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Revista de biología marina y oceanografía

On-line version ISSN 0718-1957

Rev. biol. mar. oceanogr. vol.51 no.1 Valparaíso Apr. 2016

http://dx.doi.org/10.4067/S0718-19572016000100022 

 

NOTA CIENTÍFICA

Comparison of zooxanthellae densities from upside-down jellyfish, Cassiopea xamachana, across coastal habitats of The Bahamas

Densidad de zooxantelas presentes en la medusa invertida, Cassiopea xamachana, en los hábitats costeros de Las Bahamas

 

Elizabeth W. Stoner1,2, Serina S. Sebilian1,3 and Craig A. Layman1,4

1Department of Biological Sciences, Florida International University, 3000 N.E. 151st Street, North Miami, Florida 33181, United States of America. betsy.stoner18@gmail.com
2Current Address: Loxahatchee River District, 2500 Jupiter Park Drive, Jupiter, FL 33458, USA
3Current Address: Presidio Trust, 1216 Ralston Avenue, San Francisco, CA 94129, USA
4Current Address: Department of Applied Ecology, North Carolina State University, Raleigh, NC 27695, USA


ABSTRACT

Anthropogenic disturbances may drive jellyfish blooms, and previous studies have suggested this is the case for upside-down jellyfish (Cassiopea xamachana). Cassiopea were found to have higher mean zooxanthellae densities in human-impacted areas on Abaco Island, The Bahamas, suggesting that nutrient loading in impacted sites may be one factor driving zooxanthellate jellyfish blooms. Gut contents from Cassiopea medusae were positively correlated to zooxanthellae densities, indicating that heterotrophically-derived nutrition may be an important factor in facilitating increased zooxanthellae population densities. Understanding the mechanisms driving jellyfish blooms is crucial for developing effective management strategies in impacted coastal ecosystems.

Key words: Benthic, facilitation, human impacts, heterotrophy, mutualism


INTRODUCTION

Jellyfish blooms may be increasing in both magnitude and frequency in certain parts of the world since the 1970s, likely due to various anthropogenic disturbances (Condon et al. 2013). Some of the main drivers for jellyfish blooms include nutrient loading, overfishing, global climate change, development of artificial marine structures, introduction of nonindigenous jellyfish species, and sedimentation (Graham et al. 2001, Brodeur et al. 2008, Hoover & Purcell 2009, Condon et al. 2012, Purcell 2012, Riisgard et al. 2012, Stoner et al. 2014). Recently, Stoner et al. (2011) suggested that populations of the benthic, zooxanthellate upside-down jellyfish, Cassiopea spp. Péron & Lesueur, 1810, are larger and more abundant in human-impacted coastal systems in The Bahamas. This pattern suggests that human activity may be initiating or facilitating blooms of this relatively little-studied epibenthic jellyfish.

One mechanism suggested to contribute to Cassiopea spp. blooms in anthropogenically-disturbed habitats may be increased nutrient availability, driving higher zooxanthellae densities in jellyfish tissues (Stoner et al. 2011). Because zooxanthellae are nutrient limited (by both nitrogen and phosphorus), increased nutrient supply may result in increased primary production, thereby providing higher levels of photosynthate (i.e., autotrophic nutrition) to their hosts (Muscatine et al. 1989, Falkowski et al. 1994, Koop et al. 2001). Higher zooxanthellae densities may enhance host growth and fitness, as has been well-documented in coral reefs (Muscatine & Porter 1977, Berkelmans & van Oppen 2006, Yellowlees et al. 2008).

In this study, we explored whether there was a difference in zooxanthellae densities from Cassiopea xamachana Bigelow, 1892 (hereafter Cassiopea) between anthropogenically-disturbed and relatively-pristine coastal sites on Abaco Island, The Bahamas. It was hypothesized that zooxanthellae densities in the tissue of Cassiopea would be higher in sites adjacent to human population centers, likely as a function of elevated nutrient concentrations.

 

MATERIALS AND METHODS

This study was conducted in nearshore habitats on Abaco Island, The Bahamas, from June to July 2011. Study sites were located within mangrove wetlands, embayments, or low energy coastlines < 2 m in depth at low tide. All sites were characterized by silty-sandy sediment (~0.05 mm particle size, as classified by the USDA soil classification triangle; Schoeneberger et al. 2002), which suggests low localized water velocities. Following Stoner (2011), sites were categorized a priori as being adjacent to high or low human population
densities. The number of buildings (the proxy for human impact) within a 3 km radius from the mid-point of each site was estimated using Google Earth v. 5.1 (Google Inc. 2010). High human population density sites (hereafter referred to as HP sites) had a mean number of 563 residential buildings (range of 84-1712 buildings; Little Harbour, Marsh Harbour, Treasure Cay, Cherokee and Little Abaco South), while low human population density sites (hereafter referred to as LP sites) had a mean number of 4 residential buildings present (range of 0-10 buildings; Snake Cay, North Bight of Old Robinson, Twisted Bridge, and Little Abaco North) (Stoner et al. 2011).

For each site, 15 jellyfish between 8 to 10 cm in bell diameter were collected. Cassiopea of this size were comparable to the range of bell diameters of Cassiopea examined for zooxanthellae densities in previous studies (Table 1). All jellyfish had 8 oral arms with no tears or deformities on the bell, as any injury to the animal may affect zooxanthellae population densities or the ability of the animal to acquire prey. To enumerate zooxanthellae densities, we first selected the `outpocketings' or secondary and tertiary mouths from the primary oral arms following protocol outlined by Estes et al. (2003). We chose oral arms as they have been found to have the highest zooxanthellae densities in C. xamachana (Estes et al. 2003). Oral arms were then homogenized using a mortar and pestle. We extracted 10 µl of jellyfish homogenate, which we added to 1 ml of seawater and mixed for 45 s using a vortex. Zooxanthellae densities in each sample were determined from 3 aliquots (10 µl per sample), which were viewed using a Neubauer hemocytometer under a plain light microscope at 400x. Zooxanthellae density data were averaged across replicates per specimen for each site. Zooxanthellae density across LP and HP sites were analyzed using a nested univariate analysis of variance (ANOVA) with site nested within disturbance regime (i.e., HP and LP sites) (IBM SPSS v. 20.0).

 

Table 1. Comparison of reported zooxanthellae density values (cells g-1 ww) from
Cassiopea
xamachana medusae sampled in the Florida Keys and The Bahamas
Tabla 1. Comparación de las densidades de zooxantelas (células g-1 ww) de
Cassiopea xamachana
muestreada en Florida Keys y Las Bahamas

 

Nutrient concentrations (NH4+, total phosphorus, and %P) were evaluated to elucidate whether elevated nutrients may be a potential driver in changes to zooxanthellae populations from Cassiopea in human-impacted sites. To analyze ammonium (NH4+) concentrations, water samples were collected and filtered with 0.45 µm nylon membrane filters. Unfiltered water samples were also collected for total phosphorus (TP) analysis in acid rinsed HDPE bottles, placed on the dark on ice, and stored in the freezer until analysis. In addition, %P was also analyzed from seagrass tissue, as nutrients from seagrass may reflect nutrient availability in a system over a longer time period (i.e., weeks), whereas ambient water nutrient concentrations represent a `snapshot' of nutrient concentrations in a given system (Allgeier et al. 2010, Stoner et al. 2011). To analyze blade tissue %P, Thalassia testudinum K.D. Koenig, 1805 (turtle grass) leaves were harvested, then scraped to remove epiphytes and dried at 80°C for 48-72 h. Dried seagrass was ground into a fine powder, and both water (TP) and seagrass (%P) samples were analyzed using dry oxidation acid hydrolysis extraction in addition to the use of a colorimetric analysis (Fourqurean et al. 1992). Ammonium samples were processed using the Indophenol blue method in addition to the use of the colorimetric analysis.

Gut content weight (i.e., the dry weight of food in the gut) was also examined, as we wanted to explore the potential relationship between zooxanthellae densities and the amount of food that individual Cassiopea had consumed. It has been suggested that heterotrophically-derived nutrition may affect zooxanthellae densities and cell division as a result of increased energy translocated to the symbionts (McAuley & Cook 1994, Szmant-Froelich & Pilson 1984). In other words, nutrients acquired heterotrophically may be utilized by the zooxanthellae, potentially stimulating zooxanthellae productivity. Gut contents were removed from the stomach of each jellyfish by carefully removing the bell from the oral arms and extracting any food items present. Gut contents were then analyzed to obtain wet and dry weight for each specimen. Gut content dry weight across LP and HP sites was analyzed using a nested ANOVA (IBM SPSS v. 20.0). Pearson correlations (bivariate) were then run to evaluate the relationship between mean zooxanthellae densities, mean gut dry weight (g d-1) and nutrient concentrations across sampling locations (IBM SPSS v. 20.0).

 

RESULTS AND DISCUSSION

Mean zooxanthellae densities from both site types (HP and LP) were found to be somewhat lower than previously reported for Cassiopea (Table 1). We found a significant difference between zooxanthellae densities between LP and HP sites (nested ANOVA, F8,125= 8.0, P < 0.001; Fig. 1) in which the mean zooxanthellae density from LP sites was 2.3 x 106 ± 1.6 (cells g-1 ww), while the mean zooxanthellae density from HP sites was 3.3 x 106 ± 1.90 (cells g-1 ww). Cherokee, an HP site, had the highest zooxanthellae density (9.64 x 106 cell g-1 ww) and North Bight (an LP site) had the lowest zooxanthellae density (3.54 x 105 cell g-1 ww). Zooxanthellae densities were found to be negatively correlated to %P concentrations in seagrass tissue (Pearson bivariate correlation, r= -0.40, P = 0.003; Fig. 2C), but were not correlated to water column nutrient concentrations (Figs. 2A, B).

 

Figure 1. Mean (± SE) gut content dry weight values from Cassiopea xamachana medusae (A) and
mean (± SE) zooxanthellae density values (B) collected from relatively-pristine sites
(black bars) and human-impacted sites (grey bars) on Abaco, The Bahamas
Figura 1. La media (± EE) para el peso seco del contenido del tracto digestivo en la medusa Cassiopea
xamachana
(A) y la densidad media (± EE) de zooxantelas (B) recogidas de los sitios relativamente
pristinos (barras negras) y los sitios impactados por actividades humanas
(barras grises) en Abaco, Las Bahamas

 

Figure 2. Correlations between zooxanthellae densities and (A) ammonium concentrations in water,
(B) total phosphorus concentrations in water, and (C) percent phosphorus in
Thalassia testudinum
tissue. r= Pearson correlation coefficient and
P =
p-value for Pearson correlation. A trendline is included
for correlations where P < 0.05
Figura 2. Correlaciones entre las densidades de zooxantelas y (A) concentraciones de amonio en agua,
(B) concentraciones de fósforo total en el agua, y (C) porcentaje de fósforo en el tejido de
Thalassia testudinum
. r= coeficiente de correlación de Pearson y P= valor p
de correlación de Pearson. Una línea de tendencia se
incluye para correlaciones P < 0,05

 

Mean dry gut content weight was not different between HP and LP sites (nested ANOVA, F8,125= 1.4, P= 0.19; Fig. 1); however, the highest gut content weight (0.02 g per jellyfish) came from an HP site (Marsh Harbour). There was a significant positive correlation between zooxanthellae densities and gut content weight (Pearson bivariate correlation, r= 0.26, P= 0.003). Neither zooxanthellae densities nor gut weight values in jellyfish were correlated to jellyfish bell diameter (Pearson bivariate correlation, r= -0.35, P= 0.39 and r= -0.34, P= 0.39, respectively).

Our results suggest that mean zooxanthellae densities from Cassiopea medusae are elevated in disturbed nearshore systems compared to systems with little to no anthropogenic activity. Anthropogenic disturbances in coastal areas of The Bahamas have been shown to lead to increased densities and size of Cassiopea (Stoner et al. 2011). Herein we extend these findings by showing that some nearshore, impacted areas also may be related to higher densities of zooxanthellae in Cassiopea tissue, a potential mechanism driving Cassiopea blooms. Jellyfish tissues from Abaco had lower zooxanthellae densities than medusae collected from the Florida Keys (Table 1; Vodenichar 1995, Verde & McCloskey 1998, Estes et al. 2003). The Florida Keys are more heavily populated than Abaco, so it is conceivable that higher zooxanthellae densities from Florida Cassiopea reflect increased nutrient availability derived from human activities.

Correlations between ambient nutrient concentrations (NH4+ and TP) and zooxanthellae densities were not observed. We did, however, find a negative correlation between %P of seagrass and zooxanthellae densities. It is unclear what mechanism may drive this correlation, but competition between jellyfish and seagrasses is one possibility (e.g., zooxanthellae rapidly uptake nutrients, reducing nutrient availability to other autotrophs). Nevertheless, because of the complex nature of coastal ecosystems in The Bahamas and the scarce knowledge of the ecological relationships between biological components, it is clear that more work is needed to elucidate the extent to which nutrients are responsible for elevated zooxanthellae densities in HP sites.

Elevated zooxanthellae densities may also be an indirect function of heterotrophically-derived sources of nutrition (e.g., external food resources for jellyfish). Although we did not detect a difference in gut weight between LP and HP sites, we did find that there was a strong, positive, correlation between zooxanthellae densities and gut weight. This is consistent with the idea that increased heterotrophically-derived nutrition may stimulate zooxanthellae population growth. It is also possible that higher ambient nutrient concentrations may support greater zooplankton biomass in some human impacted coastal areas, providing a readily available food source for jellyfish.

In some parts of the world, jellyfish blooms are increasing; however, little empirical evidence exists to support specific mechanisms driving these blooms in human-impacted environments (Condon et al. 2013). Our results suggest that nutrient loading is possibly one of the main drivers of jellyfish blooms in nearshore regions of The Bahamas. Bloom events of Cassiopea, in which hundreds of individual jellyfish aggregate, may have severe consequences on ecosystem processes in seagrass beds. For example, high Cassiopea densities have been shown to drastically reduce seagrass densities and shift benthic community composition (Stoner et al. 2014a, b). Understanding the mechanisms that drive jellyfish blooms is crucial for developing effective coastal management strategies where these events are a recurring problem.

 

ACKNOWLEDGMENTS

This study was funded by the Environmental Protection Agency Science to Achieve Results (STAR) fellowship, NSF OCE #0746164 and OCE #1405198, and Florida International University. It was conducted as part of a National Science Foundation Research Experience for Undergraduates. We thank Friends of the Environment for logistical support. The Vega-Thurber lab, Joseph Peters, and Jim Richard assisted with sample processing. We thank Sean Giery, Lauren Yeager, and two anonymous reviewers whose comments greatly improved the quality of this manuscript.

 

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Received 27 August 2015 and accepted 18 January 2016
Editor: Claudia Bustos D.

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