Non-predatory mortality of planktonic copepods in a reef area influenced by estuarine plume
Introduction
Zooplankton are of fundamental importance for marine food chains because they are responsible for the predatory control of phytoplankton and for transferring energy to the subsequent trophic levels (Jones and Henderson, 1987), such as benthic organisms (Coma et al., 1999; Houlbrèque et al., 2004) and several planktivorous fish, which directly require this food source (Hamner et al., 2007). In terms of abundance, zooplankton are mainly represented by copepods (Dressel et al., 1972), which, in addition to facilitating the transfer of carbon through classic chains, can generate dissolved organic matter for bacterial communities, which in turn serves as food for other organisms in the microbial chain (Vargas et al., 2007). Another form of participation of copepods in the marine food chains occurs through deceased carcasses, which can be available in the environment for several days in the water column and follows three routes: (i) becoming food for necrophagous animals, (ii) serving as a carbon source for the microbial loop, or (iii) sinking and increasing the benthic chains (Elliott et al., 2010).
For copepods, one of the main factors that acts on population dynamics is mortality (e.g., Mauchline, 1998), which may be of predatory or non-predatory origin; although the latter has been poorly evaluated in studies, it is as relevant as the first and results in the disposal of a significant number of carcasses in the environment (Tang et al., 2006). Non-predatory mortality results from the natural aging of organisms, diseases or physical and chemical environmental stresses (reviewed by Tang et al., 2014). Methodological difficulties in differentiating the in situ contributions of the groups of living and dead individuals has led to the widespread lack of knowledge of the occurrence of non-predatory mortality (Martínez et al., 2014). However, a technique using neutral red dye was developed by Dressel et al. (1972) that identifies the proportions of living and dead individuals. Recently, this technique was improved and adapted by Elliott and Tang (2009) to apply this method to newly collected samples in situ. Adopting this method, researchers evaluated non-predatory mortality in various environments, relating it to potential causes and describing the importance of the occurrence of carcasses in marine systems (Elliott et al., 2010; Elliott and Tang, 2011b; Martínez et al., 2014). Since then, it has been proven that not considering carcasses in ecological studies in the copepod community can lead to errors in results and interpretations, as previously reported for secondary production by Yáñez et al. (2018).
Estimating non-predatory mortality in situ leads to understanding its spatial and temporal patterns, in addition to establishing the relationship of the causes to the influencing agents (Kimmerer et al., 2018). Recent studies have shown that the non-predatory mortality of copepods may differ in relation to the contributions of carcasses from different stages of life, with the nauplii constituting higher percentages of the carcasses because this stage is generally more vulnerable to non-predatory mortality than later stages (Elliot and Tang, 2011b). In general, the contributions of different types of copepod carcasses are highly variable and are most often influenced by environmental variables (Di Capua and Mazzocchi, 2017; Elliot and Tang, 2011a; Martínez et al., 2014). Seasonal changes can also influence and result in high non-predatory mortality values during winter, as previously recorded in estuarine environments (Giesecke et al., 2017). Carcasses that are disposed of in the environment can participate in the vertical flow of material (Giesecke et al., 2019) and possibly in the horizontal flow to other systems since zooplankton are an important component exported from estuaries in terms of biomass, and a considerable portion of the living plankton are exported (Melo Júnior et al., 2007). However, no study to date has concentrated on evaluating the non-predatory mortality in areas with estuarine plumes, especially in areas with tropical reefs.
Due to their high productivity, estuaries can become exporters of organic carbon in the form of nutrients, particulate debris and organic matter for adjacent coastal systems (Odum, 1980). The export from estuaries occurs through estuarine plumes (Morris et al., 1995), which are formed by a mass of water ejected from the estuary that extends into the superficial layer of the sea due to its lower density compared to that of salt water for a period of hours, depending on the tidal dynamics and river flow, until waters become mixed (Garvine and Monk, 1974). The water in estuarine plumes is characterised by a high amount of dissolved organic carbon compared to waters in coastal regions (Wu et al., 2017) and may differ in the composition and abundance of organisms compared to those of marine waters (Kingsford and Suthers, 1994). In some coastal regions, estuaries may influence reef areas through their estuarine plumes due to the dynamics of the export and import of zooplankton with the waters of adjacent ecosystems (Hamner et al., 2007). Reefs are complex systems with very high marine biodiversity and are responsible for substantial protection of coastal areas (McLean et al., 2001), which are considered environments of great ecological importance and provide a series of resources that support the existence and maintenance of countless species of this ecosystem as well as others (Moberg and Folke, 1999). Despite the importance of reef areas, only one study considered the presence of carcasses in this ecosystem, as reviewed by Daase et al. (2014), and suggested that these carcasses resulted from incomplete consumption by their predators (see Genin et al., 1995).
In this study, the neutral red method was applied following Elliot and Tang (2009) to evaluate the percentages of carcasses of nauplii and copepodites. The non-predatory mortality rates were investigated adopting a simplified approach, which considered the percentage of the carcasses in the field and the decomposition time of carcasses (Di Capua and Mazzocchi, 2017; Tang et al., 2006) to test the hypothesis that the non-predatory mortality of copepods varies spatially in a complex mosaic of interconnected ecosystems, when the different families (in distinct life stages) are subjected to different combined hydrological conditions. Mortality in these coastal ecosystems, according to some studies (e.g., Giesecke et al., 2017; Beşiktepe et al., 2015), is expected to be dynamic and induced by distinctive environmental conditions of marine or estuarine waters. Besides, we also hypothesised that the mortality of copepods in the rainy season is increased due to the higher fluvial flow in the region, considering that the mortality of estuarine copepod families results from osmotic stress when they are subjected to diluted marine waters (e.g., Krautz et al., 2017), and vice versa when typical coastal copepod families are subjected to estuarine waters.
Section snippets
Study area
The Tamandaré Bay (8°46′07.5″S, 35°06′03.6″W) is located on the southern coast of Pernambuco, Brazil, and is influenced by the estuaries of the Ilhetas and Mamucabas Rivers, which launch their plumes into the bay, reaching the reefs found in the region (Fig. 1). The bay is located within the Conservation Unit: Environmental Protection Area “Costa dos Corais”. The reefs of the Tamandaré Bay are part of the shallow reefs that stretch across the coast of northeastern Brazil and are differentiated
Environmental data
The water temperature showed a low variation throughout the study, with values surrounding 27.6 ± 1 °C. The other environmental variables showed that there were differences between the rainy seasons and collection areas (PERMANOVA; p < 0.001). Among the seasons, lower values were observed in the dry season for rainfall (ranging from 30 to 95.7 mm), total suspended solids (37.1 ± 17.6 mg L−1), pH (7.6 ± 0.5) and dissolved oxygen (4.7 ± 1.8 mg L−1), while the rainy season recorded higher values
Discussion
The present study describes the first in situ estimates of the percentage of carcasses and the mortality rate of the planktonic nauplii and copepodites in tropical reefs influenced by an estuarine plume. The results of the present study revealed that the non-predatory mortality of copepods (in both stages, nauplii and copepodites) varies spatially in a complex mosaic of interconnected ecosystems (estuarine plume, reef and bay), showing that higher fractions of dead copepods and mortality rates
Conclusions
Non-predatory mortality varies spatially between interconnected coastal ecosystems, influenced by different combined hydrological conditions. In addition, it was demonstrated that the estuarine plume differed temporally, induced by distinctive environmental conditions considering the rainfall. The mortality of copepods in this season is increased, possibly caused by a complex combination of hydrological factors. In addition, the average percentage of carcasses was close to the minimum for
FUNDING
The present work was carried out with the support of Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Financing code 001. It was also supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq, which funded the PELD Tamandaré, Pernambuco (Brazil).
CRediT authorship contribution statement
Alef Jonathan da Silva: Conceptualization, Methodology, Validation, Formal analysis, Writing - original draft, Writing - review & editing. Pedro Augusto Mendes de Castro Melo: Conceptualization, Methodology, Writing - review & editing. Sigrid Neumann-Leitão: Conceptualization, Methodology, Writing - review & editing. Mauro de Melo Júnior: Conceptualization, Methodology, Validation, Writing - review & editing, Supervision.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgement
We would like to thank the Federal Rural University of Pernambuco (UFRPE), which assisted this study through the Research in Motion program and the Pró-Reitoria de Pesquisa e Pós-Graduação as well as the Postgraduate Program in Ecology (PPGE), which supported this work through the Brazilian Graduate Support Program (PROAP/CAPES). We would also like to thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq for financing the PELD Tamandaré: Spatial and temporal dynamics of
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Present address: Departamento de Hidrobiologia, Universidade Federal de São Carlos, São Carlos, São Paulo, 13565-905, Brazil.