Non-predatory mortality of planktonic copepods in a reef area influenced by estuarine plume

https://doi.org/10.1016/j.marenvres.2020.105024Get rights and content

Highlights

  • The percentage of carcasses and non-predatory mortality rates of copepods differed between nearby coastal areas in Brazil.

  • Between 4 and 30% of individuals from both nauplii and copepodites are carcasses.

  • The mortality rates for copepods had a maximum mean of 0.04 d−1 and higher rates were observed during the rainy season.

  • The mortality rates of some copepod families were related to high salinity and low values of chlorophyll-a, oxygen and pH.

Abstract

Although it has been proven that non-predatory mortality accounts for a large proportion of copepod mortality, there is still a lack of knowledge of the temporal and spatial patterns and influence of environmental variables on non-predatory mortality, especially in tropical areas where reefs are influenced by estuarine plumes. This study evaluated the percentage of carcasses and the non-predatory mortality rates for planktonic nauplii and copepodites in a bay with the presence of reefs under the influence of an estuarine plume, in the Atlantic tropical region. The average percentage of carcasses was less than 13% for both nauplii and copepodites, and was close to the minimum for other marine environments. However, there was a variation according to the different families and life stages of planktonic copepods. Nauplii had the highest mortality rate, with a mean rate of 0.04 ± 0.02 day−1 (maximum, 0.11 day−1), while the copepodites had a mean of 0.03 ± 0.01 day−1 (maximum of 0.06 day−1). Non-predatory mortality was higher in the rainy season, and differed between the nearby studied areas (bay, plume and reefs). Considering the three areas separately, only the estuarine plume showed higher percentages of carcass and non-predatory mortality rates of nauplii and copepodites. The increase in mortality rates for some copepod families was influenced by high salinity and low values of chlorophyll-a, dissolved oxygen and pH. These results demonstrate that the non-predatory mortality of copepods varies in a complex mosaic of interconnected ecosystems, and that the relationships between environmental variables with some groups may indicate susceptibility of different stages and families to death due to specific environmental conditions.

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

References (85)

  • F. Moberg et al.

    Ecological goods and services of coral reef ecosystems

    Ecol. Econ.

    (1999)
  • A.W. Morris et al.

    The estuary plume zone: source or sink for land-derived nutrient discharges? Estuarine

    Coast Shelf Sci.

    (1995)
  • E.P. Odum

    The Status of Three Ecosystem-Level Hypotheses Regarding Salt Marsh Estuaries: Tidal Subsidy, Outwelling, and Detritus-Based Food Chains. Estuarine Perspectives

    (1980)
  • G.S. Santos et al.

    Two new methods for sampling zooplankton and larval assemblages in tropical reef ecosystems

    J. Exp. Mar. Biol. Ecol.

    (2017)
  • C. Sedlacek et al.

    Egg production of the copepod Acartia tonsa: The influence of hypoxia and food concentration

    J. Exp. Mar. Biol. Ecol.

    (2005)
  • M.O. Soares et al.

    Oil spill in South atlantic (Brazil): environmental and governmental disaster

    Mar. Pol.

    (2020)
  • L. Svetlichny et al.

    Salinity tolerance of alien copepods Acartia tonsa and Oithona davisae in the Black Sea

    J. Exp. Mar. Biol. Ecol.

    (2014)
  • K.W. Tang et al.

    Occurrence of copepod carcasses in the lower Chesapeake Bay and their decomposition by ambient microbes

    Estuar. Coast Shelf Sci.

    (2006)
  • S. Yáñez et al.

    Copepod secondary production in the sea: errors due to uneven molting and growth patterns and incidence of carcasses

    Prog. Oceanogr.

    (2018)
  • C.A. Alvares et al.

    Köppen’s climate classification map for Brazil

    Meteorol. Z.

    (2013)
  • K.E. Arendt et al.

    Effects of suspended sediments on copepods feeding in a glacial influenced sub-Arctic fjord

    J. Plankton Res.

    (2011)
  • M.S. Barroso et al.

    Anthropogenic impacts on coral reef harpacticoid copepods

    Diversity

    (2018)
  • F. Benedetti et al.

    Identifying copepod functional groups from species functional traits

    J. Plankton Res.

    (2016)
  • Ş. Beşiktepe et al.

    Seasonal variations of abundance and live/dead compositions of copepods in Mersin Bay, northeastern Levantine Sea (eastern Mediterranean)

    Turk. J. Zool.

    (2015)
  • S.L. Bickel et al.

    Use of aniline blue to distinguish live and dead crustacean zooplankton composition in freshwaters

    Freshw. Biol.

    (2009)
  • T.S.K. Björnberg

    Copepoda

  • D. Boltovskoy
    (1999)
  • G.A. Boxshall et al.

    An Introduction to Copepod Diversity

    (2004)
  • D. Calliari et al.

    Salinity modulates the energy balance and reproductive success of co-occurring copepods Acartia tonsa and A. clausi in different ways

    Mar. Ecol. Prog. Ser.

    (2006)
  • C. Castellani et al.

    Feeding and egg production of Oithona similis in the North Atlantic

    Mar. Ecol. Prog. Ser.

    (2005)
  • E. Castro-Longoria

    Egg production and hatching success of four Acartia species under different temperature and salinity regimes

    J. Crustac Biol.

    (2003)
  • R. Coma et al.

    Prey capture by a benthic coral reef hydrozoan

    Coral Reefs

    (1999)
  • M. Daase et al.

    Non-consumptive mortality in copepods: occurrence of Calanus spp. carcasses in the Arctic Ocean during winter

    J. Plankton Res.

    (2014)
  • I. Di Capua et al.

    Non-predatory mortality in Mediterranean coastal copepods

    Marine Biol.

    (2017)
  • D.M. Dressel et al.

    Vital staining to sort dead and live copepods

    Chesap. Sci.

    (1972)
  • O.P. Dubovskaya et al.

    Estimating in situ zooplankton non-predation mortality in an oligo-mesotrophic lake from sediment trap data: caveats and reality check

    PloS One

    (2015)
  • D.T. Elliott et al.

    Simple staining method for differentiating live and dead marine zooplankton in field samples

    Limnol Oceanogr. Methods

    (2009)
  • D.T. Elliott et al.

    Influence of carcass abundance on estimates of mortality and assessment of population dynamics in acartia tonsa

    Mar. Ecol. Prog. Ser.

    (2011)
  • D.T. Elliott et al.

    Spatial and temporal distributions of live and dead copepods in the lower chesapeake bay (Virginia, USA)

    Estuar. Coast

    (2011)
  • D.T. Elliott et al.

    Dead in the water: the fate of copepod carcasses in the York River estuary, Virginia

    Limnol. Oceanogr.

    (2010)
  • H. Escobar

    Mystery oil spill threatens marine sanctuary in Brazil

    Science

    (2019)
  • (1993)
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    1

    Present address: Departamento de Hidrobiologia, Universidade Federal de São Carlos, São Carlos, São Paulo, 13565-905, Brazil.

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