Environmental biology of fishes, tập 94, số 4, 2012

Environ Biol Fish (2012) 94:579–590
DOI 10.1007/s10641-011-9964-2

Ontogenetic shifts in the habitat associations
of butterflyfishes (F. Chaetodontidae)
Nicholas J. Clark & Garry R. Russ

Received: 20 April 2011 / Accepted: 4 November 2011 / Published online: 18 January 2012
# Springer Science+Business Media B.V. 2012

Abstract The habitat associations of species are vital
in determining an organism’s vulnerability to environmental and anthropogenic stress. In the marine
environment, post-settlement processes such as ontogenetic shifts in habitat use can affect this vulnerability by subjecting a species to differing biological and
environmental conditions at various life stages. This
study documents the habitat associations of adult and
juvenile butterflyfishes on an inshore reef of the Great
Barrier Reef (GBR) to investigate if ontogenetic shifts
in habitat use occur, and if such shifts relate to the
trophic ecologies of species. Coral-feeding species
displayed highly concordant distributions among
adults and juveniles. In contrast, adults and juveniles
of species with wider dietary selectivities (generalists)
displayed significantly different distributions across
reef zones. Juvenile generalist feeders were limited to
the shallow, patchy areas of the reef flat whilst adult
conspecifics displayed comparatively wide distributions. Butterflyfishes with a heavy reliance on corals
for food appear to settle preferentially in areas with
high abundances of adult conspecifics, which may
partially explain why coral specialists are more
vulnerable to localized depletion events. In contrast,

generalist species utilize distinct habitats as adults and
N. J. Clark (*) : G. R. Russ
School of Marine & Tropical Biology and the ARC Centre
for Coral Reef Studies, James Cook University,
Townsville QLD 4811, Australia
e-mail:

juveniles, suggesting that generalist butterflyfishes
expand their ranges and are therefore subjected to
changing environmental conditions as they reach
adulthood.
Keywords Habitat association . Ontogeny .
Abundance . Coral reef . Butterflyfish . Chaetodontidae

Introduction
The larvae of coral reef fishes utilize a suite of
sensory cues to settle into specific regions of the reef
(Stobutzki 1998; Leis and Carson-Ewart 2003), areas
that may differ from habitats occupied by adult
conspecifics (Mumby 2006). Recruits and juveniles
of reef fish often utilise distinct habitats compared to
adults (Jones et al. 2010) and thus each life-stage may
be subject to different ecological and environmental
influences. Moreover, alterations to benthic composition and complexity, for example coral bleaching
events (Graham et al. 2009), may modify recruitment
patterns (Moore and Elmendorf 2006; Feary et al.
2007). Thus, post-settlement processes, such as
ontogenetic shifts in habitat use, may influence a
species’ vulnerability to stress. Therefore, we can
better understand how disturbances may affect reef

fish population dynamics by determining the habitat
associations of vulnerable species.
Butterflyfishes (Family Chaetodontidae) are a
conspicuous, diverse group of fishes that exhibit


580

strong associations with coral reefs (Pratchett et al.
2008b). The heavy reliance of these fish on coral reefs
is due to an abundance of coral-feeding species, with
butterflyfishes making up 61% of all corallivorous
fishes (Bellwood et al. 2010). Moreover, several
species exhibit considerable feeding selectivity, preferentially feeding on only a few species of coral
(Pratchett 2007) despite relatively wide geographic
distributions (Allen et al. 2003; Froese and Pauly
2008). Consequently, butterflyfishes often show
marked decreases in abundance following disturbance
to coral reefs (Jones et al. 2004; Pratchett et al. 2006).
Lower abundances could in turn lead to reduced larval
production and decreased recruitment (Donelson et al.
2008), exacerbating population declines. Given their
strong ties to reefs and high vulnerability to disturbance (Wilson et al. 2006; Pratchett et al. 2008a),
butterflyfishes are a model study group to explore
ontogenetic variation in habitat association on coral reefs.
The habitat associations of butterflyfishes indicate
a heavy reliance on living corals as adults and variable
associations with coral as juveniles (Harmelin-Vivien
1989; Pratchett et al. 2008b). This suggests that
some species of butterflyfish may display ontogenetic

shifts in habitat. In addition to ontogenetic shifts in
habitat association, the distributions of juvenile reef
fishes may also be strongly regulated by both interand intra-specific competition (e.g., Munday 2001).
For instance, in a study conducted at Lizard Island on
the mid shelf of the Great Barrier Reef (GBR),
Berumen and Pratchett (2006) found that dominant
butterflyfish competitors such as Chaetodon baronessa aggressively defended territories against both
conspecifics and subordinate species and increased
their territory sizes as abundance of coral prey
declined. This propensity for aggression, particularly
against conspecifics, may directly influence the settlement preferences and spatial distributions of juveniles.
Therefore, some recruits may be forced to settle into
sub-optimal habitats due to antagonistic interactions
with adults (e.g., Munday 2001). In particular, competition among coral feeders may result in intraspecific
spatial partitioning in areas with relatively low
cover of commonly preferred Acropora and Pocillopora corals, such as the inshore reefs of the GBR
(Emslie et al. 2010). Therefore, the objective of this
study was to document the distributions and habitat
associations of adult and juvenile butterflyfishes on
inshore fringing reefs of the GBR. It was predicted

Environ Biol Fish (2012) 94:579–590

that coral-feeding butterflyfishes would display ontogenetic variation in habitat association in response to
low prey availability. For generalist feeders, which
exhibit higher dietary versatilities than coral feeders
(Pratchett 2005), we also predicted an ontogenetic
shift in habitat association. Generalist feeders expand
their range of prey items as they reach adulthood
(Harmelin-Vivien 1989), which has been suggested to

result in an expansion in habitat use upon maturity
(Pratchett et al. 2008b).

Methods
Study sites
This study was conducted in September and October
2010 in the Palm Islands (18˚34′S, 146˚29′E) on the
inshore GBR (Fig. 1). The Palm Island group consists
of nine islands located approximately 15 km off the
mainland. Surveys were made at three levels of
exposure to winds and currents (sheltered, obliquely
exposed, and exposed; Fig. 1) to investigate if
exposure affected coral and butterflyfish communities
(following Pratchett et al. 2008b). The degree of
exposure was determined according to multiple
observations of surge, wind speed, and the overall
direction of currents during the study. Sites with full
protection from prevailing winds were considered
sheltered, sites in which the reef faced parallel to
oncoming surge and currents were considered
obliquely exposed, and sites that faced directly into
surge, currents, and prevailing winds were considered
exposed. The fringing reefs of the Palm Islands have
an extensive shallow reef flat and mild reef slope
gradient at sheltered sites, and a relatively narrow reef
flat and steeply sloping reef wall at exposed sites.
However, despite the variation in gradients of the reef
slope between exposed and sheltered sites, the
physiognomic reef zones of flat, crest, and slope are
typically distinguishable at each location. At all

locations, the reef flat has patchy coral cover and
extensive areas of rubble, sand, and algae-covered
rock. In contrast, the reef crest and reef slope are
relatively rugose areas consisting of large bommies
(coral heads) and crevasses. In general, the study sites
are characterized by high abundances of Alcyoniid
soft corals and scleractinian corals belonging to the
family Poritidae (Emslie et al. 2010).


Environ Biol Fish (2012) 94:579–590

581

Fig. 1 Map of sampling
sites within the Palm
Islands on the inshore Great
Barrier Reef

N

Pelorus

sheltered sites
obliquely exposed
sites
exposed sites

Prevailing wind direction

Australia

Orpheus

Curacoa

3 km

Surveys
Twenty-seven sites were surveyed for butterflyfish
abundance and benthic cover (Fig. 1). Butterflyfish
abundance was estimated by underwater visual census
(UVC) along 50 m transects using a combination of
SCUBA and snorkel. Surveys were made in the three
reef zones (flat, crest, and slope), as coral reef fishes
often occur in assemblages that are characteristic of
each physiognomic zone (Russ 1984a, b). Study sites
were chosen to be relatively well-spread around the
coasts of Pelorus, Curacao and northern Orpheus Islands
(Fig. 1). To maintain safe dive practice, study sites
were selected daily at sea based on weather conditions. Transects were delineated by a 50 m fibreglass tape laid parallel to the reef crest in each of the
three reef zones, with depths ranging from 1–2 m
along the flat and crest and from 4–10 m along the
slope. The first observer counted butterflyfish within
1 m either side of their body while simultaneously
laying the transect tape. Individual butterflyfish were
visually placed into one of three size classes [<3 cm, 3–
10 cm, and >10 cm total length (TL)] corresponding to
the life-stage categories of new recruit, juvenile, and adult
(following Fowler 1990 and Pratchett et al. 2008b).

Size estimations were checked periodically underwater using a ruler printed on the back of the datasheets.
Benthic composition was measured by a second
observer. This permitted investigation of butterflyfish
habitat associations. Live coral cover was estimated
using a variation of the line point intercept technique
(Lam et al. 2006). A total of 100 randomly placed
points on the 50 m transect tape were sampled and

recorded into one of six categories (table Acropora,
staghorn Acropora, Pocillopora, Porites, other hard
coral, and soft coral). The sample points were placed
on the tape using a randomly generated number table
prior to the survey period. Three replicate transects
were surveyed in each zone at each site, yielding a
total of 243 transects across the 27 sites and a survey
area of 24 300 m2.
Analysis
Coral cover was analysed with an analysis of variance
(ANOVA) to investigate if variation in butterflyfish
abundance was related to spatial variation in coral cover.
To test for variations in the distributions of adult and
juvenile butterflyfish conspecifics, a series of 3-factor
multivariate analyses of variance (MANOVA) were
implemented. Prior to analysis, coral cover data and
butterflyfish abundance data were pooled at the site level
and standardised by area surveyed. Butterflyfish abundances were also pooled by trophic guild (i.e. hard coralfeeders, soft coral-feeders, or generalists) to investigate
the role of trophic guild in determining ontogenetic
variation in habitat association. All analyses of variance
were tested using a 3-factor orthogonal model, with island
(random), exposure (fixed), and reef zone (fixed) included

as the test variables. Butterflyfish abundance data were
square-root transformed and benthic cover data were
arcsine-root transformed to meet (M)ANOVA assumptions of normality, sphericity and homoscedasticity of
variance. Tukey’s HSD post-hoc tests were used to
identify homogenous groups following all analyses of
variance. Rather than performing correlations between


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Environ Biol Fish (2012) 94:579–590

Results

juvenile butterflyfish. Obligate hard-coral feeders
were the most abundant trophic guild, accounting
for 60.7% of individuals. Generalist and soft-coral
feeders accounted for the remaining 39.3%. Due to
the relatively low numbers of juveniles recorded for
several species, only the six most abundant species
(Chaetodon aureofasciatus, C. rainfordi, C. melannotus, C. lunulatus, C. vagabundus, and Chelmon
rostratus; 91.5% and 87.9% of juvenile and adult
recordings, respectively) were included in the PCA.

The butterflyfish assemblage

Benthic composition

A total of 1409 individual butterflyfish were recorded
on the 243 transects. The majority of individuals

recorded were adults or juveniles (Table 1). Recent
recruits were rare (except for C. aureofasciatus,
accounting for 48 of 50 total recruits). Thus, this
study only quantifies habitat associations of adult and

Among the 27 study sites, mean scleractinian (hard) coral
cover was 17.4±1.3%. In addition, hard coral cover was
variable among reef zones (Fig. 2). However, this
variation was not statistically significant (ANOVA,
Table 2). Most hard corals belonged to the ‘other hard
corals’ category (mean 8.5±1.6%; Fig. 2). Corals

butterflyfish and coral taxa, a principal components
analysis (PCA) was used to display variation in the
community structure of both butterflyfish and corals. The
analysis was performed using the correlation matrix
generated from the transformed butterflyfish and benthic
cover data. Statistical analyses were performed using
Statistica 10.0 (www.statsoft.com).

Table 1 Total abundances of butterflyfish (displayed by size class) within the Palm Islands. Totals are derived from 243 transects.
(HC), hard-coral feeder; (SC), soft-coral feeder; (G), generalist feeder
Orpheus Island
Adults

Pelorus Island
Juveniles

Adults

Curaoa Island
Juveniles

Adults

Juveniles

Total abundance
Chaetodon aureofasciatus (HC)
Chaetodon baronesssa (HC)
Chaetodon plebius (HC)

174

100

99

58

84

43

10

–

13

–

5

–

1

6

3

3

1

3

Chaetodon lunulatus (HC)

18

1

68

11

15

2

Chaetodon rainfordi (HC)

23

7

25

6

12

0

4

6

3

2

0

0

230

120

211

80

117

48

Chaetodon melannotus (SC)

47

11

86

8

101

10

Chaetodon trifascialis (HC)
Total hard-coral feeders
Total soft-coral feeders

47

11

86

8

101

10

Chaetodon auriga (G)

7

2

3

1

2

–

Chaetodon ephippium (G)

3

1

1

–

2

–

Chaetodon lineolatus (G)

14

1

4

–

5

–

Chaetodon lunula (G)

10

–

1

–

1

–

Chaetodon rafflesi (G)

14

–

14

1

4

–

Chaetodon vagabundus (G)

57

3

30

1

6

1

Chelmon rostratus (G)

24

1

26

4

30

3

Total generalist feeders

129

8

79

7

50

4

Mean abundance per site
Obligate hard-coral feeders

3.49±0.28

1.82±0.18

3.52±0.17

1.33±0.10

3.25±0.17

1.33±0.09

Soft-coral feeders

0.47±0.09

0.11±0.04

0.96±0.09

0.09±0.03

1.53±0.28

0.15±0.05

Generalists

1.68±0.69

0.10±0.03

1.13±0.49

0.10±0.06

1.19±0.50

0.10±0.07


Environ Biol Fish (2012) 94:579–590

belonging to the genus Porites were relatively
abundant (mean 6.7±1.2%), while both Acropora
(staghorn and table morphologies) and Pocillopora
were in much lower abundance (mean cover of 1.6±
0.04% and 0.6±0.01%, respectively; Fig. 2). Table
Acropora was rare in all locations. However, overall
cover of table Acropora was strongly related to
exposure, peaking along the exposed reef flat of

583

Orpheus and Pelorus Islands (Table 2) where wave

action and surge were strongest. Pocillopora and table
Acropora were in relatively low abundance on
Curacoa Island, where soft corals were abundant
(Table 3). Porites species showed no patterns of
abundance among islands (Table 2), having peak
cover in sheltered locations along the crest and slope
(Fig. 2). Soft coral was the dominant benthic
component surveyed, with a mean cover of 29.3±
2.2% among sites (Fig. 2). Nevertheless, the total
cover of both hard and soft corals was variable across
study sites. Total hard coral cover was lower in
obliquely exposed sites than either sheltered or
exposed sites (ANOVA, Table 2). In contrast, soft
coral cover was higher in obliquely exposed sites
(ANOVA, Table 3), where extensive beds of soft coral
were frequently observed. Additionally, soft coral was
more abundant on Curacoa Island than either Orpheus
or Pelorus Islands (ANOVA, Tables 2 and 3). No other
benthic components varied across islands. The remaining benthic categories surveyed (Pocillopora, staghorn
Acropora, and other hard corals) exhibited no variation
among zones or exposures (ANOVA, Table 2).
Habitat associations of adult vs. juvenile butterflyfish

Fig. 2 Mean cover of benthic components within the Palm
Islands according to reef zone and exposure. a flat; b crest; c
slope. TA, table Acropora; SA, staghorn Acropora; POC,
Pocillopora; POR, Porites; OHC, other hard coral; THC, total
hard coral; SC, soft coral. (■) sheltered locations; ( ) obliquely
exposed locations; (□) exposed locations

Butterflyfish abundances varied considerably among
locations and benthic compositions. Comparisons
among adults and juveniles revealed significant
intraspecific variation in the distributions of generalist
feeders and the soft coral feeder C. melannotus. For
the generalist feeders, ontogenetic variation in the use
of reef zones occurred (MANOVA, Table 4). Adult
generalists were abundant in all reef zones, while
juveniles were typically recorded only in the shallows
of the reef flat [Fig. 3(c), (d)]. In addition, abundances
of adult and juvenile generalists did not vary
significantly according to either island or level of
exposure (MANOVA, Table 4). For C. melannotus,
adult and juvenile distributions varied across exposures. Adults of C. melannotus were significantly
associated with exposed and obliquely exposed
locations (MANOVA, Tukey’s Homogenous Groups;
Table 4) while juveniles exhibited no clear pattern
among locations (Fig. 4). However, adults and
juveniles of C. melannotus were both significantly
more abundant on Curacoa Island than on either
Orpheus or Pelorus Islands (MANOVA, Tukey’s
Homogenous Groups; Tables 1 and 4), showing a


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Environ Biol Fish (2012) 94:579–590

Table 2 3-factor ANOVA results comparing benthic components among locations. Island (random), exposure (fixed), and
reef zone (fixed) were included as test variables. Results are

based on mean cover of benthic components, pooled across

Benthic component

Island
(random:
Orpheus,
Pelorus,
Curacoa)

Exposure
(fixed:
sheltered,
obliquely
exposed,
exposed)

2, 54 df

2, 54 df

sites. Benthic cover values were arcsine-root transformed to
meet ANOVA assumptions. Numerical values are F-statistics.
(*) significant at α=0.05

Island X
Exposure

Zone
(fixed:

flat, crest,
slope)

Island X
Zone

Exposure X
Zone

Island X
Exposure X
Zone

4, 54 df

2, 54 df

4, 54 df

4, 54 df

8, 54 df

Table Acropora

2.889 (ns)

2.569 (ns)

0.650 (ns)

3.725 (*)

0.229 (ns)

1.189 (ns)

0.273 (ns)

Staghorn Acropora

2.159 (ns)

2.529 (ns)

1.674 (ns)

0.562 (ns)

2.113 (ns)

0.955 (ns)

0.887 (ns)

Pocillopora

2.803 (ns)

2.640 (ns)

1.166 (ns)

1.170 (ns)

0.233 (ns)

0.288 (ns)

0.985 (ns)

13.688 (*)

0.662 (ns)

6.203 (*)

0.570 (ns)

0.665 (ns)

0.211 (ns)

13.513 (*)

2.331 (ns)

2.435 (ns)

0.519 (ns)

0.852 (ns)

0.825 (ns)

Porites
Soft Coral

0.248 (ns)
70.567 (*)

Other Hard Coral

0.106 (ns)

2.309 (ns)

2.554 (ns)

1.064 (ns)

0.204 (ns)

0.083 (ns)

0.341 (ns)

Total Hard Coral

0.633 (ns)

3.612 (*)

1.995 (ns)

1.632 (ns)

0.203 (ns)

0.423 (ns)

0.216 (ns)

similar abundance pattern across islands to that of soft
coral cover. In contrast to generalists and soft coral
feeders, hard coral feeding butterflyfishes showed no
significant variation in the distributions of adults and
juveniles across islands, exposures, or reef zones
(MANOVA, Table 4). Both adult and juvenile coral
feeders were significantly more abundant in sheltered
sites than either obliquely exposed or exposed sites
(MANOVA, Tukey’s Homogenous Groups: Table 4),
showing a similar pattern to that of hard coral cover.
Both hard- and soft-coral feeders showed no clear
intraspecific pattern in abundance across reef zones
[Fig. 3(a), (b)].
The PCA revealed some intraspecific variation in
benthic association for the six most abundant butterflyfishes (Fig. 5). For two of the coral-feeding species (C.
aureofasciatus and C. lunulatus), adults and juveniles

Table 3 Mean cover of benthic
components at each study
island within the Palm Islands

displayed comparable intraspecific distributions
among reef locations (Fig. 4). However, juveniles of
both C. aureofasciatus and C. lunulatus differed
substantially in their associations with benthic components compared to adult conspecifics (Fig. 5). For C.
aureofasciatus, adult abundance was positively correlated with several benthic categories (namely Porites,
other hard corals, and soft corals), while juveniles
were primarily associated with staghorn Acropora
(Fig. 5). In contrast, adults of C. lunulatus were
predominately associated with staghorn Acropora and
Pocillopora, while juveniles were more common in
areas with high coverage of Porites (Fig. 5).
In contrast to C. aureofasciatus and C. lunulatus,
the remaining four species analysed displayed similar
correlations among age groups and benthic categories
(C. rostratus, C. vagabundus, C. melannotus, and C.

Orpheus Island

Pelorus Island

Curacoa Island

Table Acropora

0.011±0.003

0.007±0.004

0.003±0.002

Staghorn Acropora

0.011±0.002

0.007±0.002

0.007±0.003

Pocillopora

0.008±0.002

0.006±0.002

0.004±0.001

Porites

0.033±0.008

0.044±0.011

0.034±0.013

Soft Coral

0.275±0.027

0.157±0.014

0.555±0.031

Other Hard Coral

0.120±0.015

0.107±0.020

0.120±0.015

Total Hard Coral

0.183±0.016

0.172±0.027

0.164±0.022


Environ Biol Fish (2012) 94:579–590

585

Table 4 3-factor MANOVA results from intraspecific comparisons of adult and juvenile butterflyfish abundances, pooled by
trophic guild. Island (random), exposure (fixed), and reef zone
(fixed) were included as test variables. Abundance and coral

Island
(random:
Orpheus,
Pelorus,
Curacoa)

Exposure
(fixed:
sheltered,
obliquely
exposed,
exposed)

Island X
Exposure

cover data were pooled across sites and standardised by survey
area. Butterflyfish abundance data were square-root transformed to meet MANOVA assumptions. Numerical values are
Pillai’s trace statistics. (*) significant at α=0.05
Zone
(fixed:
flat, crest,
slope)

Island X
Zone

Exposure X
Zone

Island X
Exposure X
Zone

Trophic guild

4, 108 df

4, 108 df

8, 108 df

4, 108 df

8, 108 df

8, 108 df

16, 108 df

Hard coral feeders
(6 species)
Soft coral feeder
(C. melannotus)
Generalist feeders
(7 species)

0.693 (ns)

1.745 (ns)

1.493 (ns)

0.380 (ns)

0.488 (ns)

1.778 (ns)

0.568 (ns)

1.778 (ns)

2.601 (*)

1.665 (ns)

1.428 (ns)

1.110 (ns)

0.332 (ns)

0.554 (ns)

1.325 (ns)

1.319 (ns)

1.195 (ns)

2.882 (*)

0.472 (ns)

0.780 (ns)

0.816 (ns)

rainfordi; Fig. 5.). For the two generalists (C. vagabundus and C. rostratus), adults and juveniles
displayed similar associations with the benthos
despite contrasting distributions across zones
(Fig. 4), though juveniles of both species were more
strongly associated with the ‘other hard corals’
category than adults (Fig. 5). Benthic associations
among adult and juvenile C. melannotus (soft coral

feeder) were also similar, correlating primarily with
soft coral cover, though once again juveniles were
more strongly associated with ‘other hard corals’ than
adults (Fig. 5). For C. rainfordi, an obligate hard coral
feeder, both adults and juveniles associated primarily
with table Acropora and Pocillopora species (Fig. 5).
No species analysed was strongly associated with
non-coral benthos (Fig. 5).

Fig. 3 Mean abundances of adult and juvenile butterflyfishes,
pooled by trophic guild: (a) adult hard coral feeders; (b)
juvenile hard coral feeders; (c) adult generalist feeders; (d)

juvenile generalist feeders. (■) sheltered locations; ( ) obliquely
exposed locations; (□) exposed locations


586
Fig. 4 Mean abundances
(± SE) of adults (top graphs)
and juveniles (bottom
graphs) of the six most
abundant species of
butterflyfish in the Palm
Islands. (F) flat; (C) crest;
(S) slope

Environ Biol Fish (2012) 94:579–590


Environ Biol Fish (2012) 94:579–590

Fig. 5 Principal components analysis (PCA) showing intraspecific variation in the associations of the six most abundant
butterflyfishes (a) with individual benthic components (b) in
the Palm Islands. Capital letters indicate adults while lower
case letters indicate juveniles. Species are as follows:
Chaetodon aureofasciatus, Chaetodon lunulatus, Chaetodon
rainfordi, Chaetodon vagabundus, Chaetodon melannotus, and
Chelmon rostratus

Discussion
Ontogenetic variation in the distributions of coral reef
fishes has been observed in a variety of species, with

evidence suggesting that dietary preference, the
availability of shelter, and the presence of adult
conspecifics may all contribute to this pattern of habitat

587

association (Lecchini and Galzin 2005; Mumby 2006;
Jones et al. 2010). The results of this study agree
strongly with a previous study of butterflyfish
distributions on coral reefs (Pratchett et al. 2008b),
indicating that some species of butterflyfish also
display variations in their distributions as they mature.
Furthermore, the patterns revealed in both studies
appear to relate strongly to trophic guild. However, in
contrast to the study by Pratchett et al. 2008b, which
was carried out on mid-shelf reefs of the Great Barrier
Reef (GBR) with relatively high abundance of
Acropora and Pocillopora corals, this study was
performed on an inner-shelf GBR reef with significantly lower prey abundance for hard coral feeders
(Emslie et al. 2010). Thus, our results further
highlight the importance of trophic guild in determining ontogenetic differences in butterflyfish distributions. For example, although Berumen and Pratchett
(2006) noted an increase in territory size among adult
coral-feeders as abundance of coral prey declined, our
results found that juvenile hard-coral feeders displayed comparable distributions to adult conspecifics
in habitats dominated by soft coral. This indicates that
either recruits of hard-coral feeders settle preferentially
into habitats occupied by adult conspecifics, or alternatively, that juveniles exhibit higher survival rates in
these areas (e.g., see Harmelin-Vivien 1989; Pratchett
et al. 2008b). However, hard-coral feeders were not the
only species to exhibit such limited ontogenetic variation in abundance. Adult and juvenile abundances of the

soft-coral feeder C. melannotus were similar across
locations and ontogenetic variation was displayed
only according to degree of exposure. In contrast to
coral feeders, generalist feeders displayed substantial
ontogenetic variation in distribution. Juvenile generalist feeders were limited almost exclusively to the
shallow, patchy areas along the reef flat, whilst adults
displayed comparatively wide distributions.
Our original hypothesis of spatial variation in
abundance of adult and juvenile generalists was
supported by our results (see Table 4; Fig.3). This
ontogenetic variation in distribution suggests a correlation between distribution and dietary versatility. The
expansion in dietary flexibility often shown by
generalists may partially explain the relatively limited
distributions of juveniles compared to adults. Juveniles typically feed only on benthic invertebrates,
whilst adults have been shown to feed on a variety of
items including scleractinian coral polyps and


588

gastropods (Harmelin-Vivien 1989). As generalists
were restricted almost entirely to the reef flat as
juveniles, this study supports previous evidence that
immature generalist butterflyfishes often feed in
rubble or sandy areas of the shallows while adults
display comparatively wider distributions (Pratchett
et al. 2008b). However, despite being limited to
relatively patchy habitats with low coral cover, the
abundances of C. vagabundus and C. rostratus
juveniles correlated strongly with the ‘other hard

corals’ category. This suggests that the low abundance
of living corals was nevertheless important in attracting immature individuals (e.g., see Feary et al. 2007).
Moreover, areas devoid of living coral were typically
unoccupied by butterflyfish, regardless of trophic
guild. Juvenile reef fishes often exhibit strong habitat
selection upon settlement (Williams and Sale 1981;
Doherty et al. 1996; Feary et al. 2007), and habitat
structure has been shown to be an important factor in
recruitment and post-settlement success among reef
fishes (Almany 2004). This study supports the
conclusion that living coral may be essential to the
recruitment of butterflyfish regardless of trophic guild
(Pratchett et al. 2006).
For C. melannotus, only exposure was a significant
factor in explaining ontogenetic variation in habitat
association. Whilst generally labelled as a soft-coral
feeder, C. melannotus does take a considerable
portion of bites from scleractinian corals (Pratchett
2005), a feeding preference that may or may not vary
with the onset of maturity. For instance, the adult
distribution observed in this study strongly reflected
soft coral abundance, peaking at exposed and semiexposed locations. In contrast, juveniles displayed a
stronger correlation with ‘other hard corals’ than did
adults, and showed no variation in abundance
according to exposure. This finding supports the
results of Pratchett et al. 2008b, who found that C.
melannotus juveniles displayed substantially different
distributions to adults at Lizard Island. Whilst both
adults and juveniles of C. melannotus displayed
similar patterns across islands to that of soft coral

cover in this study, it may be that juveniles rely more
heavily on hard corals than adults, either for food or
shelter. Indeed, many reef fish species depend greatly
on live coral during settlement and early juvenile life
(Syms and Jones 2000; Jones et al. 2004). However, it
must be noted that this study did not determine the
feeding behaviours of butterflyfish, and thus we can

Environ Biol Fish (2012) 94:579–590

only speculate if C. melannotus demonstrated a shift
in feeding preference with growth. We therefore
suggest that future studies investigate ontogenetic
dietary shifts in soft-coral feeding butterflyfish.
As coral-feeding butterflyfish begin feeding on
scleractinian corals almost immediately upon settlement
(Harmelin-Vivien 1989), concordant patterns in the
distributions of adult and juvenile hard-coral feeders
are to be expected. Indeed, an abundance of resident
adults may indicate high resource availability, and
selection may favour individuals that settle in areas
with high abundances of preferred prey (e.g., see
Strathmann et al. 2002). However, despite the
similarities in juvenile and adult abundance displayed
by hard-coral feeders, some ontogenetic variation in
benthic association was displayed by the two most
abundant obligate corallivores, C. aureofasciatus and
C. lunulatus. C. aureofasciatus juveniles were associated strongly with staghorn Acropora, while adults
displayed moderate correlations with a variety of
benthic components. On the other hand, juveniles of

C. lunulatus were mostly associated with Porites
species; however, adults were seen in abundance near
Pocillopora and staghorn Acropora. The differences
in benthic associations exhibited by C. aureofasciatus
and C. lunulatus suggest that post-settlement forces
may have affected the within-site distributions of
juveniles. Possible factors that may have contributed
to these differences are the availability of shelter
within microhabitats (e.g., Almany 2004) and antagonistic interactions between adults and juveniles (e.g.,
Jones 1987; Webster and Hixon 2000; Ben-Tzvi et al.
2008). Juvenile reef fishes often associate more
strongly with high-shelter areas than do their adult
counterparts to increase post-settlement survival
(Mumby 2006; Jones et al. 2010). This may partially
explain why C. aureofasciatus juveniles associated
strongly with staghorn Acropora corals that provide a
high degree of protection. In addition, Berumen and
Pratchett (2006) suggest that both inter- and intraspecific competition may be important in determining
the distributions of butterflyfish. However, the lack of
sub-transect observations of fish and relatively low
sample sizes for individual species in this study prevent
such conclusions. Although butterflyfish typically recruit
year-round on coral reefs (Abesamis and Russ 2010),
recruits are seen in highest abundance in the summer
months from January to April on the GBR (Leis
1989). As this study was performed during September


Environ Biol Fish (2012) 94:579–590

and October, we may have missed the peak of
recruitment. This could explain why sample sizes
were biased towards adults and late-stage juveniles. Therefore, we recommend future observations
of individual butterflyfish be carried out at different time
periods to elaborate on the trends shown in this study.
Several conclusions from our results may prove
beneficial to the study of butterflyfish population
dynamics. Firstly, the marked ontogenetic variations
in habitat association displayed by generalist feeders
indicate a distinction between habitats utilized by
adult and juvenile conspecifics. This pattern of habitat
use suggests an ontogenetic shift between new recruit/
juvenile and adult habitats, providing valuable ecological data to supplement genetic and demographic
analyses of population connectivity. Such elucidations
can also be incorporated into refined larval dispersal
models, making future predictions regarding the
ability of populations to survive disturbances more
tangible (i.e., see Werner et al. 2007; Jones et al.
2009). Additionally, the concordant patterns of habitat
use displayed by adult and juvenile hard-coral feeders
suggest that the abundance of juveniles may be partly
related to the presence of conspecific adults (HarmelinVivien 1989) rather than to habitat alone. Such
dependence may partially explain the common lag in
recovery of butterflyfish populations following
declines in abundance after bleaching events (Jones
et al. 2004; Pratchett et al. 2008a). In fact, a range of
coral reef fishes has been shown to exhibit a delayed
response to recovery of reefs following disturbance
(Williams 1986; Mclanahan et al. 2002; Halford et al.
2004; Graham et al. 2007). This indicates that a

partial reliance of recruits on the presence of adults
may be a common phenomenon among reef fishes.
In conclusion, this study indicates that the varying
degrees of ontogenetic shifts in the habitat associations of butterflyfish may be influenced by a number
of factors. These may include trophic guild, competition, and the presence of adult conspecifics. Our
results may prove useful in developing an understanding of the mechanisms contributing to demographic and genetic connectivity in butterflyfish
populations. Ultimately, this work emphasizes the
need for detailed ecological observations in the study
of reef fish population dynamics.
Acknowledgments The authors would like to thank D.
Simonson, J. Kerry, J. Hopf, D. Buchler, N. Summers, and

589
T. Heintz for invaluable assistance in the field and five
anonymous reviewers for comments that vastly improved
the manuscript. We are also thankful to H. Burgess and the
staff at OIRS for ongoing logistical support. This research
was supported by a grant to G.R.R. from the Australian
Research Council (ARC) Centre of Excellence for Coral
Reef Studies.

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Environ Biol Fish (2012) 94:591–599
DOI 10.1007/s10641-011-9965-1

Homatula laxiclathra (Teleostei: Balitoridae), a new species
of nemacheiline loach from the Yellow River drainage
in Shaanxi Province, northern china
Jin-Hui Gu & E. Zhang

Received: 19 May 2011 / Accepted: 4 November 2011 / Published online: 16 November 2011
# Springer Science+Business Media B.V. 2011

Abstract Homatula laxiclathra, new species, is here
described from the Wei-He of the Yellow River
drainage in Shaanxi Province, northern China. It is
similar to H. berezowskii, H. longidorsalis, and H.
variegata in the shared possession of a shallower
body with a uniform depth, a character distinguishing
all of them from all other congeners, but differs from
these three species in the width of vertical brown bars
on the caudal peduncle. This new species, along with
H. berezowskii, differs from H. longidorsalis, and H.
variegata in head length, caudal-peduncle depth,
length of the dorsal adipose creast of the caudal
peduncle, body squamation, and intestinal coiling.
Homatula laxiclathra and H. berezowskii are further
distinct in the caudal-fin shape and interorbital width.
Keywords Homatula laxiclathra . New species .
Yellow River drainage . Shaanxi Province

J.-H. Gu : E. Zhang (*)
Chinese Academy of Sciences, Institute of Hydrobiology,
Wuhan 430072 Hubei Province,
People’s Republic of China
e-mail:
J.-H. Gu
e-mail:
J.-H. Gu
Graduate School of Chinese Academy of Sciences,
Beijing 100039, People’s Republic of China

Introduction

Hu and Zhang (2010), in their describing Homatula
pycnolepis from the Yangbi-Jiang of the upper
Mekong River drainage of Yunnan Province, southern
China, provided a re-definition of Homatula, and
placed in the genus all species previously included in
Paracobitis in the Chinese literature with the exception of three hypogean species: P. longibarbata, P.
maolanensis and P. posterodorsalus. Nearly at the
same time, Min et al. (2010) preferred to use Paracobitis as the generic name for the species here placed
in Homatula, and described P. nanpanjiangensis as a
new loach species from the Nanpan-Jiang of the Pearl
River drainage in Yunnan Province, South China. Min
et al.’s generic classification, though, is not in
agreement with the consensus of workers outside
China; e.g., Kottelat (1990), Bǎnǎrescu and Nalbant
(1995) and Nalbant and Bianco (1998). Paracobitis,
as defined by these workers, is known only from
Western Asia. Chinese species previously recognized
in Paracobitis have a great geographical gap with the
western Asian species of this genus, and thus belong
to a distinct genus Homatula (Bǎnǎrescu and Nalbant
1995). For this reason, we insist that Homatula is the
available generic name for the epigean species that
were referred to Paracobitis in the Chinese literature.
So far ten valid species are designated to Homatula:
H. acuticephala, H. anguillioides, H. berezowskii, H.
erhaiensis, H. nanpanjiangenis, H. oligolepis, H.


592

pycnolepis, H. potanini, H. variegata, and H.
wujiangensis.
Hu and Zhang (2010) cleared up some taxonomic
problems surrounding H. variegata. They concluded
that the type locality of H. variegata is in the upper
Yangtze River drainage; that H. berezowskii, which
was formerly considered as a junior synonym of H.
variegata, is a valid species, and that the specimens
previously recognized as H. variegata from the WeiHe of the Huang-He (= Yellow River) drainage in
Shaanxi Province represent an unnamed species of
Homatula. The purpose of the present investigation is
to provide a detailed description of this unnamed
species.

Environ Biol Fish (2012) 94:591–599

Holotype
IHB 73V10738, 136.7 mm SL, Wei River, a tributary
of Yellow River drainage, at Zhouzhi County,
Shaanxi Province, North China; collected in 1973;
no information about collectors.
Paratypes
IHB 80VI0956-7, 80VI0959, 80VI0961, 80VI0964-8,
80VI0971-3, 80VI0976, 80VI1185, 82VI0103,
82VI0106-8, 82VI2279, 82VI2283-4, 21, 67.6–
121.9 mm SL, same locality as holotype.
Diagnosis

Material and methods
Measurements were taken using digital calipers

connected to a computer to the nearest 0.1 mm. The
last two branched rays in dorsal and anal fins are
closely approximated at the base, we thereby count
them as a single ray each. Measurements and counts
were made on the left side of specimens whenever
possible, following the methods of Kottelat (1990).
Predorsal, prepectoral, prepelvic and preanal lengths
were taken, respectively from the anteriormost tip of
the snout to the dorsal-, pectoral-, pelvic- and anal-fin
origins, Measurements of parts of the head are given
as proportions of head length. Head length and
measurements of other parts of the body are given
as proportions of standard length. Statistics 5.0
(Wilkinson et al. 1992) was used for the basic statistic
analysis on morphometric data and also for the
principal component analysis on the variancecovariance matrix of the log–transformed measurements. Abbreviations for collections are: IHB, Institute of Hydrobiology, Chinese Academy of Sciences,
Wuhan; YU, Yunnan University, Kunming, and KIZ,
Kunming Institute of Zoology, Chinese Academy of
Sciences, Kunming. Abbreviations: SL, standard
length, and HL, head length.

Results
Homatula laxiclathra, new species (Fig. 1a)
Paracobitis variegatus: Gao 1992: 86 (Zhouzhi
and Huxian)

Homatula laxiclathra is similar to H. variegata, H.
berezowskii, and H. longidorsalis in the shared
presence of slender bodies with uniform depth [9.3–
15.8% (mean 12.5) SL; see Figs. 1 and 2a, and

Table 1], a character distinguishing them from all
remaining species of this genus where they have
deeper bodies [13.6–23.9% (mean 16.6) SL] and
their body depth evenly decreases posterior to the
posterior end of the dorsal-fin base. The new
species differs from H. variegata, H. berezowskii,
and H. longidorsalis in having vertical brown bars on
the caudal peduncle twice as wide as (vs. much
narrower or slightly wider than) their interspaces
(Fig. 1). This new species, along with H. berezowskii,
is further distinguished from H. variegata and H.
longidorsalis by the presence of a shorter head (length
15.6–21.1% SL vs. 18.3–25.3; Fig. 3a, Table 1), a
shallower caudal peduncle (depth 8.4–11.4% SL vs.
9.6–13.6; Fig. 3b, Table 1), a shorter adipose crest
along the dorsal midline of the caudal peduncle
anteriorly not extending to the midway of the analfin base (vs. extending beyond the vertical through
the anal-fin origin) (Fig. 1a–d), a scaleless (vs.
partially scaled) predorsal body, and an intestine with
(vs. without) a loop or bend behind the stomach
(Fig. 4). It is further distinct from H. berezowskii in
having an oblique (vs. truncate) posterior margin of
the caudal fin, and a narrower interorbital space
[width 19.9–24.9 (average 22.5)% HL vs. 24.1–29.7
(average 27.0); see Fig. 2b]. The new species has an
intestine with a loop anteriorly reaching the posterior
surface of the U-shaped stomach, whereas the other


Environ Biol Fish (2012) 94:591–599

593

Fig. 1 Lateral view of four
species of Homatula: a H.
laxiclathra, IHB 73VI0738,
136.7 mm SL; China:
Yellow River drainage:
Wei He; b H. variegata,
IHB uncat., 127.9 mm
SL; China: Sichuan: Yangtze
drainage: Yalong-Jiang;
c H. berezowskii,
IHB 73IV1044, 123.3 mm
SL; China: Shaanxi:
Fengxian: Yangtze drainage:
Jialing-Jiang; d H.
longidorsalis, KIZ 874050,
80.92 mm SL; China:
Yunnan: Yiliang: Pearl
River drainage:
Nanpan-Jiang

related species do not have a loop at this portion of
the intestine (Fig. 4a, c).
Description
Morphometric data for type specimens are given in
Table 1. Body elongate and cylindrical, anteriorly a

b

25

Interorbital width (mm)

Body depth (mm)

a

20

15

10

5
45

little depressed and posteriorly compressed laterally.
Head, thorax, abdomen and anterior half of predorsal
body scalesless; scales only present on back and sides
of posterior half of predorsal body as well as
postdorsal body. Caudal peduncle compressed laterally.
Lateral line complete, extending along midline of body
directly.

75

105

135

165

195

SL (mm)

Fig. 2 a relation between body depth and SL for H. laxiclathra
(black up-pointing triangle), H. variegata (white circle), H.
berezowskii (white diamond), H. longidorsalis (white square),

6.5

5.5

4.5

3.5

2.5
11

14

17

20

23

HL (mm)

and all remaining species (black circle); and b relation between
interorbital width and HL for H. laxiclathra (black up-pointing
triangle) and H. berezowskii (white diamond)


Caudal peduncle depth

13.8–18.0
35.5–45.3

60.5
12.9
44.1
23.4

Eye diameter

Snout length

Interorbital width

19.9–24.9

47.1–68.0

43.5

Head depth

42.7–56.5

41.2–66.2

15.5–22.0

43.8–52.2

Head width

In percentage of HL

41.6

8.4–11.4

8.5
22.8

Caudal peduncle depth

Caudal peduncle length

In percent of CPL

69.5–75.8

44.4

68.5

Prepelvic length

15.9–21.1

41.9–50.6

6.9–10.4

Preanal length

7.0

Anal-fin length

9.0–12.7

10.8–14.9

42.5

9.4

Ventral-fin length

16.5

9.6

Pectoral-fin length

8.7–12.7

Prepectoral length

8.8

Dorsal-fin length

15.9–21.1

10.0–15.8

67.6–121.9

Predorsal length

9.8
16.9

Body depth

136.7

Range

22.5

40.7

16.0

57.0

48.1

50.2

18.6

9.2

73.0

48.5

18.8

46.6

8.8

10.9

13.1

10.5

18.8

12.5

88.9

Mean

1.39

2.53

1.23

5.74

3.61

6.51

1.70

0.66

1.71

1.88

1.24

2.28

0.96

0.90

1.10

1.11

1.28

1.75

15.5

SD

20.0–28.4 (25.5±1.72)

40.0–50.0 (44.5±2.47)

11.3–15.9 (13.7±1.08)

50.8–65.5 (58.1±3.67)

43.7–56.8 (49.4±3.32)

43.6–78.8 (59.6±7.69)

16.1–22.7 (19.6±1.61)

9.6–13.6 (11.6±1.04)

69.8–77.6 (73.2±2.15)

43.9–51.1 (48.3±1.84)

17.2–24.4 (20.7±1.63)

41.7–49.7 (46.9±1.84)

8.6–11.7 (10.0±0.83)

9.4–13.3 (11.0±0.87)

10.4–15.5 (12.4±1.21)

9.3–14.1 (11.1±1.05)

18.3–22.7 (20.5±1.33)

9.9–15.3 (12.9±1.27)

66.1–129.6 (90.7±16.95)

Range (Mean ± SD)

Holotype

Paratypes (n=21)

H. variegata (n=37)

H. laxiclathra

Head length

In percentage of SL

SL (mm)

Characters

24.1–29.7 (27.0 ±2.80)

40.4–46.3 (42.5 ±3.02)

13.8–16.9 (15.2 ±1.54)

56.7–69.0 (61.9 ±6.17)

45.3–49.9 (47.8 ±2.31)

42.8–54.4 (49.5±5.85)

18.7–21.7 (20.2±1.52)

9.1–10.9 (10.0±0.89)

69.2–73.6 (72.1±2.23)

42.9–47.5 (45.3±2.30)

15.9–18.9 (17.2±1.51)

43.0–47.7 (44.8±2.40)

7.4–10.8 (8.7±1.72)

10.1–12.6 (10.9±1.29)

11.0–13.0 (12.0±1.00)

9.2–11.2 (9.9±1.01)

15.6–18.5 (17.2±1.43)

9.3–12.3 (10.9±1.51)

65.4–125.41 (105.8±30.6)

Range (Mean ± SD)

H. berezowskii (n=10)

Table 1 Morphometric data for type specimens of Homatula laxiclathra and for examined specimens of its related species

23.7–29.7 (27.2±2.01)

41.3–48.4 (44.0±2.06)

13.8–18.4 (16.7±1.57)

52.2–61.8 (56.4±2.74)

47.2–53.9 (50.4±2.59)

62.1–70.0 (65.9 ±2.58)

17.1–19.6 (18.7±0.82)

11.4–13.3 (12.3±0.73)

74.6–83.6 (78.3±3.01)

50.5–56.7 (52.6±1.91)

22.0–26.0 (23.7±1.31)

48.1–52.8 (50.4±1.67)

10.2–12.0 (11.1±0.52)

11.0–13.5 (12.0±0.80)

13.0–15.5 (14.2±0.87)

10.0–11.9 (11.0±0.69)

21.5–25.3 (23.2±1.31)

13.1–14.7 (13.8±0.51)

50.3–80.9 (64.7±9.40)

Range (Mean ± SD)

H. longidorsalis (n=8)

594
Environ Biol Fish (2012) 94:591–599


Environ Biol Fish (2012) 94:591–599

b

26

Caudal peduncle depth (mm)

a

23

Head length (mm)

Fig. 3 Relation between
(a) HL and SL and (b)
caudal peduncle depth

and SL, for H. laxiclathra
(black up-pointing triangle),
H. variegate (white circle),
H. berezowskii (white diamond) and H. longidorsalis
(white square)

595

20

17

14

11
45

65

85

105

SL (mm)

Head short, and depressed in frontal view, wider
than high, roughly triangular in dorsal view. Snout
blunt, slightly shorter than postorbital length of
head. Eye small, close to dorsal profile of head,
invisible from ventral view. Interorbital space wide

and flat. Nostrils closely set, nearer to anterior
margin of eye than to snout tip; anterior nostrils
situated at a nostril valve.
Mouth inferior and arched. Lips thick, slightly
furrowed, but not papillated; upper lip with a small
median incision, and lower lip with a marked median
incision. Jaws covered by lips; upper jaw with a welldeveloped process dentiformis corresponding with a
marked notch on lower jaw. Three pairs of barbels;
two rostral pairs, inner one reaching corners of mouth
and outer one not reaching a vertical line of anterior
nostril, and one maxillary pair short.
Fins flexible; dorsal fin with 3 simple and
8 branched rays; distal margin convex as a whole;
origin nearer to snout tip than to caudal-fin base.
Fig. 4 Ventral view of
intestine coiling pattern
in: a H. laxiclathra,
IHB 80VI0963, 115.39 mm
SL; b H. variegata,
IHB 82VI0517, 119.32 mm
SL; c H. berezowskii,
IHB 73VI1045, 117.02 mm
SL. Scale bar = 2 mm

125

145

17

14

11

8

5

45

65

85

105

125

145

SL (mm)

Pectoral fin with 1 simple and 9–10 branched rays,
inserted slightly posterior to vertical through posteriormost point of operculum, tip of the longest fin ray
not extending beyond halfway to insertion of pelvic
fin. Pelvic fin with 1 simple and 6–7 branched rays,
inserted below second or third branched rays of dorsal
fin, tip of the longest fin ray extending not beyond
halfway of distance between pelvic-fin insertion and
anal-fin origin. Anal fin with 3 simple and 5 branched

rays, with a convex distal edge; origin closer to
pelvic-fin insertion than to caudal-fin base. Posterior
margin of caudal fin oblique. Caudal peduncle
uniformly deep; with adipose crests along its dorsal
and ventral midlines. Adipose crest along dorsal
midline of caudal peduncle anteriorly not extending
through anteriorly the position of the anal-fin origin.
Intestine forming a loop anteriorly reaching posterior surface of U-shaped stomach (Fig. 4a). Gas
bladder osseous, anterior chamber invisible, fully
enclosed in capsule; posterior chamber degenerative.


596

Environ Biol Fish (2012) 94:591–599

Coloration

Etymology

In formalin-stored specimens, head yellowish brown.
Ground color of body pale. Four or five brown blotches
on median predorsal region of body. 15 to 17 rectangular
yellowish brown vertical bars along each side of body (5
or 6 predorsal, 3 subdorsal, and 7 to 8 postdorsal) twice
as wide as interspace. Dorsal and caudal fins with dark
brown spots. A dark brown vertical bars on caudal-fin
base. Dorsal surface of pectoral, pelvic and anal fins
grayish, and caudal fin gray.

The specific epithet, used as an adjective, is made
from the combination of Latin words “laxus”(wide)
and clathrus (barred), alluding the presence of wider
vertical bars on each side of body.

Distribution
Known only from the Wei He of the Yellow River
drainage in Shaanxi Province, North China (Fig. 5)

Fig. 5 Map showing distribution of all Homatula species in China

Discussion
The description of a new species brings the total number
of species of Homatula to 12. Zhu (1989), in his
monograph of Chinese species of the Nemacheilinae,
recorded five species of the genus under the generic
name Paracobitis: P. anguillioides, P. erhaiensis, P.
oligolepis, P. potanini and P. variegatus. His generic


Environ Biol Fish (2012) 94:591–599

classification of Paracobitis was subsequently accepted widely, and four new Chinese species or subspecies were added to the genus. Ding and Deng (1990)
described P. wujiangensis from the Wu-Jiang, a
tributary flowing to the upper Yangtze River in
Sichuan Province; Zhou and He (1993) described P.
acuticephalus from the Erhai Lake system in Yunnan
Province; Yang et al. (1994) described P. variegatus
longidorsalis from the Nanpang-Jiang of the Pearl
River drainage in Yunnan Province; and Min et al.

(2010) described P. nanpangjiangensis from the
Nanpang-Jiang of the upper Pearl River drainage in
Yunnan Province. However, all above-mentioned
species or subspecies of Paracobitis exclusive of P.
nanpangjiangensis were transferred to Homatula by
Hu and Zhang (2010) when they described H.
pycnolepis from the Yangbi-Jiang, a tributary of the
upper Mekong River drainage in Yunnan Province;
meanwhile, they validated Nemachilus berezowskii
Günther 1896 from the synonym of H. variegata. P.
nanpangjiangensis was not included in Homatula by
Hu and Zhang (2010), because Min et al’s (2010)
paper was published only a little earlier and Hu and
Zhang could not include it in their revision. This
species is here transferred to Homatula. Given that the
subspecies P. variegatus longidoralis is here considered as a full species of Homatula, the here described
species H. laxiclathra is the twelfth species of this
genus.
Prior to the present investigation, the status of P.
variegatus longidoralis remains contentious. Min et
al. (2010) considered it as valid, but Hu and Zhang
(2010) commented that it was not quite distinct from
H. variegata. The ongoing molecular phylogenetic
analysis, however, indicates that samples of P.
variegatus longidoralis form a monophyletic lineage
(Chen X. Y., KIZ; pers. comm.). Based on this,
combined with no subspecies status under phylogenetic species concept, this subspecies is here rendered
as a full species. In terms of Min et al. (2010), H.
longidorsalis differs from H. variegata in having an
anterior nostril placed at a short tube (vs. a valve), 9

(vs. 8; rarely 9) branched dorsal-fin rays, maxillary
barbels extending to the vertical of the anterior or
middle (vs. middle or posterior) margin of eye; and
numerous vermiform markings on the top of head (vs. 1–
4 vermiform markings on the parietal area or obscure).
Twelve species here recognized in Homatula can
be tentatively subdivided into four groups on the basis

597

of squamation, completeness in the lateral line, and
body shape. The first group comprises four species
having a densely scaled body except for head: H.
acuticephala, H. anguillioides, H. erhaiensis and H.
pycnolepis. They occur close to each other in a small
area in the upper Mekong River drainage (the
Yangbi Jiang and the Erhai Lake system) in
Yunnan Province, South China. The second group
is composed of two species with an incomplete
lateral line, H. potanini and H. wujiangensis, and
both are known only from the upper Yangtze River
drainage. The third group includes four species,
namely H. laxiclathra described here, H. variegata,
H. berezowskii and H. longidorsalis, currently known
from the Yellow River, Yangtze River and Pearl River
drainages; these four species have slender bodies with
uniform depth (9.3–15.8% SL; see Fig. 2a). The
fourth group includes two species, P. nanpanjiangensis, and H. oligolepis, both confined only to the upper
Pearl River drainage in Yunnan and Guizhou provinces. The two species have a scaleless body, or with
rudimentary scales present only on the caudal-fin

base.
The results of the principle component analysis
performed on the variance-covariance matrix of
log-transformed measurements for the examined
specimens of four species of the third group
(Table 2, Fig. 6) revealed that the combination of
PC2 against PC3 enabled the separation of H.
laxiclathra and H. berezowskii from H. longidorsalis
and H. variegata. These two pairs were distinguishable by PC2, the main shape axis, on which the main
loadings are head length and caudal peduncle depth.
Homatula laxiclathra and H. berezowskii are distinguished from H. longidorsalis and H. variegata in
having a shorter head (length 15.6–21.1% SL vs.
18.3–25.3; see Fig. 3a), and a shallower caudal
peduncle (depth 8.4–11.4% SL vs. 9.6–13.6). Both
are also distinct from H. longidorsalis and H.
variegata in having a shorter adipose crest along the
dorsal midline of the caudal peduncle anteriorly not
extending beyond (vs. extending beyond) the
vertical through the anal-fin origin (Fig. 1a–d), a
scaleless (vs. partially scaled) predorsal body, and an
intestine with (vs. without) a bend or loop behind the
thickened portion of intestine. Apparently, our study
further confirms Hu and Zhang (2010) conclusion that
H. berezowskii is a valid species distinct from H.
variegata.


598

Environ Biol Fish (2012) 94:591–599

Table 2 Loadings on the first three principal components
extracted from morphometric data for: H. laxiclathra, H.
variegata, H. berezowskii, and H. longidorsalis
Characters

PC 1

PC 2

PC 3

Standard length

−0.248

0.224

−0.099

Body depth

−0.221

−0.012

−0.029

Dorsal-fin length

−0.235

0.081

−0.337

Pectoral-fin length

−0.228

0.346

−0.146

Ventral-fin length

−0.240

0.186

−0.178

Anal-fin length

−0.232

−0.234

−0.095

Caudal peduncle length

−0.243

0.142

−0.153

Caudal peduncle depth

−0.233

−0.329

−0.031

Predorsal length

−0.248

0.203

−0.080

Prepectoral length

−0.242

−0.184

0.112

Prepelvic length

−0.249

0.207

−0.009

Preanal length

−0.248

0.214

−0.023

Head length

−0.248

−0.095

−0.013

Head depth

−0.238

−0.232

0.183

Head width

−0.246

−0.111

0.082

Snout length

−0.231

−0.339

0.123

Eye diameter

−0.188

0.316

0.845

Interorbital width

−0.218

−0.389

0.025

Variance coverage (%)

83.58

5.82

2.67

Comparative materials
Homatula acuticephala, IHB 78IV365-6, 78IV368,
78IV387, 4, 89.2–103.9 mm SL; -YU 784130,
784132, paratype, 2, 107.8–119.5 mm SL; China:

2

PC III

1

0

-1

-2

-2

-1

0

1

2

PC II

Fig. 6 Scatter plot on the 2nd and 3th principle components
extracted from morphometric data for H. laxiclathra (black uppointing triangle), H. variegata (white circle), H. berezowskii
(white diamond) and H. longidorsalis (white square)

Yunnan Province: Eryuan County: Haixihai (=lake, in
upper Mekong River drainage).
Homatula anguillioides, IHB 820134, holotype, 1,
134.8 mm SL and 820119–29, 820131, 820135,
820137, paratypes, 14, 49.3–134.3 mm SL; China:
Yunnan Province: Eryuan County of upper Mekong
River drainage. -IHB 820533–5, 820538–40, topotypes,
6, 114.1–126.0 mm SL; China: Yunnan Province:
Eryuan County: upper Mekong River drainage.
Homatula berezowskii, IHB 73VI1191-3, 73VI1194,
4, 89.0–125.4 mm SL; China: Shanxi Province:
Lueyang County: Jialing River of Yangtze River
drainage. -IHB 73VI1044, 1, 120.7 mm SL; China:
Shanxi Province: Fengxian County: Jialing River of

Yangtze River drainage.-IHB 82VI2489, 1, 122.6 mm
SL; China: Gansu Province: Chengxian County: Jialing
River of Yangtze River drainage. -IHB 82 V2386, 1,
85.8 mm SL; China: Gansu Province: Huixian County:
Jialing River of Yangtze River drainage. -IHB
82VI2753, 82VI2755, 82VI2757, 3, 97.3–117.0 mm
SL; China: Gansu Province: Wudu County: Jialing
River of Yangtze River drainage. -IHB, uncat., 3, 74.89–
113.35 mm SL; China: Hubei Province: Zhushan
County: Du He, a tributary to Han Jiang of middle
Yangtze River drainage.
Homatula erhaiensis, IHB 64VI0012, holotype, 1,
68.8 mm SL; -IHB 64VI0001-11, 64VI0013-5,
646775–7, 646779, paratypes, 18, 64.4–86.8 mm
SL; China: Yunnan Province: Eryuan County: upper
Mekong River drainage. -IHB 1270142–8, 1270150–
4, 12, 49.1–79.9 mm SL; China: Yunnan Province:
Eryuan County: upper Mekong River.
Homatula longidorslis, KIZ 874042–3, 874045–6,
874050, 1987005739, 1987005748, 1987005752, 8,
50.26–80.92 mm SL; China: Yunnan Province: Yiliang
County: Nanpan Jiang of Pearl River drainage.
Homatula nanpanjiangensis, KIZ 1994000021,
1994000025, 1994000028–9, 1994000031,
1994000033–5, 1994000037, 9, 65–90.55 mm SL;
China: Yunnan Province: Qujing County, Nanpan Jiang,
Pearl River drainage.
Homatula oligolepis, KIZ 774557–9, 774560,
856145, 652099, 6, 83.51–171.05 mm SL; China:
Yunnan Province: Zhanyi County: Pearl River drainage.

Homatula potanini, IHB 42IX0661-2, 42IX0664,
42IX0666-7, 79IV0597-8, 79IV0600, 79IV0605,
79IV0609-10, 82 V0301-4, 15, 68.6–83.3 mm SL;
China: Sichuan Province: Emei County: Yangtze River
drainage. -IHB 78IV0175, 78IV0228-9, 78IV0233-34,


Environ Biol Fish (2012) 94:591–599

78IV0239, 78IV0243, 79IV0401-2, 79IV0483-6,
820004–5, 15, 62.3–82.4 mm SL; China: Sichuan
Province: Leshan City: Yangtze River drainage.
Homatula pycnolepis, IHB 814042–3, 814045–51,
9, 90.53–118.83 mm SL; China: Yunnan Province:
Jianchuan County: Yangbi Jiang of Mekong drainage.
Homatula variegata, IHB 42VI0726, 1, 90.79 mm
SL; China: Sichuan Province: Xikang County: Jinsha
Jiang of Yangtze River drainage. -IHB 82VI0517, 1,
119.32 mm SL; China: Sichuan Province: Dechang
County: Jinsha Jiang of Yangtze River drainage. -IHB
82VI0461, 1, 89.87 mm SL; China: Sichuan Province:
Huili County: Jinsha Jiang of Yangtze River drainage. IHB 64VI0600, 1, 103.44 mm SL; China: Gansu
Province: Wen County: Jialing Jiang of Yangtze River
drainage. -IHB 572090, 1, 83.39 mm SL; China:
Chongqing City: Wuxi County: Daning He of Yangtze
River drainage. -IHB, uncat., 7, 66.08–114 mm SL;
China: Sichuan Province: Yalong Jiang of Yangtze
River drainage. -IHB uncat, 1, 120.97 mm SL; China:
Wu Jiang of upper Yangtze River drainage. -IHB,
uncat., 7, 71–129.6 mm SL; China: Gesala: Yalong

River of Yangtze River drainage. -KIZ 2004051170,
2004051172–7, 2004051181–2, 2004051179, 10,
74.37–96.77 mm SL; China: Yunnan Province: Yanjin
County: Baishui He of Yangtze River drainage. -KIZ
2004112001–7, 7, 69.32–91.17 mm SL; China: Yunnan
Province: Dayao County: Jinsha Jiang of Yangtze River
drainage.
Data for Homatula wujiangensis is from Ding and
Deng (1990).

Acknowledgements We express our thanks to X.Y. Chen and
L.N. Du (KIZ) for permitting us to take digital photographs and
measurements of the specimens of Homatula nanpanjiangensis,
H. longidorsalis, and H. oligolepis under their care. Our thanks
are also given to Z. W. Sun for her useful advices on this
manuscript. This research was supported by a grant (KSCXZ-

599
YW-0934) from the Innovation Program of the Chinese
Academy of Sciences.

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Environ Biol Fish (2012) 94:601–614
DOI 10.1007/s10641-011-9966-0

Ecomorphological analysis as a complementary tool to detect
changes in fish communities following major perturbations
in two South African estuarine systems
Antoni Lombarte & Ana Gordoa &
Alan K. Whitfield & Nicola C. James &
Víctor M. Tuset

Received: 5 November 2010 / Accepted: 6 November 2011 / Published online: 7 January 2012
# Springer Science+Business Media B.V. 2011

Abstract Ecomorphological changes as a result of
natural perturbations in estuarine fish communities
were investigated in two South African estuaries
(Swartvlei and East Kleinemonde), both before and
after the loss of aquatic macrophyte beds in these
systems. The fish communities were analysed using
an ecomorphological diversity index (EMI) and the
results compared to a traditional index, the ShannonWiener diversity index. The EMI revealed that the
major changes in fish community composition
recorded in both estuaries were associated with
quantitative variations at the species level. Both
estuaries essentially lost their macrophyte beds and
ended up with the same type of bottom habitat (bare
sediment). In both cases the fish morphological
variability decreased immediately after aquatic macrophyte loss and then increased to end above the initial
value. The ecomorphological analysis appeared to be
sensitive to major ecological disturbances that occurred

A. Lombarte (*) : V. M. Tuset
Institut de Ciències del Mar-CSIC,
Passeig Marítim 37-49,
Barcelona 08003( Catalonia, Spain
e-mail:
A. Gordoa
Centre d’Estudis Avançats-CSIC,
Blanes, Catalonia, Spain
A. K. Whitfield : N. C. James
South African Institute for Aquatic Biodiversity,
Grahamstown 6140, South Africa

during the study period and this was confirmed by the
morphospace configuration. The results indicate that the
ecomorphology of the fish community responds to
habitat changes and that this change corresponds to
alterations in the representation of the different feeding
types. These findings therefore contribute to the
measurement of morphological changes in estuarine
fish assemblages as a result of habitat changes within the
ecosystem and we propose that ecomorphological
analyses add another dimension to the information
provided by existing diversity indices in studying
changing fish communities.
Keywords Ecomorpholgy . Index of diversity . South
African estuarine systems . Fish communities

Introduction
Animal and plant communities are subjected to
numerous biotic and abiotic disturbances, caused by

different factors (including human activities) which
often modify the composition and structure of these
assemblages (Begon et al. 1986). Major disturbance
within an aquatic ecosystem can result in a shift in
fish community structure (Olden et al. 2008; Villéger
et al. 2010). The morphological differences between
species are indicative of differences in ecological
strategies (Norton et al. 1995) in relation to locomotion (Fulton et al. 2001; Wainwright et al. 2002),
habitat use (Gatz 1979; Winemiller 1991; Lombarte et


602

al. 2003; Lombarte et al. 2010) and feeding strategies
(Motta et al. 1995; Wainwright and Richard 1995;
Pouilly et al. 2003; Barnett et al. 2006; Wagner et al.
2009).
Changes in fish community structure after a
disturbance could be functional and are likely to
be related to the loss of habitats and changes in
food resources. Loss of biodiversity is likely to
affect or even threaten critical functional roles
within the ecosystem (Paddack et al. 2006;
Villéger et al. 2010). However, biodiversity species
or eveness richness indices may not detect functional
changes because these indices ignore the actual
species and consequently cannot identify their role
within the community (Green and Vascotto 1978,
Ernst et al. 2006; Petchey and Gaston 2006; Violle et
al. 2007). It is therefore important to select appropriate

criteria for assessing the impact of perturbations and
also the degree of resilience of the community
(Bellwood et al. 2006).
The most popular diversity indices used to document
community changes cover two different aspects, namely
the number of species (richness) and the proportional
abundances of species (heterogeneous diversity, evenness) (Whittaker 1960; Gray 2000). Most classical
biodiversity indices do not take into account factors
such as the phylogeny or changes in morphological
composition of species that constitute the community
(Magurran 1988). However, the extent or magnitude
of changes within a community as a result of natural
or anthropogenic perturbations can be measured using
morphological and functional traits (Ernst et al. 2006;
Mason et al. 2007; Olden et al. 2008; Flynn et al.
2009; Villéger et al. 2010).
Biodiversity assessments based on the taxonomic
relatedness of the species have been undertaken by
Warwick and Clarke (1995, 1998) and Clarke and
Warwick (1998, 1999, 2001). These indices of
taxonomic diversity take into account the “weighted”
taxonomic differences between species (Mouillot et
al. 2005). Somerfield et al. (1997) and Mouillot et al.
(2005) found no consistent pattern of decreasing
taxonomic diversity with increasing environmental
impact. At the turn of the century a taxonomic index,
based on the nearest mean nodal taxonomic distance
(MND), was created by Webb (2000). More recently,
Bohannan and Hughes (2003) introduced modern
molecular techniques for determining microbial biodiversity based largely on Webb’s taxonomic index.

Environ Biol Fish (2012) 94:601–614

The morphological characters of the species within
a community are considered essential to determine the
functional structure of that community (Schoener
1974). This has led to the concept of ecomorphology,
which defines a community or species assemblage
through a morphospace determined by the morphological data of the species that comprise that assemblage (Karr and James 1975; Gatz 1979; Bock 1990;
Lombarte et al. 2003). Morphospaces can be analysed
using geometric morphological methods (Neige 2003;
Antonucci et al. 2009), from which an ecomorphological diversity index (EMI) can be generated
(Recasens et al. 2006) to provide additional information on the morpho-functional structure of the
community (Winemiller 1991; Fulton et al. 2001;
Mason et al. 2007).
The aim of this study was to increase the range
of methods available for detecting the impact of
disturbances on aquatic systems. Based on the
premise that functional loss may alter the morphological characteristics of a fish community, the
morphotypes of two South African estuarine fish
communities, before and after major disturbances,
were examined. We also explore the sensitivity of
a traditional diversity index (Shannon-Wiener
diversity index) and recent Taxonomic Diversity
Index for detecting changes in the fish community
and compare these indices with the sensitivity of
an ecomorphological index based on multivariate
analyses of quantitative morphological data (Recasens et al. 2006).

Material and methods

Study areas and biotic characteristics
The changes in two fish assemblages over time were
analysed in two warm-temperate South African
estuaries, the Swartvlei (34°01′51′′S; 22o47′49′′E)
and East Kleinemonde (33°32′21′′S; 27°02′55′′E).
The data analysed in this study are derived from
different sampling programmes, details of which are
available from Whitfield (1986) for Swartvlei and
James et al. (2008) for the East Kleinemonde. Both
systems experienced river inflow changes, which
altered their habitats. Prior to the loss of aquatic
macrophytes, the estuaries analysed in this study
presented differences in habitat complexity. The


Environ Biol Fish (2012) 94:601–614

Swartvlei littoral zone was characterised by a more
complex habitat structure than the East Kleinemonde,
with the former system having an outer Potamogeton
zone, a Chara zone and an inner Potamogeton zone,
whereas the East Kleinemonde had either a Ruppia or
Potamogeton zone only. In addition, the Swartvlei
system is classified as an estuarine lake whereas the
East Kleinemonde is classified as a temporarily open/
closed estuary (Whitfield 1992).
The fish community associated with the
Swartvlei littoral zone was monitored between
1979 and 1982 (Whitfield 1986). During this period
the littoral zone was covered by extensive Potamogeton pectinatus beds in 1979, epipsammic filamentous algal mats in 1980 and bare sand in 1982. The

fish community of the East Kleinemonde Estuary was
monitored between 1999 and 2007 (James et al.

Fig. 1 Examples of the features used in the geometric
morphological analysis of
selected fish species from the
East Kleinemonde Estuary: a
Liza dumerili, b Liza
richardsonii, c Mugil
cephalus, d Myxus capensis,
e Valamugil cunnesius, f
Pomadasys commersonnii,
g Rhabdosargus holubi,
h Lithognathus lithognathus, i Oreochromis mossambicus, j Monodactylus
falciformis. Images were
obtained from the SAIAB
image collection
(:8080/
saiab/index.html)

603

2008). Similar major changes occurred in the littoral
zone of this estuary where extensive Potamogeton
pectinatus and Ruppia cirrhosa beds were recorded
between 1999 and 2002 but were mostly absent
between 2003 and 2007 (Sheppard et al. 2011).
Analyzed biodiversity indexes
The Ecomorphological Diversity Index (EMI) was
calculated for the fish assemblages from standardised

images of the left side of each species. A total of
27 metrics (Fig. 1) were selected for each specimen
(Recasens et al. 2006). After digitalising the metric
maps of each species, they were rotated, scaled (to
unit centroid size) and translated using a generalised
least-square superimposition procedure (generalised
Procrustes) to remove scale and orientation distortions