Distributions of two sea urchins, Paracentrotus lividus and Arbacia lixula, and their
habitat associations in the northwestern Mediterranean Sea at STARESO, Corsica,
France
T. McHugh and K. Elsmore
Department of Ecology and Evolutionary Biology, University of California, Santa Cruz
2012
ABSTRACT
Understanding the population structure of individual species within a community
allows us to make predictions about the dynamics and the future health of an ecosystem.
Studies on Paracentrotus lividus and Arbacia lixula conducted in the northwestern
Mediterranean conflict in regards to diet, habitat occupation, and species interactions,
leaving the questions of habitat associations unresolved. In this study, we provide an
accurate and thorough assessment of Paracentrotus lividus and Arbacia lixula
distributions and habitat associations for the fall season at STARESO, Corsica, France.
We found statistically significant variations between the urchin species in density, spatial
location, depth, substrate preference, and primary placeholder preference. Understanding
the changes in the community surrounding the urchins is equally important, as it will
show the effects of fluctuations in urchin abundance and distributions.
INTRODUCTION
A clear understanding ecological community structure is important when
addressing interactions within an ecosystem. A community is bound together by the
network of influences that species have on one another. Understanding the population
structure of individual species within a community allows us to make predictions about
the dynamics and the future health of an ecosystem. Habitats within the northwestern
Mediterranean are especially vulnerable to degradation due to tourism, global warming,
and seafood collection (Chiantore et al., 2007). The niche theory generates a series of
questions relevant to the distributions of a species, their habitat preferences, and how
competition, predator presence, and resource partitioning influence their physical location
within a system (Tilman et al., 2004). Comparing a set of species' fundamental niches to
their realized niches and investigating the comparisons of available habitat to species
distributions constitute potential reasons why a species flourishes and exceeds in a
particular habitat (Tilman et al., 2004).
Ecologists have studied the cascading effects of sea urchins upon ecosystem
dynamics in various ecological systems (Mills et al., 1993). The classic example of
trophic cascades in kelp forests demonstrates the key role urchins play in a vegetative
community. The removal of sea otters, a keystone predator, allows for urchins to
overgraze the kelp, creating urchin barrens (Verlaque and Nedelec, 1983, Verlaque
1987). These barrens are poor in biodiversity and ecosystem functions, which highlights
the importance in understanding urchin densities and distributions (Privitera et al., 2011).
Two species of urchins, Paracentrotus lividus and Arbacia lixula, dominate the
near shore habitat of the Northwestern Mediterranean. Paracentrotus lividus, the purple
urchin, and A. lixula, the black urchin, coexist on hard substrate in shallow subtidal
habitats (Bulleri et al., 1999). Studies have found that A. lixula is commonly found on
vertical substrate and is considered a main grazer of coralline algae (Bulleri et al., 1999).
Paracentrotus lividus is typically found in dense algal assemblages, rocky crevices, and
under boulders (Tomas et al., 2004), grazing primarily on erect algae. Studies on P.
lividus and A. lixula conducted in the Northwestern Mediterranean, however, conflict in
regards to diet, habitat occupation, and species interactions, leaving the questions of
habitat associations unresolved.
This study investigated the fundamental niche, potential habitat, and places where
the two urchins can live, and compared it to the realized niche of the two urchin species.
We examined habitat associations of P. lividus and A. lixula in the Northwestern
Mediterranean in a nearshore habitat. Spatially accurate distributions and abundances of
each species were collected to address the question of habitat associations and niche
theory. Due to the variety in physical and biological habitat structure, STARESO harbor
provided a good study system to address all habitat attributes discussed in the conflicting
literature. In this study, we tested the hypotheses that two urchin species; Paracentrotus
lividus and Arbacia lixula:
(1) occupy distinct spatial locations within STARESO harbor
(2) occupy distinct depth ranges
(3) have specific substrate associations
(4) have specific primary placeholder associations.
METHODS
Study System
This study was conducted in October 2012 at Station Research Sous-Marine et
Oceanographique (STARESO), Point Revellata, Calvi, France. Due to the variety of
substrate types and dense algal cover, STARESO harbor provided an ideal study system
for understanding the spatial distributions of P. lividus and A. lixula. The diversity of
primary placeholders and substrate, in STARESO harbor is extremely diverse in
proportion to the small size of the study site. Substrates included sand, cobble, boulders,
bedrock, large cement jacks, and cement vertical walls. The biotic system was composed
of a wide collection/composition of algal and invertebrate species.
Sampling Design
Sampling was done entirely by SCUBA. A permanent transect line was set
through the center of the harbor, with flagging tape set every 5 meters from 0m to 50 m.
The line ran 150 degrees “east” from the permanent ladder in STARESO harbor. Eleven
transects were run perpendicular to the main line. Total lengths varied per transect due to
the shape of the harbor. Lengths ranged from 41m to 76m. To simplify sampling
methods, the harbor was then separated into two distinctive regions; (+) 60 degrees and () 240 degrees from the main line (Fig. 1). A meter tape was reeled out along the bottom,
along the substrate, until surfacing, or a physical barrier prevented the extension of the
tape.
Habitat Data Collection
We characterized depth, substrate, and primary placeholders in STARESO harbor
using uniform point contact (UPC) methods. For each of the eleven transects, we reeled
out a meter tape flush along the bottom, following the contour until reaching the water
line. The transect lengths were determined by the width of the harbor. We sampled
every other meter along each transect, using 0.68m x 0.68m quadrats. Each quadrat
contained 9 equidistant points, at which we recorded substrate and primary placeholders.
Using an Aeris XR1 dive computer, we collected depth readings for every meter per
transect. Depths were recorded and analyzed in feet to display a more drastic and
tangible depiction of the distribution of urchins and bathymetry of the harbor. All other
distance measurements will be referred to in meters. STARESO staff members identified
five substrates and sixteen primary placeholders as the main biotic and abiotic features of
the harbor worth assessing and quantifying for habitat characterization. Substrates and
primary placeholder categories included bedrock, boulder, cobble, sand, cement, jacks,
bushy, turf, film, encrusting algae, living Posidonia oceanica, dead Posidonia oceanica,
colonial tunicates, solitary tunicates, bryozoans, octopus dens, polychaetes, black
sponges, red sponges, hard coral, and anemones.
Urchin Data Collection
We used the swath method to measure urchin density and distribution along the
eleven transects in STARESO harbor and the UPC method to characterize their substrate
and habitat associations. Urchin data collection was restricted to the hours of 20:00:00 23:00:00 to account for the nocturnal feeding displayed by both urchin species (Guidetti,
2004). We swam along each transect, looking for both P. lividus and A. lixula. Surveys
were restricted to the width of the quadrat (0.68 meters) and the west side of the meter
tape. Upon finding an urchin, we placed the quadrat on the closest meter mark.
Substrate and primary placeholder data was collected for each of the 8 point surrounding
the urchin, in addition to the substrate and primary placeholder beneath the urchin.
Species, depth, and coordinates were recorded for each urchin sampled.
Analysis
To determine if the spatial location of A. lixula and P. lividus differ, recorded
depths were used to create a bathymetric map of the STARESO harbor in SYSTAT and
SURFER programs. Paracentrotus lividus and A. lixula depths and exact locations were
added to the habitat map to display their specific distributions within STARESO harbor.
To determine if the depth ranges in which A. lixula and P. lividus inhabit differ, analysis
of variance (ANOVA), followed by pairwise comparisons, were done to compare urchin
distributions as a function of depth. An analysis of similarities (ANOSIM) was run to
determine if substrate associations differ between the two urchin species. A similarity
percentages (SIMPER) analysis was then used to determine the driving factors of
substrate association differences. ANOSIM analyses were run to determine if primary
placeholders associations differ between the two urchin species. SIMPER analyses were
used to determine the driving factors of primary placeholders association differences.
RESULTS
According to our harbor map (Fig. 2, Fig. 4), P. lividus and A. lixula were found
within distinct geographic locations. Paracentrotus lividus occupied a uniform region,
gradually sloping with the contours of the seafloor. The abundance of P. lividus exceeded
that of A. lixula within the STARESO harbor (Fig. 4). Arbacia lixula individuals were
pressed along the shallower outer edges of the cove, towards the zero depth mark (Fig. 2).
An ANOVA analysis, followed by pairwise comparisons, indicates all
comparisons of available depths and actual depths on which urchins were found to be
highly significant (Table 1). Confirming our harbor map, A. lixula occupied an average
depth of 7.2 feet (Table 2, Fig. 3). Alternatively P. lividus inhabited an average depth of
10.6 feet (Table 2, Fig. 3). Arbacia lixula populated a depth range higher in the water
column and at a steeper depth gradient than that of P. lividus (Fig. 4).
The p-values yielded from the substrate PERMANOVA analysis indicate that
there are significant differences between each of the pairwise comparisons (Table 3).
Boulder and cobble are the major components responsible for the statistical difference
between available substrate and the substrate P. lividus inhabits (Table 4a). Boulders and
cement are the major components responsible for the statistical difference between
available substrate and the substrate A. lixula inhabits (Table 4b). Boulders cement, and
cobble are the major components responsible for the statistical difference between the
substrate P. lividus inhabits and the substrate A. lixula inhabits (Table 4c).
The p-values yielded from the primary placeholder PERMANOVA analysis
indicate that there are significant differences between each of the pairwise comparisons
(Table 5). Bushy algae, turf algae and encrusting algae are the major components
responsible for the statistical difference between available primary placeholders and those
associated with P. lividus (Table 6a). Bushy algae, film, and encrusting algae are the
major components responsible for the statistical difference between available primary
placeholders and those associated with A. lixula (Table 6b). Bushy algae, film, and
encrusting algae are the major components responsible for the statistical difference
between primary placeholders associated with P. lividus and A. lixula, respectively (Table
6c).
DISCUSSION
Our graphical depiction of the urchins in STARESO harbor indicates that both
species of urchins occupy the perimeters of the north and south edges of the harbor.
Urchins were absent from the harbor’s central sand and P. oceanica channel. This
implies that the deeper, flat channels of the harbor are not ideal conditions for the
urchins, contrary to what some literature states (Kempf, 1962; Regis, 1978). Our results
provide support for the idea that morpho-functional features such as attachment tenacity,
spine length, and test robustness of sea urchins could be involved in affecting their
distributions (Guidetti & Mori, 2005). Support for this hypothesis, spatial locations of A.
lixula and P. lividus differ, was the motivation for looking at possible mechanisms of
habitat occupation.
One probable mechanism driving the difference in habitat occupation between the
two species is depth. Arbacia lixula dominates the shallower regions of the harbor at an
average depth of 7.2 feet, while P. lividus is found in deeper regions at an average depth
of 10.6 feet. One possible mechanism could be due to wave action exposure. Organisms
found at shallower depths are more exposed to wave action and stresses from water
movement. Hydrodynamics appear to play a key role in affecting the distribution across
depths in several species of sea urchins (Ebert, 1968; Littler, 1980; Monteiro Marques,
1982; Denny and Gaylord, 1996). Despite being subject to dislodgement by high
magnitude waves, A. lixula is found most commonly on vertical walls at shallower depths
(Kempf, 1962; Regis, 1978). Morphological studies of A. lixula have concluded that
strength and arrangement of calcareous plate connections composing the test increase
tolerance to physical stresses caused by wave action (Regis 1978; Chelazzi et al., 1997).
Alternatively, P. lividus shows a distinct behavioral adaptation to wave action, by
preferring deeper waters and occupying crevices and self-burrowed refuges (Chelazzi et
al., 1997).
Deeper waters also provide refuge from seasonal, annual, and storm-related water
condition changes (Fernandez et al., 2001). Urchins are generally considered to be
stenohaline organisms, unable to tolerate fluctuations in salinity (Roller and Stickle,
1993). Bressan et al. (1995) suggests that the distribution of P. lividus may be due to the
water quality tolerances of adults. Urchins found at shallower depths are more
vulnerable to salinity decreases (Fernandes et al., 2001), suggesting that A. lixula may be
more robust in tolerating salinity and temperature fluctuations.
Another possible mechanism driving the difference in habitat occupation is
substrate. The substrate preference of an urchin influences its ability to hide from
predators, forage, and maintain homeostasis. Morphological limitations may be another
factor in substrate choice. Test robustness and attachment tenacity were significantly
greater for A. lixula than those for P. lividus, and the difference decreased in relation to
smaller sea urchin size. These morphological adaptations and limitations confine the two
urchin species to exploit two very contrasting substrates within the STARESO harbor.
The abundance of P. lividus found on boulders is more than double what would
be expected, given the available boulder habitat (Table 4a). Due to the morphological
constraints and predator defense weakness of P. lividus, boulders provide large stable
surface area on which to attach, as well as crevasses to hide from predators (Guidetti and
Mori, 2005). Boulders maintain a surface area to provide sufficient lighting for algae to
grow. Additionally, A. lixula were found in high quantities within the boulder substrate
(Table 4b). The size and orientation of boulders provide the vertical landscape and refuge
that A. lixula seek (Kempf, 1962; Regis, 1978).
Despite the abundance of cobble in the harbor, this substrate contained fewer
urchins than expected (Table 4). Contrasting boulders, cobble provides less surface area
to hang onto, which is a stress for P. lividus. As previously stated, P. lividus attachment
tenacity is extremely weak, and individuals can be dislodged easily when force is applied.
Cobble within the harbor was found in extremely shallow depths and can move around
during rapid water flow (Guidetti and Mori, 2005). Additionally, the small surface area,
and shallow depth does not sustain the algae to which P. lividus individuals have been
known to graze on (Chiantore et al., 2008). Although A. lixula is morphologically more
adept at clinging onto a substrate with more force, they were not found on cobble in high
abundances. The minimum amount of food and horizontal orientation that cobble
provides may be the limiting factor that restricts A. lixula from this habitat.
Previous studies within the Northwestern Mediterranean have associated P.
lividus with patches of P. oceanica (Thomas et al., 2004). Contrary to these results, our
studies did not record any P. lividus or A. lixula individuals in P. oceanica meadows,
which were located within the sand substrate (Table 4a, 4b). Sand does not support the
food types commonly consumed by either species in STARESO harbor, nor does it
provide protection. In comparison to sand, boulders are a more appealing and viable
substrate providing the protection and food P. lividus needs to maximize growth.
Historically, there is a strong association between A. lixula, and anthropogenically
created cement walls (Sala et al., 1998). Our studies found that A. lixula was found on
cement over three times as often as what we expected (Table 4b). The solid, vertical
orientation of cement walls provides the perfect substrate on which A. lixula to cling
onto. Their strong spines and their attachment tenacity allow the urchin to be exposed
without risk of predation or removal. The algal assemblage on cement walls was diverse,
consisting of erect, film, and encrusting algae, which are ideal food types for A. lixula
(Privitera et al., 2008). When comparing P. lividus to A. lixula, there were zero P. lividus
individuals found on cement substrates (Table 4c). The exposure to predators and their
weak attachment strength may limit their ability to utilize this area. Each of the
substrates harbors different types of food, refuge, and attachment surfaces. The
characteristics of STARESO’s substrates limit P. lividus and A. lixula to inhabit these
areas based on their morphological and physiological constraints.
Another possible mechanism driving the difference in habitat occupation is
primary placeholders. When looking at P. lividus, it was found in association with bushy
algae nearly twice as often as what we would have expected, based on amounts available
in the habitat (Table 6a). The most plausible reason is that bushy algae is their preferred
food source. Studies on diet have confirmed that P. lividus primarily consumes erect
algae such as Dictyotales and Padina (Chiantore et al., 2008, Privitera et al., 2011), which
are algae that collectively compose our bushy algae category. Another possible reason
for this is because bushy algae is found most commonly on their preferred substrate,
boulders, which provides shelter essential for survival, as discussed above. Turf algae
was found associated with P. lividus far less that what we had expected (Table 6a). The
only factor distinguishing bushy and turf algae is their height from the substrate, so we
predicted that P. lividus would be consuming both bushy and turf algae. Perhaps due to
the abundance of erect algae available in STARESO harbor, P. lividus was able to
demonstrate a preference toward the larger, bushy algae. Paracentrotus lividus was
found in association with encrusting algae almost twice as often as we expected (Table
6a). While encrusting algae could be a food source for P. lividus, literature more strongly
suggests that encrusting algae provides a better attachment surface for refuge than other
algae (Guidetti and Mori, 2005; Barrios et al., 2010). Most of the encrusting algae was
found in the crevices (where P. lividus resides for protection from predators) as bushy
and turf algae dominated the completely exposed surface areas (personal observation).
We found that A. lixula was less commonly associated with bushy algae than we
would have expected (Table 6b). This could be due to the fact that bushy algae is not
found as commonly on their preferred substrate, cement, or as commonly at the depths in
which they are found. While there is little dispute about P. lividus’ diet, studies have yet
to confirm A. lixula’s preferred diet. This is attributed to the differences in resource
availability across study sites. In our particular study site, bushy, turf algae, and P.
oceanica were the dominant primary placeholders (Fig. 5). Our sample design and data
set would not be sufficient to address diet preference of urchins at STARESO, however,
substrate and primary placeholder associations we found suggest that erect algae may not
be their primary food source.
Arbacia lixula was found in association with film ten times more than expected,
perhaps because film is found in high abundances on their preferred substrate (Table 6b).
Arbacia lixula was found in association with encrusting algae almost twice as often as
we expected (Table 6b). It is possible that encrusting algae is a food source for A. lixula
(Bulleri et al., 1999; Privitera et al., 2008), however, literature also suggests that
encrusting algae provides a strong attachment surface for refuge than other alga (Guidetti
and Mori, 2005; Barrios et al., 2010). Aside from being a food source or attachment
surface, it is possible that encrusting algae is merely what is left behind after grazing
bushy or turf algae.
Our comparison of habitat associations between P. lividus and A. lixula yielded
some compelling results. Paracentrotus lividus was found with bushy algae more than
twice as often as A. lixula (Table 6c). We think this may be mostly due to bushy algae
being P. lividus’ food source (Privitera et al., 2008). Film had no association with P.
lividus whatsoever, which is what we would expect, as P. lividus was not found on the
cement wall’s vertical surfaces, on which film was found (Table 5c, 6a). Encrusting
algae had a greater association with A. lixula than P. lividus, and we attribute this to
either being a food source, or an attachment surface. The encrusting algae was found on
cement wall and hidden surfaces, such as the layers below the boulders. Further
investigation of this association is necessary to address reasons for the association.
CONCLUSION
On the surface, it appears as though STARESO harbor could be on the verge of a
stable system shift from lush algal assemblages to urchin barrens. Due to the apparent
abundance of food and shelter STARESO’s harbor supports, we suspect that there is
another mechanism inhibiting the two urchin species from dominating the available
habitat (their fundamental niche). Additional studies should concentrate on abiotic
factors that may be inhibiting the proliferation of these urchins in this system. Results
from this baseline study should be used, in addition to results from future repeated
studies, to properly address the questions of habitat associations at STARESO harbor. In
this study, we hoped to provide an accurate and thorough assessment of Paracentrotus
lividus and Arbacia lixula distributions and habitat associations for the fall season at
STARESO. It is important for future studies to examine the effects of annual and
temporal changes of distributions. Understanding the changes in the community
surrounding the urchins is equally important, as it will show the effects of fluctuations in
urchin abundance and distributions. Understanding the roles of P. lividus and A. lixula
within a community will allow us to make predictions about STARESO harbor’s
ecosystem dynamics.
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TABLES AND FIGURES