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Seasonal and Latitudinal Patterns in Rocky Intertidal Communities of Ecuador
Running head: Intertidal communities of Ecuador
Lamb, R.W. ¹*, Franco, A.², Vinueza, L.R.¹
¹Maestría en Ecología, Universidad San Francisco de Quito, Cumbayá, Ecuador
¹Pontificia Universidad Católica del Ecuador, Quito, Ecuador
*Email: [email protected] 9
Abstract
Ecuador is located at the confluence of two major, opposing marine currents: the 13 Humboldt
Current and the North Equatorial Counter current (NECC). This creates a 14 unique mix of nutrient
levels, water temperatures, and larval supply that may influence 15 intertidal community structures.
However, the nature of these effects is largely unknown, 16 in part because the intensity and
location of the convergence zone is strongly affected by 17 seasonal changes and by the strength of
El Niño-Southern Oscillation. To examine how 18 communities vary along a gradient of
productivity and temperature, we surveyed rocky 19 intertidal shores at each of 10 sites ranging 360
km along the Ecuadorian coast. We 20 sampled each site during both warm and cold phases of the
seasonal cycle. Community 21 structure was significantly different between sites, and this variation
was explained by 22 both biogeographic region (North vs. South) and phase of the local seasonal
cycle (warm vs. cold). Biomass increased gradually from southern to northern sites, as did diversity,
evenness, species richness, and abundance of mobile invertebrates. Temperature readings over the
course of the study supported the hypothesis that the southern coast was dominated by the
Humboldt Current and the northern coast was dominated by the NECC. This study provides
baseline data for rocky shores along the continental coast of Ecuador, and illustrates the seasonal
interplay between opposing current systems and its impacts on intertidal communities.
Key Words: intertidal, community structure, Humboldt Current, productivity, temperature, Ecuador
Introduction
Ecuador is located directly on the equator at the confluence of two major marine current systems:
the North Equatorial Counter current (NECC), which brings warm, waters of relatively low
productivity southwards, and the Humboldt Current, which brings cold, productive waters
northwards (Strub et al. 1998). As a result, the Ecuadorian coast 51 harbours marine life that is
characteristic of both tropical and sub-tropical regions (Cruz et al. 2003). However, we lack basic
information regarding biodiversity patterns and community structure in Ecuador’s mainland coast
and how these patterns relate to oceanographic processes. Such understanding is essential for
enabling scientists to discern natural variation from that caused by human or environmental
perturbations (Harley et al. 2006), and to provide information for those managing and conserving
marine systems (Tundi 2000, Edgar et al. 2004-B). In addition, the potentially stark contrast in
temperature combined with the mixing of propagules from cold- and warm-adapted species from
these two current systems presents an ideal setting for ecological research. Our study aimed to
assess patterns of community structure and marine productivity in rocky intertidal communities of
Ecuador, and how these patterns vary in time and space.
Marine conditions on the western coast of equatorial South America vary as the relative
strengths of the NECC and Humboldt Current affect the position of the Intertropical Convergence
Zone, creating annual warm and cold phases, with particularly strong El Niño or La Niña years
occurring on a semi-decadal basis (Wang & Fiedler 2006). This marine seasonality, commonly
referred to as the El Niño-Southern Oscillation (ENSO), can produce substantial local variation in
water temperatures and
nutrient supply, with corresponding impacts on marine ecosystems (Alheit & Niquen 2004, Vinueza
et al. 2006). The variation in these abiotic conditions plays a key role in shaping intertidal
communities, whether by directly limiting species distributions through physiological restraints and
larval recruitment (Dayton 1971, Sousa 1979, Menge & Sutherland 1987, Scrosati & Heaven 2007),
or by affecting the outcomes of biological interactions (Dayton 1975, Posey et al. 1995, Kraufvelin
et al. 2010). In addition, previously inferior competitors or invading species newly entering the
system can become dominant as habitats become more favourable (Gilman et al. 2010). Under most
global climate change models, ENSO events are predicted to become more frequent and stronger
(IPCC 2001), causing more extreme temperature changes for longer durations, suggesting that we
need to understand ENSO-related effects in much more detail at different spatial and temporal
scales.
Within the Humboldt current bioregion, strong El Niño years are characterized by a heavy
influx of warm water from the equator (Fleischbein et al. 1987), which creates stagnant water
conditions with decreased upwelling that can produce local extinctions and regime shifts (Glynn
1998, Harley et al. 2006). Conversely, La Niña years produce intense, persistent upwelling,
although the baseline levels of productivity in this 86 bioregion are generally high, which can
preclude significant ecological changes during strong La Niña events (Firstater et al 2010). Even so,
such variations in temperature and upwelling regimes can affect predation rates, feeding efficiency
and recruitment patterns (Menge 1992, Witman et al. 2010). Less is known regarding how ENSO
variation affects marine habitats of the eastern tropical Pacific north of the equator, but the impacts
in this region are somewhat less pronounced (Glynn 1990).
While a given year may involve a strong La Niña, El Niño, or neither, some level of
seasonal variation can be expected to occur on an annual basis. In addition, inter-annual variation in
the ENSO has been shown to produce community turnover as the growth and survival of certain
species are favoured over others (Vinueza et al. 2006). Although seasonal variation in a given year
may not be sufficient to have this same effect, differences in recruitment from propagules carried by
one dominating current or the other could potentially affect species assemblages. For these reasons,
the continental coast of Ecuador presents a unique opportunity for examining the potential effects of
global climate change on marine ecosystems, since substantial variation in water temperatures and
nutrient availability could be expected over relatively short periods of time.
Marine conditions and their impacts on ecological relationships can generally be
characterized based on latitude (Menge & Lubchenco 1981, Broitman et al. 2001). In more
distinctly tropical areas of the eastern Pacific (located north of the equator, with usually warm water
and low nutrient levels), intertidal communities tend to be dominated by crustose algae (SibajaCordero & Cortés 2010), and species that could potentially be more competitively dominant (e.g.,
foliose algae, sessile invertebrates) are intensely predated upon by a diverse assemblage of
consumers (Lubchenco et al. 1984, Menge et al. 1986). Conversely, studies in areas of strong subtropical upwelling off the coast of Peru indicate that in these colder, nutrient-rich waters, bottom-up
processes such as nutrient availability and structural habitat play a more important role in
determining intertidal community structure (Firstater et al. 2010, Firstater et al. 2011). In the
Galápagos Islands, which are located 1000 km directly west of Ecuador, intertidal communities
representative of both regions can be found within a very small area, due to a confluence of warmand cold-water currents (Vinueza 2009). In addition, dramatic shifts in community structure can be
produced at a single site between different phases of the ENSO (Vinueza et al. 2006). We sought to
determine whether similar differences in intertidal community structure could be observed within
relatively small spatial and temporal scales in mainland Ecuador.
Our study describes patterns of intertidal community structure along the Ecuadorian
coastline, which stretches approximately 650 km from north to south. Understanding the similarities
and differences between northern and southern coasts is very important, as any disparities in abiotic
conditions between phases of the ENSO and between biogeographical regions may create
differences in patterns of diversity and community structure. The continental coast of Ecuador has
long been overlooked as a potential research site for intertidal community ecology, with most
studies focusing on qualitative assessments of diversity (Cruz et al. 2003). This has left the area
virtually unstudied, creating a large knowledge gap regarding intertidal community composition and
the ecological processes and oceanographic phenomena that affect local marine habitats. With this
in mind, we sought to investigate how latitudinal differences in oceanographic conditions and
ENSO-driven seasonality affects intertidal communities along the coast of Ecuador, whether
distinct biogeographical regions exist based on closer proximity to warm or cold water currents, and
if so, how these regions might react differently to warm and cold phases.
Methods
Study Sites
We sampled rocky intertidal communities at 10 different sites stretching 361 km from North
to South along the Ecuadorian coastline. We took visual quadrat surveys and physical samples of
algae and associated invertebrates from intertidal communities at each site during a peak cold La
Niña event (August-October) and a normal warm phase (February-April) of the seasonal cycle. Our
choice of sites was determined by the presence of relatively flat rocky benches with similar abiotic
conditions at the landscape level and with semi-regular spacing throughout the entire study area.
We measured temperature using HOBO Pendant® data loggers at 15-minute intervals from
December 2010 to April 2011 (warm phase) at one northern and one southern site. We also
measured the physical characteristics of each study site, including sand burial (mean percent cover
of sand in the low zone at each site) and wave height (visual observations at each site at the same
time of day during the same tide series) to account for confounding environmental variables
between sites.
Intertidal Community Surveys
Within each site, we sampled two locations that were separated by at least 100 meters. At
each location, we defined the low intertidal zone based on natural zonation patterns of major
primary space occupiers and the relative positioning of each area with regard to tidal height. We
then laid out a 100 meter transect tape parallel to shore that followed the contour of the shoreline at
a consistent tidal height. Along this transect we sampled 10 quadrats of 50 x 50 cm placed
horizontally on the substrate at 10 m intervals. Within each quadrat, we identified organisms down
to the family, genus, or species level, and quantified the presence of each taxonomic group. Mobile
species were counted individually, and percent cover was determined for primary space-occupying
organisms (e.g., barnacles, algae, etc.). Additionally, we removed all algae from a 10 x 10 cm
square at the centre of each quadrat and froze it in a plastic bag for weighing. We took samples and
quadrats during both cold (August-October 2010) and warm (February-April 2011) ENSO phases at
each site.
Sample Processing
We separated out each algal biomass sample in water in a plastic container to remove the
sediment. We then removed all fauna from within the blades of algae and identified and recorded
their abundance. We placed the algae in individual tin foil cups and placed them in a drying oven at
70° C for 48 hours. We then measured dry mass for each sample.
Statistical Analyses
We assessed differences in community structure in low zone quadrats between phases
(warm/cold) and between biogeographical zones (North/South). We performed a multivariate
analysis using PRIMER statistical software, version 6.0, of differences between these groups using
two different types of data: percent cover of algae and sessile invertebrates, and diversity of algal
species. We first calculated mean percent cover for each species observed across all 10 quadrats
from both transects taken at each site during each seasonal phase. Algal species were grouped into
functional categories following the classification system proposed by Steneck and Dethier (1994).
We performed a Bray-Curtis similarity analysis using a square root transformation of the mean
percent cover data for each functional group of algae and sessile invertebrates. We then performed
two non-metric multi-dimensional scaling (MDS) analyses, one for the North region and another for
the South. We added vectors leading from the cold phase data point for each site to the
corresponding warm phase data point to show the overall trend in the transition of percent cover
data between phases. Based on our a priori study design, we performed a crossed analysis of
similarity (ANOSIM) with replicates to test for significant differences in community composition
between phases at each site, and a nested ANOSIM (sites within regions) to test for significant
differences between sites from different regions. We then repeated this same analysis using
diversity of algal species, with a 1 denoting the presence of a species in each quadrat, and a 0
denoting absence. Instead of individual MDS plots for each region, we grouped all transects from
both phases, producing one data point for each site.
We analyzed mean dry algal biomass between sites with R statistical software, using a
generalized linear model with a gamma distribution correction to test for differences between
regions and/or between phases. We also assessed the differences in the invertebrate community
living in algal biomass samples by quantifying evenness (J’), species richness and abundance, and
diversity (H’) at each site during each phase. Finally, we assessed the difference in mean daily
water temperature between site N1 and site S7 using a paired two-sample t-test.
Results
Mean distance between sites was 41.63 km, with a range of 0.50 – 132.32 km. For ease of
interpretation of the results, we labelled the sites 1-10 from North to South. Our 208 results also led
us to classify these sites into two regions: five northern and five southern 209 sites, denoted from
here forward as N1-5 and S6-10. There were no significant differences between regions in terms of
sedimentation, wave height, or exposure (data not shown).
Our analysis of percent cover of sessile organisms grouped into functional classes
demonstrated that sites were significantly grouped by phase (p < .05). The vector arrows connecting
cold phase to warm phase data points in the North and South MDS plots 215 (Figure 1 – A and B)
demonstrate that the direction of the shift in percent cover data 216 between phases was fairly
consistent among sites located within each region. However, using this same multivariate metric of
percent cover for each functional class, sites were not significantly grouped by region or by region
crossed with phase.
Southern sites had higher percent cover of articulated calcareous algae (p = .0002) and
corticated foliose algae (p = .0051) during the cold phase (14% vs. 5%, 15% vs. 7%, respectively),
and higher cover of corticated macrophytes (p > .0001) during the warm phase (17% vs. 3%).
Conversely, northern sites had higher percent cover of filamentous algae (p = .0054) and sessile
invertebrates (p = .0001) during the cold phase (36% vs. 25% and 11% vs. 4%, respectively), and
higher cover of corticated foliose algae (p = .0021) and crustose algae (p = .032) during the warm
phase (12% vs. 4% and 13% vs. 9%, respectively) (Figure 2).
Our assessment of the diversity of algal species assemblages also indicated that sites might
be grouped by phase and/or region. The two-way crossed analysis of these presence/absence values
confirmed that sites were significantly grouped by phase (<.006). Again, the analysis of sites nested
within region did not produce a significant result. However, we performed a second analysis by
crossing region with phase, which demonstrated that, when multivariate diversity values were
averaged across both phases, sites were significantly grouped by region (p <.006). Figure 3
illustrates this relationship, in which southern sites cluster into a distinct group in multivariate
space.
The generalized linear model indicated that dry algal biomass did not vary significantly
between phases, but did vary significantly by region (Figure 4), with higher biomass values in the
South. This trend was evident both when grouping sites into North vs South regions (p < .01) and
when assessing sites by latitudinal position in a linear relationship (p < .01). The community of
mobile invertebrates living within each algal sample also varied between sites, with patterns similar
to those seen in biomass results. Mean values were higher in southern sites than in northern sites
during both warm and cold phases for Shannon-Weaver diversity index (p = .0029), evenness index
(p = .0034), species richness (p = .0051), and invertebrate abundance (p = .019) (Figure 5).
Temperature was significantly higher in site N1 (mean: 27.26 ± 0.89 °C) than site S7 (mean: 26.18
± 0.93 °) during the warm phase (p < .0001; Figure 6).
Discussion
Our study offers the first quantitative assessment of intertidal community structure along the
coastline of continental Ecuador. The oceanographic patterns of the eastern tropical Pacific have
long been studied in correlation with the long-lasting and far-reaching impacts of ENSO events
(Strub et al. 1998, Wang & Fiedler 2006).
However, it has not previously been shown how the dynamic convergence zone of the
Humboldt Current and the NECC impacts local intertidal ecological processes in mainland Ecuador.
Our temperature readings demonstrated that the southern coast of Ecuador experienced cooler water
temperatures than the northern region during the study period (>1°C mean difference). While this
difference may be relatively small, it does show that environmental conditions can vary
significantly along this latitudinal gradient within a very limited geographic area. The Humboldt
Current extends well into Ecuador during strong La Niña years such as this one (Strub et al. 1998,
Wang & Fiedler 2006), but the differences in temperature that we observed could indicate that the
influence of the NECC was still felt in northern sites. Conversely, during El Niño years, when a
mass of warm surface seawater can extend as far as 7°-10° S (Fleischbein et al. 1987), such
disparities between temperatures on the northern and southern Ecuadorian coast would probably
disappear.
Coastal areas affected by the Humboldt Current are generally very productive (Alheit &
Niquen 2004, Firstater et al. 2011), which is characteristic of areas with high nutrient concentrations
and frequent upwelling (Blanchette et al. 2009). While we were unable to directly evaluate nutrient
levels, these are positively correlated with primary production (Cebrian et al. 2009), which we
measured using dry algal biomass. Our results show that a gradient does exist in standing algal
biomass along the coast of Ecuador, suggesting that southern sites, with their closer proximity to the
cold water Humboldt Current, are more productive than northern sites. Our results also indicate a
dividing point in marine productivity between sites S6 and N5 (corresponding to the towns of
Puerto Cayo and Manta), which could signify that, at least during the course of our study, a mixing
zone existed in this area between the Humboldt Current and the NECC. This evidence for the
location of the mixing zone coincides with satellite images measuring marine productivity in this
area (Saba et al. 2008). Conversely, we did not observe the hypothesized trend of higher biomass
during the cold phase than during the warm phase across all sites. We expected to observe this trend
since, in the nearby Galápagos Islands; seasonally higher nutrient levels produce greater levels of
biomass along a range of baseline productivity rates (Vinueza 2009). However, we probably would
need to examine biomass values over longer periods of time in order to better assess local variation
in intertidal productivity between phases of the ENSO.
In our study, diversity, evenness, species richness, and abundance of the mobile
invertebrates found in algal samples all followed similar trends to that of dry algal biomass, with
greater values in southern sites, evidence that the impacts of higher productivity levels on the
southern Ecuadorian coast are also felt in consumer groups. This was to be expected, since the
larger quantities of algae in samples from southern sites would provide more habitat for the small
marine organisms evaluated in this analysis. Despite this bias, differences in marine productivity
have been shown to propagate up through higher trophic levels in previous studies from both
tropical and temperate systems (Menge 1992, Vinueza et al. 2006, Cloern et al. 2007). Our results
also provide further evidence that nutrient supply and diversity in marine ecosystems are closely
related (Worm et al. 2002).
Several studies have observed this type of variation along geographical gradients (Broitman
2001, Schoch et al. 2006, Konar et al. 2010), but not at such a small scale. One striking exception
has been described in the Galápagos, where different marine a mixing zone existed in this area
between the Humboldt Current and the NECC. This evidence for the location of the mixing zone
coincides with satellite images measuring marine productivity in this area (Saba et al. 2008).
Conversely, we did not observe the hypothesized trend of higher biomass during the cold phase than
during the warm phase across all sites. We expected to observe this trend since, in the nearby
Galápagos Islands; seasonally higher nutrient levels produce greater levels of biomass along a range
of baseline productivity rates (Vinueza 2009).
As is the case for the Galápagos, the continental coast of Ecuador is located in a very
dynamic oceanographic setting with dramatic differences in temperature and productivity, which
produces distinctly tropical and subtropical biogeographic regions (Jennings et al. 1994, Edgar et al.
2004). While studies from Peru (Firstater et al. 2010) are representative of subtropical communities,
other locations such as Panama (Lubchenco et al. 1984, Menge et al. 1986) and Costa Rica (SibajaCordero & Cortés 2010), are more in line with what has been described for tropical rocky shores.
There, communities are dominated by encrusting algae, mostly as a result of a strong top down
effect of a diverse assemblage of consumers. In contrast, the low shore in our study sites was
dominated by more complex forms of algae, not only crustose species, which exemplifies the
predominance of the Humboldt Current in this region during the study period.
Our visual analyses using MDS plots for percent cover and diversity values pointed out
phase and region as possible grouping factors for the differences observed in community structure.
Both analyses showed that transects carried out at all sites during the months of the strong La Niña
event from August to October 2010 were significantly different in community composition from
transects carried out during the normal warm phase during February-April 2011. These trends
coincide with the results of previous studies that demonstrated how significant differences in water
temperature (Sanford 1999, Yamane & Gilman 2009, Meager et al. 2011) and nutrient or food
supply (Bustamante et al. 1995, Vinueza et al. 2006, Witman et al. 2010) can change both the
amount of biomass present and the dominance patterns of primary space occupiers. While Figure 1
demonstrates that the composition of intertidal communities along the coast of Ecuador changes
with variation caused by the seasonal cycle, Figure 3 shows how sites within northern and southern
regions group differently, once the interaction with the seasonal phase is accounted for.
We did not observe a clear pattern of typically tropical communities in northern Ecuador
and subtropical communities in the South, but when the interaction between region and phase was
taken into account, region did serve as a significant predictor of community structure. This would
indicate that cold and warm phases of the ENSO cycle impact the northern and southern coasts of
Ecuador differently. For instance, during a strong El Niño year, we might expect to observe
recruitment of more tropical species, as occurred in the Galápagos (Vinueza et al 2006), which
could be expected to bring about more conspicuous changes in southern sites. A comparison of
community structure values between strong El Niño and La Niña years would facilitate the
elucidation of
whether these patterns are more heavily dependent upon which current provides the majority of
propagules for settlement (high turnover), or if species are able to resist temperature fluctuations
between ENSO phases (low turnover).
Certainly, intertidal communities on the Ecuadorian coast exhibit substantial temporal and
spatial variation within a very small area (<400 km) and time frame (<1 348 year). These dramatic
differences could have important implications in the management of marine fisheries and reserves
on the Ecuadorian coast. For example, the Galera-San Francisco marine reserve, located near sites
N1-N3, might require different management tactics than the Machililla National Park, located near
sites S6-S8. In addition, the management of Ecuador’s major near shore artisanal fisheries, namely
billfishes, lobster, and demersal fishes, must take into account seasonal fluctuations in marine
currents (Castleberry & Riebensahm 2011). A large portion of Ecuador’s coastal rural population
work in these fisheries, which have few regulations in place or supporting technology to reinforce
long-term stability (Guest 2003). As current patterns fluctuate, they bring unique nutrient and
temperature conditions as well as larval supply, which may favour certain species over others
(Alheit & Niquen 2004). By referencing this information, policy-makers can better predict the
response of each species to harvesting and make management decisions accordingly.
We also observed an extremely high level of removal of intertidal organisms at our study
sites, including predatory snails, chitons, limpets, octopus, and fish. This removal was higher at
sites close to human populations, and as many as 500 individuals were observed to be collected per
site during a single low tide (pers. obs.). This could produce significant changes in community
structure, which would be expected to vary based on location. At northern sites especially, where
consumer-driven processes could be predicted to have a stronger impact in governing community
structure (Menge et al. 1986, Vinueza 2009) due to the predominance of the NECC, the absence of
these consumers could affect species dominance patterns. This could have important implications,
since the demersal habitat in intertidal communities is effectively bio-engineered by primary space
occupiers such as algae and sessile invertebrates (Jones et al. 1994, de Juan & Hewitt 2011).
Ocean temperatures and productivity levels along the western coast of South America may
experience even greater levels of variation as the global climate continues to change. Globally, sea
surface temperatures have risen by 0.6°C over the past 100 years (Pachauri 2007). In addition, most
climate change models predict stronger and more frequent ENSO events in coming decades (IPCC
2001). Oceanographic conditions are very strong drivers of community structure (Broitman et al.
2001), and are susceptible to large-scale variation driven by forces such as ENSO and climate
change (Wang and Fiedler 2006). Climate change may also affect basic water chemistry
components such as dissolved oxygen concentrations and pH (Harley et al. 2006), which can have
profound impacts on the structure and functioning of local marine communities (Przeslawski et al.
2008). Long-term monitoring of oceanographic conditions and ecological responses along the coast
of Ecuador may serve as an indicator for how climate change affects ENSO phenomena and marine
ecological relationships, and how these impacts differ between tropical and sub-tropical
communities.
Our study has produced many new questions that need answering in order to better
understand the ecological processes at work along the continental coast of Ecuador.
For instance, given the complex and often site-specific interactions between herbivores and
nutrients in determining algal community structure (Burkepile & Hay 2006), what role are
herbivores playing in the patterns we have described here? How do bottom-up and top-down
processes control community structure as compared to the patterns observed in Peru, Galápagos,
and Panama? How does the removal of molluscs and fish through collection by local inhabitants
affect intertidal community structure? Certainly, the continental coast of Ecuador presents a number
of intriguing opportunities for ecological research, and merits increased attention from the scientific
community.
Acknowledgements
We would like to thank the Rufford Small Grants Foundation, the Universidad San Francisco de
Quito, and the Pontificia Universidad Católica for funding this study, and A. Encalada and the
Laboratorio de Ecología Acuático (Universidad San Francisco de Quito) for the use of their
laboratory space. We would also like to thank W. Goodell, M. Hirschfeld, J. Montalvo, F. Ordoñez ,
and GAIAS students from the Methods of Marine Research Module for assistance in the field and
laboratory, and D. Johnson, M. Frenock, and A. Barragán for assistance with data analysis. Finally,
we would like to thank the Parque Nacional Machalilla and Reserva Marina Galera-San Francisco
for granting access to our study sites.
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