Habitat specialization in the Mediterranean cardinalfish, Apogon imberbis
Mykle Hoban
ABSTRACT: The cardinalfish Apogon imberbis is a major member of nearshore
rocky reef fish assemblages in the Mediterranean. The nocturnal foraging cardinalfish are known to display a high degree of fidelity to their daytime resting
sites. However, the specific composition of habitat chosen as resting sites as well
as the degree of specialization on particular substrate type have not been investigated. Here, I investigated habitat specialization of Apogon imberbis on shallow
subtidal rocky reefs at STARESO field station on Corsica in the Western Mediterranean. Specifically, I examined the contribution of rock size and refuge quality to
the determination of resting habitat. Cardinalfish exhibited strong specialization to
rocky habitat providing complex internal space for refuge and retreat, driven
largely by the presence of boulders (30cm-1m) and bedrock (>1m). This supports
the hypothesis that refuge from predation is a major driver in the selection of daytime resting sites. Additionally, the high degree of habitat specialization allows us
to better predict impacts of anthropogenic activity on Apogon communities.
Introduction
Organisms vary widely in their use of available habitat, both across the range of
possible habitat as well as the degree to which they exhibit preference for or association
with particular habitat types. Understanding the distribution of organisms relative to their
habitat may allow us to predict the types of ecological processes by which their
populations are regulated (Syms 1995). The degree to which a species specializes on a
particular habitat may vary along a spectrum, with specialists existing only in very
specific habitat types and generalists being able to live in multiple areas. A species’
position along this continuum may influence its interactions with other species as well as
the types of species with which it can coexist (Gardiner & Jones 2005). Generalists may
theoretically coexist with specialists as each has competitive advantages in different areas
and specialists may coexist with one another as past competition has lead partitioning of
resources.
Species-habitat relationships have applied as well as theoretical implications.
Species that are more closely specialized on habitat type are more strongly affected by
habitat degradation (Swihart et al. 2003). Thus, an understanding of the strength of a
species’ association to its habitat may allow for prediction and potential mitigation of
community impact of anthropogenic influence (shoreline development, pollution, etc.). It
is also important to understand habitat associations in the context of population
assessment. Knowledge of the degree of specialization on a particular habitat type can
contribute to better sampling protocol design for population estimates. Broad, random
sampling for strongly associated organisms or highly targeted sampling for loosely
associated organisms can produce skewed and inaccurate estimates. Proper assessment of
species-habitat associations can make these estimates both more accurate and more
efficient. Overall, understanding of habitat selectivity can provide valuable input to
applied ecosystem-based management systems (Dissanayake & Stefansson 2012).
The cardinalfish Apogon imberbis (Perciformes: Apogonidae) is a commonly
occurring predatory fish associated with rocky reef habitat throughout the eastern
Atlantic and Mediterranean. Apogon imberbis occupies crevices and caves during the
day, emerging at night to forage on small fish and invertebrates across both hard and softbottomed areas (Azzurro et al. 2007, Bussotti et al. 2009). In tropical systems, apogonids
have been shown to exhibit a high degree of fidelity to their daytime resting sites,
returning from up to 2km distance after displacement, in addition to strong habitat
specialization (often to individual coral species) (Marnane 2000, Gardiner & Jones 2005,
Døving et al. 2006). Despite its position as the sole endemic cardinalfish species in the
Mediterranean (it is the only species present at the study site), Apogon imberbis has
received little attention regarding these features of its life history. Its diel movement
(from refuge sites during the day to foraging sites at night), in combination with site
fidelity and a high degree of habitat specialization, may provide a significant source of
organic material movement onto rocky reefs and marine caves in the Mediterranean
(Bussotti et al. 2009). Additionally, stable isotope studies have revealed A. imberbis,
despite its small size, to be an important high trophic level feeder (Pinnegar & Polunin
2000) and an integral member of Mediterranean subtidal food webs.
The goal of this study was to elucidate the degree of habitat specialization shown
by Mediterranean cardinalfish. As cardinalfish are nocturnal feeders and daytime habitat
use appears to be driven primarily by its suitability as a refuge or resting site, I examined
habitat use in the context of its refuge quality. Specifically, to understand whether A.
imberbis shows habitat selectivity based upon daytime refuge quality, I quantified overall
available rocky-bottomed habitat as well as specific habitat in which cardinalfish were
found. For both surveys, I assigned qualitative scores based on resting site or refuge
suitability and then compared overall habitat and refuge availability to cardinalfish
habitat and refuge use. Additionally, I noted cardinalfish habitat use (i.e. their position in
the water) relative to available refuge.
Methods
Study System and Species
I characterized cardinalfish habitat and distribution in subtidal communities
adjacent to STARESO (Station de Recherches Sous-Marines et Oceanographique) field
station near Calvi, Corsica (8°45'E, 42°35N, Figure 1). The nearshore marine
environment consists largely of granitic substrate ranging from contiguous bedrock to
small cobble fields. The bottom slopes to extensive beds of the seagrass Posidonia
oceanica beginning at 4.5m-14m depth. Available hard-bottom space is primarily
occupied by low-lying red and brown algal communities. The nocturnal cardinalfish,
Apogon imberbis (Apogonidae) is found over rocky substrate throughout the
Mediterranean and the eastern Atlantic coast (approx. Morocco to the Gulf of Guinea).
Apogon imberbis forages at night and resides in or near rock crevices and caves during
the day (Bussotti et al. 2009).
Figure 1. Location of STARESO, Pte. Revellata, Corsica
General Approach
I surveyed cardinalfish assemblages and available habitat on scuba at depths
between 2.5m and 13.5m along 50m transect lines to the north and south of the
STARESO harbor. I conducted four surveys to the north and one to the south. Transect
locations were determined by the presence of cardinalfish in these areas (Figure 2).
Cardinalfish surveys were carried out during the day, to ascertain daytime resting habitat
use.
Figure 2. Location of 50m fish and habitat survey transects relative to STARESO harbor (not to scale)
Cardinalfish abundance and habitat use
To characterize habitat use by Apogon imberbis, I laid 50m transect lines parallel
to shore, beginning in areas where fish assemblages were noticed. Divers counted total
individuals 3m to either side of the transect. We placed 0.25m2 quadrats with 9 uniform
points over sites occupied by fish and quantified habitat makeup based on rock size and
substrate categories (0-5cm – “golf ball”, 5-10cm – “fist”, 10-30cm – “head”, 30cm-1m –
“boulder”, >1m – “bedrock”, sand, Posidonia seagrass) as well as fish position relative to
the available habitat (“inside” – within an enclosed space, “outside” – near, but not inside
an enclosure, “water column” – positioned completely above the substrate). In addition to
a quantitative measure of habitat composition, we assigned a qualitative score (1-4) to
rate the area by suitability of refuge. Low scores (1-2) indicated relatively flat substrate
without internal volume into which fish could escape. Higher scores (3-4) denoted more
complex space for retreat and cover (Table 1).
Table 1. Description of qualitative refuge scores
Habitat availability
I quantified available habitat by performing uniform (every 2.5m, =20 points)
sampling along 50m transects through the areas where fish habitat use was surveyed. We
placed 2.5m2 quadrats with 9 uniform points on either side of the transect line and
quantified habitat and refuge quality using the methods outlined for habitat use.
Do cardinalfish exhibit daytime habitat specialization?
To test the hypothesis that cardinalfish occupy a specific subset of available
habitat, I used performed a multivariate analysis of group similarities (ANOSIM) to
compare composition of space occupied by fish and available habitat using the R package
vegan (R Development Core Team 2011, Oksanen et al. 2012). I analyzed significant
differences with vegan using similarity of percentages (SIMPER). Specifically, I
determined the contribution of each substrate type/size to the dissimilarity between
available and utilized habitat. For this and subsequent statistical analyses I chose a critical
alpha value of 0.05.
Do cardinalfish specialize their daytime habitat use based on refuge quality?
To test the hypothesis that cardinalfish occupy daytime resting sites based upon
the quality of refuge, I used a chi-square goodness-of-fit test to compare the distributions
of fish and available habitat across the range of refuge scores.
Do cardinalfish exhibit location preference relative to available refuge?
To test the hypothesis that cardinalfish location with respect to the available
habitat is non-random, I used a chi-square analysis to compare fish locations to an evenly
distributed expected distribution.
Results
Overall Patterns
The two most commonly available substrate types within the surveyed areas were
boulder and bedrock (mean 16.1% and 57.9% cover, respectively). Cardinalfish habitat
was also characterized largely by boulder and bedrock (mean 39.0% and 36.3% cover,
respectively) (Figure 3).
Figure 3. Mean proportion of substrate cover by survey type (fish habitat and available habitat)
Do cardinalfish exhibit daytime habitat specialization?
Substrate composition of habitat utilized by Apogon imberbis differed
significantly from overall available habitat (ANOSIM, R=0.1082, p=0.001). Among
substrate types, head, boulder and bedrock contributed to 80.27% of the dissimilarity
between available and utilized habitat (SIMPER, bedrock: 37.69%, boulder: 28.19%,
head: 14.39%). Multidimensional scaling ordination shows distinct spatial partitioning of
overall habitat and habitat utilized by cardinalfish (Figure 4).
Figure 4. Non-metric multidimensional scaling (MDS) plot of substrate composition between available
and utilized habitat.
Do cardinalfish specialize their daytime habitat use based on refuge quality?
Cardinalfish habitat used based on refuge quality varied significantly from
expected (Chi-square goodness-of-fit: χ2=109.41, df=3, p << 0.001). Fish were most
often assigned refuge scores of 3 and 4, whereas habitat surveys primarily fell within
refuge scores 1 and 2 (Figure 5).
Figure 5. Distribution of cardinalfish and available habitat across qualitative refuge scores.
Do cardinalfish exhibit location preference relative to available refuge?
I found Cardinalfish outside of possible refuge spaces more frequently than inside
(Chi-square goodness-of-fit: χ2=8, df=1, p=0.0046). To satisfy the assumptions of the
goodness-of-fit test and since no fish were found in the water column (completely above
the substrate), analyses included only the “inside” and “outside” location categories.
Discussion
Apogon imberbis displayed strong association to specific habitat types,
particularly areas comprised of boulder and bedrock substrate providing interior space for
refuge and retreat. Previous studies in the tropics have shown apogonids to exhibit strong
habitat selectivity, both across broad substrate types (Vivien 1975, Chave 1978) as well
as within finer scale microhabitat (Gardiner & Jones 2005). My results suggest that
microhabitat (i.e. substrate composition and shape) and refuge availability play a strong
role in the daytime resting site selection of rocky reef associated apogonids. One factor
that may explain specialization to areas of boulder and bedrock with interior space is
refuge from predation. Structural habitat complexity and shelter quality plays a
significant role in the survivorship of coral reef fish, specifically with regard to their
relationship to predators (c.f. Beukers & Jones 1998, Nemeth 1998, Willis & Anderson
2003). Survey data and personal observation indicate that habitat with better refuge (i.e.
deeper or more complex internal space for retreat) tends to consist most often of boulder
and bedrock. This trend is maintained for both overall available habitat and areas
occupied by cardinalfish, supporting the claim that cardinalfish specialization on habitat
consisting largely of these substrate types (as shown by the SIMPER contribution
percentages) is driven by its suitability as refuge from predation.
In addition to habitat association, I found patterns in cardinalfish habitat use
relative to available refuge. Fish were found outside of refuge more frequently than
expected. Some tropical cardinalfish species have been shown to supplement nocturnal
foraging during the day (Marnane & Bellwood 2002). It is possible that Apogon imberbis
behaves similarly to these species: remaining outside (but close to) refuge preserves the
possibility for opportunistic feeding while simultaneously providing a space for quick
retreat from potential threats. Another possibility behind the patterns found in this study
relates to historical change in the composition of Mediterranean fish assemblages.
Fishing has long been the primary factor driving such changes (Sala 2004), particularly
with regard to the depletion of predatory species (Bearzi et al. 2006, Ferretti et al. 2008).
Thus, it is possible that cardinalfish location outside of refuge is a recent development
arising from the release of pressure from predation. Further studies comparing sites with
greater and lesser degrees of depletion (e.g. marine protected areas, reserves) may help
explain these patterns.
The strong preference of Apogon imberbis to specific habitat is likely driven to
some degree by the availability of refuge from predation. However, I observed a number
of sites throughout the study area that contained no cardinalfish (particularly to the south
of STARESO harbor), despite being predicted by my results as prime habitat. Thus,
refuge from predators may only be one factor influencing selection of daytime resting
sites. Another potential factor influencing spatial distribution of reef fishes is social
interaction. Specifically, the presence of conspecifics may increase the likelihood that a
given site will be chosen. A number of species of cardinalfish exhibit gregarious behavior
(e.g. Kuwamura 1985). Habitat preference in gregarious cardinalfish was shown to be
affected by the presence or absence of conspecifics (Gardiner & Jones 2010), showing a
strong influence of both habitat preference and social interaction on their spatial
distribution. Further study with Apogon imberbis, including multi-way choice
experiments, will elucidate the degree to which the presence of conspecifics influences
distribution and habitat preference in Mediterranean cardinalfish. Døving, et. al. (2006)
have suggested olfaction as a potential mechanism behind cardinalfish aggregation and
site fidelity. Olfaction is one of the few processes in fishes that has been shown to be
affected by ocean acidification (Munday et al. 2009, Devine et al. 2012). Since the
Mediterranean is likely to be particularly susceptible to increased acidification due to
climate change (Touratier & Goyet 2011), further investigation of mechanisms driving
Apogon imberbis distribution will help understand the impact of climate change on an
important fish community in this area.
This study has shown that Apogon imberbis, like its counterpart species in coral
reef systems, displays strong habitat specialization. Evidence suggests that refuge from
predation is a key driver in creating this specialization. This may help us better
understand which ecological processes regulate Apogon populations in the
Mediterranean. Additionally, further work investigating possible sensory and social
influences driving habitat selectivity deserves attention, as it could provide important
insight into future effects of changing ocean conditions on a key member of
Mediterranean fish communities.
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