attention to the complexity of the habitat, which is
considered a useful predictor of the abundance, distribution and diversity of various
taxa including birds (MacArthur & McArthur 1961, Anderson & Shugart 1974),
lizards (Pianka 1966) and invertebrates (Lawton 1983). In aquatic habitats, the
positive effects of features providing structural complexity in an otherwise
unstructured habitat have been repeatedly demonstrated in a range of environments
and for a whole host of taxa including both invertebrates (Heck & Wetstone 1977,
Kelaher 2003, Underwood 2004) and fish (Connell & Jones 1991, Pihl et al. 1994,
Holbrook et al. 2002). The significance of structural complexity has many
explanations including the relationship between resource availability and surface
area (Heck & Wetstone 1977). In addition, it has been suggested that ecological and
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life-history strategies can diversify in response to increased structural complexity,
given the higher number of possible microhabitats and niches to occupy within the
habitat, thus promoting coexistence and high taxonomic richness (MacArthur &
McArthur 1961). Perhaps most importantly, structural complexity reduces predator
efficiency (Beukers & Jones 1997) and its availability is hence directly related to
predator-prey interactions.
Habitat alteration, or the reduction of a specific habitat or microhabitat in favour of
another, will affect habitat heterogeneity and complexity with consequences for
associated organisms, and those selective towards the affected habitat in particular
(Swihart et al. 2003, Jones et al. 2004). In recent time, the degradation of vital
habitat has caused the both local decline and global extinction of a number of taxa
(Pimm & Raven 2000) and further loss is imminent (Thomas 2004) with
consequences for many functional aspects of ecosystem services (Dobson et al.
2006).
The tropical coral reef
The coral reef provides an environment, which is heterogeneous and complex on a
wide range of spatial and temporal scales (Jackson 1991). At a scale of centimetres
there are differences between substrate components including corals, algae, rubble,
sponges, bare rock and sand. On this small scale there may also be significant
differences in growth forms among coral and algal taxa, as well as among other
components. At a scale of metres, reefs consist of hard substrate patches with
considerable structural complexity, sometimes mixed with sand, algal ridges or
rubble flats. On a yet larger scale, reefs are divided into zones including fore-reef,
reef crest, flat and slope, all providing quite distinct conditions in terms of substrate
cover, vertical relief, depth and water movement. Reefs that are situated hundreds of
metres apart may differ both in structure and in hydrodynamic conditions. Finally,
the scale can be extended to include reef systems and biogeographic zones.
Reef fish assemblages are open communities (for review, see Sale 1991), in which
local replenishment of the adult population is typically decoupled from local
reproduction, and occurs via the settlement of dispersive larvae (but see Jones et al.
1999, Swearer et al. 1999, Jones et al. 2005). Given the variability of the
environment and the active swimming behaviour of the larvae (Stobutski &
Bellwood 1997), the competent larvae should theoretically be confronted with a
large array of available habitats in which to settle. The settling larvae require
suitable habitat in which they can maximise energy gain (growth) while minimising
the risk of mortality. Early post-settlement mortality is typically high for coral-reef
fishes (Almany & Webster 2006), and preferential settlement may increase the
chances of post-settlement survival by escaping predation (Wellington 1992),
obtaining food resources (Levin 1994) and avoiding aggression from adults (Sale
1972, Almany 2003). Differential use of habitat at settlement (Sale et al. 1984,
Caselle & Warner 1996, Öhman et al. 1998) as well as habitat-specific variability in
post-settlement survival (Connell & Jones 1991, Beukers & Jones 1997, Risk 1997,
Lecchini et al. 2007) may in some species persist and shape adult distributions
(Wellington 1992, Sponaugle & Cowen 1996, Gutiérrez 1998). Yet in other species,
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ontogenetic shifts decouple the distributions of respective life stage (Sponaugle &
Cowen 1996, Lecchini & Galzin 2005).
Fishes may, at least during certain life stages, be closely associated with specific
habitat features, including live coral (Jones et al. 2004) distinct coral taxa (Munday
et al. 1997) and potential shelter (Chabanet et al. 1997, Friedlander & Parish 1998,
Gratwicke & Speight 2005a). Distinct fish assemblages may also be related to reef
zone (Munday et al. 1997, Ault & Johnson 1998), depth (Wellington 1992,
Srinivasan 2003), flow regimes (Breitburg et al.1995) and connectivity among
different habitats (Grober-Dunsmore et al. 2007). Several studies have demonstrated
how the distribution of habitat units can explain variations in species distribution
and abundance among zones and sites (Risk 1997, Tolimieri 1998, Holbrook et al.
2000), as well as among geographic locations (Holbrook et al. 2000, Munday 2002).
While the temporal component of larval distribution patterns remains debated (for
review, see Doherty 2002), benthic habitat is becoming increasingly recognised as a
predictor of reef fish assemblage structure within as well as among sites.
Understanding local recruitment patterns and the factors that contribute to their
variability is critical to the comprehension of reef fish populations and hence
invaluable for sound management of local fish stocks.
Habitat alteration and disturbance in the reef environment
Disturbances of different origin are frequently occurring on coral reefs. They vary in
scale, intensity, duration, frequency and degree of impact on associated biota, direct
or indirect (Connell 1997, Jones & Syms 1998). They are commonly limited to
single reefs or at the most, to reef areas on a regional scale (Connell 1997, Halford et
al. 2004). Habitat disturbance, defined as killing, displacing or damaging structural
components, may result in both physical (e.g. change of flow, turbulence etc) and
biological (e.g. loss of refuges or food sources) habitat alteration, and as a
consequence indirectly affect associated fauna. Disturbance response is typically
related to the location, the nature of the impact, as well as to the site-specific history
of disturbance (Hughes 1989). Few reefs today can be considered pristine and
previous impacts may for example have increased the vulnerability or resistance of
both habitat and associated biota to additional disturbance. Reef recovery is
generally related to the intensity of the disturbance, whether or not the original
environmental conditions can be restored and whether or not there is potential for
regrowth of survivors. If most structuring components (i.e. corals) are killed,
regeneration is dependent on the arrival of propagules from elsewhere, in which case
the location of the impact is vital. It should be noted that the reef at any time exhibits
a mosaic of multiple processes including mortality and regeneration of the reef
framework and that moderate disturbance regimes have been suggested to explain
the exceptionally high biodiversity of reef (Connell 1978, Karlson & Hurd 1993,
Connell 1997). In contrast, high frequency disturbances with no intermittent time for
recovery (e.g. destructive fishing practises, sedimentation, pollution) will cause a
situation of chronic disturbance (Connell et al. 1997) and continuous degradation.
Recovery from acute disturbance (e.g. storm or bleaching episodes) is typically
related to local levels of chronic disturbance (Connell et al. 1997).
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The impacts of coral degradation on reef fish assemblages
Close association between fish and habitat should leave fish assemblages highly
vulnerable to habitat disturbance while rendering studies of habitat perturbation a
question of both ecological and managerial interest. Secondary effects of coral loss
have previously been documented following infestations of the coral-feeding
starfish, Acanthaster planci (Sano et al. 1987, Berumen & Pratchett 2006), storm
damage (Halford et al. 2004) and experimental coral destruction (Sano et al. 1984,
Lewis 1997, Syms 1998, Syms & Jones 2000). In the last decades coral bleaching,
typically followed by coral death and erosion, has become a veritable menace to
coral reef ecosystems (Hughes et al. 2003, Hoegh-Guldberg 2004). Recent evidence
suggests that rising sea surface temperature, driven by climate change, will cause
increasingly frequent and widespread bleaching in the near future, with detrimental
consequences to reefs worldwide (Donner et al. 2005). Concurrently, changes in
ocean chemistry are threatening to reduce coral calcification rates and rates of reef
accretion, further endangering coral reef recovery (Kleypas et al. 1999). In the light
of these threats, focus has shifted and the direct and indirect effects of widespread
bleaching-induced coral loss with limited recovery have become a key topic in reef
ecology and conservation. As a result, there is an emerging consensus among reef
ecologists that major impacts of coral bleaching events on associated fish
communities can be anticipated (Munday 2004, Jones et al. 2004, Pratchett et al.
2004, Sano 2004, Bellwood et al. 2006, Wilson et al. 2006, Graham et al. 2006).
The 1997/1998 El Niño Southern Oscillation (ENSO) was unprecedented, affecting
seawater temperatures worldwide (McPhaden 1999). As a result, extensive
bleaching occurred on nearly all coral reefs, followed by as much as 90 % coral
mortality at some localities (Wilkinson 2000). Given the structural properties of
corals, bleaching and subsequent coral death may dramatically change the reef
framework. Immediate effects of coral death include the reduction or loss of coral
tissue followed by rapid colonisation of turf algae (Diaz-Pulido & McCook
2002), with consequences for the re-colonisation by coral larvae (Birrell et al. 2005).
With time, dead corals typically break into pieces and coral rubble may, hence,
become the dominant substratum (Sano et al. 1987, Riegl 2001). Subsequently, other
sessile organisms such as macroalgae may take over, which further interfere with
recruitment and subsequent recovery of the coral community (McCook et al. 2001).
Although live coral and branching taxa in particular, are considered to provide
favourable habitats for a number of demersal fishes (Bell & Galzin 1984, Chabanet
et al. 1997), there are only a few species that are known to be entirely dependent on
live coral for food (Reese 1981, McIlwain & Jones 1997), while the majority of
associations are due to shelter-dependence. Consequently, erosion may be more
dramatic to fish assemblages than the initial coral death. In addition, the longevity of
the typical adult reef fish (Choat and Robertson 2002), as well as their mobility
compared to conspecific recruits, make responses among them less likely to be
manifested in short-term studies. Hence, consideration of long-term impacts of reef
fish assemblages to coral death is crucial.
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The algal habitat
Evidence from temperate regions show that submerged vegetation has the potential
to impact distribution patterns of both marine and freshwater fish (DeMartini &
Roberts 1990, Jones 1992, Pihl et al. 1994, Duffy & Balz 1998) in particular by
increasing the amount of available refuge and altering the availability of food
resources (Rozas & Odum 1988) for herbivores, invertebrate feeders and omnivores,
which predate on associated epifauna. Although herbivory is widespread among
fishes in the tropics, macroalgae is of minor importance as a direct food resource for
herbivorous fish (Choat et al. 2004). Late successional algae typically have lower
photosynthetic rates and net production, as well as a reduced nutritive content and
increased chemical defences resulting in lower palatability than early successional
and opportunistic turf algae (Hay 1997). Consequently, most herbivorous fish, with
the exception of a small guild of macrophyte browsers, forage in turf algae (Choat et
al. 2004), and the overgrowth of turf algae and encrusting corallines by fleshy algae
is likely to restrict foraging among herbivorous fish (McClanahan et al. 1999,
Williams & Polunin 2001, but see Ceccarelli et al. 2005). Meanwhile, herbivory has
on many reefs has been hampered by intense fishing (Hughes 1994, Jackson et al.
2001) and the lack of this function may affect the balance between the coral and
algae community, potentially causing advantages for algal proliferation (Hughes
1994). Combined with chronic disturbances, such as nutrient loading, coral disease
and systematic overfishing, acute disturbances such as bleaching-induced coral
mortality may cause the reef environment to shift from coral to algae dominance (for
review, see McManus & Polsenberg 2004).
Concurrently, lagoon environments in the Indo-Pacific are cleared from coral and
seagrass to provide for the cultivation of macroalgae, which is harvested for the
production of food, agar and carageenan (Jensen 1993). While the effects of this
mariculture on associated plant and invertebrate communities have been documented
(Johnstone & Ólafsson 1995, Ólafsson et al. 1995, Eklöf et al. 2005, 2006a) there is
still limited information on how algal farming may influence fish assemblages (but
see Eklöf et al. 2006b).
Objectives in brief
The overall aim of this thesis was to understand in which ways spatial variation in
fish assemblage composition is related to habitat structure, and subsequently to
explore the effects of alterations in habitat structure on associated fish assemblages.
Paper I
Paper II
Paper III
Paper IV
To assess the influence of habitat structure on the distribution and
abundance of Pomacentrus sulfureus, a western Indian Ocean
damselfish.
To examine reef fish assemblage patterns over a range of sites in
relation to spatially variable habitat structure, largely influenced by a
recent bleaching event.
To describe habitat use and distribution patterns by reef fish recruits in
relation to adult habitat use and distribution patterns, at a number of
sites which vary in their degree of degradation due to recent bleaching.
To assess the influence of habitat alteration related to algal farming
(Eucheuma spp) on shallow lagoon fish assemblages.
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Paper V
Paper VI
To assess the influence of habitat alteration caused by extensive
macroalgal reduction on reef fish assemblages.
To assess the influence of habitat alteration caused by coral bleaching
on reef fish assemblages.
PAPERS IN BRIEF
Paper I. Linking the abundance of one species to habitat variables,
while comparing two measures of structural complexity
The first study explored the spatial variation of P. sulfureus among sites situated
around Zanzibar Island, Tanzania. The ecology of this damselfish, which is
relatively common on many reefs in the western Indian Ocean, had not been
previously described. Damselfishes (Pomacentridae) constitute a diversified family
of conspicuous fishes that are found in shallow habitats throughout the tropical seas.
Densities of juvenile and adult P. sulfureus were examined in relation to both
taxonomic and structural features of the habitat, on a scale relevant to the study
species. With the hypothesis that fine-scale structural complexity may be important
to this damsel, the percent cover of all branching structures (potentially providing
shelter to small fish) was included as a measure of structural complexity, in addition
to the commonly used contour measure (Risk 1972). Quantitative surveys of P.
sulfureus revealed that this species was distributed in an uneven pattern around
Zanzibar Island and that the distribution reflected local and regional differences in
habitat structure, which in turn may have been related to variations in flow and
exposure regimes. The multiple regression models, which identified relationships
between juvenile and adult P. sulfureus abundance and specific habitat features,
revealed that the majority of the variation in juvenile numbers was attributed to
percent cover of branching structures, the high-resolution measure. In contrast, the
low-resolution measure of structural complexity (rugosity) did not influence neither
adult nor juvenile abundance and may not have been a relevant measure for this
small reef fish. The best predictor of adult abundance was substrate diversity
(inverse relationship). The results indicated that P. sulfureus exhibit an ontogenetic
shift in habitat use and that the limited habitat use of juvenile P. sulfureus is
contained within that of conspecific adults, and that juveniles are likely to adopt
more general habitat associations as they grow.
Paper II. A study of whole-fish assemblages in a locality affected by
recent coral bleaching
The second paper moves on from the investigation of a singe species (Paper I) to
the study of whole-fish assemblages at a number of sites within the Mafia Island
Marine Park (MIMP), Tanzania. Given that coral cover in MIMP had been severely
is impacted by the 1998 bleaching event (Souter et al. 2000, Lindahl et al. 2001),
this study aimed to explore fish-habitat associations with special attention given to
the potential effects of live coral, dead coral and structural complexity. Although the
effects of coral cover on fish abundance and diversity have been rigorously explored
(e.g. Bell & Galzin 1984, Chabanet et al. 1997), reports on how dead coral
influences fish assemblages are limited (but see Sano et al. 1984, Lewis 1997). This
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study was further intended as a framework for a comparison of pre- and postdisturbance fish assemblages (Paper VI) conducted in a more limited area (included
among the sites of Paper II), as well as a study of habitat use among recruits (Paper
III). Paper II constitutes one of few comprehensive quantitative descriptions of
coral reefs and associated fish assemblages in Tanzania. In total, 395 species
belonging to 56 families were recorded. Multivariate ordinations, based on the data
from 11 sites demonstrated that reef communities in MIMP differed among reefs
and in relation to depth, exposure and geographic location, and that fish assemblage
composition varied among sites in concordance with the habitats provided. In all,
mean live coral cover in the park was 14 %, while dead coral cover comprised close
to 50 % of the substrate. Sites with highest proportion of dead coral exhibited
highest degree of among-transect variability. Stepwise multiple regressions showed
that habitat variables explained a large part of the variation in species numbers and
in total, and taxon-specific, abundance. Live coral cover was the foremost predictor
of both numerical and species abundance, as well as of corallivores, invertivores,
planktivores and of the families Pomacentridae, Chaetodontidae and Pomacanthidae.
In contrast, the proportion of branching substrates, the foremost predictor of P.
sulfureus (Paper I), did not explain any of variation in the fish descriptors. Given
the demonstrated influence of live coral cover, as well as the large proportion of
dead coral recorded in the area, it is likely that the recent coral mortality had had an
influence on the distribution and abundance of reef-associated fish in MIMP.
Paper III. Exploring microhabitat use by reef fish recruits, comparing
sites subjected to varying degree of coral degradation
While Paper II demonstrated that habitat structure is an important regulator for
adult reef fish and that live coral may be particularly important, Paper III explored
the habitat use of recruits. The study examined the habitat use by almost 3000
recruits comprising 56 taxa at seven sites in MIMP. In the light of ongoing habitat
degradation, the presence of both recruit- and adult habitat has been suggested as a
requirement for the local persistence of habitat-dependent reef fishes (Jones et al.
2004). Among coral reef fish, selective habitat use has been recorded in one or more
life-stages for a number of species and identified at various scales from among
microhabitats to across shelf (Williams 1982, Sale et al. 1984, Fowler et al. 1992).
The study compared both species-specific densities and habitat use among sites and
in relation to adult distribution patterns. The quantitative estimates revealed that
recruit densities ranged between 0·10 (± 0·03 SE) m-2 and 0·69 (± 0·23 SE) m-2.
Although live coral represented only 15 % of the overall measured substrate
composition, almost half of all observed recruits were found in this substrate. Pooled
across all sites, 46 % of the recruits used live coral cover in disproportion to
availability. Among the 11 most common recruit taxa 10 exhibited non-random
habitat use and six associated with live coral in disproportion to availability. Among
adults, four of these showed significant relationships with live coral. In contrast, the
abundance of both recruits and adults was inversely related to that of dead coral in
MIMP. Only 25% of all recruit recordings were made in dead coral, despite dead
coral and rubble being the dominating substrate at all but one site in MIMP.
According to predictions, the lack of recruitment habitat at the most degraded site
was manifested as a discrepancy between recruit and adult community composition.
Paper III demonstrated that reef fish recruits used habitats non-randomly and that a
17
substantial proportion was selective towards live coral. Close associations between
fish and habitat for both recruits and adults are likely to result in substantial impacts
of habitat degradation.
Paper IV. Investigating the effects of algal farming on fish assemblages
in shallow lagoons
In the same way coral cover and structural complexity exerts a major influence in
the reef environment (Papers I-III), the influence of submerged vegetation on
associated fish distribution and abundance has repeatedly been demonstrated
(DeMartini & Roberts 1990, Jones 1992, Duffy & Balz 1998). Paper IV ventured
away from the reef and into the shallow coastal lagoons. This environment shares a
number of species with the reefs and has been identified as a potential nursery area
for some of the fishes that in later stages enter the reef habitat (Nagelkerken et al.
2001, Adams & Ebersole 2004). Macroalgae are cultivated and harvested in a
number of tropical countries, including Tanzania (Lirasan & Twide 1993), where
shallow lagoons along the eastern coast of Zanzibar Island constitute favourable
environments for algal farming. The farms consist of numerous ropes called
monolines, to which the thalli of the red algae, Eucheuma, are attached. With these
dense rows of algae, a different habitat is introduced in an environment where earlier
there was only sand, seagrass and the occasional coral thicket. Fish assemblages in
two lagoons where Eucheuma was farmed were investigated and compared to those
at control sites situated within the same lagoons. Visual belt transect counts
identified 101 species of fish belonging to 31 families. Only 15 of the species were
present at both locations. Multivariate analyses revealed that fish community
composition was related to the nature of the substrate in respective lagoon. Algal
farms hosted distinct fish assemblages in terms of abundance, species richness and
trophic identity. At one of the locations, where farming was intense and had a longer
history, and where non-farmed habitats exhibited low structural complexity and
diversity, algal farms hosted a more abundant and diverse fish fauna than controls.
At the other location, where farming started more recently and remained less
intense, and where the surrounding lagoon provided more varied and structurally
complex substrates, overall fish abundance was lower in farms than at control sites.
The results indicate that the impact of habitat alteration is related to the history of
disturbance as well as to the pre-disturbance species composition and the
characteristics of the pre-disturbance habitat.
Paper V. A study of reef fish assemblages subjected to experimental
algae reduction
The relationship between macroalgae and fish was further explored in Paper V,
which described a large-scale algae removal experiment on Glovers Reef, Belize, to
understand the consequences of large-scale macroalgal overgrowth for coral reef
fish. In this study macroalgae was manually reduced on eight patch reefs (average
size ~1000 m2), among which half were situated in a new no-fishing zone and half
in an unrestricted fishing zone. Another eight reefs were left as non-manipulated
controls in each respective zone. The immediate response of fishes to the algal
reduction were examined with particular focus on the response of species feeding on
algae or in the epilithic algal matrix (EAM) such as surgeon (Acanthuridae), damsel
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(Pomacentridae) and parrotfishes (Scaridae). A similar study had recently been
carried out in Kenya (McClanahan et al. 1999) and an additional objective was to
test the generality of the obtained results by using this West Atlantic site as a
comparison. Multivariate ordination of fish assemblage data indicated that the algal
removal had marginal effect on whole-fish assemblages but that the effect was
highly significant on the biomass of common grazers. In addition, increased activity
was recorded for major grazing fish following the algal reduction. The results of this
experiment supported the Kenyan study (McClanahan et al. 1999) suggesting that
overgrowth of turf algae and encrusting corallines by fleshy algae could suppress
foraging and limit distributions grazers and EAM feeders. Following the reduction
of macroalgae, increased accessibility and net production of early successional turf
were likely to have accounted for the increase in numbers, biomass and feeding
rates of the dominant grazers.
Paper VI. Exploring the response of fish assemblages on small patch
reefs to bleaching-induced coral mortality
While Papers I-V demonstrated that fish assemblages vary with habitat structure
and particularly implicated the importance of live coral, Paper VI was following
fish assemblages on patches of transplanted coral over time, recording immediate
and long-term impacts of bleaching-induced coral mortality. In this study the coral
plots were re-investigated six years after the 1997-1998 bleaching event and fish
assemblage composition was compared to that recorded by Lindahl et al. (2001) six
months after the disturbance. Given the poor post-bleaching recovery on these reefs
(Papers II-III), we predicted a long-term response in fish community composition
related to the reduction of structural complexity in the habitat. Multivariate
ordination of fish community data demonstrated significant changes in composition
related to the habitat alteration. Within-site variability increased with disturbance,
the increase being most apparent following substrate erosion. The discrepancies
between long-term and short-term responses were striking and underline the
importance of long-term monitoring of fish assemblages following habitat alteration.
Six years after the impact, the initial post-disturbance increase in fish abundance
observed in 1998 (Lindahl et al. 2001) was reversed and more variable fish
assemblages with comparatively less individuals and taxa than both before and
shortly after the 1998 bleaching were recorded in the resulting low-relief
environment. Functional groups, with documented affiliations with coral, were
particularly influenced by the habitat alteration and most eventually disappeared
altogether. The abundance of species feeding on algae or associated detrital
resources increased as an immediate response to bleaching, but was subsequently
decimated in the eroded habitat. In conclusion, it was evident that widespread
catastrophic bleaching may have long-term effects on associated fish fauna.
19
GENERAL METHODS
Study sites
Western Indian Ocean
The majority of the work displayed in this thesis (Papers I-IV, VI) was conducted
in the western Indian Ocean. Historically most reef fish ecologists have conducted
their research in the Indo-west Pacific as well as in the Caribbean. In the light of this
geographic imbalance, the recent interest in reef fish ecology in the western Indian
Ocean reef is much welcomed (e.g. Graham et al. 2006, Graham et al. 2007).
Zanzibar, Tanzania
Two studies were conducted in the waters surrounding Zanzibar Island (Unguja),
Tanzania (Papers I, IV). The island is situated 35 km from the African mainland in
the western Indian Ocean. Narrow reefs situated close to shore, fringe most of the
eastern coast of Zanzibar, while on the western coast, reefs of limited extent
circumscribe rock island and sandbanks (for details, see Nsajigwa et al. 2002). The
western reefs are generally more protected in terms of waves and currents than the
eastern reefs. The study of Pomacentrus sulfureus (Paper I) included 11 reef sites
around Zanzibar with substantial among-site differences in hydrodynamic conditions
and habitat structure. The degree of anthropogenic disturbance is likely to have
varied among sites, with western sites likely to be more impacted than eastern sites.
Western reefs were situated at different distances to Zanzibar Town, from where
sewage was discharged untreated into the sea, with consequential elevations of e.g.
nutrient levels (Björk et al. 1995) and water turbidity (Muhando et al. 2002). Degree
of protection against resource use also varied among reef sites at the time of the
survey. The study of algal farming (Paper IV) was conducted in two shallow
lagoons on the eastern coast of Zanzibar. In Kiwengwa, the fringing reef was
situated approximately 800 – 900 m offshore, and along the coast large sandy flats
with minor patches of algal turf and seagrass were interspersed with seagrass beds.
In Matemwe, the distance from the shore to the reef was only 400 – 500 m and the
natural substrate in the coastal back-reef lagoon was heterogeneous, including a
mixture of sand, soft corals, small colonies of scleractinian coral (< 1 m2), rubble
and small patches of algae and seagrass.
Mafia Island Marine Park, Tanzania
Three studies (Papers II-III, VI) were conducted in the waters of Mafia Island
Marine Park (MIMP), situated ~120 km south of Zanzibar, 60 km south of Dar es
Salaam and 21 km east of the Rufiji delta, at the edge of the continental shelf of the
African mainland. The marine park, which was declared in 1995, covers an area of
822 km2. Within the park, there are restrictions on resource usage, and although
fishing is conducted within the park, destructive fishing practices and coral mining
are prohibited. In total 11 sites within the park have been investigated (all presented
in Paper II). Typically, the reefs surveyed were not uniform in structure, nor did
they exhibit similar and predictable zonation patterns, as those described in other
geographical regions (e.g. Done 1982). Tanzanian reefs are subjected to the East
African Coastal Current, which flows north along the coast of Tanzania and Kenya.
Currents are locally modified by prevailing monsoon and tidal patterns causing a
complex and multidirectional current system. Further, the reefs experience mixed
semidiurnal tides with mean spring amplitude of 3.3 m. From November to March,
20
the northeast monsoon blows with moderate force whereas the stronger southeast
monsoon prevails from May to October.
Caribbean
Coral reefs in the Caribbean have experienced repeated disturbance over the past
few decades, resulting in the loss of hard coral cover and reefs dominated by various
forms of fleshy algae (Hughes 1994, McClanahan & Muthiga 1998, Gardner et al.
2003). This ecological change has been associated with disease-induced coral
mortality (Aronson & Precht 2001), loss of the important grazing sea urchin
(Diadema antillarum, Carpenter 1990), cyclones (Mumby 1999), increased fishing
pressure (Hughes 1994, Jackson et al. 2001), coral bleaching (Ostrander et al. 2000,
but see Mumby 1999) and seawater nutrient concentrations (LaPointe 1999).
Glovers Reef, Belize
Glovers Reef is a 260 km2 atoll located approximately 15 km east of the Belizean
Barrier reef. The atoll is a nearly continuous reef with three large tidal channels and
~ 850 patch reefs within the lagoon. The outer edge of the atoll drops into deep
water (> 500 m) while the central lagoon seldom exceeds 20 m in depth. Patch reefs,
the focus of the study, occurred in the lagoon and varied in size from ~25 m2 to
~10,000 m2 and were separated by sand and seagrass beds with the distance between
the nearest-neighbour patch reef seldom exceeding 30 m. The Belizean Fisheries
Department zoned the atoll into four fisheries management zones and began
management in June 1996. The southern half of the atoll is divided into Wilderness,
Conservation and General Use Zones. The Wilderness and Conservation Zones
exclude virtually all forms of fishing. The General Use Zone allows the controlled
continuation of existing fisheries practices while the fourth zone is a seasonal
closure area of a grouper spawning ground on the north-east end of the atoll. Algae
removal and subsequent fish surveys were carried out in the Wilderness and the
General Use Zones.
Field methods
Fish sampling
For the purpose of this thesis, fish have been surveyed in various ways including
simultaneous belt transects (Papers I-III, IV), timed counts on whole patch reefs
(Paper V), timed counts in quadrates of limited size (Paper VI) and nonquantitative sampling of habitat use by recruits within a set site (Paper III). In the
belt transect method a 20 (Papers I, IV) or 25 m (Papers II-III) transect was laid
out parallel to the reef slope while simultaneously counting large, fast-swimming
and shy species within 4 (Papers I, IV) or 5 m (Papers II-III) width. After waiting
10 minutes, the investigator returned along the transect, while recording site attached
fish larger than 10 cm. The diver then swam the transect once more while counting
recruits, cryptic species and pomacentrids within a width of 1 m. The investigators
(KCG in Papers I, III, SS in Paper IV) spent a set amount of time on each count
and replicates ranged between five (Paper I) and 10 (Papers II-IV). Fishes were
identified to lowest taxa and the abundance of schooling fish and fishes occurring in
higher densities were estimated using abundance categories in a log3 scale (1, 2 - 3, 4
- 9, 10 - 27, 28 - 81, 82 - 243, etc.).
21
The timed counts used on Belizean patch reefs sampled a limited number of species
during each single search-sampling period of 5 min. In Paper V seven such distinct
groups were sampled during the total sampling period, during which the investigator
(KCG) swam haphazardly over each patch reef. The counts were restricted to
individuals > 3 cm and fishes of special interest were assigned to different size
classes. The 35 min sampling period was repeated twice.
When examining the response of fish assemblages to coral death and erosion in plots
of transplanted coral (Paper VI), a stationary survey method modified from
Bohnsack & Bannerot (1986) was used. During the census, the diver rested at the
seabed approximately 1 m from the edge of the plot and counted all fishes in the
plot, including transient as well as stationary fishes, for a period of 10 minutes on
each occasion. Only fish occurring up to 1.5 m above the seabed were counted. Each
count was replicated three times on different days.
In order to identify patterns of microhabitat use by recruits (Paper III) at seven of
the MIMP sites, the investigator (KCG) spent on average 160 min per site, while
recording the depth and microhabitat of each recruit encountered. Many fishes
exhibit gregarious settlement and while each group of individuals was recorded as
an independent observation, the number of individuals in each group was also
documented. As with the transect counts, the number of individuals in larger groups,
were estimated applying abundance categories in log3 scale. The microhabitats used
by recruits were typified using the same categories as in point-base surveys of the
transect substrate (Papers I-III). In addition, depth and the occurrence of overhangs
near the recruits were recorded. Recruits were identified by morphology, colour and
size (typically < 2.5 cm although depending on taxon).
In order to estimate the potential effects of the algal reduction on herbivorous fish
feeding and aggression patterns (Paper V), direct observations on bite rates and
aggression were carried out on a few dominant grazers. The observer (KCG)
followed each haphazardly selected individual for a 1 min observation period during
which all bites on substrate were recorded, as well as all interactions with other fish
(McClanahan et al. 1999).
Substrate sampling
In five of the six studies substrate was examined by a either a point-base method
(Wiens & Rotenberry 1981, Papers I-III) or line intercept method (LIT, English et
al. 1994, Papers IV-V). The point-base method included a rope which at 1-m
intervals, and perpendicular to the transect line was positioned, stretching out on
alternating sides of the main transect tape. The nature of the substrate was recorded
at five random points along this 1 m rope. The method yielded a number of sampling
points within the transect area, which were then used to calculate the proportional
cover of different substrates. At each point, the substrate was characterised
according to both taxonomic and structural properties. Within each site, transects
were separated by a minimum distance of 45 m and replicated five (Paper I) to 10
times (Papers II-III). The LIT method records the exact substrate composition
underneath the transect line. The fractional lengths of the components intercepting
the transect were measured to the nearest centimetre.
22
In the sixth study dealing with coral degradation due to bleaching (Paper VI) live
coral fragments were transplanted to 2.5 x 2.5 m2 plots. The character of the
substratum, including live and dead coral, coral rubble and sand, was estimated in
1997 and 1998 by point-sampling on projections of slide photographs taken at
several random positions in each plot. In addition, coral relief was estimated in 1998
and 2004 by placing two transect tapes, each with five regularly spaced 10 cm
sections, across each plot. The height above the substrate of the tallest coral branch
under each of the 10 cm sections was recorded, and the average of 10 such readings
was used to represent the relief of each plot.
Data analysis
In Papers II and IV fishes were divided into groups according to their feeding
ecology: corallivores, piscivores, invertebrate feeders, omnivores, herbivores and
planktivores, based on published material (Randall et al. 1990, Burgess et al. 1990,
Smith & Heemstra 1991) supplemented by field observations. Fishes typically
categorised as ‘herbivores’ constitute a heterogeneous group exhibiting various
feeding behaviours, such as browsing, scraping and excavating (Bellwood & Choat
1990). Some species commonly seen foraging on turf-covered substrates do not even
feed on vegetative material but on detritus caught in algae (epilitic algal matrix or
EAM, Choat et al. 2004). However, throughout this thesis, ‘herbivores’ is commonly
used to denominate all species foraging in algal habitat. In Paper V size-frequency
data was converted to biomass, using length-weight relationships (Bohnsack &
Harper 1998). Estimates of fish and substrate diversity (Papers I-II, IV) were
calculated using the Shannon-Wiener index (H’) using log base e. Finally, structural
complexity was described by the index R (Papers I-II), calculated as the average of
bottom contour to transect ratio (Risk 1972) as well as by the proportion of
branching structures (Papers I-III), calculated by adding the percentages of all
branching substrates, live or dead.
Given the objective of understanding patterns in of multi-species assemblages in
relation to among-site variability in habitat structure, multivariate techniques
provided valuable tools (Papers I-VI). Statistical differences among sites, depths
and exposure were typically analysed using analysis of similarity (ANOSIM,
Papers II-VI), which is an analogue of the analysis of variance (ANOVA) with a
randomisation test for significance. The analysis generates a measure of the degree
of separation among sites, R, which is close to zero when similarities between and
within sites are, on average, the same. An R value of one indicates that all replicates
within sites are more similar to each other than any replicate from different sites.
For valuable graphic display, the multivariate non-metric multi-dimensional scaling
ordination (MDS, Papers II-IV) provides a representation of community patterns
generated from a ranked similarity matrix based on the Bray-Curtis similarity
measure (Clarke 1993). Each point within the configuration represents the
community composition (e.g. fish or substrate) in one sample, in relation to other
samples. The closer two points are, the more similar are the associated communities.
The degree to which the distances between all points in the plot accurately represent
the similarity between them is quantified by the stress value, which shall remain
23
small for accurate interpretation. In Papers II and IV the RELATE procedure
(Clarke & Ainsworth 1993) examined the degree of agreement between two
multivariate scaling ordinations, using a modified form of Spearman rank correlation
called the weighted Spearman rank correlation, with a coefficient, ρw (Global rho),
which always lies between –1 and 1.
Similarity percentage analysis (SIMPER) was used in Papers IV-VI to identify δi
%, which is the proportional contribution of individual species (i), to the average
among-site dissimilarity (δ, Warwick et al. 1990). The Bray-Curtis measure of
dissimilarity δ takes on values in the range of 0 to 100 with δ = 100 representing
the case of no species in common and δ = 0 being two samples with identical
species patterns. SIMPER hence enables the identification of taxa to which specific
clustering of the MDS is attributable.
PCA is another exploratory ordination technique, which reduces data into fewer
dimensions. Variables are projected onto new axes or principal components (PC),
which account for a certain amount of variance of the sample. In Paper III
correlation-based PCA ordinations was carried out on square-root transformed
proportional substrate use by common recruits. PCA was further used to determine
taxon-specific among-site flexibility in microhabitat use.
Variability within communities has been suggested to be a symptom of disturbance
(Warwick & Clarke 1993). Comparing variability among sites (Paper II, VI) and
over time (Paper VI) was carried out by using the program MVDISP. To downweight large numbers and account for variation, all variables have been square root
or double square-root transformed prior to multivariate analyses.
Multivariate tools were complemented by several univariate tests including one-way
and two-way analysis of variance (Papers IV-V respectively), Kruskal-Walllis test
(Papers I, V), Spearman rank correlations (Paper III), t-tests (Papers V-VI),
Wilcoxon Signed Ranks, Mann Whitney U-tests and randomisation test (Paper VI).
When more than one statistical test is performed, the risk of incorrectly declaring
significance increases. In order to ensure that this risk remained at the commonly
applied limit of 5 %, a downwards adjustment of the alpha value of each individual
test may be used. In Papers III-V the Bonferroni correction method was chosen,
which divides the alpha value by the number of tests performed (Holm 1979).
In an attempt to reveal potential relationships between fish abundance data and
habitat characteristics in Papers I-II, forward stepwise multiple regression analyses
were performed (Sokal & Rohlf 1995). Among a set of independent variables
(habitat characteristics), the forward selection procedure identifies the minimum set
of predictors, which together explains the maximum total variance accounted for by
the regression, and consequently represent the most plausible causal links to the
dependent variables, which in our case included site averages of fish abundance,
species richness, diversity and abundance of the major fish families and feeding
categories.
24
GENERAL DISCUSSION
Evidence of non-random habitat use
This thesis provides evidence that coral reef fish, like many other organisms, exhibit
non-random and predictable spatial distribution associated with habitat structure.
The results comply with previous work, clearly pointing out the significance of live
coral and structural complexity for both the abundance and richness of fish
communities (Paper I-III, VI). Three life stages of reef fish were studied: recruits
(Paper III), juveniles (Paper I) and adults (Paper I-VI), and while preferences or
use may differ among life stages, non-random habitat use was demonstrated in all of
them.
Non-random habitat use at one or more life-stage has been recorded in a number of
taxa and identified at various scales from among microhabitats (Sale et al.1984, Ault
& Johnson 1998) to across continental shelf (Williams 1982, Fowler et al. 1992).
Among newly recruited coral reef fish in Mafia Island Marine Park, only a small
fraction used microhabitat in proportion to availability while the rest appeared
selective. Approximately half of the encountered recruits (species and individuals)
were selective towards live coral and two thirds of all recorded individuals were
observed in structurally complex substrates (Paper III). These results can be
compared with those of Jones et al. (2004), who in a study from Papua New Guinea
found 65 % of all recruits to use live coral cover in disproportion to availability.
Corresponding to a decline in coral cover, Jones et al. (2004) further documented a
decrease in the abundance of species with coral-selective recruits. Thus, it appears
that the presence of recruitment habitat is vital in order to maintain adult population
size. Similarly, results from MIMP demonstrated that species, which as recruits
exhibited high selectivity towards coral, were limited in number or even absent from
sites suffering severe degradation and lack of live coral cover (Papers II-III).
Although a relationship between availability of required microhabitat and
recruitment have been demonstrated for many specialised taxa (Caselle & Warner
1996, Light & Jones 1997, Schmitt & Holbrook 2000, Holbrook et al. 2000), spatial
stochasticity in larval supply and/or post settlement mortality (Ault & Johnson 1998)
could potentially weaken it. It should further be noted, that contrary to one of the
early theories of reef fish distribution patterns (Smith & Tyler 1972), near-pristine
coral reefs (if they exist) are typically not filled with fish; in other words,
recruitment may be insufficient to fill available habitat and create observable
correlations between abundance and habitat availability (Ault & Johnson 1998).
Even when habitat is filled, it is typically difficult to evaluate whether a species is
constrained by the availability of suitable habitat or by larval supply. However,
given the current rate of reef degradation, the significance of habitat as a limiting
factor could be increasing, resulting in species-specific alterations in distribution
patterns and assemblage change due to short supply of e.g. live branching coral.
Reef fish recruits are typically sedentary and their microhabitat use is rather easy to
assess. Having survived the critical first period on the reef, they commonly go
through one or more ontogenetic shifts in habitat use (Light & Jones 1997, Lecchini
& Galzin 2005) often accompanied by changes in resource use (McIlwain & Jones
1997). Whether similar in habitat features, or entirely distinct from those of
25
conspecific recruits, home ranges typically expand with individual size (Alimov
2003, Paper I). Among Pomacentrus sulfureus, the focal species of Paper I,
juveniles were rarely found far from adults and it was suggested that the habitat
preferences of juveniles may have been contained within the larger home ranges of
adult conspecifics. In terms of habitat requirements, it should be noted that adults
may be more versatile due to their need not only of foraging habitat and potential
shelter, but of habitat in which successful reproduction can be achieved.
For many species in MIMP, habitat patterns of adult fish corresponded to those
observed at recruitment and hence live coral cover was the foremost habitat variable
explaining spatial variation in overall adult abundance and species richness (Paper
II). At least for specialised species, adult distribution patterns may also be related to
habitat availability (Munday et al. 1997, Holbrook et al. 2000). Besides, the density
of species undergoing ontogentic shifts in habitat use may be directly related the
local availability of nursery habitat (Adams & Ebersole 2004). However,
distribution over larger scales, like among reefs, lagoons, around islands and across
continental shelves, will always have to take many more features than microhabitat
and substrate into account. Hydrodynamic conditions are likely to differ among
reefs, typically affecting local habitat structure as well as fish recruitment and adult
distribution. Further, it is possible that the suitability of a given microhabitat is
context-specific, which means it will only be used if it occurs in a particular reef
area (Doherty et al. 1996). While distribution patterns appear related to habitat
variables (substrate, microhabitat), they may instead be responding to co-varying
environmental variables (e g hydrodynamic features) rather than the substrate
features. For example, in Paper I, we found juvenile P. sulfureus to be associating
with structurally complex substrates. Accordingly, they were common on the
sheltered site of the island where structurally complex habitat was dominating while
almost absent at exposed sites which were devoid of structurally complex habitat.
Yet, it would have been necessary to manipulate the structural features of the
habitat, offering similar substrate at all sites, in order to single out the potential
effect of location and specific environmental conditions associated with it, on
species distribution. This example clearly illustrates the difficulties of interpreting
single factor approaches for such complex organisms as reef fish. Although
desirable to simultaneously assess all habitat variables on all scales, it is for obvious
reasons not practical, and thus full understanding of these communities can only be
approached in small steps, ideally including both descriptive and experimental work.
Then, hopefully, together these pieces of information will provide an increasingly
more comprehensive understanding of fish distribution patterns.
The influence of structural complexity
Generally, the response of fish to habitat characteristics and particular substrates
may differ at different scales of spatial resolution as well as with taxonomic identity
and life stage. For instance, reef fishes range in adult body size over two orders of
magnitude, and they occupy home ranges from as small as a coral head to as large as
a reef. To facilitate interpretation, the scale at which the study object might perceive
the environment, should dictate the method used. However, although multiplespecies studies reduce the chances of targeting all taxon-specific habitat-relations, in
reality the practicality of different techniques often dictate the choice. Structural
26
complexity has been recorded using various techniques, including chain: link
measurements (Risk 1972), visual qualitative assessment (Caselle & Warner 1996,
Gratwicke & Speight 2005b), remote sensing (Kuffner et al. 2007) and detailed
measurements of variations in substrate height and angle (McCormick 1994). This
thesis includes several measures of structural complexity. For example, and as a
complement to the commonly used rugosity measure, the proportion of branching
structures, was introduced as a high resolution measure and correctly assumed more
relevant to small demersal reef fish, juveniles (Papers I) and recruits (Paper III). In
contrast, this measure had no effect on the broad taxonomic and trophic groups
examined in MIMP.
Despite the different methods used, there is a large body of evidence that structural
complexity plays a major role in shaping patterns of distribution and abundance of
tropical demersal fish (Chabanet et al. 1997, Friedlander & Parish 1998, Gratwicke
& Speight 2005a, Lingo & Szedlmayer 2006, Graham et al. 2006, Papers I, III,
VI). Although high structural complexity on a reef is commonly associated with
high live coral cover, live coral cover may decline without significantly reducing
structural complexity, as is typically the case shortly after coral mortality due to
bleaching or crown of thorn damage (Papers II-III, VI). In due course internal and
external erosion take their toll and colonies are reduced to rubble. However, shortly
following a major bleaching event, dead coral colonies may largely dominate. With
recurrent bleaching episodes, this ephemeral habitat may become increasingly
widespread, yet how fish relate to it has rarely been investigated. Papers II-III are
based on data recorded two years after the 1997-1998 bleaching event. At this time,
the loss of structural complexity was not as obvious as the loss of coral cover. Yet,
the fish fauna appeared already affected, as evidenced by distinct community
composition, low abundance, species richness and impoverished recruitment to
impacted sites (c.f. Bellwood et al. 2006, Wilson et al. 2006). Paper III reports that
25 % of all encountered recruits were observed in dead coral, and among those more
than half in dead coral with its structural complexity still retained, a highly
ephemeral habitat. Although community change was significant already six months
after coral death (Paper VI), the major loss of all species except a few generalists
occurred only after the erosion of the corals, which supports the fact that fish
assemblages are more affected by disturbances resulting in loss of habitat
complexity than those that cause coral mortality without reducing the reef
framework (Wilson et al. 2006, Paper VI). Extrapolating these results to all sites in
MIMP (Paper II), and considering that dead coral, consisting mainly of branching
and tabular corals, constituted almost half of examined substrate in 2000, the erosion
that since then inevitably has followed is likely to have had severe consequences for
associated fish assemblages.
Alteration in algal abundance
As a result of coral degradation many coral-dominated reefs have shifted towards
algae dominance (Hughes 1994, Bellwood et al. 2004), with potential consequences
for all reef-associated fauna, including fish (Paper V). Although the relationship
between coral death, algal increase, eutrophication and herbivory remains debated
(Williams & Polunin 2001, Burkepile & Hay 2006, Aronson & Precht 2006, Mumby
2006, Hughes et al. 2007), reduced herbivory due to the mass mortality of Diadema
27
and overfishing is believed to have facilitate algal increase (Hughes 1994,
McClanahan & Muthiga 1998, Jackson et al. 2001), which in turn may have
suppressed coral settlement and survival (Hughes 1989, McCook et al. 2001) with
consequences for coral recovery. Although potential for coral recruitment following
the restoration of Diadema populations was documented by Carpenter & Edmunds
(2006), there is generally little optimism about the future of Caribbean coral reefs
(Aronson & Precht 2006, Mumby 2006). With current levels of anthropogenic
disturbance, the algal dominance appears practically irreversible and according to
Aronson & Precht (2006), only major reef protection schemes in conjunction with
the reduction of green house gas emissions, could possibly promote coral recovery
in the Caribbean.
Given the previously limited spread of macroalgae on tropical reefs, this habitat has
received little attention, particularly among fish ecologist. With current rates of coral
degradation and subsequent algal increase, attention has increased, but the response
of associated fish assemblages to alterations in algal distribution and abundance
remain poorly understood (but see McClanahan et al. 1999, Sano 2001, Paper IVV). Sano (2001) reported increased species richness and densities in fish
assemblages following macroalgal overgrowth on a rubble reef in Iriomote Island,
Japan. Similar results were obtained following the transplantation of Sargassum to
sand, rock and rubble habitats on Cousin Island, Seychelles (Garpe, unpublished
data). Preliminary results indicated that fish assemblage alteration, in part the result
of recruitment, was dependent on the underlying substrate, as well as on macroalgal
height and density (c.f. Paper IV). It should be noted, however, that although
increased macroalgal abundance on a non-complex substrate (e.g. rubble) can
contribute to increased structural complexity with positive effects on associated fish,
it probably cannot be compared to coral recovery. Sano (2001) compared fish
assemblages on reefs where habitat had shifted towards macroalgae (dense
Sargassum) to those where coral had fully recovered, and found that although the
two habitats had many species in common, species richness was three times higher,
and density eight times higher in live coral than in algae.
The reverse process was explored in Paper V, in which fish abundance, biomass and
behaviour were analysed following experimental reduction of late successional
algae. The short-term (Paper V) and longer-term effects (McClanahan et al. 2001)
of algae removal on Glovers Reef, Belize, were limited. The increase in abundance
of a few species was interpreted as relocation from nearby reefs and related to the
increased accessibility of food resources, in terms of turf algae and associated
resources.
Where algae are cultivated, effects on the habitat include alteration in terms of
macrophyte abundance, macrobenthos, meiobenthos and sediment organic matter
(Ólafsson et al. 1995, Eklöf et al. 2005, Eklöf et al. 2006a). The farmed algae
typically increase the structural complexity while reducing the diversity of lagoon
habitats including sand, coral thickets and seagrass. Although far from conclusive,
significant influences on fish assemblage composition have been documented
visually (Paper IV) as well as inferred from local fishery catches (Eklöf et al.
2006b).
28
Reef fish communities facing habitat degradation
The influence of altered and/or degraded habitat structure on fish is typically
species-specific with versatility and vagility being important determinants of species
response (Swihart et al. 2003, Bellwood et al. 2006). Immediate assemblage change
is likely to be the result of species redistribution due to alterations in resource
patterns (Paper V, VI). In contrast, long-term change can be the result of processes
such as recruitment failure and increased post-settlement mortality. At first, coral
death is likely to deter coral associated species while favouring species foraging on
turf algae or associated resources (Paper VI). Given only partial mortality and/or
the persistence of structural complexity, the response may be minor or delayed
(Wilson et al. 2006, Feary et al. 2007). However, macroalgal overgrowth and/or
erosion will almost inevitably reduce the reef framework and alter habitat structure
with increasingly severe consequences for the associated fish assemblage (Feary et
al. 2007, Paper VI). A recent meta-analysis demonstrated that 62 % of examined
species (34 of 55) exhibited significant declines in abundance following ≥ 10 %
coral mortality (Wilson et al. 2006). The full long-term effects of major and
recurrent disturbances on fish assemblages have not yet been fully understood (but
see Halford et al. 2004, Bellwood et al. 2006, Berumen & Pratchett 2006) but from
other ecosystems the result of habitat degradation has typically included the decline
of specialists, leaving diminished communities dominated by mobile and widespread
habitat generalists (Swihart et al. 2003, Warren et al. 2001). While habitat
generalists may remain unaffected and perceive the fragmented coral reef habitat
simply as more heterogeneous, the loss of habitat may severely limit the distribution
of habitat specialists, which may be particularly true for coral feeders (Pratchett et
al. 2006) and dwellers (Munday 2004, Schmitt & Holbrook 2000, Feary et al. 2007,
Paper VI). Given evidence of high specialisation among reef fish recruits (Lecchini
& Galzin 2005, Jones et al. 2004, Paper III), the lack of suitable recruitment habitat
may effectively limit the distribution of species (Adams & Ebersole 2004, Jones et
al. 2004).
If habitat loss limits the settlement of certain species or if post-settlement survival is
reduced due to inferior habitat conditions (Booth & Beretta 2004), the response to
altered and/or degraded habitat would be discernable in the recruit community first.
Comparing recruit and adult communities among sites, Paper III revealed that
differences between proportional adult and recruit abundances of some of the most
common species were greatest at the most degraded reef. Although adults are
generally more mobile and hence potentially able to expand their home ranges or
relocate within sites, this pattern could also suggest that sublethal effects in adult
physical condition (from e.g. increased competition, reduced resources and
increased predation due to crowding) had not yet been manifested as a decline in
population size (Pratchett et al. 2004). Evidence from assemblages of small-bodied
cryptic fauna with limited life spans, has shown that the impacts of extensive
bleaching are still manifested in assemblage composition 5-35 generations following
the impact (Bellwood et al. 2006).
It should be noted that temporal patterns of assemblage change cannot automatically
be related to e.g. bleaching or other major disturbances. Assemblages may naturally
change over time, due to temporal variability in recruitment (Doherty 2002), fishing
pressure (Hawkins et al. 2006) and/or minor disturbance regimes (Graham et al.
29
2007). Due to natural variation, the lack of pre-disturbance data, long time series and
undisturbed control sites, may confound results where habitat disturbance is
widespread. In Paper VI the survival of four coral plots enabled a comparison over
time and allowed the identification of bleaching-induced coral mortality and
subsequent erosion of the reef framework as the factor foremost responsible for
assemblage change.
Coral reefs are among the most diverse ecosystems on earth (Reaka-Kudla 1996)
and throughout the tropics people are dependent on them for food, income and
coastal protection (Moberg & Folke 1999). As the frequency and magnitude of reef
disturbance increase, due to human activities and climate change, live coral is
declining worldwide (Wilkinson 2004, Gardner et al. 2003, Hughes et al. 2003,
Hoegh-Guldberg 2004). There is reason to believe that the impact of coral loss will
be significant, and almost certainly cause the decline of numerous reef species, with
recovery being slow and directly related to coral recovery (Halford et al. 2004, Sano
2000) and/or degree of protection (Hawkins et al. 2006). While there is evidence of
resilient reefs regaining almost full resemblance to pre-perturbation states (Halford
et al. 2004, Sano 2000), reefs experiencing widespread, multiple and/or recurrent
disturbance and reefs with limited connectivity to non-disturbed habitat face
diminished chances of recovery (Berumen & Pratchett 2006, Graham et al. 2006).
Although substantial dispersal ability generally reduces vulnerability to local habitat
degradation (Ford et al. 2001), global threats diminish the chances of restocking
depleted fish populations from unaffected source reefs. Consequently, fish
distributions may be altered and/or limited, potentially resulting in distorted food
webs and ultimately loss of ecosystem functions. Whether post-disturbance
alteration of fish assemblage composition will affect future resistance to disturbance
remains to be seen. There is much to learn about synergistic and sequential effects of
multiple disturbances on fish distribution and abundance patterns, but by now it is
clear that an increasing number of reef habitats, and their associated fish
assemblages, are being forced into alternative states and structures, the stability of
which remains to be evaluated.
30
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