Hydrobiologia (2006) 553:337–344 Ó Springer 2006

DOI 10.1007/s10750-005-1246-6

Primary Research Paper

Coastal resources exploitation can mask bottom–up mesoscale regulation

of intertidal populations

Fernando Tuya1,*, Rubén Ramı́rez2, Pablo Sánchez–Jerez2, R.J. Haroun1,

Antonio J. González-Ramos1 & Josep Coca1
1
BIOGES, Department of Biology, Faculty of Marine Sciences, Campus de Tafira, University of Las Palmas de G.C,
E-35017, Las Palmas de Gran Canaria, Canary Islands, Spain
2
Department of Marine Sciences, University of Alicante, POB 99 E-03080, Alicante, Spain
(*Author for correspondence: Tel.: 0044928457456; Fax: 0044928452922; E-mail: ftuya@yahoo.com)

Received 2 March 2005; in revised form 15 June 2005; accepted 27 July 2005

Key words: community regulation, spatial patterns, upwelling, intertidal populations, grazing molluscs, hierarchical
design, Canary Islands

Abstract
We describe the spatial distribution patterns of rocky intertidal Patella spp. limpets (heavily collected by
shellfishers) and top-shell snails belonging to the genus Osilinus (comparatively slightly harvested) through
a multiscaled sampling design spanning five orders of magnitude of spatial variability (from 10s of m to
100s of km) throughout the Canarian Archipelago (eastern Atlantic); where rocky intertidal assemblages on
opposite sides of the Archipelago (western vs. eastern islands) are subjected to different regimes of bottom-
up effects, as large spatial variation in oceanographic conditions is recorded across an east–west gradient.
We tested the hypothesis that the response of rocky intertidal populations to mesoscale oceanographic
bottom-up variability (quantified using differences in Chlorophyll-a concentration among islands as an
approximation to bottom-up effects) depends on the exploitation status of coastal resources, by means of a
correlative approach. Our study represent another case in which mesoscale shore-associated physical
processes seem to be correlated to large-scale differences (variability among islands, 10s to 100s of km
apart) in the abundance of slightly harvested intertidal grazers (topshell snails). In contrast, we did not
observe large-scale spatial differences for heavily collected grazers (limpets). In conclusion, our study
suggests that the signal of bottom-up processes in coastal populations may be difficult to demonstrate under
intense human exploitation.

Introduction sive collecting by humans of intertidal popula-

The influence of bottom-up mesoscale processes
on the spatial abundance patterns and structure
of rocky intertidal populations has been docu-
mented in recent publications (Bustamante et al.,
1995a, b; Menge et al., 1997; Menge, 2000; Niel-
sen & Navarrete, 2004). Variability of oceano-
graphic conditions at the appropriate scales may
influence low trophic levels and further propagate
up the food web (Menge, 2000). However, inten-
tions makes it difficult to demonstrate and
quantify the signal of bottom-up processes in
coastal habitats (Nielsen & Navarrete, 2004).
How these factors interact in human-influenced
environments is a key factor in our understanding
of intertidal systems.
Two groups of rocky-intertidal grazing molluscs,
(1) limpets (Patella rustica Gould, 1846; Patella
candei crenata Orbigny, 1840; and Patella aspera
Gmelin, 1791) and (2) topshell snails (Osilinus spp.),
338
are widely found at the Macaronesian region in the
eastern Atlantic. These invertebrates graze on
epilithic algal resources of the same functional
groups (microalgae, filamentous and foliar
ephemeral algae; Crothers, 2001; Jenkings et al.,
2001). Patellid limpets are heavily collected by
both recreational and professional shellfishers
throughout the Macaronesia (Corte-Real et al.,
1996; Navarro et al., 2005), whereas topshell snails
are comparatively slightly harvested. We used
these two groups of molluscs to hypothesize that
the responses of intertidal assemblages to meso-
scale oceanographic events (bottom-up effects) are
highly dependent on the human-perturbed status
of intertidal species. More specifically, we analyzed
the spatial distribution patterns by means of a
multiscaled perspective spanning five orders of
magnitude of horizontal variability (from 10s of m
to 100s of km), of the abundance of intertidal
limpets and topshell snails. The aim was to cor-
relate the recorded patterns at large spatial-scales
(10s to 100s of km) with (1) the dominant ocean-
ographic regime along the overall Canarian
Archipelago and (2) the exploitation status of the
studied species. We predicted that herbivore
abundances would be higher where bottom-up
resources were greater, and that inconsistencies in
this pattern could be attributable to overexploita-
tion of targeted intertidal species. In this context,
Chlorophyll-a concentrations were used as an
approximation to assess bottom-up effects on
large-scale distribution of the target intertidal
assemblages.
Materials and methods
Oceanographic context and intertidal community
structure
The Canary Islands are located off the north-west
African coast at about 28° N and comprise seven
major islands, as well as a group of small islets
(Chinijo Archipelago), lying between 100 and
600 km offshore. Nearshore waters of north-wes-
tern Africa are characterized by almost year-round
wind-driven upwelling that brings cold, nutrient-
rich sub-surface waters to the surface, extending as
a 50–70 km band along shore (Mittelstaedt, 1991;
Davenport et al., 2002). Large spatial variation in
sea surface temperature is recorded across an east–
west gradient perpendicular to the coast (Daven-
port et al., 2002). Therefore, the Canarian Archi-
pelago lies in the transition between the oligotrophic
open ocean and the northwest African upwelling
(so-called Northwest African Coastal Transition
Zone [NACTZ], Pacheco & Hernandez-Guerra,
1999), which is characterized by high mesoscale
activity. Quasi-permanent cold-water filaments
advected westward away from the upwelling cores
have been extensively recorded (Van Camp et al.,
1991; Barton et al., 1998; Davenport et al., 2002).
As a result, nearshore waters of the eastern islands
(Lanzarote, A. Chinijo, Fuerteventura and Gran
Canaria) are under regular influence of these
upwelled cold-water inputs (Davenport et al.,
2002). Moreover, island-induced eddies have been
widely observed in the south-face of the islands,
inducing mesoscale variation on chlorophyll-a
distribution around the islands (Arı́stegui et al.,
1994, 1997).
A decrease in nutrient concentrations and
plancktonic primary productivity (from 237 g C
m)2 yr)1 at the eastern islands to 145 g C m)2 yr)1
at the western islands; Davenport et al., 2002) has
been observed almost year-round along an east–
west linear gradient throughout the Canarian
Archipelago (Barton et al., 1998; Bode et al.,
2001; Davenport et al., 2002). Consequently, rocky
intertidal assemblages on extreme islands are likely
subjected to different regimes of bottom-up
effects (sensu Menge, 2000). In this sense, we take
advantage of natural conditions across the Ca-
narian Archipelago to asses the role of bottom-up
factors on intertidal populations.
Rocky intertidal platforms of the Canarian
Archipelago exhibit classic patterns of zonation
(Navarro et al., 2005), with the vertical arrange-
ment of the communities in several zones or bands.
The lower band is characterized by turf-forming
macroalgae. The intermediate band is dominated
by the cirriped Chthamalus stellatus, whereas the
superior band is dominated by scattered cyano-
bacterial colonies or mats. A reasonable assumption
on the rocky shores throughout the Canarian
Archipelago is that higher-order carnivores (sea-
stars, whelks, etc.) other than humans have negli-
gible effects on intertidal slow-moving herbivore
species (R. Ramı́rez, unpublished data).

Sampling design
In each island, 3 rocky substrate locations were
chosen. In each location we randomly selected 3
sites separated by 10s to 100s of m (Fig. 1). The
use of this criterion allowed us to adopt a hierar-
chically organized multiple spatial scales perspec-
tive for the study of intertidal populations
(Underwood & Chapman, 1996; Underwood,
1997; Menconi et al., 1999; Benedetti-Cecchi et al.,
2000; Benedetti-Cecchi, 2001), which included:
islands (104–105 m apart), locations (103–104 m
apart) and sites (101–102 m apart). All of the
studied locations were easily accessible and were
unprotected from extraction of natural resources.
In each band of the three rocky substrate sites
within each location, we randomly placed ten
squares of 50 by 50 cm (0.25 m2), and counted all
the limpets and topshell snails present in each
square (see Hawking & Jones, 1992, for a review).
Two species of the genus Osilinus occur in the
Canary Islands, but they are difficult to identify in
situ. We therefore pooled both species into an
Osilinus spp. category. All sampling were carried
out during March-2003.
Figure 1. Map of the Canarian Archipelago showing sampling locations.
339
Data analysis
Abundance data recorded for each species were
analyzed by means of mixed ANOVA models to
test for differences in the mean abundance among
intertidal bands and the different spatial scales
considered. The model therefore incorporated the
following factors: (1) ‘Island’ (fixed factor with
eight levels corresponding to the seven main is-
lands plus Chinijo Archipelago), (2) ‘Band’ (fixed
factor with three levels, and orthogonal to the
previous factor), (3) ‘Locations’ (random factor
nested within islands with three levels) and (4)
‘Sites’ (random factor nested within the interaction
term ‘Band  Location (Island)’ (Underwood,
1997). Before analysis, Cochran’s test was used to
check for homogeneity of variances. Since no
transformation rendered homogeneous variances
(Cochran’s test, p < 0.01), the significance level
was set at the 0.01 level instead of 0.05, as ANO-
VA is robust to heterogeneity of variances, par-
ticularly for large balanced experiments
(Underwood, 1997). If ANOVA detected signifi-
cant differences for the interaction between the
factors ‘Island’ and ‘Band,’ further analysis were
340

done as independent comparisons of islands for
each intertidal band, by using the SNK a-posteriori
multiple comparison test (Underwood, 1997).
The absence of data on in situ phytobenthic
productivity in the Canarian Archipelago implied
the use of plancktonic chlorophyll-a as an indica-
tor on the regimen of availability of bottom-up
resources across the studied area imposed by the
upwelling and mesoscale advection near the is-
lands. In this sense, distributions of nearshore
chlorophyll-a can be viewed as an approximation
to assess correlatively the effects of mesoscale
oceanographic variability on intertidal assem-
blages (Menge et al., 1997).
Near-surface chlorophyll-a concentration (in
mg m)3) was determined from daily OrbView-2
SeaWIFS satellite images (Davenport et al., 2002)
during the sampling period at each island, and
averaged for each island. As the purpose of this
paper was the detection of variability among is-
lands, we pooled abundance data among intertidal
bands and locations within each island to check
for graphical and correlative evidence of our stated
hypothesis. In this context, a regression analysis
was carried out to asses the relationship between
the mean densities of organisms per island and the
averaged concentration of Chlorophyll-a per is-
land.
SNK tests for each intertidal band, as the inter-
action between these factors was significant
(F = 5.59, p < 0.01, Table 1). In general, higher
abundances were registered at the eastern islands
(Lanzarote, A. Chinijo, Fuerteventura and Gran
Canaria) with respect to the western islands of the
Archipelago (Fig. 2). Thus, mean abundance of
topshell snails across pooled eastern islands were
about three times higher than that averaged for the
western islands. In contrast, the mean abundance
of the three studied limpet species did not fluctuate
among surveyed islands (Table 1, Fig. 2), with
extremely low abundance throughout the overall
Canarian Archipelago.
OrbView-2 SeaWIFS satellite images revealed
chlorophyll-a concentrations oscillating between
0.15 mg m)3 (western islands) to 0.30 mg m)3
(eastern islands) for the studied period. The
regression analyses showed a significant and posi-
tive correlation (y = 1.016x )0.0092, R2 = 0.76,
p < 0.0001, Fig. 3) between the mean abundances
of Osilinus spp. snails per island and the chloro-
phyll-a concentrations. In contrast, no significant
relationship was found for any of the limpet species
(Patella rustica: y = )0.338x + 0.11, R2 = 0.24,
p > 0.01; Patella candei crenata: y = 0.08x +
0.005, R2 = 0.05, p > 0.01; Patella aspera: y =
0.0076x ) 0.009, R2 = 0.27, p > 0.01).

Results Discussion

Statistically significant differences in the abun- Our observational and correlative approach de-
dance of topshell gastropods Osilinus spp. were tected a significant large-scale spatial difference
detected among islands and corroborated by the (variability among islands, 10s to 100s of km

Table 1. Results of ANOVA on mean abundance for each species

DF Patella rustica Patella candei Patella aspera Osilinus spp.

crenata

MS F MS F MS F MS F

Island = I 7 1.5680 1.74 0.0081 1.26 0.7960 1.90 401.95 8.9**

Band = B 2 4.5500 10.18** 0.0168 2.69* 0.7904 3.76* 284.53 9.22**
IB 14 0.6489 1.45 0.0094 1.50 0.4661 2.22* 172.38 5.59**
Location (I) = L(I) 16 0.9032 1.81* 0.0065 1.16 0.4185 4.76** 45.15 0.36
L(I)  B 32 0.4470 0.90 0.0062 1.12 0.2103 2.39** 30.84 0.24
Site L (I  B) 144 0.4991 1.85** 0.0056 1.86** 0.0879 6.03** 126.49 9.17**
Residual 944 0.2705 0.0030 0.0146 13.78

*: 0.01 < p < 0.05. **: p < 0.01.

 341

Figure 2. Mean pooled overall abundance of intertidal molluscs’ populations at each surveyed island of the Canarian Archipelago.
Error bars represent SE of means.
342
Figure 3. Regression analysis between the mean abundance of Osilinus spp. snails per island and the chlorophyll-a concentration
pooled for each island, as obtained from satellite imagery.
apart) in the abundance of intertidal snails of the
genera Osilinus. This could represent another case
in which mesoscale shore-associated physical
processes seem to be related to large-scale differ-
ences in the abundance of intertidal grazers
(Bustamante et al., 1995a, b; Menge et al., 1997;
Menge, 2000; Nielsen & Navarrete, 2004), as the
primary underlying cause. The location of the
Canarian Archipelago along the NACTZ (Pach-
eco & Hernandez-Guerra, 1999) makes rocky
intertidal populations highly susceptible to re-
spond to this mesoscale variability in the oceano-
graphic conditions and, consequently, in the
availability of bottom-up resources.
Large-scale variations in oceanographic condi-
tions are usually associated with different magni-
tudes of availability of nutrients and particulate
food, affecting algal and/or phytoplankton abun-
dance (reviewed by Menge, 2000). Therefore we
suggest that environmental gradients of nutrients
and primary productivity between the eastern and
western islands (Barton et al., 1998; Bode et al.,
2001; Davenport et al., 2002) could be responsible
for differences in food supply (microalgae and fast-
growth opportunistic filamentous and ephemeral
algae) and/or recruitment rates for both studied
groups of molluscs, as survival of larval molluscs
increase with high phytoplankton availability lead-
ing to higher recruitment (Menge et al., 1997).
Consequently, it would be expected that grazer
abundance will be high at the eastern islands of the
Canarian Archipelago, where bottom-up input of
resources are greater, as we recorded for topshell
snails. These gastropods are only slightly collected by
humans along the Canaries, presenting mean abun-
dance values similar to other temperate rocky shores,
as the Mediterranean Sea (Menconi et al., 1999).
In contrast, we did not observe the above-cited
large spatial-scale differences among islands for
the three Patella species. Limpets are intensively
collected across the entire Canarian Archipelago
(Navarro et al., 2005). In fact, the mean abun-
dance recorded by our study is about two to three
orders of magnitude lower than overall limpet
abundance at nearby temperate coastal areas, such
as the Mediterranean (Menconi et al., 1999) or the
Portuguese coast (Boaventura et al., 2002). Hence,
a top-down force (collection by humans) could
mask the expected bottom-up mesoscale regula-
tion of intertidal populations.
It is difficult to manipulate bottom-up factors
at large spatial scales. The comparison of areas
located far apart and exposed to different envi-
ronmental conditions can provide some clues
about the role of bottom-up processes, although
geographic distance can introduce uncontrolled
factors that may confound results. Our paper
provides correlative evidence that the signal of
bottom-up processes in coastal populations may
be difficult to demonstrate under intense human’s
exploitation. Of course, our observational ap-
proach is a simplistic conceptualization of the
interactions between the studied grazers and the
availability of bottom-up resources across the
Canarian Archipelago. In this sense, we have to
bear in mind Schiel’s (2004) consideration con-
cerning the correlative nature of most papers
testing large-scale processes related to upwelling

and physical events, instead of experimental evi-
dence. While our observational findings and
speculations are intriguing, future research at both
small and large spatial scales over long time peri-
ods, coupled with laboratory and field studies, will
be necessary to asses the nature and significance of
the effects of bottom-up inputs in rocky intertidal
communities. Our study therefore encourages the
development of quantitative replicated manipula-
tive and mensurative experiments that explain the
mechanisms that are responsible for differences in
the abundance patterns of intertidal populations
along gradients of oceanographic conditions.
Acknowledgements
Research was economically supported by the
Spanish ‘Ministerio de Medio Ambiente’ in the
framework of the ‘Canarias, por una costa viva’
project (www.canariasporunacostaviva.org). Sa-
tellite images were provided by the SeASAP service
(http://www.gobiernodecanarias.org/agricultura/pes-
ca/seasap/default.htm). We gratefully thank all the
voluntaries and students for helping us with the
data collection. Comments by two anonymous
referees improved significantly a previous draft of
this paper.
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