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Journal of Experimental Marine Biology and Ecology 441 (2013) 90–98
Contents lists available at SciVerse ScienceDirect
Journal of Experimental Marine Biology and Ecology
journal homepage: www.elsevier.com/locate/jembe
Fish community features correlate with prop root epibionts in Caribbean mangroves
James A. MacDonald ⁎, Judith S. Weis
Department of Biological Sciences, Rutgers University, 195 University Ave, Newark NJ, 07102, USA
a r t i c l e
i n f o
Article history:
Received 30 May 2012
Received in revised form 17 January 2013
Accepted 20 January 2013
Available online xxxx
Keywords:
Epibiota
Fish
Habitat heterogeneity
Mangroves
a b s t r a c t
Using visual census, fish and sessile epifaunal communities were compared in Rhizophora mangle (red mangrove) prop roots in Bocas Del Toro, Panama, and Utila, Honduras. A separate field experiment where epibionts were removed was also conducted at the Panama site. The results revealed a significant positive
correlation between epibiont diversity and fish species diversity as well as between epibiont abundance
and fish biomass. The trend was consistent in both sites, although there were differences in the details at
each location. Depth also weakly correlated with fish diversity in Panama, but not in Honduras. Results of
field experiments also support a correlation between epibiont communities and fish habitat, although primarily for smaller individuals.
© 2013 Elsevier B.V. All rights reserved.
1. Introduction
Mangrove forests and seagrass beds are important juvenile habitat
for some species of reef fish and influence fish communities on associated reefs (Dorenbosch et al., 2004; Halpern, 2004; Mumby et al.,
2004; Nagelkerken et al., 2000a, 2002; Parrish, 1989). Mangroves
have many ecological and hydrological functions, all of which can benefit fish populations, with or without a direct nursery function. There
are several benefits mangroves may offer to juvenile fish, particularly
their role as predator refuges, recruitment areas for larvae, feeding
grounds, shade providers, or resting places in the heterogeneous environment provided by the prop roots (e.g. Cocheret de la Moriniere
et al., 2004; Laegdsgaard and Johnson, 2001; Verweij et al., 2006a,b).
Mangroves may benefit fishes through multiple mechanisms at once,
and the benefits are frequently species-, size class-, or life-historyspecific (Manson et al., 2005; Nagelkerken et al., 2000a; Verweij et
al., 2006a).
In some areas there is no direct evidence that juvenile fish move directly from mangroves to reefs at all. In such a situation, mangroves
would function as an alternative fish habitat and not as a habitat utilized by juveniles prior to a shift towards the reef (Beck et al., 2001).
It remains difficult to draw any widespread general conclusions
about links between mangroves, related shallow habitats, and reefs
(Faunce and Serafy, 2006).
One point of uncertainty is that not all mangroves are equally valuable as nursery habitat; even within one geographic area, not all mangroves have the same density of juvenile fish relative to surrounding
habitats and relative to each other (Chittaro et al., 2005; Huxham
⁎ Corresponding author at: New York Sea Grant, c/o NYSDEC, 47-40 21st street, L.I.C.,
NY 11101, USA. Tel.: +1 718 482 4920; fax: +1 718 482 4502.
E-mail address: [email protected] (J.A. MacDonald).
0022-0981/$ – see front matter © 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.jembe.2013.01.019
et al., 2004), although not all studies have observed this (Sheridan,
1992). This site level variability can be true even for the same species
or closely related species, and has been observed specifically at one of
this study's locations in Honduras (Jaxion-Harm et al., 2011). Other
habitat attributes important to mangroves' nursery function, specifically predation pressure, can vary between equivalent mangrove
plots and times (Chittaro et al., 2005). Seasonal or temporal variation
has also been widely reported, with abundance typically peaking during the rainy season (Barletta et al., 2003; Lugendo et al., 2007).
In order to better understand the role mangroves play as fish habitat, it is necessary to understand what influences the relative value of
some mangroves compared to others. In reefs and sandy habitats,
variation in the complexity or composition of the habitat has an important impact on the fish community, specifically that rugose or diverse habitat increases diversity and abundance in fish communities
(Gratwicke and Speight, 2005a,b; Luckhurst and Luckhurst, 1978).
In addition to habitat complexity, the availability of shelter in the
form of holes or other hiding places has also been shown to influence
the abundance and community structure of coral reef fish, especially
given the numerous predators in tropical systems (Caley and St.
John, 1996; Eggleston et al., 1997). Removing or manipulating the
availability of shelter has been shown to have a corresponding effect
on juvenile fish; removing shelter reduces fish abundance, while additional shelter increases it (Finstad et al., 2007; Piko and Szedlmayer,
2007).
As in coral reefs, habitat complexity may also be important to fish
use of Caribbean mangrove habitats, which also demonstrate extensive variation in habitat characteristics. Shade availability, the density
or orientation of prop roots, and depth all have an influence on the fish
assemblage in mangroves (Cocheret de la Moriniere et al., 2004; Ellis
and Bell, 2004; Nagelkerken et al., 2010). Furthermore, mangroves
are a biologically complicated environment, consisting of much more
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J.A. MacDonald, J.S. Weis / Journal of Experimental Marine Biology and Ecology 441 (2013) 90–98
than just prop-roots. Particularly in parts of the Caribbean, many mangroves harbor a diverse collection of sessile epibiont organisms living
directly on the prop roots, including algae, sponges, tunicates, and bivalves, among others. In addition to the contribution that some of
these organisms make to the health of the mangrove trees themselves
(Ellison and Farnsworth, 1990), many of these organisms can significantly alter the structural heterogeneity and the character of prop
root habitats on a local scale.
There are numerous potential interactions between prop-root
epibiota and fishes. For instance, certain epibionts are themselves
prey for mangrove-utilizing fish species (e.g. Holocanthus spp.). Certain epibionts, if not themselves fed upon, provide prey habitat for
crustaceans and other common prey items of fishes (Cruz-Rivera and
Paul, 2006). On rocky shorelines, sessile fauna were found to be one
of the largest contributors to diversity and density of fishes (Ferreira
et al., 2001). Despite widespread evidence of links between fish communities and sessile fauna, these connections have not been closely
examined in mangroves.
Some authors have examined connections between epibiota and
fish communities in a variety of habitats, with mixed results. A study
utilizing simulated epibionts in artificial mangroves attracted a more
numerous and diverse fish community than controls lacking simulated epibionts (MacDonald et al., 2008). In a similar finding examining
live growths, these organisms have also been shown to attract fish to
artificial structures, such as dock pilings and artificial roots (Clynick
et al., 2007; Laegdsgaard and Johnson, 2001). Mussels, in particular,
were associated with a higher diversity and density of fishes around
dock piling (Clynick et al., 2007). However, Jaxion-Harm and Speight
(2012) found the opposite, finding that an increase of algae growing
on substrate below mangrove roots reduced predatory fish density,
suggesting that the nature of the epibiota is important to its influence.
Most of these studies only considered artificial structures, only JaxionHarm and Speight (2012) examined living mangroves.
This study examined the hypothesis that the community of sessile
organisms on the prop-roots influences fish communities in mangroves by examining a wide variety of mangrove transects and conducting removal experiments across an archipelago in Caribbean
Panama and separately examining transects in Caribbean Honduras.
Specifically, it was hypothesized that within contiguous mangrove
areas, those sections with a more diverse community of prop-root
epibionts would hold a more diverse community of reef fish compared
to similar areas with fewer epibionts, while the greatest density of
fishes would be found at sites with the densest epibiont growth.
2. Methods
2.1. Study sites
The first study area was the Bahia Almirante, Bocas Del Toro
Archipelago, Bocas Del Toro Province, Panama (9° 18´ 56´´N, 82° 13´
46´´ W) (Fig. 1A). Sites were established on five of these islands(Fig. 1A).
The majority of land cover in the area is pasture, with some secondary forest. The eastern half of I. Bastimentos, including associated marine areas, is
a National Park, with fishing restricted to hand capture limited exclusively
to indigenous residents.
All study sites were exclusively red mangroves, Rhizophora mangle
L, although there were white mangroves (Laguncularia racemosa L)
behind the R. mangle in a few areas. On Bastimentos, the total thickness of the mangrove fringe was nearly 500 m, while the site with
the thinnest fringe (on Isla Cristobal) had only 7 m of R. mangle.
All sites were permanently submerged. The tidal range in the Bahia
Almirante is small, ranging between 2 cm and 15 cm under standard
conditions (Guzman et al., 2005). The shallowest site averaged
33.2 cm deep at low tide, while the deepest was 72.6 cm; the mean
was 52.2 cm. Salinity in the Bahia Almirante varies by time of year,
but within any season it has been fairly consistent, with a mean of
91
Fig. 1. Bahia Grande and the Bocas del Toro Archipelago, Panama (A) and Isla Utila, Bay
Islands, Honduras (B). Transect locations are indicated by dots. The hashed area in
(A) indicates the approximate area of the reduction experiment.
30.14 (D'Croz et al., 2005). In most cases, coral reefs were close to
the mangrove fringe, from a minimum of 2 m to a maximum of
1.9 km, averaging 200 m. Seagrass beds were directly adjacent to
the mangroves in some sites, but varied up to 7.6 m from the mangrove edge. Intervening areas were muddy bottoms with scattered
weeds. Underwater secchi visibility ranged from a low of 3.4 m to a
high of 6.2 m, with a mean of 4.6 m.
The second study area was Isla Utila, Honduras (16°06′ 25″N, 86°
53′ 53″ W), a small island consisting primarily of mangrove-fringed
lagoons, lowland flooded forest, and tropical savannah (Fig. 1B). Mangrove fringes are mostly confined to the lagoons and some inlets on
the northern shore. Dwarf varieties are common in the lagoons. Extensive forests surround the lagoons, exhibiting the standard Caribbean pattern of R. mangle on the water, backed by black mangrove,
Avicennia germinans (L) and white mangrove further inland.
In the lagoon sites (Fig. 1B), there were no dense seagrass beds. In
fringe sites on the north coast, Thallassia testudinum (Banks and Sol. ex
K. D. Koenig) beds were immediately adjacent to the mangrove fringe,
with no intervening mudflat. Coral reefs were present immediately
outside the lagoons and within 100 m from the fringe. Underwater
secchi visibility ranged from 3 m to 5.3 m, with a mean of 4.3 m. As
in Panama, all sites were permanently submerged, although the tidal
range was considerably higher in Utila, almost 30 cm. Detailed Utila
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salinity data are not available, although no sites had any freshwater
input.
2.2. Fish surveys
In Panama, twenty-four 2 × 50 m belt transects were measured
and marked along the edge of the mangroves, and the markings left
in place for the duration of the study. An additional 11 transects
(2 × 40 m, due to restricted space) were established in Utila. Sites
were chosen to keep root density as constant as possible; in Panama
the prop root density varied from 25 to 29 roots m −2. Honduran mangroves had considerably denser prop roots, ranging from 33 to 54
roots m −2. Fish were surveyed by means of underwater visual census
(UVC) similar to that of (Nagelkerken et al., 2000b). Each transect in
Panama was surveyed 11 times on non-consecutive days between
5 June and 1 September, with 12 transects surveyed in 2005 and another 12 in 2006. In Isla Utila, Honduras, all transects were surveyed
11 times between 1 July 1 and 26 August, 2007. Each UVC lasted
10 min. A single highly trained observer counted every fish observed
inside each transect, identified each individual to species, and estimated total length using a reference ruler attached to a slate. The observer
was the same throughout the study to keep observational bias consistent. A second observer accompanied the main observer and kept a
separate count. The two counts were compared at the end of every
survey so that in the event of discrepancies greater than a few individuals the count could be repeated on another day, although that situation never arose. The exceptions were species of the genus Haemulon;
in the mangroves, juvenile Haemulon frequently formed large mixed
aggregations. In Panama, these schools were dominated by bluestriped grunts, Haemulon sciurus (Shaw); In Honduras the French
grunt, Haemulon flavolineatum (Desmarest), was most common.
Given the sometimes poor visibility, observers could not be absolutely certain of the identification of every individual, so this genus
was therefore treated as one taxon. Metrics for H. sciurus and
H. flavolineatum were used in all analyses. Large aggregations were
counted three times and the average number used. In order to avoid
double counting, any fish that approached from behind was not included. Neither cryptic species (e.g. Gobiosocidae spp.) nor the ubiquitous schools of Atherinidae and Clupeidae were included in the
census.
2.3. Epibiont surveys
In each transect, sessile organisms on the prop roots were surveyed
on one root per meter of transect. A 50 m logging tape was laid down
the length of each transect, and the root closest to each meter mark
(50 roots total in Panama, 40 in Honduras) was selected. In Panama,
where epibiont diversity was considerably higher, an additional 5 random roots were surveyed, for a total of 55 roots per transect; this
number was chosen based on species area curves generated from
pilot data taken in 2004 (unpublished). The epibiont survey was always conducted after the fish census had been completed.
Root organisms were tentatively identified to the lowest taxon
possible using keys provided by the Smithsonian Tropical Research Institute (STRI) and assistance from local experts. Species that could
not be identified with confidence were classified as unknowns. Identification of Cyanobacteria and hydroids to species was not always possible, so these were each considered as one taxon. The percent area
covered by each taxon per root was measured using a framed grid of
5 × 5 cm squares (75 cm long × 10 cm wide). Each 25 cm 2 square
was the base unit of measurement, and any growths smaller than approximately 0.25 of a square were virtually impossible to identify and
were treated as trace amounts. In every site, depth, underwater secchi
distance, and distances from the nearest reef, seagrass bed, and entrance to open ocean were also measured.
2.4. Experimental reduction of epibionts (ERS)
2.4.1. ERS surveys
Fish in three small mangrove islands located at the edge of the
Bastimentos Marine Park in the gulf between Isla Bastimentos and
Cayo Solarte (Fig. 1) were surveyed on eight separate days between
July 15 and July 25, 2006. This area is mostly undisturbed and dotted
with shallow reefs and thousands of mangrove cays, although it is not
located within the national park. During each survey, fish in a 2-m
wide belt transect around the circumference of each island were surveyed as described in the “Field Surveys” section. Each island was divided in half, and a coin toss determined which side would be the
experimental treatment and which side the control. A summary of
characteristics of each island is shown in Table 2; summary fish community characteristics are shown in Table 4.
2.4.2. Treatments
In the treatment half of each replicate island, every root was divided in half (upper and lower) and all epibiota growing on one of the
halves were completely removed with a wire brush or dive knife.
The half that was scrubbed (i.e., upper or lower) was alternated on
every root. The result was that 50% of epibiont coverage, measured
in terms of area covered, was completely removed from every root,
regardless of species. No particularly dense clusters of any given species were present, ensuring that removal was relatively even across
species. Epibionts in control sites were left undisturbed, although
they were exposed to a comparable level of disturbance as the treatment sites (walking, etc.).
The islands were left alone for 21 days to allow disturbance from
the clearing process to subside. Each replicate island was then resurveyed ten times over fifteen days between August 14 and August
29, 2006; abundance and species richness of fishes were counted
and biomass estimated in both control and experimental transects.
2.5. Statistical analysis
2.5.1. Field surveys
Two particular relationships were examined, the relationship between diversity of epibiont organisms and fish diversity, and separately the relationship between epibiont abundance and fish biomass.
Fish and epibiont Species Richness (SR), Shannon Wiener Diversity
Index (H′), epibiont density (measured by total epibiont coverage
area per root), and mean fish biomass per m 2 of transect were all calculated. Fish biomass was estimated based on established length–
weight (L–W) relationships published on www.fishbase.org (Fraese
and Pauly, 2007) and measured in kg. Species Richness is not a
mean, it is the total number of species that were observed repeatedly
in each transect over the course of the study. Any fish species observed
during only one survey was not included in SR calculations or any
other analysis.
The two relationships described above were analyzed using three
separate Generalized Linear Mixed Models (GLMM). One model considered fish SR as a dependent variable, with epibiont species richness
as well as all measured habitat features — depth, root density, turbidity (measured by underwater secchi distance), distance to nearest
reef, and distance to nearest sea grass — as the explanatory variables.
This model considered count data and thus the Poisson error structure was required. A separate model contained fish H′ as the dependent variable, including epibiont H′ and all the habitat features as
explanatory. The third model used fish biomass as a dependent variable with epibiont abundance and habitat features as the explanatory
factors.
Additionally, each model also measured effects of site (Panama v.
Honduras) and interaction effects with the year of the study as random effects. Models were compared using Aikake's Information Criterion (AIC). Complex models were simplified by removing factors
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J.A. MacDonald, J.S. Weis / Journal of Experimental Marine Biology and Ecology 441 (2013) 90–98
determined to be non-significant until only the most efficient explanatory model remained.
In multivariate space, the ratio of epibiont species present to sample size was too high for most analyses, and a Principal Component
Analysis run of the epibiont data by species showed that no particular
components explained substantial variance. Therefore, community
analysis was performed at a suprageneric level for epibionts (e.g.
poriferans, corals). As the hypothesis of the study was examining the
influence of epibionts on fish, epibionts were treated as a landscape
characteristic and Canonical Correspondence Analysis (CCA) was
used to correlate the epibiont community (measured by covered
area/root) with fish species biomass, log n + 1 transformed. The null
hypothesis of this procedure is that there is no connection between
the fish and landscape characteristics (epibiont taxa).
2.5.2. Experimental reduction of epibionts
Community composition data were analyzed to the family level
in order to consolidate low-occurrence species. For example, the
Lutjanidae as a whole were very common but certain species occurred
only infrequently; the family level was chosen to maintain coherency
in the data. Only the 11 most abundant families were used in analysis,
as these accounted for more than 99% of individuals. Observed
biomass was estimated as described in the previous section. One
extremely large species, the nurse shark Ginglymostoma cirratum
(Bonnaterre) was not included in biomass analysis as one individual
can have more biomass than an entire transect combined, severely
distorting results. Once standardized, all data were log n + 1 transformed and mean fish density and species richness among sites and
treatments were compared using 2-way Repeated Measures Multivariate Analysis of Variance (R-M MANOVA). Biomass was likewise separately compared using R-M MANOVA.
At the species level, log-transformed abundance data for the 12
most abundant species were compared using Repeated Measures
MANOVA. Finally, fish were also separated into three size classes:
b10 cm, 10.1–20 cm, and > 20 cm, and the relative abundance of
each class analyzed by MANOVA. (This was not done to species level
due to insufficient abundance.)
GLMM and all analyses in the experimental epibiont reduction experiment were performed using SPSS v. 20.0 for Macintosh. Ordination was performed using PC-ORD v 4.0.
93
Table 1
List of fish species observed during visual surveys at both sites. In the location column,
P = Bocas Del Toro, Panama, and H-Utila, Honduras. Under prevalence, A= abundant
(>10/survey/transect), VC = very common (5–10/per survey/transect), C = common
(1–5/survey/transect), U = uncommon (b1 per survey/transect, but found in most
transects) and R — rare (≤5 per study area).
Common name
Latin name
Location
Prevalence
Foureyed butterflyfish
Spotfin butterflyfish
Banded butterflyfish
Grunts
Porkfish
Great barracuda
Dusky damselfish
Threespot damselfish
Cocoa damselfish
Sergeant major
Schoolmaster
Gray snapper
Yellowtail snapper
Lane snapper
Cubera snapper
Yellowfin mojarra
Flagfin mojarra
Striped parrotfish
Yellowtail parrotfish
Stoplight parrotfish
Bucktooth parrotfish
Redband parrotfish
Barred hamlet
Rock hind
Doctorfish
Blue tang
Slippery dick
Bluehead wrasse
Puddingwife
Bridled gobi
Cleaner gobi
Gray angelfish
Southern stingray
Yellow stingray
Atlantic needlefish
Inshore lizardfish
Western Atlantic seabream
Chain moray
Checkered puffer
Mangrove rivulus
Common snook
Chaetodon capistratus
Chaetodon ocellatus
Chaetodon striatus
Haemulon spp.
Anisostremus virginicus
Sphyraena barracuda
Stegastes adustus
Stegastes planifrons
Stegastes variabilis
Abudefduf saxatilis
Lutjanus apodus
Lutjanus griseus
Ocyurus chrysurus
Lutjanus synagris
Lutjanus cyanopterus
Gerres cinereous
Eucinostomus melanopterus
Scarus iseri
Sparisoma rubripinne
Sparisoma viride
Sparisoma radians
Sparisoma aurofrenatum
Hypoplectrus puella
Epinephelus adscensionis
Acanthurus chirurgus
Acanthurus coeruleus
Halichoeres bivittatus
Thalassoma bifasciatum
Halichoeres radiatus
Coryphopterus glaucofraenum
Elacatinus randalli
Pomacanthus arcuatus
Dasyatis americanus
Urobatis jamaicensis
Strongylura marina
Synodus foetens
Archosargus rhomboidalis
Echidna catenata
Sphoeroides testudineus
Kryptolebrius marmoratus
Centropomus undecimalis
P,H
H
H
P,H
P
P,H
P,H
H
H
P,H
P,H
P,H
P
P,H
H
P,H
P,H
P,H
P,H
P,H
P,H
H
P
P
P,H
P
P,H
H
H
P
P
P
P
P,H
P,H
P
P
H
H
H
H
C
U
U
A-P;VC-H
C
C
C
U
U
A
A
C
C-P; U-H
U
U
A
VC
A-P; C-H
C
U
U
C
A
R
C
U
A
C
U
C
U
U
C
U
U
U
U
U
VC
C
U
3. Results
3.1. Surveys-general results
2 species of colonial tunicates were also present in addition to
cyanobacteria, hydroids, feather duster worms, and barnacles.
In Panama a total of 9622 individual fish, representing 41 species
from 21 families were observed. 29 different species and 18 families
were observed more than once and thus included in the analysis. Grunts
(Haemulidae spp.) and schoolmasters were dominant, although striped
parrotfish were most abundant in certain locales (Table 1). At least 59
species of root epibionts were observed. Green algae consisting of at
least 4 species and sponges of at least 27 species were the most common taxa. Other common taxa included three sessile mollusc species,
cnidarians (including seven corals, one hydroid, and one anemone)
Rhodophyta, Phaeophyta, Annelida, and cyanobacteria. Barnacles as
well as colonial and solitary tunicates (10 species of tunicate in total)
made up the rest. The annelids consisted primarily of calcareous tubes
created by colonial worms.
In Honduras, a total of 4560 individuals from 38 species and 16
families of fish were observed. 28 of these species from 13 families
were included in the analysis (Table 1). As in Panama, L. apodus was
the dominant species, but second most abundant was the mangrove
rivulus, Kryptolebias marmoratus (Poey). Root epibiont diversity was
lower in Honduras than in Panama, only 37 species of epibionts
were observed. Green algae (8 species) were more common than
sponges (14 species). 4 species of sessile mollusc, 4 rhodophytes and
3.1.1. Relationship of fishes to epibionts
None of the GLMM procedures testing the influence of epibiont
and abiotic variables on fish revealed any significant interactions
with either country or year (highest Z = 0.722, p ≤ 0.470). Consequently, Honduras and Panama data from all three years of the study
were analyzed together.
GLMM using fish species richness as a response variable with epibiont species richness plus all abiotic variables as predictors revealed
that epibiont species richness (Fig. 2A) plus two habitat variables,
depth and turbidity, had significant influence on the model (Epibiont
SR p ≤ 0.005, Depth p ≤ 0.004, Turbidity p ≤ 0.001). The four other variables tested (Mean distance to the nearest reef, distance to nearest sea
grass bed, root density, and mangrove fringe thickness) were not
found to exert significant influence on the model (lowest p ≤ 0.76).
Of the significant variables, turbidity had the highest coefficient and
thus the greatest magnitude influence on fish species richness (coefficient = 0.8) (Fig. 2B). Epibiont SR had the next largest coefficient
(0.369) followed by depth (0.121) (Fig. 2C).
When Shannon Weiner diversity index (H′) was substituted for
fish SR as the response variable and epibiont SR as a predictor variable,
results were similar, but with a few important differences. Unlike the
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fish diversity and increasing water clarity is driven by the oceanic Utila
sites (Fig. 2C).
It is worth noting that for the three epibiont taxa that displayed
a significant diversity of species (corals, sponges, and tunicates), SR
strongly correlated with abundance, so abundance of these taxa is a
fair proxy for species diversity (Linear Regression-corals: R2 =0.7844,
p ≤ 0.0001; sponges: R2 = 0.3953, p≤ 0.001; tunicates: R2 = 0.5789,
p ≤ 0.0001).
Residual analysis revealed that two Panama sites, both adjacent to
one another on the eastern edge of Isla Cristobal, exerted undue influence on the model, so as a result these 2 transects were excluded
from the final GLMM. (Even with these sites included, epibiont density was very nearly significant (p ≤ 0.055). Both of these sites have exceptionally lush growth of algae and cyanobacteria, the highest levels
observed in any site in either Panama or Honduras, in an area that has
registered elevated levels of inorganic nutrients (D'Croz et al., 2005)
and is influenced by creek discharge. Thick algae beds in mangroves
reduce the presence of many fishes (Jaxion-Harm and Speight, 2012).
With these sites excluded from analysis, the relationship is much
stronger. The GLMM found that only one variable, epibiont density,
had significant influence on fish biomass across both Honduras and
Panama (p ≤ 0.001, coefficient 0.485, Fig. 3). None of the other habitat
variables noted above was significant in this model (lowest p ≤ 0.182).
3.1.2. Community level effects
CCA of all combined species biomass and root taxa data from both
areas revealed no strong influences of particular taxa. While for axis 1
the connections between the fish and epibionts were significantly
greater than randomized data (Monte Carlo test, p ≤ 0.02), the first
two ordination axes in CCA explained only 20.4% of the variance in
the fish community data. No strong vectors are present when the
data are graphed (Fig. 4). These results suggest that the null hypothesis can be rejected in that there is some connection between epibiont
taxa and fish biomass. However, the influence of taxa on any particular
fish species or group of species is limited.
3.2. Experimental reduction of epibionts
Over the course of the study, 1721 individuals, comprising 22 fish
species from 16 families were observed in the Panama islands (treatment or control half) either before or after the manipulation. 58.5%
of those individuals were grunts (Haemulon spp.). Three additional
Fig. 2. Epibiont species richness v. fish species richness. Epibiont species richness,
depth, and low turbidity were all significant predictors for fish species richness,
while root density was not. Trend lines are derived from simple linear regression of
each pair of variables, and are not representative of the combined model. A.) Epibiont
species richness v. fish species richness, B.) Water clarity v. fish species richness, and
C.) Depth v. fish species richness.
species richness GLMM, only root H′ and turbidity were found to be
significant (root H′ p ≤ 0.01, turbidity p ≤ 0.001). Depth was not significant in this model, nor were any of the other habitat variables previously discussed (lowest p ≤ 0.120). Another difference is that root H′
had a higher coefficient (0.387) than depth (0.114), a reverse of the
species richness model. Taken together, diversity of epibiont organisms and water clarity are the most consistent predictors of fish diversity out of all the variables examined (Fig. 2). The correlation between
Fig. 3. Mean fish biomass by mean total area of epibionts per root. The open circles represent 2 sites adjacent to one another on the Northwest edge of Isla Cristobal, which
were both outliers due to exceptional algal growth (see results). Equation on chart reflects linear trendline w/o these sites.
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95
Fig. 4. CCA biplot of all fish species by sessile taxa abundance. Species abbreviations are listed below. Achir: Acanthurus chirurgus. Acoer: Acanthurus coeruleus. Ar: Archosargus
rhomboidalis. As: Abudefduf saxatilis. Av: Anisotremus virginicus. Cc: Chaetodon capistratus. Cg: Coryphopterus glaucofraenum. Co: Chaetodon ocellatus. Cs: Chaetodon striatus.
Da: Dasyatis americana. Ea: Epinephelus adscensionis. Ec: Echidna catenata. Eg: Eucinostomus gula. Em: Eucinostomus melanopterus. Er: Elacatinus randalli. Gc: Gerres cinereus.
Hb: Halichoeres bivittatus. Hp: Hypoplectrus puella. Hr: Halichoeres radiatus. Hspp: Haemulon spp. Km: Kryptolebrias marmoratus. La: Lutjanus apodus. Lc: Lutjanus cyanopterus.
Lg: Lutjanus griseus. Ls: Lutjanus synagris. Oc: Ocyurus chrisurus. Pa: Pomacanthus arcuatus. Sa: Stegastes adustus. Sau: Sparisoma aufrenatum. Sb: Sphyraena barracuda. Sf: Synodus
foetens. Si: Scarus iseri. Sm: Strongylura marina. Sp: Stegastes planifrons. Sra: Sparisoma radians. Srub: Sparisoma rubripinne. St: Sphoeroides testudineus. Sv: Sparisoma viride. Svar:
Stegastes variabilis. Tb: Thalassoma bifasciatum. Uj: Urobatis jamaicensis.
species, Lutjanus apodus, Chaetodon capistratus (L), and Scarus iseri,
made up another 32% of observed individuals. In total, 12 species
in 10 families — Abudefduf saxatilis (L), C. capistratus, Gerres cinereous
(Walbaum), G. cirratum, Haemulon spp., Halichoeres bivittatus (Bloch),
Hypoplectrus puella (Cuvier), L. apodus, L. griseus (L), S. iseri, Sphyraena
barracuda (Walbaum) and Stegastes adustus (Troschel), accounted for
more than 99% of all individuals.
In the removal transects, overall fish abundance remained stable;
however, in the control transects, abundance increased significantly during the period of the experiment (Fig. 5A) (Repeated measures
MANOVA, F48,1 = 10.68, p ≤ .002, time * treatment; F48,1 = 13.98,
p ≤ .02, time * location; F48,2 = 7.39, p ≤ .002).
Unlike abundance, mean biomass of fish decreased in both treatments and controls but the reduction was significant only in experimental transects (Fig. 5B). (Repeated measures ANOVA, time F48,1 =
0.79, p ≤ .006, time * treatment; F48,1 = 5.40, p ≤ 0.026, time * site;
F48,2 = 0.574, p ≤ 0.57, time * site * treatment F48,2 = 1.73, p ≤ 0.19.).
Biomass also varied significantly by site (Table 2).
Species richness was significantly affected during the experiment as well (Fig. 5C). SR decreased slightly in experimental transects, and increased significantly in control transects, although the
effect was stronger in some sites than others. (Time: F48,1 = 2.84,
p ≤ .115, time * treatment; F48,1 = 3.99, p ≤ 0.05, time * site; F48,2 =
4.15, p ≤ .023, time * site * treatment; F48,2 = 14.69, p ≤ 0.001).
When fish were separated into size classes, the significant changes
in abundance in controls relative to experimental transects applied
mostly to smaller fish (0–10 cm TL: time * treatment, F48,1 = 20.43,
p ≤ 0.001) although there were significant increases in some control sites among slightly larger fish (10.01–20 cm TL; F48,2 = 4.31,
p ≤ 0.02). The smallest fish increased in abundance in most replicates,
while abundance of intermediate-sized fish decreased in treatments
and increased in controls, but the increase was not significant. Densities of large fish (≥ 20.01 cm) did not change significantly (p ≤ 0.69).
There were also significant differences in location for all size classes.
The R-M MANOVA results are summarized in Table 3.
3.2.1. Community composition
Reducing the density of epibionts did not affect overall community
structure significantly. There were significant differences in the abundance of the top 11 individual species among sites and treatments
(MANOVA, F48,1 = 4.84, p ≤ .001 treatment; F48,1 = 4.03, p ≤ .0001
site) For the most part the pattern of abundance/species followed
the pattern for overall fish abundance (increased in controls, stayed
flat in experimental treatments) with the exception of H. bivittatus
(slippery dick), which increased in experimental treatments. Other
species, e.g. G. cinereous (yellowfin mojarra), followed a geographic
pattern, decreasing between surveys in some islands, regardless of
treatment, but not in others. The species data are summarized in
Table 4.
4. Discussion
The results in this study are consistent with the hypotheses that a
greater diversity and abundance of prop-root epibionts in mangroves
contribute to higher fish biomass and a more diverse fish community.
Epibiont density and diversity were the most consistent predictors of
fish density and diversity, a trend observed across two geographically
separate sites and in spite of confounding factors such as variable
prop root density. Certain abiotic variables, particularly water clarity
and depth, also influenced diversity of fishes, although none of the
habitat variables examined influenced fish biomass significantly. Results of the experimental reduction experiment support the survey
results regarding epibiont density and fish biomass.
Of the abiotic and habitat variables, water clarity had the largest
influence on fish diversity, but not biomass. For one thing, visual census is more effective in clearer water, making it easier to spot additional species. However, a look at the graph in Fig. 2 suggests that this
trend is driven primarily by much higher fish diversity in sites with
the clearest waters, rather than a continuous trend of decreasing turbidity and increasing fish diversity. The clearest sites were the
ocean-facing sites in Honduras, the only ocean facing sites in the entire
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Table 2
Mean fish abundance, biomass, and species richness by experimental reduction location. Letters indicate significant differences.
Island Circumference Depth Density
Richness Richness Biomass
(m)
(m)
(mean/10 m2) (mean) (total)
(mean kg/m2)
1
2
3
20
34.5
42
.55
.55
.7
21.43 b
4.69 a
10.36 a
3.84 b
2.30 a
2.51 a
10
13
12
0.53 b
0.09 a
0.64 b
simultaneously increased with water clarity, a result of increased primary production.
The distance between the mangroves and neighboring habitats did
not seem to influence epibiont or fish communities. This was surprising, as connectivity in mangrove-seagrass-reef habitats is important
(Dorenbosch et al., 2004, 2007; Jaxion-Harm et al., 2011; Jelbart
et al., 2007; Sheaves, 2005; Verweij et al., 2006a). The lack of differences in this study probably reflects the shorter distances between
habitats compared to previous studies; the largest mangrove-reef distance in this study was 1.9 km, and most were less. These results support findings that reef-mangrove trends may be evident at an island
scale rather than on individual reefs (Dorenbosch et al., 2006).
There are a few potential mechanisms underlying the relationship between epibionts and fishes, and the relationship is likely driven
more by the epibionts than the fish. Competition and water flow have
a larger influence on benthic communities than predation (Palardy
and Witman, 2011; Wulff, 2005). Therefore, the fish community is
more likely to be influenced by the epibionts rather than vice-versa.
Epibionts might influence diversity and biomass of fishes in a number of ways. For example, epibiota such as algae may attract diurnal
herbivores for feeding (Verweij et al., 2006b). Some of the species
observed, e.g. foureye butterflyfish, C. capistratus, may also feed directly on certain epibionts, e.g. sponges. At the same time, excess algae
may reduce habitat value for predatory fishes (Jaxion-Harm and
Speight, 2012). Furthermore, the extent to which fish feed in mangroves may be limited to certain species or populations (Grol et al.,
2008; Nagelkerken and Van der Velde, 2004; Verweij et al., 2006b).
Overall, there is no evidence in the current study that feeding plays a
major role in the epibiont fish relationship.
Another possible function of epibionts is to provide shelter for
fish. As diversity and density of epibionts increases, increased structure as well as diversity of shapes and forms becomes available. Increasing habitat complexity, particularly rugosity, hard cover, and
refuge holes increases reef fish richness and abundance due to the increased diversity of available shelter (Gratwicke and Speight, 2005a,b;
Luckhurst and Luckhurst, 1978). Experiments with artificial mangrove
roots have demonstrated that structures such as epibionts do attract a
greater diversity and abundance of fishes (MacDonald et al., 2008).
Many of the commonly observed epibionts, e.g. the sponge Spongia
tubulifera (Hyatt), exhibit a complicated or massive body shape (or
both), and their presence can increase rugosity substantially or create
shade that can help hide smaller fish from predators (Cocheret de la
Moriniere et al., 2004; Ellis and Bell, 2004) or ambush sites for those
predators.
Fig. 5. Experimental reduction of density: changes in controls relative to sites with
epibiota reduced for fish Density (A), Biomass (B) and Species Richness (C). Asterisks
indicate significant pre/post experimental differences; error bars are +/−1 SE. All
sites are standardized to a 10 m transect. Gray bars are controls.
Table 3
Mean fish abundance/treatment by size class of fish, before and after the epibiont reduction. Actual observed densities (#/10 m) are shown, but significance is based on
log transformed data.
Size class of fish
*= Significant before/after difference, p ≤ 0.0001
Treatment
study. As there were numerous differences (continuity with neighboring habitats, currents, etc.) between these sites and the others in the
study, there is no way to conclude that turbidity is the major factor
setting diversity in these sites apart. Furthermore, epibiont diversity
Density reduced
Control
10.1–20 cm
20 cmb
Before
0–10 cm
After
Before
After
Before
After
2.63
1.02
2.89
5.89*
2.62
2.49
2.05
2.85
.141
.113
.101
.170
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Table 4
Family response to epibiont reduction. Actual mean densities/10 m transect are given,
but p values are based on log transformed data. Significant increases/decreases are
marked by an asterisk.
Species
Reduced
Control
Before
After
Before
After
P≤
Chaetodon capistratus
Haemulon spp.
Sphyraena barracuda
Pomacentridae
Lutjanus spp.
Gerres cinereous
Scarus iseri
Serranidae
Halichoeres bivittatus
Ginglymostoma cirratum
0.45
5.66
0.09
0.77
3.46
0.12
0.52
0.46
0.08
0.16
0.64
3.11
0.41
1.02
4.52
0.00
0.00
0.38
0.37*
0.05
0.22
2.55
0.20
0.53
3.10
0.10
1.59
0.14
0.18
0.18
0.64
9.43*
0.58
1.19
6.34*
0.04
0.00
0.34
0.23
0.00
0.108
0.001
0.148
0.487
0.005
0.592
0.597
0.267
0.002
0.137
Nagelkerken et al. (2010) observed that the interstitial distance between roots had a major impact on fish richness and abundance,
suggesting that distance to refuge may be vital. Epibiotic organisms
serve to decrease interstitial distances, filling the between-root spaces
in multiple dimensions, and moving refuge closer to fishes swimming
or hovering between roots. Structure created by epibiota also causes a
direct increase in surface area of the habitat in addition to increasing
heterogeneity.
The results of manipulating epibiont density mostly support the
survey results. Overall fish density and species richness increased during the experiment. However, the increase was significant only in the
untouched transects. At the same time, mean biomass decreased, but
the decrease was much larger in experimentally reduced transects.
Similar results, including significant but relatively weak effects, have
been observed in epibiont removal experiments on artificial pilings
(Clynick et al., 2007). Evidently, in the current study, a pulse of smaller
fish moved into the study area during the experiment while some
other larger individuals moved out, and these newcomers preferentially settled in the undisturbed transects. The results suggest that different sizes of fishes may interact with the epibionts in different ways.
Fish biomass and diversity did decrease in experimental transects
compared to controls, while the numbers of the smallest fish increased dramatically in controls but not in the experimentally reduced transects, possibly reflecting settling of new juveniles. A lot of
coralline algae was removed in these transects; its removal decreased
some heterogeneity and a lot of hard substrate, but not of as many
complicated structures where larger fish may hide. Smaller individuals of some species have been shown to make greater use of structure compared to larger individuals (MacDonald et al., 2009). The
smallest fish are able to utilize a broader range of structure sizes as
shelter, or feed more easily in the crevices of the coralline algae.
These results are consistent with the increase in biomass in proportion to total area of epibionts observed during the field surveys.
Gratwicke and Speight (2005b) found that the best predictor for fish
abundance and diversity was height of structure. These results are
consistent with that finding, as epibiont removal reduced the overall
habitat height (measured horizontally from the surface of each root),
and abundance was higher where height was unaffected. The simultaneous increase in fish diversity observed in controls may be an artifact
of a larger number of fish entering control sites, but it is also consistent
with survey results as well as past studies (e.g. Gratwicke and Speight,
2005b; MacDonald et al., 2008).
The most common species, particularly Haemulon spp., L. apodus,
and C. capistratus, followed the overall pattern of increase in control
transects, causing community composition to remain more or less intact, changing only in overall number rather than proportions of particular species. Since the habitat alterations were consistent, it makes
sense that the overall community would be affected. These results are
consistent with those of Jaxion-Harm and Speight (2012) in that the
97
effect in both the experimental reductions and in the surveys was noticeable only in broad community measures (e.g. biomass) rather
than on a species by species basis.
Adult fishes, for their part, were relatively unaffected by the
change in epibionts. A possible explanation is that many adult fish diurnally present in mangroves are there due to temporary, short-range
migration, rather than residency (Dorenbosch et al., 2007). Furthermore, the majority of the adult fish species observed during the experiment (e.g. L. apodus) are primarily piscivorous (Rooker, 1995).
These fishes most likely are not feeding on small prey living in the
crevices between epibionts. While they may benefit from the presence
of ambush sites, larger predators in the mangroves are not as likely to
require shelter and were most frequently observed right at the mangrove edge than directly by the roots. However, the presence of large
predators may encourage smaller fishes to seek out habitats with better shelter.
One caveat is that the magnitude of the changes varied considerably according to location, consistent with previous observations of
local scale variability (Jaxion-Harm et al., 2011). It is difficult to assess
the impact of the starting epibiont configuration, the nature of the
structure removed/remaining, or important independent factors
such as landscape configuration (Ashton-Drew and Eggleston, 2008).
In the area of the reduction experiment in Panama, the numerous
mangrove cays are part of a very diverse shallow water environment
including reef, Thalassia beds and a habitat known as coral garden.
The influx of smaller fish over the course of the experiment presumably came from the surrounding habitat. The variability of the landscape is a probable influence on spatial and temporal small-scale fish
variation among cays, particularly important when comparing sites
(Ashton-Drew and Eggleston, 2008). Connections with nearby habitat
types make a greater variety of species available to move in or out of
the experimental sites (Jaxion-Harm et al., 2011).
5. Conclusions
The results of this study are consistent with the hypothesis that
epibionts enhance mangrove habitats for use by fishes. The similar results across two completely separate locations imply that the basic
trend of correlation between epibionts and more abundant and diverse fish communities is widespread.
The experimental results additionally provide evidence that the
effects are connected to both fish size and geographic location at
both local and large scales. In areas where root organisms are common, epibionts can exert influence, and these communities should
not be ignored in habitat management or conservation decisions.
Acknowledgments
The authors wish to thank R. Collin, G. Jacome, and P. Gondola at
the Smithsonian Tropical Research Institute (STRI) Bocas Del Toro Research Station for the logistical support, A. Lawrence for field assistance in Panama, Operation Wallacea, Coral View Dive Center, and
the staff of the Utila Iguana Research and Breeding Station for logistical support in Utila, and T. Glover for the comments. This work was
funded in Panama by a STRI short-term fellowship, and in Honduras
by the PADI Foundation with additional support from Operation
Wallacea, llc. [ST]
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