Multi-Year Changes of a Benthic Community in the Mid-Intertidal Rocky Shore of a Eutrophic Tropical Bay (Guanabara Bay, RJ
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Estuarine, Coastal and Shelf Science 226 (2019) 106265 Contents lists available at ScienceDirect Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss Multi-year changes of a benthic community in the mid-intertidal rocky shore T of a eutrophic tropical bay (Guanabara Bay, RJ – Brazil) ∗ Camila A. Pugaa, , Arthur S.S. Torresa, Paulo Cesar Paivab, Yocie Yoneshigue-Valentinc, Andrea O.R. Junqueiraa a Departamento de Biologia Marinha, Laboratório de Bentos, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil b Departamento de Zoologia, Laboratório de Polychaeta, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil c Departamento de Botânica, Laboratório de Botânica Marinha, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil ARTICLE INFO ABSTRACT Keywords: Intertidal zone of rocky shores is influenced by a wide variety of abiotic and biotic drivers. These variables can Rocky shore affect the species abundance at different temporal scales. In the present study our goal was toevaluatethe Benthic community community changes over the years using different temporal scales (fortnightly, monthly, seasonal and annual) asa Temporal variation tool to understand the effects of biotic (i.e. competition or facilitation) and abiotic drivers (i.e. water temperature, Bioinvasion air temperature, tidal regime, rainfall and water quality) in abundance pattern of dominant species (Crassostrea Guanabara bay rhizophorae, Saccostrea cuccullata, Tetraclita stalactifera and Amphibalanus amphitrite). The samples were seasonally Monitoring carried out in the mid-intertidal zone in the Boa Viagem Beach in Guanabara Bay over 7 years (2010 July - 2017 June). From June 2015 to June 2017 fortnightly samplings were made in addition to seasonal sampling. The inter- annual scale was the main scale in which the differences in the percent cover of the benthic community wasnoted (pseudo-F = 15.96, p = 0.0001). Hierarchical ANOVA indicated that for the dominant species only the annual scale was significant while to the cryptogenic macroalgae Ulva spp. only the seasonal scale. Among the environ- mental variables selected, dbRDA indicated 6 of them that were significantly relevant to percent cover variation of all species explaining 86,61% of data variation (p < 0.05). While C. rhizophorae e S. cucullata and T. stalactifera exhibited similar response to the relevant environmental variables, A. amphitrite exhibited opposite response to these variables. The species responded to abiotic drivers in different temporal scales. Water temperature was avery important variable, but its effect in the population dynamics of these long-lived species needs long time scales(60 days) to manifest responses at detectable levels as well as the biotic interactions, such as competition, and the effects of bioinvasion. The niche overlap observed among S. cucullata and C. rhizophorae with A. amphitrite was highly significantly (p < 0.001) (i.e.,negative SES). Conversely for the oyster species the observed niche overlapis greater than the niche overlap expected by chance (i.e., SES positive). Environmentally constrained null model approach showed a significant (p = 0.004) relationship only between A. amphitrite and S. cucullata (C-score obs = 1200; C-score exp = 716.6), indicating a negative association. During this long and continuous monitoring, we verified that each environmental variable affects the same species at distinct temporal scales, affectingalso some biotic interactions (S. cucullata × A. amphitrite) and consequently the community structure. 1. Introduction indicators because they are composed of sessile organisms, most of them filter-feeders. The intertidal zone of rocky shores is influenced by Rocky shore benthic communities are one of the most productive a wide variety of abiotic and biotic drivers such as tidal regime, in- marine environments since a great part of its biomass is represented by creasing air exposure, wave action, anthropogenic impacts, changes in macroalgae and microphytobenthos which have great importance to temperature and in the frequency of storms, predation, competition and the primary productivity of this area (Mann, 1973). This ecosystem is introduction of exotic species (Thompson et al., 2002; Murray et al., home to many economically important groups, such as bivalves 2006). These factors and the interaction among them are responsible (Davenport and Wong, 1992; Douillet and Langdon, 1994). These for the non-homogeneous patterns of population distribution in the benthic communities are also considered quite suitable biological intertidal zone (Murray et al., 2006; Zamprogno et al., 2012). All these ∗ Corresponding author. E-mail address: [email protected] (C.A. Puga). https://doi.org/10.1016/j.ecss.2019.106265 Received 31 August 2018; Received in revised form 29 January 2019; Accepted 23 June 2019 Available online 28 June 2019 0272-7714/ © 2019 Elsevier Ltd. All rights reserved. C.A. Puga, et al. Estuarine, Coastal and Shelf Science 226 (2019) 106265 different processes can affect the species distribution at different tem- Crassostrea gigas (Thunberg, 1793) and the indigenous Saccostrea glo- poral scales (Benedetti-Cecchi et al., 2000). Thus, only through long merata (Gould, 1850) increased with a large initial population, regardless and continuous monitoring that it is possible to identify patterns of of the species identity (Hedge and Johnston, 2014). This result could species distribution and how the interplay of abiotic and biotic drivers indicate a facilitation process, i.e., an interaction that can expand the affects them (Benedetti-Cecchi et al., 2000; Junqueira et al., 2000; realized niche of the facilitated species through of ameliorating abiotic Zamprogno et al., 2012). stresses (Bulleri et al., 2016). This interaction is very common among The importance of long-term studies to verify biotic responses was benthic organisms and it is well established in the literature. Most of highlighted by Hampton and Schindler (2006), since these take more time them are ecosystem engineers which can increase habitat complexity and to manifest responses at detectable levels. Mazzuco et al. (2015) state that heterogeneity (Sousa et al., 2009; Pereyra et al., 2017). the temporal replication over time series is a valuable tool for investigating Many researchers tried to evaluate the temporal changes of benthic relationship between ecological processes and environmental variables. In communities (Teixeira et al., 1987; Pagola-Carte and Saiz-Salinas, 2000; this context, the temporal replication in different time scales decreases the Taouil and Yoneshigue-Valentin, 2002; Zamprogno et al., 2012), but just a “background noise” in addition to facilitating the distinction among nat- small part of these studies does it in a continuous way. There are two very ural responses from those caused by anthropic activities or climate common types of temporal studies: those that are single or infrequent changes (e.g. El niño) (Underwood and Chapman, 2005). Environmental (‘one-off') or those that are frequent during a small period of time, butthat conditions are also important drivers in the pattern of distribution of the are not repeated in a yearly basis (‘snapshot’) (Hawkins and Hartnoll, species, since they influence animal behavior and most of the physiolo- 1983; Franke and Gutow, 2004). Both of them are only useful to identify gical characteristics which may cause responses in distinct intensity and major changes in community dynamics, following dramatic changes, such time lag. According to the level of benthic species resistance or sensibility as hot summers or cold winters. However, this type of sampling is in- to abiotic variables, it is possible to infer the environmental conditions. efficient to detect more subtle changes or delays in species response tothe Temperature can impact the performance and survival of marine organ- environmental conditions. In other words, the lack of temporal replication isms (Zamprogno et al., 2012). In marine bivalves this environmental may hinder the distinction between natural variation from those resulting condition can influence most ecological, biological and physiological as- from a particular event (Murray et al., 2006). pects (Cáceres-Puig et al., 2007). While for oyster species such as Saccos- Although, monitoring studies in rocky shore benthic communities trea cuccullata (Born, 1778) the low temperature decreases the embryonic have been given more importance, there still exists a huge knowledge development, for the barnacle species Tetraclita stalactifera (Lamarck, gap in this sort of studies (Franke and Gutow, 2004; Nicoletti et al., 1818) it may increase the density of larvae (Kalyanasundaram and 2007; Jung et al., 2017). A wide problem in several long-term studies is Ramamoorthi, 1986; Skinner and Coutinho, 2002). Other environmental the lack of continuous monitoring. Most of the surveys that are titled as conditions can cause different biotic responses, for instance, Ulva lactuca long-term studies just compare two short-term samplings or even mere Linnaeus, and Amphibalanus amphitrite (Darwin, 1854) are known as im- one-off sampling over different periods at the same place(Taouil and portant indicators of eutrophication, since they have more resistance to Yoneshigue-Valentin, 2002; Oliveira and Qi, 2003; Franke and Gutow, deal with high levels of pollution (Shalla et al., 1995; Fletcher, 1996; 2004; Nicoletti et al., 2007). This type of comparison may