Physical factors contributing to the benthic dominance of the alga Caulerpa sertularioides(Caulerpaceae, Chlorophyta) in the upwelling Bahía Culebra,north Pacific of Costa Rica
Cindy Fernández-García1*,2*,3*, Jorge Cortés1,2, Juan José Alvarado1,3 & Jaime Nivia-Ruiz1
Caulerpa sertularioides has been spreading in Bahía Culebra, a seasonal upwelling bay in the north Pacific of Costa Rica, since 2001. The survey was carried out from December 2003 to March 2005, in several locations around Bahía Culebra, located inside the Gulf of Papagayo. This study investigated spatial and temporal patterns, percent coverage, monthly growth rate, reproductive adaptations, and morphological variations of frond length and stolon diameter of Caulerpa sertularioides, at different environmental physical and chemical factors at the bay. The alga extended to depths of 23 m on a variety of substrates. The stolons extended quickly, with a maximum growth rate of 31.2 cm month-1. This alga grows mainly by fragmentation of its fronds and stolons; nevertheless it can also reproduce sexually by releasing gametes in the water column. These two modes of spreading promote the adaptation of this opportunistic species to environmental, chemical, and physical changes at this bay. At the same time the alga showed variations in the length of its fronds and stolons, adapting to conditions such as depth and season. Average percent cover and frond density increased during the dry season when the upwelling of nutrients and cold water occurs. In the rainy season the average percent cover and frond density decreased; however there was a peak in September, when high precipitation resulted in runoff into the bay of nutrient-rich waters. The morphological and physiological plasticity of C. sertularioides, in synergy with its predominant clonal propagation and sexual reproduction provided this species with a great adaptability to changes in temperature and nutrient concentration at Bahía Culebra.
Resumen ]]>
Desde el 2001 se ha observado una propagación del alga verde Caulerpa sertularioides en Bahía Culebra, zona de afloramiento costero, en el Pacífico norte de Costa Rica. El muestreo se llevó acabo entre Diciembre 2003 a marzo 2005, en varias localidades de Bahía ]]>
Caulerpa sertularioides, a diferentes factores ambientales físico-químicos en Bahía Culebra. Esta alga se extiende hasta profundidades de 23 m, en una gran variedad de sustratos. Los estolones se extienden rápidamente, con un crecimiento máximo de 31.2 cm mes-1. Esta alga se ]]>
C. sertularioides, en sinergia con su propagación clonal, proveen ]]>
Palabras clave:Caulerpa sertularioides, afloramiento costero, América Central, Bryopsidales, nutrientes, tasa de ]]>
The genus Caulerpa has 86 current accepted species (Guiry & Guiry 2011) distributed throughout the world oceans, and in Central America 8 species have been reported (Fernández-García
et al. 2011). It is a common inhabitant of intertidal and subtidal tropical and semitropical marine waters. These algae have a creeping green stolon with root-like colorless rhizoids and erect uprights called fronds (Lee 2008). Propagation of Caulerpa is mainly clonal, and its phenotypic plasticity provides an opportunity to adapt to different changes in physical environments (Sernerpont et al. 2003). Most species in the genus have been studied, mainly due to its invasive capacity and the consequent economical ]]>
et al. 2009).
The species Caulerpa sertularioides (S.G. Gmelin) Howe, 1905, is characterized by feather-like fronds, sometimes branched, with cylindrical and needle shaped branchlets 20 cm length and 1-2 cm wide (Howe 1905). This species is distributed ]]>
Caulerpa species (Scrosati 2001).
In the Eastern Tropical Pacific ]]>
Caulerpa sertularioides is distributed from the Gulf of California, Mexico (Dawson 1944) to a reported southern limit of Gorgona Island, Colombia (Schnetter & Bula-Meyer 1982). It has been reported for Mexico (Taylor 1945, Scrosati 2001), Nicaragua (Dawson 1962), Costa Rica (Fernández & Cortés 2005), Panama (Wysor 2004, Smith et al. 2010) and Colombia (Schnetter & Bula-Meyer 1982). ]]>
In the Pacific coast of Costa Rica, at Bahía Culebra, a coastal upwelling zone, this green alga has been spreading around the bay since 2001 (Fernández & Cortés 2005). As a result, C. sertularioides has become dominant with the subsequent replacement of native algae species and overgrowth on coral colonies. This has ]]>
C. sertularioides has exhibited similar bloom patterns, some of them ephemeral such in Panama (Glynn & Maté 1997) and Gulf of California (Scrosati 2001), while in Costa Rica and other localities of Panama (Fernández & Cortés 2005, Smith et al. 2010) the alga has maintained high densities over several years.
Under specific conditions Caulerpa species can easily spread and cover high percentages of the substrate (Withgott 2002). Is well-known, that the spreading of some species of Caulerpa is triggered by changes in environmental conditions such as: water temperature, an increase in nutrient concentrations and light intensity (Raven & Geider 1988, ]]>
et al. 2005). Furthermore, this factors, combined with water motion and depth, can induce variations in the morphology, which is an advantage in adapting to different environments (Ohba et al. 1992, Collado-vides & Robledo 1999, De Senerpont Domis et al. 2003, Malta et al. 2005).
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In addition the spreading of Caulerpa species is favored by intrinsic characteristics of this genus, such as toxins to avoid herbivory, morphological and physiological plasticity, asexual reproduction by fragmentation (Graham et al. 2009), rapid nutrient uptake, rapid lateral growth of stolons and ]]>
et al. 2010).
In the Gulf of California, Scrosati (2001) found that water temperature is one of the most important abiotic factors that affect growth rates of C. sertularioides. However ]]>
C. sertularioides, by analyzing the spatial and temporal coverage, density and growth rates patterns. Also to determine, if there are morphological adaptations, of fronds and stolons, in relation to environmental conditions. ]]>
Materials and methods
Study site: The survey was carried out in Bahía Culebra (10º35’N-85º40’W), located in the Gulf of Papagayo, north Pacific coast of Costa Rica, from December 2003 to ]]>
Fig. 1). The Gulf of Papagayo is highly influenced by trade winds that move southward during the dry season (December to April). These winds displace surface waters away from the coast. This results in the upwelling of cold and nutrient rich water (Brenes et al. 1995, Jiménez & Cortés 2003). During the dry season, when upwelling occurs, the mean water temperature is ]]>
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Environmental conditions: The following environmental factors were measured monthly at five sites: Islas Huevos, Playa Blanca, Punta Flor, La Penca and Isla Pelonas (Fig. 1): Salinity (‰), using a manual refractometer (ATAGO, model S/Mill-E). Temperature (ºC), measured at 30 min intervals with in situ continuous logging sensors (Stow ]]>
-1) according to Lorenzen and Jeffrey (1978). Also we calcu-lated the concentration of suspended sediments (mg l-1), collected with a 3.8 l bottle, filtered with fiberglass filters (Whatman GF/C) that were dried and weighted, and sedimentation rate (mg cm-2 day-1) measured with three sedi-ment traps at each sampling site, following the methodology of ]]>
et al. (1994) and Rog ers et al. (1994). These two last factors were measured as an indirect measurement of runoff.
Nutrients were analyzed from water samples collected with a Niskin bottle at 15 m deep, ]]>
Fig. 1). Each sample was transferred to 1 L dark bottles, which were placed in a cooler with ice. We estimated the concentration (µM) of: phosphate (PO4-3), nitrite (NO2-), nitrate (NO3-), ammonium (NH4+) and silicate (SiO4). These nutrients were measured following Strickland ]]>
To determine climatic changes, precipitation (mm), solar intensity (sun hours day-1) and wind ]]>
-1) data were obtained from the National Meteorological Institute of Costa Rica, at the Daniel Oduber Quirós International Airport Station (10º35’ N-85º32’ W, 80 m above sea level); the closest station to Bahía Culebra.
To determine the most important marine environmental factors influencing Bahía Culebra, we applied a principal component ]]>
Ecology and morphology of Caulerpa sertularioides: With a manta tow method (Rogers et al. 1994), we identified the main C. sertularioides patches in Bahía Culebra. At each site we ]]>
In order to determine morphological variations of the fronds and stolons of C. sertularioides at different depths and seasons, we collected thalli of the green alga, ]]>
et al. 1995, Dumay et al. 2002 and De Senerpont Domis et al. (2003), who found that ]]>
10 (x+1) transformed, while stolon diameter data fit a normal distribution.
Growth rate: Growth rate of C. sertularioides was estimated from stolon growth rates per month. In ]]>
measurements of re-growth stolon length at three sites in the bay (Islas Huevos, Playa Blanca and Playa La Penca: Fig. 1) were collected at approximately 4 m deep. At each site, we removed all the thali from five permanent 50 cm2 quadrats, marked with construction rods, located over a patch of C. sertularioides. After a month, we measured all the re-growth stolons inside the fixed quadrat using a caliper (±0.05 mm). Plots were cleared at the end of November 2003, February 2004 and August 2004 and were allowed to re-grow until the end of December 2003, March 2004, and ]]>
10 (x+1) transformed.
Temporal algal percent coverage and frond density: Between March 2004 and March 2005 we measured the frond density and percent coverage of C. ]]>
Fig. 1). At each site we calculated the percent coverage, as a visual estimation of how much substrate fronds and stolons cover the substrate, from five 50 x 50 cm2 quadrats permanently located over a C. sertularioides patch. From these quadrats we choose six 10 cm2 subquadrats where we counted the fronds. Finally, to determine coverage and frond density differences between sites and seasons we applied an ANOvA. Data were tested for assumptions ]]>
Results
Environmental factors: ]]>
Table 1). The rainy season begins in May and ends in October, the rainiest months of this season are September and October. The dry season extends from December to April. Relative to the rainy season, the dry season had 212 mm less precipitation, an average of three more hours of sun light and an increase of 8.8 km h-1 in wind velocity (Table 1). ]]>
According to the Principal Component Analysis (PCA), five main environmental factors explained 65.2% of the variance of the environmental conditions in Bahía Culebra from March 2004 to March 2005. Nitrate, phosphate and suspended sediments (PC1) contributed 26.7% of the variance, while sedimentation rate contributed 22.5% (PC2) and temperature contributed 16.0% (PC3) (Fig. 2). Of these factors, only the mean temperature was significantly different between seasons (F1,11 = 12.099, P < 0.005).
Water temperature exhibited high season-ality, showing decreased temperatures in the dry season, when the wind velocity increased, producing a displacement of the thermocline to the surface and coastal upwelling (Table 1, Fig. 3A). The lowest temperature was recorded in March 2004 (22.9°C, dry season), while the highest was recorded in September 2004 (29.6°C, wet season). Salinity was higher during the dry season (34.3‰) and lowest (30.0‰) during the rainy season (Table 1). The highest chlorophyll a concentration (3.8 µg l-1) was recorded in October (wet season) (Table 1). Suspended sediments showed similar fluctuation patterns to precipitation during the wet season, when streams and rains carry sediments and nutrients into the sea (Table 1, Fig. 3A). Sedimentation rates were less variable than suspended sediments (Table 1, Fig. 3A).
Nutrient concentration differed between seasons. Average phosphate, nitrate and ammonium were higher in the dry season, while average silicate and nitrite were higher during the wet season (Table 1). However, nutrient concentrations were highly variable within seasons. phosphate increased in December 2004 (PO4-3=1.45) and September (PO4-3=0.69 µM), while nitrate was higher in December 2004 (NO3-1=15.6 µM) (Fig. 3B)
Ecology and morphology of Caulerpa sertularioides: We found C. sertularioides ranged in Bahía Culebra from the intertidal zone to 23 m deep. It was present on different substrates (rocks, sand, and live and dead corals) forming patches that can cover 6 ha. The greatest coverage (~90%) was observed in sites between 3 to 6 m deep, where we found 108 fronds 10 cm-2. However, at depths >12 m, the coverage and frond density decreased, and only isolated stolons were observed.
We also observed some algal patches simultaneously releasing gametes (Fig. 4A) at Punta Flor at 07:40 a.m., on January 3rd 2005 (Fig. 1). After gamete releases finished, all stolons and fronds turned white (Fig. 4B). This signal was later used to recognize other spawning events. Thus, most spawning events were observed in months when water temperature changes occured (February 2004, January 2005) and rain intensity was high (October 2004).
Caulerpa sertularioides showed different frond lengths at different depths (Fig. 5). The average stolon diameter of all the thalli measured was 0.18 mm (Min=0.04 mm, Max= 0.34 mm), while frond length average was 5.3 cm (Min=0.79 cm, Max= 15.9 cm). Stolon diameter was larger at 5 m than 2 m depth (F2,1055 = 9.5, P < 0.000), while fronds were significantly longer at greater depths (F2,985 = 116.8, P <0.000) (Fig. 5).
Growth rate: Mean stolon growth rate was 11.7 ± 6.2 cm month-1, minimum in December 2004 (1.4 cm month-1) and maximum in September 2004 (33.2 cm month-1, Fig. 5). Significant differences were found between the stolon growth rates during the three sampling months (F2,144 = 5.797 p<0.004), mainly between March and September 2004 (Fig. 6).
Temporal algal percent coverage and frond density: Average percent coverage and frond density had similar dynamic patterns throughout the sampling time (Fig. 7). During the wet season the values of cover percentage tended to be <40%, however in September 2004 we documented a peak of 46.3%, while the frond density during those months was <29.5 fronds 10 cm-2. After November bothparameters increase continuously until they reach the maximum values at February 2005, 70.7% cover and 50 fronds 10 cm-2, dropping in March to less than 20% of cover and 20 fronds 10 cm-2 (Fig. 7).
The average percent cover (F5,183=7.9, p<0.0001) and frond densities (F5,183=13.5, p<0.0001) were statistically different between seasons (Fig. 8), being higher during the dry season (Fig. 8A and 8B). Also we found differences in coverage (F5,183=12.1, p=0.02) and frond density (F5,183=20.5, p<0.03) values, between sites. Playa Blanca exhibited the highest percent coverage and frond density values while Isla Huevos showed the lowest values (Fig. 8A). When comparing seasons, we found higher during the dry season (Fig. 8B).
Discussion
Caulerpa sertularioides is a native alga from the Pacific coast of Costa Rica, but since 2001 its abundance and growth rate have increased, colonizing a wide range of substrates and depths at Bahía Culebra (Fig. 9). In fact, we documented the greatest depth (23 m) reported for the species. In the Pacific coast of Panama, C. sertularioides grows from the intertidal zone to 16 m (Wysor 2004), while in Colombia, it grows to 1 m deep (Schnetter & Bula-Meyer 1982). In the Caribbean and Central Pacific, C. sertularioides grows in reef habitats to a depth of 10 m (Littler & Littler 2000, 2003). However, C. sertularioides has not been found as deep as other Caulerpa species, such as C. taxifolia in the Mediterranean that grows from 0-30 m deep, with highest densities between 5-15 m (Belsher & Meinesz 1995). C. sertularioides at Bahía Culebra grew faster (1.1 cm day-1) than some other Caulerpa species. For example, Williams et al. (1985) reported that C. mexicana grew 1.0 cm day-1, while C. cupressoides 0.8 cm day-1, and C. prolifera 0.4 cm day-1. But slower than other Caulerpa species, such as C. taxifolia (8 cm day-1) and C. racemosa (2 cm-1day-1) (Dalton 2000), the first being one of the most invasive species of the genus. ]]>
We often observed floating C. ]]>
fronds and stolons during the study period, which suggest that local spreading is mainly driven by fragmentation of the thallus and dispersion around the bay by currents. As described by Benzie et al. (2000), C. sertularioides can has the capacity to resist high solar radiation allows its thalli to float for several days without desiccation until it reaches a substrate to grow. Once a thallus has colonized a substrate, it can easily spread, due to intrinsic characteristics of the species, such as rapid ]]>
et al. 1983, Cortés 1997, Jiménez 1998) which provide an appropriate surface that favors the attachment of the
C. sertularioides stolons and rhizoids (Dumay et al. 2002). While substrates composed by fine sediments are less likely to be colonized by C. sertularioides. Sites with the highest coverage of C. sertularioides were located adjacent to coastal development, such as hotels, human communities, boat anchorage sites as well as complex coral reef structures. At sites, such as Playa Penca, Ocotal and Playa Blanca (Fig. ]]>
), with coral reefs present, the bottom was composed of coarse sediments from fragments of dead coral (Pocillopora spp.), where the algae can attach easily.
In addition, frond and stolon morphology can adapt also to a combination of physical factors such as depth and substrate, as has ]]>
Caulerpa species (Meinesz et al. 1995). When C. sertularioides grew on rocky substrates in shallow water the stolon was thicker, this adaptation allows the alga to hold to the substrate and resist the swell. Fronds in theses shallow depths (high solar radiation) tended to be smaller, and sometimes were not present. At greater depths and in finer sediments, stolons were thinner and more ]]>
Caulerpa cupressoides, where fronds size decreased as the swell influence increased (Collado-vides & Robledo 1999). This adaptation provides (i) resistance to strong hydrodynamic forces (Collado-vides & Robledo 1999) in high energy coastal zones, and (ii) efficiency of ]]>
High genetic variability due to sexual reproduction of this opportunistic species at Bahía Culebra may promote adaptation to different environmental physical-chemical conditions (i.e depth, temperature, water motion, nutrients) (Allendorf & Lundquist 2003). This is evident at the bay, where C. sertularioides showed ]]>
Caulerpa, C. sertularioides in Bahía Culebra exhibit a synchronous release of sexual gametes and fertilization occurs in the water column. This green alga transforms all its vegetative inner content into gametes (holocarpic) that are released by papillae in the stolons and fronds (Dawes 1981, Bold & Wynne 1985, van den Hoek et ]]>
1998), leaving the cell walls empty, which make the thallus turn white (van den Hoek et al. 1998).
Bahía Culebra, as in Gulf of California (Mexico), percent coverage and frond density of C. sertularioides seasonally fluctuated ]]>
]]>
Coverage and frond density decreased 40% in March (2004, 2005), one month after the upwelling peak (Fig. 7). This is consistent with Rodríguez-Sáenz (2005) who found that phytoplankton concentration and zooplankton density decreased after upwelling in Bahía Culebra as evident with other algal biomasses (e.g. Ulva spp. and Dictyota spp., pers. observ.) ]]>
Although coverage and density of C. sertularioides decreased during some months of the rainy months when nutrients decrease, it remained covering an average of 10% of the substrate (Fig. 7). In Uva Island, Panama, Smith
et al. (2010) found that the maintenance of C. sertularioides patches, where there are no external nutrient inputs from the upwelling, is due to an association with epiphytic cyanobacteria, together with spatial refuges, suggesting mechanisms that maintain C. sertularioides near reef systems in the absence of high nutrients. Then from August to September the cover and frond density increased again when precipitation, organic material as well as ]]>
Algal frond density and cover porcentage may be related to nutrient concentration in the environment, and our study suggests that a non-natural supply of nutrients during the wet season may trigger algae overgrowth, as has ]]>
Although decreasing and increasing nutrient concentrations may have an important role in driving algal patterns, it can act in synergy with ]]>
Fig. 3). Coverage and frond density of C. sertularioides can increase with nutrient uploads, however there is a peak in the values of those measurements in February with lower temperatures, during the upwelling, than in September, during the rainy season (Fig. 7). ]]>
According to Terrados and Ros (1992) seasonal adaptations of macroalgae, are more common in temperate regions and in areas where upwelling occurs. These seasonal temperature variations can cause algal physiological adaptations in response to photosynthetic and growth requirements. At Bahía Culebra, we registered temperature differences of ]]>
C. sertularioides abundance. Other Caulerpa species, such as C. taxifolia, have demonstrated the capacity to adapt to low temperatures (Jousson et al. 2000), providing the ability for growth at deeper depths and large temperature ranges (Belsher & Meinesz 1995), thus increasing its ]]>
& Lundquist 2003). Another important factor may be the attenuation of herbivory in upwelling environments, as suggested by Floeter et al. (2005) and Smith (2008), however this factor was not measured in our study.
Acknowledgments
We are grateful to Davis Morera, Eva Salas, Bernadette Bezy, Eddy Gómez and Eleazar Ruiz for their collaboration in the field and in the laboratory. Specially thank to Bernadette Bezy for revising the English. We also want to thank the Costa Rican Institute of Tourism (ICT) by facilitating us ]]>
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*Correspondencia a: Cindy Fernández-García.Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), Ciudad de la Investigación, Universidad de Costa Rica, San Pedro, 11501-2060 San José, Costa Rica; cindy@biologia.ucr.ac.cr.Escuela de Biología, Universidad de Costa Rica, San Pedro, 11501-2060 San José, Costa Rica. Posgrado en Ciencias Marinas y Costeras, Universidad Autónoma de Baja California Sur, Carretera al sur km 5.5, La Paz, C.P. 23080, México. Jorge Cortés. Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), Ciudad de la Investigación, Universidad de Costa Rica, San Pedro, 11501-2060 San José, Costa Rica. Escuela de Biología, Universidad de Costa Rica, San Pedro, 11501-2060 San José, Costa Rica. Juan José Alvarado. Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), Ciudad de la Investigación, Universidad de Costa Rica, San Pedro, 11501-2060 San José, Costa Rica. Posgrado en Ciencias Marinas y Costeras, Universidad Autónoma de Baja California Sur, Carretera al sur km 5.5, La Paz, C.P. 23080, México. Jaime Nivia-Ruiz. Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), Ciudad de la Investigación, Universidad de Costa Rica, San Pedro, 11501-2060 San José, Costa Rica. ]]>
1. Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), Ciudad de la Investigación, Universidad de Costa Rica, San Pedro, 11501-2060 San José, Costa Rica; cindy@biologia.ucr.ac.cr 2. Escuela de Biología, Universidad de Costa Rica, San Pedro, 11501-2060 San José, Costa Rica. 3. Posgrado en Ciencias Marinas y Costeras, Universidad Autónoma de Baja California Sur, Carretera al sur km 5.5, La Paz, C.P. 23080, México.
Received 28-II-2011. Corrected 28-VI-2011. Accepted 05-III-2011.
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