Investigation into the patchy coastal distribution of Chromis
chromis in Revellata Bay, Corsica
Astrid Leitner and Stephanie Nguyen
Abstract
Chromis chromis is one of the most important species in the Mediterranean rocky
littoral zone; it is not only the most abundant fish but also one of the few
planktivorous water column feeders. We found that this species forms large
aggregations in consistent areas, mainly over the transition zone where sloping
granite meets Posidonia oceanica meadows. We also showed that these fish
consistently school around the densest copepod aggregations available as predicted
by the optimal foraging theory. We then attempted to correlate daily copepod
fluctuations with the observation of these consistent plankton patches, but this
yielded only preliminary results that highlight the need for further exploration.
Introduction
The distribution of marine organisms is highly variable and is often influenced by
predator-prey interactions (Benoit-Bird 2009). Many organisms rely on schooling
and aggregated prey species for feeding (Benoit-Bird 2009). A vital aggregated prey
species in the marine environment are plankton. Recent advances have allowed us
to investigate feeding behavior in relation to phytoplankton by utilizing vertical
towing methods. This method, different from the standard horizontal tows, have
allowed for scientists to observe plankton distribution within the water column by
using nets that are capable of being towed vertically. This method has revealed that
phytoplankton form high-concentrated smaller aggregations that stretch
horizontally in the ocean called “thin layers” (Leising 2001). These “thin layers” also
contain organisms called zooplankton that exist in dynamic 3-dimensional
structures. These structures are organized in pancake-like stacks that are thought to
stimulate fish schooling (Benoit-Bird 2009). In addition to these natural
aggregations, feeding patterns of plankton that fluctuate daily also change their
positioning within the water column throughout the day (Noda et al. 1992). To
further investigate what encourages fish schooling, we chose to use the optimal
foraging theory, which states that predators aggregate in areas of high prey
densities (Krebs 1978).
Previous studies of the effects of plankton distribution on fish schooling
have been focused on larger scale patterns. The goal of our project was to test smallscale horizontal patchiness in zooplankton communities and the response of
planktivorous fish to this 3-dimensional patchiness. We focused our study on the
planktivorous fish Chromis chromis, the most common schooling fish in the
Mediterranean Sea (Bracciali et al 2012). The goals of this work were to: (1) observe
fish schooling behavior; (2) determine whether fish accumulation was a result of
plankton aggregation; (3) track diel fluctuations of copepod densities. The general
question we asked was: What factors influence the distribution of C. chromis
schools? The specific questions that were asked were: (1) Are there areas where C.
Chromis schools occur consistently? (2) Are these regions correlated to the densest
plankton aggregations? (3) How do plankton densities fluctuate over a 24 hour
cycle?
Methods
Study Site
This study was conducted at the Station de Recherches Sous-Marines et
Océanographiques (STARESO) located on the Mediterranean Sea near Calvi, France
during the month of October, 2012. All tows, surveys, and observations were made
at depths ranging from the surface to 15 m and within 400 m of the mouth of the
STARESO harbor with study sites both to the north and the south of the harbor. In
this region, granitic walls and boulders drop steeply into the water, transitioning
approximately 6 m in depth to flat substrate, mostly sand, covered by Posidonia
oceanica, a seagrass endemic to the Mediterranean Sea and very common in this
part of Corsica.
Figure-1: This figure shows the island of Corsica and our study site at STARESO on the northwest side of the
island. The last inlet shows our 9 survey transects and our larger study area.
Study Species
In a study near the Island of Ischia, Chromis chromis was the most abundant fish
species, comprising 38% of all fish collected (Zupo et al. 2010). In another area of
the Southern Adriatic Sea, Fasola et al. (1997) found C. chromis made up 52% of
observed fish species. The sheer abundance of the species, despite its small size,
makes C. chromis a key species in the coastal ecosystem of the western
Mediterranean Sea (Bracciali et al. 2012). C. chromis through the process of
consumption and excretion stimulate nutrient transport from the pelagic zone by
driving down the carbon cycle to the benthic system in the water column. This
nutrient export is the reason why C. chromis are important to the Mediterranean
ecosystem.
Reaching up to 25 cm in length, with an average length of 13cm, C. chromis
form large dense schools that exhibit diel feeding patterns (Bracciali et al. 2012,
Loris et al. 1990). Schools feed in the water column during daytime and resting at
night within the shelter of rocks. These patterns are variable and are affected by the
amount of light attenuation observed daily (Bracciali et al 2012).
School Distribution
In order to test the idea that schools were patchily distributed and that certain
locations supported consistent schools, a series of parallel 30 m fish transects were
run twice per day at specific times in three regions (1) the north side of the
STARESO harbor (2) the mouth of the harbor, and (3) the south side of the harbor.
All transects were conducted from a 90°N bearing in the late morning and late
afternoon. Late morning transects were run between 9 and 11AM, and late
afternoon transects were performed between 2-5PM. Presence or absence of fish
schools were marked along each meter, and a map of the school distribution was
developed for each time by measuring the length of the schools and estimating the
horizontal extent – the approximate area along the transect where the schools were
observed. The physical conditions and the vertical location of the patches within the
water column were also noted. If the average depth of the school was within 2m of
the bottom the school was considered over the bottom; any other school was
marked as within the water column. Patch area was calculated instead of school
density because the large number of individuals in each school was too big to
accurately estimate.
Plankton Tows
For our study we conducted phytoplankton tows at various depths with a 200micron phytoplankton net. All surveys were completed using SCUBA, swimming
either north or south of the harbor and searching for large, dense schools of feeding
planktivorous fish. A picture of every school was taken before sampling, and the
depth of the middle of the school was noted as well as the presence or absence of
other schooling species in the sampling and their depths. We would then run out a
weighted transect tape along the length of the fish school and tow through the
school for a minimum of 60m. The first tow would always be done directly through
the school. The net would then be twisted shut and brought to the surface where the
sample would be initially processed. This was done by removing the cot-end and
emptying the contents into a cleaned jar. The cot-end was then rinsed several times
with filtered seawater and emptied into the same sample jar. The cot-end was then
reattached onto the plankton net, twisted shut, and brought back down to the depth
of the school. Subsequent tows would then be conducted above, below, right, and/or
left depending on the positioning of the school relative to the geomorphology of the
sample area. Horizontal tows were always at least 5m from the edge of the school to
ensure no overlap. Tows above and below the school were only conducted if the
school was in water deep enough and the school was compressed enough to make it
possible to tow without overlap.
All samples were preserved in 2.5% formalin within two hours of sampling. The
samples were filtered down to less than 50 mL using the cod-end of the
phytoplankton net. For processing, the exact volume of the sample was determined
by pouring the filtered down vial into a graduated cylinder. Then two 1mL
subsamples were extracted from the homogenized samples. The zooplankton within
each subsample were counted under a dissecting microscope using broad
categories: copepods, mollusks, larva, amphipods, chaetognaths, and cladoceres.
Nauplii were counted as copepods. These large categories were chosen because the
goal of quantifying zooplankton was not to note compositional changes in the
plankton community but merely to quantify the concentration of prey items with
schools relative to surrounding water. The total number of zooplankton in each
sample was extrapolated from the average number of each category between the
two subsamples. This total was then divided by the total volume of water sampled
by the plankton tow (the area of the net opening multiplied by the total length of the
each tow).
Fluctuations in Prey Availability
To test the hypothesis that the consistently present schools take advantage of
a relatively permanent local concentration of copepods, we sampled one area two
hours after sunset, just before sunrise, and every three hours subsequently for 10
hours. We chose this region based on the results of our surveys, choosing one
transect based on a region of significantly higher than expected presence of C.
chromis schools and another transect 10 m offshore from the first in an area of
lower than expected presence of C. chromis. These samples were processed using an
identical methodology to the one described in the plankton tows section.
Statistical Analyses
In order to get a picture of the distribution of C. chromis schools, we first
found the overall probability of a school being at each meter mark within the grid.
We then ran a binomial probability analysis to determine what number of successes
is counted as a significant number of positive and negative deviations from the
overall expected probability of school presence. From this calculated value we
created a map of our sample area from expected, greater than expected, and less
than expected regions.
In order to test the hypothesis that the clearly defined vertical and horizontal
location and orientations of the C. chromis schools were associated with the densest
aggregations of prey items in the region as predicted by the optimal foraging theory,
we ran ANOVA tests on the plankton tows done within the schools, vertically
outside the schools, and horizontally outside the schools.
In order to get a picture of the distribution of C. chromis schools, we first
found the overall probability of a school being at each meter mark within the grid
(0.279). We then ran a binomial probability analysis to determine what number of
successes is counted as a significant number of positive and negative deviations
from the overall expected probability of school presence (0.556). From this
calculated value we created a map of our sample area from expected, greater than
expected, and less than expected regions.
Results
School Distribution
As shown in figures one and two, schools were generally more likely to be
found near the rocks and less likely to be found further offshore over the Posidonia
oceanica. Schools were consistent from 0 to 7 meters along each transect in our
sampled grid with the noteworthy exception at the 30°S transect. This transect was
slightly different than the others as it began at the Posidonia oceanica meadow
cobble interface instead of at the foot of the sloping granite. This occurred due to the
position of the transect at the mouth of a small bay lined on either side by granite
slopes (sampled by the 20°S and 40°S transects).
Another notable exception to the general pattern was a consistent school at the
offshore end of the furthest northern transect. There was an interesting feature on
the benthos at this point. Here there was a ledge approximately two meters in
height formed by disturbances to the Posidonia oceanica meadow.
Stability of Schools
30
Metermark
25
20
15
10
5
0
50
40
a)
30
20
10
0
-10
-20
-30
-40
-50
Transect (meters)
b)
Figure 2: a) On this chart .279 is the overall probability of encountering a school on our sampled
grid. The red meter marks represent those marks that have a significantly higher probability of
schools than the overall probability, and the blue meter marks highlight which regions have a
significantly lower probability of schools. b) This is a three dimensional visualization of the same
statistical data where red areas represent the highest probability of encountering a school and blue
areas represent the lowest probability. This image is oriented so that the observer is looking into
shore with the negative transects representing the southern transects and the positive ones
representing the northern transects. Meter mark 0 is closest to shore and meter mark 40 is furthest
offshore. The Y axis shows the probability of encountering a Chromis school.
Plankton Tows
We found that copepod densities were significantly higher within schools
than outside C. Chromis schools (see Fig 3a; p-value = 0.011). We also found that
copepod densities were highest within schools, slightly lower on average below
schools, lower to the side of schools, and lowest above schools (2588, 2083, 2245,
1138).
5,000
4,000
4,000
Copepod concentration
Copepod concentration
Copepod Densities
5,000
3,000
2,000
1,000
0
a)
In
3,000
2,000
1,000
0
Out
b)
Location (relative to school)
In
Side
above
below
Location (relative to school)
Type III Tests for Fixed Effects
Effect
Numerator df
Denominator df
F-Ratio
p-Value
Code
1
19
7.844
0.011
Figure 3: a) This chart shows the average densities of copepods per square meter
inside schools and outside schools with standard error bars. b) This chart shows a
more detailed view of copepod densities relative to school locations. The side
category is a combination of left and right tows.
Fluctuations in Prey Availability
During an exploratory one-day trial where five tows were conducted within a
24-hour period, we found a peak of copepod.
3500
1.2
3000
1
2500
0.8
2000
0.6
1500
0.4
Copepod
Numbers
1000
Chromis Presence
Copepods per square meter
Diel Chromis and Copepod Patterns
0.2
500
Chromis
Abundance
0
21:30
7:30
11:30
Time of Day
2:30
0
5:30
Figure 4: This graph shows the average number of copepods per square meter
during each
Discussion
School Distribution
We found consistent schools of C. chromis day after day hugging the
geomorphology of the coastline and much less stable aggregations out in mid-water
over the Posidonia oceanica meadows. We believed this could have important
implications for the nutrient flux supporting the diverse benthic assemblages that
exist under regions of the most consistent schools of C. chromis. C. chromis were
found to school consistently over the rock-meadow interface feeding on copepods
and excreting nitrogen, phosphorous, and carbon (Pinnegar et al. 2007). Pinnegar et
al. found that via respiration, excretion, and feces, one 10.25 g C. chromis releases
37.2 mg/day carbon, 8.89 mg/day nitrogen, and 1.7 mg/day of phosphorous (2007).
Therefore large aggregations of C. chromis can drastically change nutrient levels
down current of their consistent schooling locations. In fact schools of the closely
related planktivorous damselfish C. punctipinnis have been shown to consistently
increase ammonium levels down stream of their aggregations (Bray 1986).
Ammonium is crucial to the growth many primary producers such as
macroalgae[AL1] . Moreover, many Mediterranean phytoplankton are phosphorous
limited making the phosphorous excreted by these schools even more important to
the base of the food web (Pinnegar 2007[AL2] ). Additionally, due to their diel
feeding pattern, C. chromis also bring nutrients back to their nighttime shelters
within the rocks (Pinnegar 2007). These shelter areas can house 5-10 individuals
per square meter (Pinnegar 2007). The elevated nutrients here could serve to
support the diverse invertebrate and algae communities that exist on the underside
of these boulders and rocks[AL3] (Beltran et al in prep). As the most abundant fish
in terms of both number and biomass in the Posidonia system, the nutrient fluxes
induced by C. chromis schools could be crucial to the benthic communities thriving
under consistent schooling locations (Pinnegar et al 2005, 2007; Bracciali et al.
2012).
Plankton Tows
Copepod densities were found to be significantly higher within C. chromis
aggregations than outside the schools as predicted by the optimal foraging theory
which maintains that predators will forage longer on denser prey patches to
maximize energy intake. It is interesting to subsequently consider why there are
consistent copepod aggregations in these areas in the water column over the
rock/meadow interface. We attempted to test whether water motion set up a sort of
entrapping eddy that focused the zooplankton there; however, when we attempted
to measure the current with a handheld flow-meter the water motion was too slight
to detect anywhere along our 30 m transect (30m directly offshore starting from the
rock edge). Even when attempting to qualitatively observe water motion by
releasing dyes into the water column, no directional flow was detectable. While the
plankton aggregation could still be maintained by the physical processes occurring
at the water’s edge, it may also be maintained by biological processes. The C.
chromis schools excrete nutrients into the water, including phosphorous, an
important limiting nutrient for the region’s phytoplankton (Pinnegar et al. 2007).
This could cause very small scale phytoplankton blooms in precisely the areas that
C. chromis aggregate around to feed. This in turn would result in copepods
maintaining their position in these regions as well, perpetuating the local consistent
C. chromis aggregations. This hypothesis is purely speculation derived from our
observations and the energy budget analysis done by Pinnegar et al. in the same
region; it would be an interesting future project to consider.
Another added benefit that C. chromis derive from feeding above the interface zone
is proximity to shelter. Almost daily during our school surveys we observed pairs of
hunting jack species (Serioli lalandi) swimming through the C. chromis schools. The
C. chromis responded by swimming down toward the boulders for shelter. In fact,
one group of jacks could make an entire school disappear momentarily into the
rocks only a few meters away emerging seconds to minutes later to reclaim their
previous feeding position. Schools over Posidonia oceanica meadows seemed to
have a much longer response time, often needing to swim five meters or more to
hide on the benthos within the seagrass and taking longer to regroup afterwards.
Again this needs to be examined further and tested empirically.
Fluctuations in Prey Availability
Our results showed that C. chromis presence did not mirror copepod densities
as expected. In fact they appear be directly opposite. However, it was to be expected
that there were no copepods during the night tow or the early morning tow because
of the diel feeding pattern of the C. chromis despite the high density of copepods
during this time. The peak density of C. chromis actually corresponded to the lowest
copepod density however, because this density was less than half of all other
densities recorded at that time of day (collected during the daily tows), we believe
that this is not an accurate view of copepod densities for this time of day. This could
be confirmed if weather had allowed for multiple sampling days for this question.
The highest copepod density in this location occurred at 2:30 in the afternoon, a
time period where many schools of C. chromis had been observed previously. Again
the lower C. chromis presence here is most likely an artifact of our insufficient
sample size. Pinnegar et al reports a general behavior of zooplankton in the bay of
Calvi where plankton rise to the surface at dusk and remain in the surface waters
until dawn where they sink to their day depth; however, this behavior may not
apply to the shallow coastal system we are working in.
Conclusion
C. chromis are the most abundant fish in the Posidonia oceanica community.
During daylight hours they form large schools that feed on dense copepod
aggregations influencing the nutrient levels in these localized regions as well as the
nutrient levels in their night-time resting places. We found schools consistently
aggregated over the interface between the Posidonia oceanica meadows and the
rocky slope. This may be due to food availability as well as proximity to shelter.
Copepod densities were significantly higher within schools than outside of schools.
This could be due to entrapment and retention of plankton in this region by physical
processes or maintained by biological processes. C. chromis presence did not mirror
copepod densities as expected but this may be an artifact of limited sample size.
Many questions and hypotheses remain to be examined, as this species is crucial to
the trophic web in this system.
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