A Study on the Habitat Association and Feeding Preferences of the
Red Mullet
(Mullus surmuletus)
Harrison J., Hernandez L., Williams E.
Abstract
Mullus surmuletus, the striped red mullet, is ecologically important by affecting other
species in its community via multi-species foraging interactions. Because of a lack of
understanding on M. surmuletus’ foraging behavior, we set out to identify how
environmental factors such as prey composition and available foraging habitat, affect
foraging behavior. To understand the foraging preferences of M. surmuletus in Revellata
Bay, Corsica, the invertebrate composition of the local habitat was sampled along with
stomach contents from nine individuals. Twenty transects were designed and run using
Uniform Point Contact and paired with fish surveys to examine available versus utilized
foraging habitat. Our data suggests M. surmuletus displays both generalist and specialist
tendencies, leading us to believe that the goatfish preferentially forages for specific prey
items.
Intro
Fish in the family Mullidae possess unique structures called barbels that are
responsible for a number of specialized feeding behaviors across numerous species.
These species have adapted an array of different strategies to forage for invertebrates in
sediment, algae, and rocks (Gosline 1985). Observational studies on the foraging of
different Mullidae species suggests that they have developed a distinctive ecological niche
based on their behavior, showing a variety of different preferences regarding preferred
substrate, prey species, and prey size (Labropoulou 1997, Gharbi and Ktari 1979).
Evidence of microhabitat specialization in the species Mullus surmuletus has been
observed with different foraging behaviors being favored in different habitats (Labropoulou
1997).
Ecologically, M. surmuletus are a key species because they are an important part of
multi-species foraging associations (Uiblein 2007). The digging and sifting behavior used
by M. surmuletus to forage effectively stirs up matter that follower fish species forage on
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(Yahel et al 2002). Their ecological importance based on this peculiar feeding behavior
makes M. surmuletus an important species to study and understand.
Previous research has focused primarily on stomach content analyses and not
behavioral preferences that could be influencing M. surmuletus’ observed diet. Evidence of
both generalist and specialist predatory behavior by M. surmuletus exists in the scientific
community (Labropoulou 1997) We set out to identify relationships that M. surmuletus may
have with a specific habitat or prey type.
Our initial observations revealed that individuals were foraging in a variety of
different habitats. Individuals appeared to spend unequal amounts of time foraging in
different substrate. Sandy patches and turf algae on the tops of boulders appeared to be
preferred.
We are interested to see if individuals forage randomly or if a preference exists for
specific habitat. This prompted our question of what is the relationship between foraging
behavior, habitat, and prey preferences. We hypothesize that there is variability of
invertebrate species composition between different types of habitat. We expect that M.
surmuletus will demonstrate a preference to specific habitat(s) when foraging. And lastly,
we hypothesize that M. surmuletus’ diet will be correlated with the available prey in their
preferred habitat.
Methods:
General Approach:
We conducted an observational field study that focused on foraging behavior of
Mullus surmuletus as a function of habitat and prey preference. The primary goal of this
survey was to look at how available habitat and prey affect M. surmuletus foraging
behavior. To find evidence that could be used to answer this question we collected data
concerning the invertebrate assemblages, stomach contents, and preferred foraging
habitat(s).
Species Description:
The focal species in our study is Mullus surmuletus commonly referred to as the striped
red mullet, a carnivorous fish species that feed on benthic invertebrates (Gharbi & Ktari
1979). M. surmuletus are distributed along the Eastern Atlantic from the English Channel to
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the northern part of West Africa and into the Mediterranean Sea with a depth range of 5409 meters (Bauchot, 1987).
Site Description:
This study was conducted at the Station De Recherches Sous Marines et
Océanographiques (STARESO) Marine Research Station located in Revellata Bay,
Corsica, France in October of 2014. Our study was based in the coastal marine habitat
near STARESO research station (42°34'49.0"N 8°43'26.8"E). The area where we
conducted our survey is dominated by the seagrass species, Posidonia oceanica, with a
small amount of sandy patches distributed throughout. Large, turf algae-covered boulders
line the shore for the entire area. The water system is saline and in October has an
average temperature of 20.2 degrees Celsius. All data from the field was collected on
SCUBA. Research divers were limited to a max depth of 17 meters.
Sampling Design:
Invertebrate assemblages:
We divided the area around STARESO into three distinct zones: within the harbor
(Harbor), north of the harbor (North), and south of the harbor (South). Due to the ocean
floor being covered predominantly by P. oceanica, patches of sand were chosen based on
availability in each zone. We divided sandy patches into two categories, open sand and
sand patches covered in a layer of decaying P. oceanica at least ten centimeters deep,
referred to as Posidonia mattes. We took sediment samples from all the three zones. Both
types of samples were not collected from all three zones because open sand was not
present in the South and posidonia mattes were not present in the Harbor.
Sediment in sand patches were collected using re-entry traps that consisted of PVC
pipe with an open top and a sealed bottom. The traps each had a diameter of 6 centimeters
with a depth of 5 centimeters. Traps were left in the field for two days before being
collected. When sampling in Posidonia mattes, Posidonia was cleared and then returned to
its original cover. Collected sediment traps were placed in watertight zip lock bags and
transported back to the lab.
For invertebrate collection in rocky substrate, we used a plastic kitchen sponge
called a “tuffie” as a proxy for turf algae. Each zone (north, south, harbor) had four locations
where tuffies were placed, with two replicates per location, yielding a total of eight tuffies
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per zone. The locations were standardized by going to the northernmost and southernmost
points of each region on the permanent transect and placing them in the nearest rocky
grouping at a depth of 5 and 10 meters. The tuffies were placed in their respective locations
and left for one week. They were then collected and transported to the lab in watertight zip
lock bags.
The samples from both sediment traps and tuffies were rinsed and filtered using
sieves with three different sizes; 4000, 2000, and 500 microns. The sediment was sieved
into different size groups to assist with the sorting process. There was no discernment
between larger or smaller size classes when inputting and analyzing collected data. The
categories of invertebrates were: gastropod, amphipod, isopod, worm, and echinoderm.
All data was tested for significance using a critical p-value of 0.05. PERMANOVA as
well as pairwise tests were used to determine if there was a significant difference between
invertebrate assemblages in both substrates. A SIMPER test was used to identify which
species were primarily causing the discrimination between two observed sample clusters.
Stomach Content Analysis:
Individuals for the study were caught opportunistically by SCUBA divers using pole
spears in collection dives. The stomachs were removed surgically, and then the contents
were cleaned and filtered using a saline solution. The stomach contents were counted and
categorized into their corresponding invertebrate category: gastropod, amphipod, and
worm. The number of invertebrate groups used in this portion of the study was reduced due
to only three major groups being found in the stomach contents. Each individual food item
was only counted if the “head” was intact; broken shell
pieces or detached appendages were not counted.
Data from stomach contents were statistically
analyzed using the same methods of PERMANOVA and
CLUSTER analyses. The chosen critical p-value was
again 0.05.
Fish and Habitat Surveys:
Permanent transects were set in each zone and
used for both fish and Uniform Point Contact (UPC)
surveys. These permanent transects were put in place
by Kenan Chan, who had utilized them for a
Figure 1 - Map of UPC/Fish transects used around the
STARESO harbor
This shows the “North”, “Harbor”, and “South” transects used in
the study. The permanent transects used to base sampling
transects on is outlined in red. The actual sampling
Page
transects
4 of 12
are
set in black.
different project. In the North and South zones, the permanent transects were laid parallel
to the shoreline whereas the Harbor’s permanent transect ran perpendicularly (Fig. 1). Data
for all three zones was collected every ten meters on transects perpendicular to the
permanent transects. Fish and UPC transect data were collected within a depth window of
2-17 meters. All transects ran for either a maximum length of 40 meters on each side from
the permanent transect or until the depth limits were reached.
UPC surveys were done using a 25-point quadrat every two meters along each
transect. The quadrat was placed along the transect and the substrate under each point
was recorded. Substrates were categorized into the following: P. oceanica, P. oceanica
matte, rock, and sand.
The fish surveys were designed very similar to the UPC portion of the study. The
same transects were used and divers recorded M. surmuletus individuals who were actively
foraging within 5 meters of the transect line. A foraging event was defined as any instance
where an individual was seen using its barbels to sift through any form of substrate or on
any surface. The same 25-point quadrat used in the UPC survey was placed at the location
of each foraging event and recorded.
Results:
Invertebrate Assemblages:
The results of the PERMANOVA analysis on the
invertebrate assemblages asserted that each one was
significantly different from one another (P=.001). However,
the pair-wise test performed on the three kinds of habitats
Table - 1
Groups
t
P(perm)
Sand, Matte 1.6841 0.091
Sand, Rock 7.5189 0.001
Matte, Rock 2.564 0.001
revealed that not all habitats were found to be significantly
different from one another. The sand and matte habitats
were not significantly different (P=0.091) (Table 1). The rock
habitat was found to be significantly different from both the
sand and matte habitats (P=0.001) (Table 1).
The SIMPER analysis was run on each habitat to
Difference between Habitats
Table 1, created from results of a PairWise test, shows the overall difference between
habitats and how statistically different they are. This
test takes into account all the invertebrate groups
used in our study. Comparing those groups, the
“Sand” and “Matte” habitats were found to be the
same, with a p-value of 0.091. However, the “Rock”
habitat is shown to be different from the other two
habitats with a p-value of 0.001. For a more
comprehensive analysis of how the habitats differ
from one another, see Table 2.
quantify the relative difference of invertebrate composition
between habitats (Table 2). The values given by the analysis
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show the percent chance of any given group of invertebrates being found in a sample of a
specific substrate.
Stomach Content Analysis:
Stomach content data run through a PERMANOVA analysis showed that the
composition of invertebrate species in M. surmuletus stomachs and each habitat was
Table - 2
Invertebrate Group Sand Group Matte Group Rock
Amphipod
0.16
0.13
0.77
Worm
0.66
0.25
0.08
Gastropod
1
1
0.75
Isopod
0.02
0.13
0.33
Bivalve
0.09
0.13
0.15
Average Abundances of Invertebrates between Habitats
Table 2 shows probability of a sample from the
given habitat containing a certain invertebrate group. This is
an expansion of Table 1, explaining how the habitats vary by
invertebrate group. This table was created by using a
SIMPER test on the sediment and tuffie data from Table 1
that “Rock” has a different invertebrate composition from both
“Sand” and “Matte” which are both similar to each other.
significantly different. With only 3 categories of
invertebrates used in this analysis, the
PERMANOVA test produced new results
concerning the difference between matte and
sand habitats, now stating that they are
significantly different (P= 0.01).
A CLUSTER analysis was created to show
the different calculated p-values for
determining whether the stomach contents
were significantly different from the habitat
samples. (Fig. 2).
Figure 2 - CLUSTER Analysis with PERMANOVA Results
This shows the differences between habitats alongside the results of a PERMANOVA analysis. Sand and Matte are
different habitats with a p-value of 0.01. The habitat “Rock” varies from those two by a p-value of 0.01 and the Fish
category differs from all three with a p-value of 0.01. All four categories are significantly different from one another.
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UPC and Fish Surveys:
A striking contrast was
found between the expected
foraging (produced by the
UPC surveys) and the
observed foraging (produced
by fish transects). We found
that M. surmuletus
preferentially foraged in the
sand, matte and rock habitats
Figure 3 - Bar Plot of Expected Substrate vs Foraged substrate.
This presents two pieces of information. On the y-axis is Percent Coverage, calculated from
total UPC Points. Blue bars represent the expected preference for foraging habitat and the red
bars represent the observed preferences for foraging habitat. Posidonia is largely avoided,
whereas the categories Matte, Rock, and Sand are foraged disproportionately to the amount of
each habitats actual coverage.
while completely avoiding
foraging in P. oceanica (Fig.
3). The chi-square analysis
revealed that the differences
in observed and expected values were extremely significant in every zone
(P<0.0001)(Table 3). In order to avoid any bias caused by any one category of substrate,
the chi-square analysis was repeated with different substrates removed from the equation.
All subsequent tests continued to substantiate the data (P<0.0001), showing that no one
substrate produced influential bias (Table 3).
The bar plot constructed from UPC and fish survey data revealed differences in foraging
Categories
X2
Degrees of Freedom
P-Value
All Categories
2889.703172
3
<0.00001
Posidonia Removed
2513.739285
2
<0.00001
Rock Removed
2785.901903
2
<0.00001
Sand Removed
861.7334141
2
<0.00001
Matte Removed
2409.938016
2
<0.00001
Table 3 Chi-Square Analysis
The table above shows the results of the chi-square analysis done in order to establish the significance of the data
presented in Fig. 2. Initial data was shown to be significant when analyzed with a critical p-value of 0.05. As a
precaution, certain categories were removed to eliminate bias, although resulting p-values were still well within the
range of the critical p-value.
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habits when broken down by location (Fig. 4). In the south where sandy habitat was not
available, M. surmuletus avoided not just P. oceanica but also the matte habitats, foraging
solely in rocky habitats. Both the north and harbor areas showed patterns similar to those
seen in the original bar plot (Fig 3), implying that the differences observed in the South are
due to the lack of sandy habitats. These results were all found to be significant when tested
by chi-square analysis (P<0.0001).
Figure 4 - Observed vs. Expected Foraging by Location
This is a breakdown of Fig. 2 by locations across STARESO. There are
clear differences between habitats; the “Matte” habitat is ignored by M.
surmuletus in the South while the “Rock” habitat is more preferred than in
other locations. Furthermore, there is no sand available for foraging in the
South. All habitats were found to have a p-value of <0.0001
Figure 5 - Bar Plot of Invertebrate Assemblages between Habitats
and Fish
This shows the differences between habitats and fish through use of a
bar plot. The bar plot expands on the data from Fig. 3 by showing how
exactly each category is different from the others. The Fish and Rock
categories had the most amphipods white Fish and Sand had the most
Worms. All three habitats had a significantly higher amount of
gastropods found within them that was found in the Fish category. This
analysis includes only the following invertebrate species categories;
Amphipods, Gastropods and Worms.
Discussion:
The invertebrate composition of rocky substrate exhibited significant differences
from all other substrate types, likely due to fundamental characteristics. Although there was
not an initial significant difference between the invertebrate composition between sand and
matte, they became significant once certain invertebrate species were excluded from the
data (Table 1 and Fig. 2). The two species of invertebrates that had the greatest variance
across substrates were amphipods and worms. Amphipods were found in higher numbers
in rocky areas covered in turf when compared to sandy or matted areas (Fig. 5). Worms
exhibited the opposite pattern of distribution and were abundant in sand and relatively rare
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in rock. This supports our first general hypothesis that there is variability in invertebrate
species composition between the different habitats.
This is interesting because virtually all M. surmuletus stomach content sampled
within this study contained amphipods, with worms being found in about 75% of the
samples (Fig 5). Based on this information we reject our hypothesis that M. surmuletus’ diet
is determined solely by prey availability. Past studies on M. surmuletus diet found a similar
abundance of amphipods and worms that agree with our general findings (Labropoulou
1997).
If M. surmuletus are true generalists, we do not expect to see any preference
between rock and sand. Our results from our UPC and fish surveys reject this hypothesis,
showing that M. surmuletus does exhibit a preference towards sand when foraging (Fig. 3).
We also observed that the foraging of M. surmuletus varied considerably between the
different locations sampled. Our UPC data implies that this difference is mainly due to a
considerable amount of variability in substrate coverage between locations (Fig. 4). In the
south where there was no sandy habitat available, M. surmuletus spent 100% of observed
time foraging on rocky substrate. This may imply that out of the three habitats, rock is a
secondary choice and sandy substrates are the preferred habitat for foraging. Due to the
preferential foraging behavior upon sand habitats, we hypothesized that M. surmuletus’ diet
would contain higher percentages of sand based invertebrates such as worms. Instead, our
data revealed that in a stomach sample, the likelihood of finding an amphipod is higher
than finding a worm (Fig. 5).
The difference in probabilities for amphipods and worms is a direct contradiction to our
conclusion that M. surmuletus prefers to forage for worms in sandy habitats. This supports
previous papers that argue M. surmuletus is a general forager (Gosline 1985). However,
there is the possibility of our stomach contents being biased; we believe that there may be
a difference in the decomposition times of different prey items. Worms that are soft and
fleshy would most likely have a smaller time frame for decomposition than amphipods that
have a chitinous shell. Stomach contents might disproportionately show a higher number of
amphipods regardless of whether or not a goatfish had been primarily foraging on worms.
It has been suggested that M. surmuletus may exhibit site fidelity (McFarland, 2014),
and this could be another source of bias introduced to our study. Depending on the size of
the home range, an individual may be limited to an area composed of only a single habitat.
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Any site fidelity could cause an overrepresentation of a non-preferred habitat type that
would be reflected in the diet of the individual.
Ultimately, we accept our general hypotheses that prey composition varies among
different habitats and M. surmuletus shows a preference towards specific habitats.
However, we reject our general hypothesis that the diet of M. surmuletus would reflect the
invertebrate composition of it’s prefered habitat. Instead, we found that M. surmuletus
displays some level of specialist behavior, with a preference for worms and amphipods.
Given the possibility of bias in our study, we recommend a more comprehensive
stomach content analysis, along with a paired study on site fidelity. We believe this is
essential in order to gain a better understanding of M. surmuletus’ prey preference and
foraging patterns.
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