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ORIGINAL ARTICLE
Habitat modification in tidepools by bioeroding sea urchins
and implications for fine-scale community structure
Timothy M. Davidson
1,
* & Benjamin M. Grupe
2
1 Environmental Science and Management, Portland State University (ESM), Portland, OR, USA
2 Center for Marine Biodiversity and Conservation, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA, USA
Keywords
Biological disturbance; community structure;
ecosystem engineering; intertidal ecology;
microhabitat; Strongylocentrotus purpuratus;
tidepool.
Correspondence
Timothy M. Davidson, Environmental Science
and Management, Portland State University
(ESM), PO Box 751, Portland, OR 97207,
USA.
E-mail: DavidsonT@si.edu
*Current address: Smithsonian Tropical
Research Institute, Apartado Postal 0843-
03092, Balboa, Ancon, Republic of Panama.
Both authors contributed equally to this
manuscript.
Accepted: 22 November 2013
doi: 10.1111/maec.12134
Abstract
By creating novel habitats, habitat-modifying species can alter patterns of
diversity and abundance in marine communities. Many sea urchins are impor-
tant habitat modifiers in tropical and temperate systems. By eroding rocky sub-
strata, urchins can create a mosaic of urchin-sized cavities or pits separated by
exposed, often flat surfaces. These microhabitats appear to harbor distinct
assemblages of species. We investigated how a temperate rocky intertidal com-
munity uses three small-scale (<100 cm
2
) microhabitats created by or adjacent
to populations of the purple sea urchin (Strongylocentrotus purpuratus): pits
occupied by urchins, unoccupied pits, and adjacent flat spaces. In tidepools,
flat spaces harbored the highest percent cover of algae and sessile fauna, fol-
lowed by empty pits and then occupied pits. The Shannon diversity and rich-
ness of these sessile taxa were significantly higher in flat spaces and empty pits
than in occupied pits. The composition of these primary space holders in the
microhabitats also varied. Unlike primary space holders, mobile fauna exhib-
ited higher diversity and richness in empty pits than in flat spaces and occu-
pied pits, although results were not significant. The protective empty pit
microhabitat harbored the highest densities of most trophic functional groups.
Herbivores, however, were densest in flat spaces, concordant with high algal
coverage. These results suggest the habitats created by S. purpuratus in addition
to its biological activities alter community structure at spatial scales finer than
those typically considered for sea urchins.
Introduction
By modifying or creating habitats, marine organisms can
alter the structure of marine ecosystems and communi-
ties. Many foundation species, such as oysters or kelp,
increase habitat complexity and heterogeneity through
their physical presence, thereby contributing to increased
local species abundances and biodiversity. In contrast,
other organisms modify physical heterogeneity through
their activities instead of their biogenic structure. For
example, piddocks (Pholadidae) create boreholes in inter-
tidal rock, thus enhancing topographic complexity and
hosting numerous species (Pinn et al. 2008). Similarly,
boreholes created by burrowing isopods in sandstone har-
bor a diverse assemblage compared with the adjacent flat
sandstone (Davidson et al. 2010). Ecologists tend to
emphasize the role of sea urchins as dominant grazers
capable of exerting top-down control on macroalgal com-
munities, thereby affecting habitat heterogeneity (e.g. kelp
forests, Duggins 1981; Ebeling et al. 1985; coral reefs,
Edmunds & Carpenter 2001; temperate reefs, Vance 1979;
Tuya et al. 2004); however, less emphasized is the role
temperate sea urchins play by excavating boreholes and
increasing fine-scale heterogeneity of marine habitats.
The purple sea urchin Strongylocentrotus purpuratus is
a common inhabitant of exposed rocky shores on the
Pacific Coast of North America and can occur in densi-
ties of over 100 m
2
(Ricketts et al. 1939; Ebert 1968).
Marine Ecology (2014) 1–10 ª2014 Blackwell Verlag GmbH 1
Marine Ecology. ISSN 0173-9565
Urchins excavate cavities in rocky substrata (hereafter,
pits) through a slow, bioerosive process, presumably
related to scraping from the spines and Aristotle’s lan-
terns of individuals (Fewkes 1890; Ricketts et al. 1939).
While this behavior is only possible where the substrate is
soft enough to allow bioerosion, pit microhabitats are
commonly observed in sedimentary bedrock, boulders,
and walls, both inter- and subtidally, along many of the
world’s temperate coastlines (Rogers-Bennett et al. 1995;
Davis 2009). Urchins inhabit these pits, and movement
among them appears infrequent (Grupe 2006). Urchin-
excavated pits are common features contributing to
increased substratum surface area in temperate and tropi-
cal marine systems (Fewkes 1890; Ricketts et al. 1939;
Menge et al. 1983).
On a temperate headland on the Pacific coast of North
America (Cape Arago, Oregon) we observed many tide-
pools harboring sea urchins in pits interspersed with a
mosaic of algae, encrusting marine fauna, and motile
fauna living in empty urchin pits as well as the adjacent
flat space. Preliminary measurements suggested some spe-
cies were primarily associated with empty urchin pits,
whereas others were found mostly in flat spaces. For
example, we observed that the chiton Tonicella lineata
occurs almost exclusively on encrusting coralline algae
inside urchin pits, and we suspected other intertidal
organisms might also preferentially occupy this micro-
habitat.
To investigate how Strongylocentrotus purpuratus and
its bioerosive effects may alter fine-scale intertidal com-
munity structure, we examined the flora and fauna
inhabiting three distinct microhabitats in tidepools: flat
areas of rock, pits unoccupied by S. purpuratus, and pits
occupied by S. purpuratus (hereafter, flat space, empty
pits, and occupied pits, respectively). These microhabitats
tend to have a spatial extent on the order of 100 cm
2
or
less, the approximate area of a single pit. We developed
three hypotheses to address potential relationships
between tidepool communities and microhabitat. First,
we hypothesized that the mean density, Shannon diversity
(H’), and species richness and cumulative richness (total
number of species in all samples) of mobile fauna are
higher in pit microhabitats relative to flat space. We pre-
dicted that some species might preferentially occupy pro-
tected cavities that may reduce hydrodynamic forces
compared with flat spaces. Secondly, we hypothesized
that the mean percent cover, diversity, and species
richness and cumulative richness (hereafter referred to
collectively as ‘community properties’) of primary space-
holding species are greater in flat spaces and empty pits
than occupied pits. Frequent biological disturbance via
urchin grazing and spine abrasion should have a negative
effect on the number and richness of primary space
holders in the occupied pit treatment, just as urchin bar-
rens have reduced species richness and diversity com-
pared with kelp forests (Graham 2004). Finally, we
hypothesized that the species composition differs among
microhabitats. We predicted that different suites of spe-
cies will inhabit the three distinct microhabitats, possibly
related to substratum heterogeneity or biological distur-
bance by sea urchins. Testing these hypotheses will reveal
the potential effects of urchin modifications on the sur-
rounding tidepool community. While many studies have
examined interspecific interactions (Vadas 1977; Harty
1979; Duggins 1981; Thornber et al. 2006) or broad com-
munity patterns (Dayton 1975; Tegner et al. 1995) relat-
ing to S. purpuratus, the fine-scale (<100 cm²)
community effects of urchin-created microhabitats within
tidepools have not been examined previously.
Methods
Study site
Cape Arago (43.30°N, 124.40°W) is a headland in
Southern Oregon, USA. It is adjacent to South Cove,
which faces south and is protected from predominant
westerly swells. Intertidal sedimentary benches on the east
and west sides of the cove contain large boulders, abun-
dant cobble, and tidepools and surge channels of various
sizes. The microhabitats of interest in this study are inter-
spersed within most tidepools below +1 m (mean lower
low water).
Field methods
We sampled the biological communities associated with
three tidepool microhabitats in South Cove from 15 to
18 July 2008, during a period of particularly large tidal
amplitudes (c. 2.5–2.7 m, with low tides below -0.3 m).
After identifying and numbering approximately 30 tide-
pools containing the microhabitats of interest (Fig. 1a),
we randomly selected 10 of these pools, encompassing a
shoreline distance of 650 m and containing a wide range
of wave exposures and tidal heights. This sampling design
allowed us to examine how communities associated with
microhabitats vary within replicate tidepools and among
tidepools that experience different field conditions. For
each tidepool, we recorded water temperature, salinity,
and vertical elevation (Table 1). We estimated tidepool
surface area using the measured length and width dimen-
sions, and multiplied this total by one-half the maximum
depth to estimate total volume. To determine how the
biological community may vary at small (centimeter to
tens of centimeters) scales among microhabitats, we sam-
pled the three microhabitats in multiple locations in
2Marine Ecology (2014) 1–10 ª2014 Blackwell Verlag GmbH
Community composition of urchin microhabitats Davidson & Grupe
replicate tidepools. We sampled the flat space, empty pit,
and occupied pit microhabitats nearest a randomly
selected point along each of three to five transects
(Fig. 1b). We consider these microhabitats independent
because: (i) purple urchins rarely move from their pit mi-
crohabitats (Grupe 2006) and are unlikely to interfere
with adjacent microhabitats, and (ii) many of the taxa
living in these microhabitats either do not move or are
small macrofauna that are unlikely to have wide-ranging
influences on other areas in a tidepool. The first transect
was placed perpendicular to the longest axis of the pool
at a random starting point 0–25 cm from the edge. Sub-
sequent transects were placed at regular intervals (the
specific intervals used depended on the length of the tide-
pool). However, in two tidepools we were constrained by
a small number of empty pits, which we sampled haphaz-
ardly along with the nearest occupied pit and flat space.
We used Vernier calipers to measure the diameter and
depth of every pit. We recorded the percent cover of bare
rock and primary space holders (including algae and ses-
sile fauna) in each flat space, empty pit, and occupied pit
we sampled. After removing the sea urchin (in the case of
occupied pits), we identified every organism to the lowest
possible taxonomic level. The percent cover of each taxon
was estimated visually based on the mean results from
two independent observers. Mobile, rapidly moving mac-
rofauna were collected by covering the sampled area with
a dip net (1 mm mesh) and using a kitchen baster to col-
lect the small animals. Unknown taxa were collected and
identified in the lab. We standardized density measure-
ments by the substratum surface area of each respective
microhabitat that we sampled. For empty and occupied
pits, the surface area was calculated as a half spheroid
using the measured pit depth and radius. For flat spaces,
we attempted to sample an area equivalent to the spatial
extent of adjacent pits. However, the recessed nature of
pits resulted in greater sampled surface area
(mean 95% CI) for occupied pits (80.1 8.2 cm²)
and empty pits (61.8 7.5) than for flat spaces
(30.5 3.1).
We were concerned that species-area effects could
obscure richness patterns among microhabitats, so we
used ESTIMATE S (version 8.2, R.K. Colwell, http://
viceroy.eeb.uconn.edu/estimates/) to calculate individual-
based rarefaction curves (analogous to species accumula-
tion) as an alternative method of comparing species
richness (Hurlbert 1971). This method accounts for
unequal sampling areas or sample sizes, and allows one
to predict species richness after encountering a set
number of random individuals.
Statistical analysis
We tested whether the community properties (including
mean densities of mobile fauna/percent cover for primary
space holders, Shannon diversity, and richness) differed
among microhabitats (fixed) and tidepools (random)
using two-way mixed-model ANOVA. This design
allowed us to examine how the microhabitat treatment
effect varied within tidepools but also between tidepools;
thus we examined the microhabitat effect in tidepools
while controlling for the wide range of abiotic factors that
vary naturally between tidepools. We calculated the
means and confidence intervals based on mean values
a
b
Fig. 1. Example of tidepool habitats sampled (a) and the three
microhabitats (flat space, empty pits, occupied pits, (b) associated
with purple sea urchins (Strongylocentrotus purpuratus). The white
ruler in (a) is approximately 30 cm; the pits in (b) are around 6–8cm
in diameter.
Marine Ecology (2014) 1–10 ª2014 Blackwell Verlag GmbH 3
Davidson & Grupe Community composition of urchin microhabitats
from the 10 replicate tidepools. We did not include
S. purpuratus in our measurements of the community
properties, because they were used to define the treatment
groups. Assumptions of normality and homogeneous var-
iance were evaluated visually using residual-plots,
frequency histograms, and box-plots. Data were rank-
transformed to improve normality and heteroscedasticity
and to reduce the influence of outliers. Transformations
failed to normalize the data, but reduced heteroscedastici-
ty and the influence of outliers. We used Tukey HSD
tests to control for family-wise error for a posteriori com-
parisons. Chi-squared tests were used to examine differ-
ences in cumulative richness and occurrence between the
three microhabitats.
We examined the similarity of the mobile fauna and pri-
mary space holders utilizing microhabitats in replicate
tidepools using analysis of similarities (ANOSIM) with
1000 permutations and non-metric multidimensional scal-
ing (NMDS) with the Bray–Curtis dissimilarity measure
(using R, version 2.10.1, R Foundation for Statistical Com-
puting, http://www.r-project.org/). Prior to the analysis,
we pooled the subsamples of each microhabitat type
within a tidepool, since many of the individual subsamples
harbored zero taxa (resulting in zero dissimilarity errors in
the NMDS). The relative abundances of the mobile taxa
and primary space holders were fourth-root and square-
root transformed (respectively) to down-weight the influ-
ence of dominant taxa. When the ANOSIM tests detected
a significant difference between microhabitats, we con-
ducted multiple pairwise comparisons with the sequential
Bonferroni procedure (to compensate for increased type I
error). Associations between the physical characteristics of
the tidepools (Table 1) and the community properties
were examined using Pearson correlations.
Results
A diverse assemblage of intertidal organisms was found
within the sampled tidepools, representing 76 species (48
fauna, 28 algae) from 11 phyla (ESM 1). In many of the
analyses of mobile fauna and primary space holders, we
detected a significant effect of tidepool on the community
properties (Table 2), which likely represents the normal
spatial variation that intertidal organisms exhibit in these
discrete habitats (Metaxas & Scheibling 1993). We
detected weak positive associations between the elevation
and percent cover (r
2
=0.20, P =0.014) and richness
(r
2
=0.32, P =0.001) of primary space holders but we
did not detect associations between the other physical
characteristics of the tidepools (Table 1) and any of the
community properties of mobile species or primary space
holders (P >0.05). The most abundant taxa were
coralline algae, serpulid polychaetes (Pileolaria sp. and
Dodecaceria concharum), the anemone Anthopleura
xanthogrammica, the gastropods Lacuna marmorata,
Homalopoma baculum, and Lottia scutum, the chiton
Tonicella lineata, and the crustaceans Ampithoe lacertosa,
Pagarus caurinus, and Cancer oregonensis (ESM 1). The
occurrence of these relatively common taxa varied among
microhabitats.
Mobile fauna
The density, Shannon diversity, and richness of mobile
fauna did not vary consistently between different micro-
habitats. Mobile fauna were most abundant in flat
spaces, followed by empty pits and then occupied pits
(Fig. 2); however, we did not detect a significant differ-
ence in density among these microhabitats (Table 2).
The Shannon diversity and richness of mobile fauna
were higher in empty pits than in both flat space and
occupied pits, but we did not detect significant differ-
ences. Furthermore, the cumulative richness and percent
occurrence of fauna were higher in empty pits compared
with the other treatments, although results were only
significant for percent occurrence (Table 3). Since flat
space contained, on average, less surface area than pit
microhabitats, we also compared species richness of
mobile fauna using individual-based rarefaction curves
(ESM 2). These results were consistent with the trends
Table 1. Physical characteristics of the sampled tidepools in Cape Arago, Oregon (USA).
tidepool elevation (m) area (m
2
) volume (m
3
) sub-samples salinity temperature
1 2.1 0.72 0.09 5 36 8.8
2 3.5 3.48 0.83 5 36 9.3
3 1.8 1.30 0.13 5 36 9.5
4 2.6 0.46 0.06 5 35 9.4
50.6 13.44 1.55 3 37 9.6
6 0.3 0.80 0.03 4 38 10
7 2.8 0.92 0.09 5 37 10.2
80.3 2.04 0.13 4 36 9.4
9 0.1 5.36 0.48 5 35.9 9.9
10 1.0 0.84 0.09 3 36.5 10.6
4Marine Ecology (2014) 1–10 ª2014 Blackwell Verlag GmbH
Community composition of urchin microhabitats Davidson & Grupe
for Shannon diversity and average species richness, sug-
gesting a higher rate of species accumulation inside
empty pits and occupied pits than flat spaces. When
characterized by trophic functional group, faunal densi-
ties were highest in empty pit microhabitats, except her-
bivores, which were densest in flat space, following the
patterns of primary space holders (Fig. 3).
Primary space holders
The measurements of percent cover, diversity, richness,
cumulative richness, and occurrence were greater in flat
space and empty pit microhabitats than in occupied pits.
The mean percent cover of primary space holders differed
Fig. 2. The mean density (individuals per 100 cm
2
) or percent cover,
Shannon diversity, and richness of mobile fauna and primary space
holders in three tidepool microhabitats (flat space, empty pits,
occupied pits). Different letters denote statistical differences between
treatments.
Table 2. Results of two-way mixed-model ANOVA tests examining differences in the mean density/percent cover, Shannon diversity, and richness
of mobile fauna (a-c) and primary space holders (d–f) between microhabitat (flat space, empty pit, occupied pit) and tidepool. Values in bold are
statistically significant (P <0.05).
source of variation df MS F P source of variation df MS F P
(a) density of mobile fauna (d) percent cover of primary space holders
microhabitat 2 3578 1.935 0.173 microhabitat 2 42,235 43.185 <0.001
tidepool 9 2127 1.774 0.082 tidepool 9 4326 9.801 <0.001
microhabitat*tidepool 18 1849 1.542 0.091 microhabitat*tidepool 18 978 2.215 0.007
residual 102 1199 residual 102 441
(b) shannon diversity of mobile fauna (e) shannon diversity of primary space holders
microhabitat 2 3494 2.855 0.084 microhabitat 2 14,925 17.294 <0.001
tidepool 9 1219 1.475 0.167 tidepool 9 3310 3.075 0.003
microhabitat*tidepool 18 1224 1.481 0.113 microhabitat*tidepool 18 863 0.802 0.694
residual 102 827 residual 102 1077
(c) richness of mobile fauna (f) richness of primary space holders
microhabitat 2 5266 3.132 0.068 microhabitat 2 12,978 15.161 <0.001
tidepool 9 2355 2.160 0.031 tidepool 9 5304 5.783 <0.001
microhabitat*tidepool 18 1681 1.542 0.091 microhabitat*tidepool 18 856 0.952 0.520
residual 102 1212 residual 102 900
Table 3. Cumulative richness and percent occurrence of mobile
fauna, primary space holders, and all taxa combined in three tidepool
microhabitats (flat space, empty pits, occupied pits).
flat
space
empty
pits
occupied
pits v
2
P
cumulative richness
mobile fauna 23 32 26 1.56 0.46
primary space
holders
19 20 7 6.83 0.03
all taxa 42 53 33 4.70 0.10
occurrence
mobile fauna 64% 89% 77% 11.58 0.003
primary space holders 95% 93% 82% 1.09 0.58
all taxa 100% 98% 98% 0.03 0.99
Significance values at P <0.05 are indicated by the bold type.
Marine Ecology (2014) 1–10 ª2014 Blackwell Verlag GmbH 5
Davidson & Grupe Community composition of urchin microhabitats
significantly among treatments, with flat space having the
highest and occupied pits the lowest coverage (Fig. 2,
Table 2). The Shannon diversity and mean richness of
primary space holders were significantly higher in flat
space and empty pits than in occupied pits. The cumula-
tive richness and percent occurrence of primary space
holders were also higher in flat space and empty pits than
in occupied pits; however, results were only statistically
significant for cumulative richness (Table 3). The mean
percentage of bare space in occupied pits was two times
greater than in empty pits and more than five times
greater than in flat space (Fig. 4). Coralline algae, the
dominant primary space-holding taxon, and fleshy algae
attained the highest percent cover in flat space, followed
by empty pits and occupied pits. Sedentary and sessile
fauna (e.g. anemones, sponges, bryozoans) covered con-
siderably more space in empty pits than in flat space or
occupied pits, similar to the patterns exhibited by mobile
fauna (Figs 2 and 3).
We detected a significant microhabitat-tidepool inter-
action in the percent cover of primary space holders
(Table 2d). However, in nine of 10 tidepools, we
observed a consistent microhabitat pattern: the percent
cover of primary space holders was higher in the flat
space and empty pits treatment than occupied pits.
Although the magnitude of the microhabitat effect varies
in some tidepools (thus leading to a significant tide-
pool*microhabitat effect; see ESM 3), the consistency of
this pattern leads us to conclude there is a broad effect of
microhabitat on primary space holders.
Species composition in different microhabitats
The species composition of mobile fauna was similar
across microhabitats (Fig. 5a; R =0.073, P =0.09), but
ANOSIM tests reveal that the composition of primary
space holders differed significantly among microhabitats
(Fig. 5b; R =0.292, P =0.001). The species composition
of primary space holders in occupied pits is significantly
different than that in flat space (R =0.507, P <0.001)
and empty pits (R =0.284, P =0.003). We did not detect
a difference between flat space and empty pits
(R =0.070, P =0.158). The cumulative richness of all
organisms was greatest in empty pits, followed by flat
space and then occupied pits (Table 3).
Discussion
Tidepool microhabitats created by the sea urchin Strongy-
locentrotus purpuratus have distinct assemblages of spe-
cies, despite being separated by only centimeters. The
specific associations between organisms and microhabitat
and their strengths varied with taxon, feeding mode, and
mobility. A diverse and dense assemblage of intertidal
algae and sessile and sedentary fauna inhabited the flat
space and empty pit microhabitats. In contrast, pits occu-
pied by urchins contained few primary space-holding taxa
and were primarily composed of bare space surrounded
by coralline algal halos. The community properties of
Fig. 3. Mean faunal density by functional trophic group in three
tidepool microhabitats (flat space, empty pits, occupied pits). Note
the log-scaling.
Fig. 4. Mean percent cover of exposed rock (bare space) and
primary space holding taxa (crustose and erect coralline algae, fleshy
algae, and sessile fauna) in three tidepool microhabitats (flat space,
empty pits, occupied pits).
6Marine Ecology (2014) 1–10 ª2014 Blackwell Verlag GmbH
Community composition of urchin microhabitats Davidson & Grupe
mobile fauna varied among microhabitats, but not as
strongly as the primary space holders. Although the mean
faunal densities were highest in flat space, we did not
detect a significant microhabitat effect, possibly due to
the high variability of faunal densities among tidepools.
In contrast, empty pits contained a more diverse and spe-
cies-rich assemblage in relation to adjacent flat space or
occupied pits (although our results were not significant).
We hypothesize that the differences in community pat-
terns between microhabitats for primary space holders
and mobile taxa are likely related to interactions between
biotic forces (such as urchin disturbance and herbivory;
Fewkes 1890; Benedetti-Cecchi & Cinelli 1995; Elahi &
Sebens 2012) and abiotic factors (such as wave force;
Dayton 1971). Biotic disturbance and herbivory by urch-
ins likely resulted in the relatively low abundances, diver-
sity, and richness of tidepool flora and fauna we observed
in urchin-inhabited pits. Urchin grazing and bioerosion
(grazing and spine abrasion) is a source of post-settle-
ment mortality for numerous primary space-holding flora
and fauna (Sammarco 1980; Maldonado & Uriz 1998;
Elahi & Sebens 2012). These activities are strong structur-
ing forces and can even prevent the establishment of
macroalgae and seagrasses in temperate and tropical mar-
ine ecosystems (Ogden et al. 1973; Estes & Palmisano
1974; Watanabe & Harrold 1991; Pearse 2006). Moreover,
other sheltering species of sea urchins have occasionally
been observed to impact community structure, predomi-
nantly in the vicinity of holes and crevices (Ogden et al.
1973; Vance 1979; Benedetti-Cecchi & Cinelli 1995).
Anecdotal observations further support the hypothesis
that herbivory and bioerosion by urchins are important
structuring forces in the rocky intertidal. The sudden dis-
appearance of sea urchins from mid-intertidal pools at
South Cove in 2006–2007 was followed by dramatic
changes in the associated algal community, namely an
increase in fleshy algae and a decrease in coralline algae
and bare rock (B. M. Grupe, personal observations). In
addition, the small fauna (scale worms and amphipods)
living under or on the urchins may be commensals (e.g.
Schoppe & Werding 1996) and may benefit from the
habitat the urchin provides, trapped macroalgae, and/or
the condensed, organically-rich fecal pellets excreted from
urchins (T. M. Davidson & B. M. Grupe, personal obser-
vations). Thus, numerous species may be altered by biotic
interactions and disturbance by purple sea urchins.
Empty pits may be an important habitat for intertidal
organisms seeking shelter from hydrodynamic forces and
water-borne projectiles, especially when alternative struc-
tures are not present (Pardo & Johnson 2006). Wave
force is an important component of structuring rocky
intertidal communities (Dayton 1971; Denny 1988), and
dissolution of plaster clod cards indicates that average
water velocities are reduced in urchin pits relative to
adjacent flat spaces (B. M. Grupe, unpublished data; but
see O’Donnell & Denny 2008). Waves create projectiles
out of objects in the water such as logs or rocks, which
may crush or scour individuals living on unprotected sur-
faces (Dayton 1971; Shanks & Wright 1986). In addition,
empty pits harbored a more diverse and abundant algal
community compared with urchin-inhabited pits, indicat-
ing a possible effect of reduced biological disturbance.
However, the coverage of primary space holders was
lower than in adjacent flat spaces. Empty pits may experi-
ence higher rates of particle deposition (including detritus
and organic debris) than flat surfaces (Yager et al. 1993;
Abelson & Denny 1997), which could provide important
food resources for fauna inhabiting these microhabitats.
Organisms with different feeding modes responded dif-
ferently to microhabitat. The densities of carnivores, scav-
engers, and suspension feeders were greater in empty pits
a
b
Fig. 5. Non-metric multidimensional scaling ordination plots showing
the similarity (Bray–Curtis) of the species composition in three
different tidepool microhabitats (flat space, empty pits, occupied pits)
for (a) mobile fauna and (b) primary space holders. Spatial distance in
the sites indicates the relative similarity of species composition.
Marine Ecology (2014) 1–10 ª2014 Blackwell Verlag GmbH 7
Davidson & Grupe Community composition of urchin microhabitats
than in other microhabitats. Herbivores, however, were
more abundant on flat space and empty pits than occu-
pied pits, consistent with the pattern exhibited by pri-
mary space-holding algae. These animals may be using
the complex structure and food provided by several spe-
cies of algae. However, primary space-holding fauna
exhibited higher coverage in empty pits compared with
other microhabitats. Since these were mainly suspension-
feeders, high water velocities over exposed rock could
lead to increased growth or survivorship of individuals in
sheltered microhabitats with reduced flow (Dai & Lin
1993; Ackerman 1999; Sobral & Widdows 2000). We sug-
gest that nutritive requirements may lead to these pat-
terns, but it is also possible that three-dimensional
habitat provided by algae is related to herbivore densities.
Some mid- and high intertidal limpets and microgastro-
pods are known to reside in protective crevices at low
tide and emerge to graze on exposed substrata at high
tide (Garrity 1984; Bazterrica et al. 2007), and it is possi-
ble that tidepool grazers could follow a reverse pattern,
taking cover in pits during high tide but grazing on flat
spaces at low tide. Future studies should examine whether
tidepool herbivores exhibit diel or tidal variation in
microhabitat use.
The extent of the association between individual taxa
and urchin microhabitats also varies. For example, the
anemone Anthopleura xanthogrammica was only found
inhabiting empty pits in our sampled tidepools, despite
the presence of adjacent flat space. Our data and field
observations suggest that pits rarely, if ever, contain both
an urchin and an anemone, so there may be interspecific
competition for these microhabitats.
Several relatively large organisms such as the chiton
Tonicella lineata and the crabs Pagurus caurinus and
Cancer oregonensis occurred most often in empty pits.
Their association with this microhabitat suggests a benefit
to inhabiting the pit microhabitat. Since pits persist in
intertidal rock (ranging from sandstone or siltstone to
basalt) and likely outlast the organisms that create them,
we hypothesize that some community members inhabit-
ing pits may receive a long-term benefit even if sea urch-
ins are removed from an area. Manipulative studies
should investigate the specific response of the tidepool
community to ecosystem engineering by purple urchins.
Sea urchins are widely recognized as being dominant
grazers in shallow marine ecosystems (Ayling 1981;
Harrold & Reed 1985; Shears & Babcock 2002). Our
study shows that sea urchins are also important in struc-
turing tidepool communities on a finer scale than previ-
ously recognized. By creating and maintaining a long-
lasting, novel microhabitat, these allogenic ecosystem
engineers (sensu Jones et al. 1994, 1997) modulate the
availability of resources for other organisms. The excava-
tion of pits increases the total surface area of the substra-
tum, which is considered to be limiting in the intertidal
(Dayton 1971). Pit microhabitats also likely alter the
physical forces experienced by organisms by reducing
average water velocities and preventing damage from roll-
ing boulders (B. M. Grupe, unpublished data). In addi-
tion, depressions can enhance deposition of organic
matter (Yager et al. 1993; Botto et al. 2006) and propa-
gules, including algal spores and competent larvae (Snel-
grove et al. 1993; Koehl 2007). Increased topographic
complexity can even alter light and shade on intertidal
surfaces with implications for community structure
(Menconi et al. 1999; Takada 1999; Stachowicz et al.
2008). Thus, the removal or addition of these important
ecosystem engineers by anthropogenic (e.g. altered preda-
tor densities, climate change) or natural means (e.g.
recruitment pulses, freshwater die-off events) may have
strong effects on the community structure of the rocky
intertidal at smaller scales than previously recognized.
Acknowledgements
We are grateful for the helpful comments of Erin Cooper,
Amy Larson, and two anonymous reviewers. Megan Grupe
and Amanda Wilson provided invaluable field and lab assis-
tance. Steven Rumrill of the South Slough National Estua-
rine Research Reserve and Craig Young of the Oregon
Institute of Marine Biology provided much needed field and
lab equipment. Finally, we thank Becky Richardson from
Sozo Tea and Coffee (North Bend, Oregon) for providing
coffee, food, and informal office space during this study.
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