Marine Pollution Bulletin xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Long-term functional changes in an estuarine fish assemblage J. Baptista a,⇑, F. Martinho a, D. Nyitrai a, M.A. Pardal a, M. Dolbeth a,b,⇑ a b
CFE – Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, Calçada Martim de Freitas, 3000-456 Coimbra, Portugal Biology Department & CESAM, University of Aveiro, Campus de Santiago, 3810-193 Aveiro, Portugal
a r t i c l e
i n f o
Article history: Received 27 December 2014 Revised 9 June 2015 Accepted 11 June 2015 Available online xxxx Keywords: Fish assemblages Estuaries Traits Hydrology Climate change
a b s t r a c t The functional diversity of the fish assemblages of the Mondego estuary was studied for a discontinuous 30-year period (1988–2012). During this time, hydrological changes occurred due to man-induced alterations and weather extremes. These changes led to alterations in the structure and function of the fish community. Species richness and functional richness decreased over time and the fish community started to explore new micro-habitats and food resources. Before severe hydrological changes, the community was dominated by pelagic, detritivorous and species with wider salinity ranges. After, the community became dominated by demersal, benthic, piscivorous and marine species. During a drought, omnivorous became increasingly important, reflecting greater possibilities of using available feeding resources. We have also found an increase in sub-tropical species throughout the years, which might be related to gradual temperature increases at a global scale. This study also confirmed estuaries as extremely important for restocking several commercial species. Ó 2015 Elsevier Ltd. All rights reserved.
1. Introduction A major breakthrough in community ecology studies has been the incorporation of functional approaches and functional diversity measures, as an elucidating tool to explore species coexistence and impacts on ecosystem functioning (Mouillot et al., 2007, 2013; Boucek and Rehage, 2014). Functional diversity refers to the functional component of biodiversity and is usually measured by species traits (Violle et al., 2007). A trait is a biological attribute, measurable at the individual level that influences the organism performance, determining the species effect on the ecosystem (i.e. effect trait) or influencing the species fitness in the environment (i.e. response trait) (Violle et al., 2007). The theory behind functional diversity may be applied to several trophic groups, and has the advantage to enable comparisons between systems that do not share similar taxonomical composition, and in an ecosystem functioning approach. For fish assemblages, functional approaches have been used for some decades in several studies identifying species’ functional guilds (e.g. species ecological, feeding guilds, Elliott and Dewailly, 1995; Elliott et al., 2007) and more recently, as part of multi-metric indices to evaluate the ecological condition of an
⇑ Corresponding authors at: CFE – Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, Calçada Martim de Freitas, 3000-456 Coimbra, Portugal. E-mail addresses: [email protected] (J. Baptista), [email protected] (M. Dolbeth).
water body, within the application of EU directives (e.g. Martinho et al., 2008; Cabral et al., 2012), and international policies, such has the Oceans policy (Australia), the Oceans Act and the Clean Water Act (Canada and USA) or the National Water Act (South Africa) (see Borja et al., 2010). However, a functional characterization of the community based on fish traits, such as the ones related to fish morphology as great potential to explore impacts of environmental disturbance in the ecosystem is high, and should be encouraged (Dumay et al., 2004; Goldstein and Meador, 2014; Mouillot et al., 2007; Villéger et al., 2010, 2012). In the present study, we explore the functional diversity of fish assemblages from an estuary that has been subjected to several disturbances related to human interference and climate change. Estuarine systems are important habitats for several fish, including several commercial marine and freshwater species that use them as a part of their lifecycle, by providing sheltered areas, plenty food availability, migratory routes and nursery grounds (Elliott and Hemingway, 2002; Elliott et al., 2007). The high productivity associated to these systems has attracted an important share of human population, which lives close to these coastal areas, benefiting from their ecosystem services, including fish production (Dolbeth et al., 2010). The major downside is that estuarine systems are particularly vulnerable to anthropogenic disturbance, which might be accentuated by the occurrence of weather extremes (Elsdon et al., 2009; Dolbeth et al., 2011; Vivier et al., 2010). Among major sources of anthropogenic disturbance with impact on the hydro-morphology of estuaries is river
http://dx.doi.org/10.1016/j.marpolbul.2015.06.025 0025-326X/Ó 2015 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Baptista, J., et al. Long-term functional changes in an estuarine fish assemblage. Mar. Pollut. Bull. (2015), http:// dx.doi.org/10.1016/j.marpolbul.2015.06.025
2
J. Baptista et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
regularization, margins embankment and dams (Vasconcelos et al., 2007; Neto et al., 2010; Nicolas et al., 2007), which might cause several changes in the fish communities (Costa et al., 2007). Climate change and the occurrence of extreme weather events, which are expected to increase in a nearby future (IPPC report, 2013), may accentuate these changes in the hydrology. As a consequence, estuarine fish assemblages composition and functioning are expected to change (Baptista et al., 2010; Dolbeth et al., 2010; Vivier et al., 2010), as a result of habitat degradation, loss of niches or by facilitated establishment of alien species, which compete for resources (Chessman, 2013). In this study, we use traits to understand the processes structuring estuarine fish assemblages, taking into account three critical periods over a 30-year study, when several hydrological changes occurred, due to hydromorphological reconfiguration of the riverbanks and occurrence of weather extremes. We were interested in understanding how the functional organization of the fish assemblage was affected by these hydrological changes, which are representative of changes occurring in most estuarine systems worldwide. For this task, we evaluate variations in the fish assemblage functional composition over a discontinuous 30-year period. Our hypothesis is that the observed hydrological changes affected fish community structure, composition and overall functioning, including its commercial importance.
2. Materials and methods
intertidal mudflats, and the downstream areas contain several seagrass meadows. The mouth of the estuary depth ranges from 8 to 13 m, and this area is influenced by both river flow and neritic waters. The Mondego estuary has undergone several anthropogenic pressures and hydromorphological transformations over the last decades (Neto et al., 2010; Veríssimo et al., 2013). From 1993 to 1997, the connection between the two arms was silted up, and the water circulating in the south arm was mainly dependent on tides and freshwater inputs from a small river, the Pranto River. The occlusion between the two arms resulted in an increase in water residence time and nutrients concentration, promoting macroalgae blooms and decrease of the seagrass coverage. During this time, the estuary showed symptoms of eutrophication, leading to a progressive decline in its environmental quality (Cardoso et al., 2010; Dolbeth et al., 2011). In 1998, a restoration plan was initiated to improve the ecological condition of the system, which consisted on the implementation of mitigation measures to decrease eutrophication and improve water circulation in the estuary (for more details see Lillebø et al., 2005; Neto et al., 2010; Dolbeth et al., 2011). In 2006, a second large-scale intervention was performed, consisting on the re-opening of the separation between the two arms, increasing the flow and reducing water residence time in the south arm (Veríssimo et al., 2013). In addition, extreme climatic events have also been observed, including floods in 2000–2001 and droughts in 2004–2005 (e.g. Baptista et al., 2010; Martinho et al., 2007; Primo et al., 2011).
2.1. Study site 2.2. Fish sampling and laboratory work The Mondego estuary (Fig. 1) is a small estuary (8.6 km2) located in the western coast of Portugal (40°080 N, 8°500 W), with an average freshwater flow rate of 79 m3 s1 (Dolbeth et al., 2010). The estuary comprises two arms, the north and the south, separated at 7 km from the shore that join again near the mouth. The two arms have distinct hydrological characteristics: the north arm is deeper with 5–10 m at high tide and 2–3 m tidal range. The north arm is dredged frequently to maintain its depth, since it is the main navigation channel, leading to physical disturbances of the bottom. The south arm is shallower with 2–4 m depth at high tide and 1–3 m tidal range. The south arm has nearly 75% of
8º 50’ W
Figueira da Foz
A
North Arm
D
1Km
E oR
ive
r
Atlantic Ocean
40º 08’ N
The fish assemblage of the Mondego estuary has been the subject of a long-term monitoring programme, from 1988 to 1992 and then from 2003 until the present (e.g. Jorge et al., 2002; Leitão et al., 2007; Nyitrai et al., 2012). For this study, we considered three critical periods with distinct hydro-climatic features: the first period, including 1988, 1991 and 1992; the second period, from 2004 to 2006; and the third one from 2010 to 2012. In 1988/1992 fishing was performed using a beach seine net (7 m sac and 8 mm stretched mesh size in the cod end). Fishing occurred monthly, during the day at low water of spring tides, in
Mo n
de g
B
PORTUGAL
South Arm
C Intertidal areas Saltmarshes
Pranto River
Fig. 1. The Mondego estuary, with the location of the sampling stations.
Please cite this article in press as: Baptista, J., et al. Long-term functional changes in an estuarine fish assemblage. Mar. Pollut. Bull. (2015), http:// dx.doi.org/10.1016/j.marpolbul.2015.06.025
J. Baptista et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
3
Table 1 Functional traits categories selected for the study, with the indication of the rationale for the trait selection. Traits
Categories
Traits selection rationale
Size
Small (40 cm)
Defines and correlates with other lifehistory traits and mediates structuring interactions. Size is related to the energy of individuals and to their impact on the food web
Body transversal shape
2.0
Measured as the body transversal shape, reflects the vertical position in the water column and hydrodynamic ability of fish (Villéger et al., 2012). Categories varied from fishes flattened laterally (>2) to flatfishes (30)
Reflects the ability to deal with physiological osmotic stress regarding the salinity changing nature of transitional waters (Elliott et al., 2007)
three sampling stations (A, B and D, Fig. 1), representing three estuarine habitats, freshwater, brackish and marine (Jorge et al., 2002). In 2004/2006, fishes were collected monthly and in 2010–2012 bimonthly. In these two periods, fishing took place during the night, at high water of spring tides, using a 2 m beam trawl with one tickler chain and 5 mm mesh size in the cod end, in five sampling stations (A–E, Fig. 1). At each sampling station, three trawls were towed for an average of 5 min each, covering at least an area of 500 m2. During all samplings temperature and salinity were measured in the bottom. All fish caught were identified, counted and their biomass determined (g wet weight). To compare the data from all periods, we converted the absolute biomass values into percentages, to reduce the variability from the sampling methodological differences (Mathieson et al., 2000; Leitão et al., 2007). For the rank analysis we used the 15 most abundant species. 2.3. Traits To evaluate functional diversity, the fish assemblage was characterized according to 5 traits: size, body transversal shape, feeding guild, vertical distribution in the water column and salinity tolerance (categories and rationale for traits selection are described in Table 1). For the body transversal shape, we used the formula: M = Bd/Bw, in which Bd is the body depth and Bw the body width (Villéger et al., 2010). For the feeding categories, we considered (1) omnivorous species as the ones feeding predominantly on algae, infauna and epifauna; (2) planktivores, feeding predominantly on plankton; (3) piscivorous, feeding predominantly on fish; (4) detritivorous, feeding predominantly on detritus; and (5) zoobenthivorous, feeding predominantly on invertebrates associated with the sediment. Considering vertical distribution, species were divided into 4 categories: (1) benthic – species that live in direct contact with the sediment; (2) pelagic – species that inhabit in the water column; (3) demersal – species that feed and live near the bottom (Elliott et al., 2007); (4) reef-associated – in our case study, we considered the species that are found around rocks and seaweeds (www.fishbase.org; Froese and Pauly, 2000). As our testing hypothesis is based on the effect of hydrology changes
in the fish community, we considered salinity tolerance as a trait. However, this is regarded as an indirect trait that reflects the species’ response to an environmental condition. For salinity tolerance, we considered 4 categories: (1) all – species that live in both marine and freshwater environment during part of their life cycle, essentially catadromous and anadromous species; (2) wide range – species that can endure in both salinity and freshwater environment, typically estuarine resident species; (3) freshwater – species that only tolerate low salinity values; (4) marine – species that only tolerate high salinity values. In addition, we analyzed the species economic relevance and geographical range. We used the species economical relevance to depict on the provisioning services provided by the fish community by dividing it into four levels: (1) commercial, representing the species that are consumed by humans and have high economical relevance, including species from professional and artisanal fisheries, and minor commercial species; (2) non-commercial, for the species with no economical relevance, either as food, game or for ornamental purposes; (3) aquarium, for the species that are not consumed by humans, but have an economic relevance for aesthetical purposes, i.e., used in aquariums; and (4) gamefish, for the fish that are usually captured in sports related to fishing. For the geographical range we considered two groups: sub-tropical and temperate, to depict on the possible long-term geographical displacement over the years due to climate (e.g. gradual Increase SST over the years; IPPC, 2013). 2.4. Data analyses The physic-chemical parameters were tested using a Kruskal– Wallis analysis. For the salinity parameter was performed an All Pairwise Multiple Comparison Procedure (Dunn’s Method), in order to isolate the group that differed from the others. For the fish community, we evaluated the number of species and the Simpson index as measures of fish taxonomic diversity and we estimated their equivalent functional diversity indices, functional richness and RaoQ. The functional richness expresses the amount of multidimensional trait space filled by the species
Please cite this article in press as: Baptista, J., et al. Long-term functional changes in an estuarine fish assemblage. Mar. Pollut. Bull. (2015), http:// dx.doi.org/10.1016/j.marpolbul.2015.06.025
J. Baptista et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
A
22 20
3.2. Fish assemblage A total of 67 fish species were collected, belonging to 28 families (supplemental material, Table S1), whose number decreased throughout the study period (Fig. 3). In contrast, Simpson’s index was lowest in 1988–1992, as more than 70% of the community was composed by a single species (Table 2), and increased in 2004–2006 and 2010–2012, which presented similar values. Functional richness followed a similar pattern to species richness, with a decrease during the study period. As traits are categorical, functional richness refers to the number of unique trait combinations in a community (Erõs et al., 2009). Still, functional richness was lower than species richness, particularly in 1988–1992 (Fig. 3). Rao’s quadratic entropy varied within similar values in the whole study period, being slightly higher in 2010–2012 and lower in 2004–2006; it was considerably lower than Simpson index values (Fig. 3). The 15 top species regarding biomass in each period represented 98.8% of the total biomass in 1988/1992, 97.6% in 2004/2006, and 99.1% in 2010/2012, and changed considerably
16 14 12
8
2006
2010
2011
2012
2006
2010
2011
2012
40
2005
2004
1992
B
1991
6
Year
30
Salinity
20
10
2005
2004
1992
180
700000
Precipitation
160
600000
140 500000
120 100
400000
80
300000
60
3)
C
1991
1988
0
Precipitation (mm)
200000
40
100000
20 0 Winter 10 Spring 10 Summer 10 Autumn 10 Winter 11 Spring 11 Summer 11 Autumn 11 Winter 12 Spring 12 Summer 12 Autumn 12
Winter 04 Spring 04 Summer 04 Autumn 04 Winter 05 Spring 05 Summer 05 Autumn 05 Winter 06 Spring 06 Summer 06 Autumn 06
Winter 91 Spring 91 Summer 91 Autumn 91 Winter 92 Spring 92 Summer 92 Autumn 92
0 Winter 88 Spring 88 Summer 88 Autumn 88
From this point onwards, the three periods will be color coded, for an easier understanding of the changes in environmental and fish components: 1988/1992 – white, 2004/2006 – dark gray, 2010/2012 – light gray. Surface seawater temperature remained similar throughout the study period (16.2–16.7 °C, p = 0.751), with seasonal variations typical of temperate ecosystems (10–14 °C during winter and 20–22 °C in summer periods, Fig. 2A). During the period of 1988/1992, a statistically significant lower mean estuarine salinity was observed compared to the other periods (3-year mean value of 11.3 compared to 25.0 and 22.2 for 2004/2006 and 2010/2012, p =
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Long-term functional changes in an estuarine fish assemblage J. Baptista a,⇑, F. Martinho a, D. Nyitrai a, M.A. Pardal a, M. Dolbeth a,b,⇑ a b
CFE – Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, Calçada Martim de Freitas, 3000-456 Coimbra, Portugal Biology Department & CESAM, University of Aveiro, Campus de Santiago, 3810-193 Aveiro, Portugal
a r t i c l e
i n f o
Article history: Received 27 December 2014 Revised 9 June 2015 Accepted 11 June 2015 Available online xxxx Keywords: Fish assemblages Estuaries Traits Hydrology Climate change
a b s t r a c t The functional diversity of the fish assemblages of the Mondego estuary was studied for a discontinuous 30-year period (1988–2012). During this time, hydrological changes occurred due to man-induced alterations and weather extremes. These changes led to alterations in the structure and function of the fish community. Species richness and functional richness decreased over time and the fish community started to explore new micro-habitats and food resources. Before severe hydrological changes, the community was dominated by pelagic, detritivorous and species with wider salinity ranges. After, the community became dominated by demersal, benthic, piscivorous and marine species. During a drought, omnivorous became increasingly important, reflecting greater possibilities of using available feeding resources. We have also found an increase in sub-tropical species throughout the years, which might be related to gradual temperature increases at a global scale. This study also confirmed estuaries as extremely important for restocking several commercial species. Ó 2015 Elsevier Ltd. All rights reserved.
1. Introduction A major breakthrough in community ecology studies has been the incorporation of functional approaches and functional diversity measures, as an elucidating tool to explore species coexistence and impacts on ecosystem functioning (Mouillot et al., 2007, 2013; Boucek and Rehage, 2014). Functional diversity refers to the functional component of biodiversity and is usually measured by species traits (Violle et al., 2007). A trait is a biological attribute, measurable at the individual level that influences the organism performance, determining the species effect on the ecosystem (i.e. effect trait) or influencing the species fitness in the environment (i.e. response trait) (Violle et al., 2007). The theory behind functional diversity may be applied to several trophic groups, and has the advantage to enable comparisons between systems that do not share similar taxonomical composition, and in an ecosystem functioning approach. For fish assemblages, functional approaches have been used for some decades in several studies identifying species’ functional guilds (e.g. species ecological, feeding guilds, Elliott and Dewailly, 1995; Elliott et al., 2007) and more recently, as part of multi-metric indices to evaluate the ecological condition of an
⇑ Corresponding authors at: CFE – Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, Calçada Martim de Freitas, 3000-456 Coimbra, Portugal. E-mail addresses: [email protected] (J. Baptista), [email protected] (M. Dolbeth).
water body, within the application of EU directives (e.g. Martinho et al., 2008; Cabral et al., 2012), and international policies, such has the Oceans policy (Australia), the Oceans Act and the Clean Water Act (Canada and USA) or the National Water Act (South Africa) (see Borja et al., 2010). However, a functional characterization of the community based on fish traits, such as the ones related to fish morphology as great potential to explore impacts of environmental disturbance in the ecosystem is high, and should be encouraged (Dumay et al., 2004; Goldstein and Meador, 2014; Mouillot et al., 2007; Villéger et al., 2010, 2012). In the present study, we explore the functional diversity of fish assemblages from an estuary that has been subjected to several disturbances related to human interference and climate change. Estuarine systems are important habitats for several fish, including several commercial marine and freshwater species that use them as a part of their lifecycle, by providing sheltered areas, plenty food availability, migratory routes and nursery grounds (Elliott and Hemingway, 2002; Elliott et al., 2007). The high productivity associated to these systems has attracted an important share of human population, which lives close to these coastal areas, benefiting from their ecosystem services, including fish production (Dolbeth et al., 2010). The major downside is that estuarine systems are particularly vulnerable to anthropogenic disturbance, which might be accentuated by the occurrence of weather extremes (Elsdon et al., 2009; Dolbeth et al., 2011; Vivier et al., 2010). Among major sources of anthropogenic disturbance with impact on the hydro-morphology of estuaries is river
http://dx.doi.org/10.1016/j.marpolbul.2015.06.025 0025-326X/Ó 2015 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Baptista, J., et al. Long-term functional changes in an estuarine fish assemblage. Mar. Pollut. Bull. (2015), http:// dx.doi.org/10.1016/j.marpolbul.2015.06.025
2
J. Baptista et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
regularization, margins embankment and dams (Vasconcelos et al., 2007; Neto et al., 2010; Nicolas et al., 2007), which might cause several changes in the fish communities (Costa et al., 2007). Climate change and the occurrence of extreme weather events, which are expected to increase in a nearby future (IPPC report, 2013), may accentuate these changes in the hydrology. As a consequence, estuarine fish assemblages composition and functioning are expected to change (Baptista et al., 2010; Dolbeth et al., 2010; Vivier et al., 2010), as a result of habitat degradation, loss of niches or by facilitated establishment of alien species, which compete for resources (Chessman, 2013). In this study, we use traits to understand the processes structuring estuarine fish assemblages, taking into account three critical periods over a 30-year study, when several hydrological changes occurred, due to hydromorphological reconfiguration of the riverbanks and occurrence of weather extremes. We were interested in understanding how the functional organization of the fish assemblage was affected by these hydrological changes, which are representative of changes occurring in most estuarine systems worldwide. For this task, we evaluate variations in the fish assemblage functional composition over a discontinuous 30-year period. Our hypothesis is that the observed hydrological changes affected fish community structure, composition and overall functioning, including its commercial importance.
2. Materials and methods
intertidal mudflats, and the downstream areas contain several seagrass meadows. The mouth of the estuary depth ranges from 8 to 13 m, and this area is influenced by both river flow and neritic waters. The Mondego estuary has undergone several anthropogenic pressures and hydromorphological transformations over the last decades (Neto et al., 2010; Veríssimo et al., 2013). From 1993 to 1997, the connection between the two arms was silted up, and the water circulating in the south arm was mainly dependent on tides and freshwater inputs from a small river, the Pranto River. The occlusion between the two arms resulted in an increase in water residence time and nutrients concentration, promoting macroalgae blooms and decrease of the seagrass coverage. During this time, the estuary showed symptoms of eutrophication, leading to a progressive decline in its environmental quality (Cardoso et al., 2010; Dolbeth et al., 2011). In 1998, a restoration plan was initiated to improve the ecological condition of the system, which consisted on the implementation of mitigation measures to decrease eutrophication and improve water circulation in the estuary (for more details see Lillebø et al., 2005; Neto et al., 2010; Dolbeth et al., 2011). In 2006, a second large-scale intervention was performed, consisting on the re-opening of the separation between the two arms, increasing the flow and reducing water residence time in the south arm (Veríssimo et al., 2013). In addition, extreme climatic events have also been observed, including floods in 2000–2001 and droughts in 2004–2005 (e.g. Baptista et al., 2010; Martinho et al., 2007; Primo et al., 2011).
2.1. Study site 2.2. Fish sampling and laboratory work The Mondego estuary (Fig. 1) is a small estuary (8.6 km2) located in the western coast of Portugal (40°080 N, 8°500 W), with an average freshwater flow rate of 79 m3 s1 (Dolbeth et al., 2010). The estuary comprises two arms, the north and the south, separated at 7 km from the shore that join again near the mouth. The two arms have distinct hydrological characteristics: the north arm is deeper with 5–10 m at high tide and 2–3 m tidal range. The north arm is dredged frequently to maintain its depth, since it is the main navigation channel, leading to physical disturbances of the bottom. The south arm is shallower with 2–4 m depth at high tide and 1–3 m tidal range. The south arm has nearly 75% of
8º 50’ W
Figueira da Foz
A
North Arm
D
1Km
E oR
ive
r
Atlantic Ocean
40º 08’ N
The fish assemblage of the Mondego estuary has been the subject of a long-term monitoring programme, from 1988 to 1992 and then from 2003 until the present (e.g. Jorge et al., 2002; Leitão et al., 2007; Nyitrai et al., 2012). For this study, we considered three critical periods with distinct hydro-climatic features: the first period, including 1988, 1991 and 1992; the second period, from 2004 to 2006; and the third one from 2010 to 2012. In 1988/1992 fishing was performed using a beach seine net (7 m sac and 8 mm stretched mesh size in the cod end). Fishing occurred monthly, during the day at low water of spring tides, in
Mo n
de g
B
PORTUGAL
South Arm
C Intertidal areas Saltmarshes
Pranto River
Fig. 1. The Mondego estuary, with the location of the sampling stations.
Please cite this article in press as: Baptista, J., et al. Long-term functional changes in an estuarine fish assemblage. Mar. Pollut. Bull. (2015), http:// dx.doi.org/10.1016/j.marpolbul.2015.06.025
J. Baptista et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
3
Table 1 Functional traits categories selected for the study, with the indication of the rationale for the trait selection. Traits
Categories
Traits selection rationale
Size
Small (40 cm)
Defines and correlates with other lifehistory traits and mediates structuring interactions. Size is related to the energy of individuals and to their impact on the food web
Body transversal shape
2.0
Measured as the body transversal shape, reflects the vertical position in the water column and hydrodynamic ability of fish (Villéger et al., 2012). Categories varied from fishes flattened laterally (>2) to flatfishes (30)
Reflects the ability to deal with physiological osmotic stress regarding the salinity changing nature of transitional waters (Elliott et al., 2007)
three sampling stations (A, B and D, Fig. 1), representing three estuarine habitats, freshwater, brackish and marine (Jorge et al., 2002). In 2004/2006, fishes were collected monthly and in 2010–2012 bimonthly. In these two periods, fishing took place during the night, at high water of spring tides, using a 2 m beam trawl with one tickler chain and 5 mm mesh size in the cod end, in five sampling stations (A–E, Fig. 1). At each sampling station, three trawls were towed for an average of 5 min each, covering at least an area of 500 m2. During all samplings temperature and salinity were measured in the bottom. All fish caught were identified, counted and their biomass determined (g wet weight). To compare the data from all periods, we converted the absolute biomass values into percentages, to reduce the variability from the sampling methodological differences (Mathieson et al., 2000; Leitão et al., 2007). For the rank analysis we used the 15 most abundant species. 2.3. Traits To evaluate functional diversity, the fish assemblage was characterized according to 5 traits: size, body transversal shape, feeding guild, vertical distribution in the water column and salinity tolerance (categories and rationale for traits selection are described in Table 1). For the body transversal shape, we used the formula: M = Bd/Bw, in which Bd is the body depth and Bw the body width (Villéger et al., 2010). For the feeding categories, we considered (1) omnivorous species as the ones feeding predominantly on algae, infauna and epifauna; (2) planktivores, feeding predominantly on plankton; (3) piscivorous, feeding predominantly on fish; (4) detritivorous, feeding predominantly on detritus; and (5) zoobenthivorous, feeding predominantly on invertebrates associated with the sediment. Considering vertical distribution, species were divided into 4 categories: (1) benthic – species that live in direct contact with the sediment; (2) pelagic – species that inhabit in the water column; (3) demersal – species that feed and live near the bottom (Elliott et al., 2007); (4) reef-associated – in our case study, we considered the species that are found around rocks and seaweeds (www.fishbase.org; Froese and Pauly, 2000). As our testing hypothesis is based on the effect of hydrology changes
in the fish community, we considered salinity tolerance as a trait. However, this is regarded as an indirect trait that reflects the species’ response to an environmental condition. For salinity tolerance, we considered 4 categories: (1) all – species that live in both marine and freshwater environment during part of their life cycle, essentially catadromous and anadromous species; (2) wide range – species that can endure in both salinity and freshwater environment, typically estuarine resident species; (3) freshwater – species that only tolerate low salinity values; (4) marine – species that only tolerate high salinity values. In addition, we analyzed the species economic relevance and geographical range. We used the species economical relevance to depict on the provisioning services provided by the fish community by dividing it into four levels: (1) commercial, representing the species that are consumed by humans and have high economical relevance, including species from professional and artisanal fisheries, and minor commercial species; (2) non-commercial, for the species with no economical relevance, either as food, game or for ornamental purposes; (3) aquarium, for the species that are not consumed by humans, but have an economic relevance for aesthetical purposes, i.e., used in aquariums; and (4) gamefish, for the fish that are usually captured in sports related to fishing. For the geographical range we considered two groups: sub-tropical and temperate, to depict on the possible long-term geographical displacement over the years due to climate (e.g. gradual Increase SST over the years; IPPC, 2013). 2.4. Data analyses The physic-chemical parameters were tested using a Kruskal– Wallis analysis. For the salinity parameter was performed an All Pairwise Multiple Comparison Procedure (Dunn’s Method), in order to isolate the group that differed from the others. For the fish community, we evaluated the number of species and the Simpson index as measures of fish taxonomic diversity and we estimated their equivalent functional diversity indices, functional richness and RaoQ. The functional richness expresses the amount of multidimensional trait space filled by the species
Please cite this article in press as: Baptista, J., et al. Long-term functional changes in an estuarine fish assemblage. Mar. Pollut. Bull. (2015), http:// dx.doi.org/10.1016/j.marpolbul.2015.06.025
J. Baptista et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
A
22 20
3.2. Fish assemblage A total of 67 fish species were collected, belonging to 28 families (supplemental material, Table S1), whose number decreased throughout the study period (Fig. 3). In contrast, Simpson’s index was lowest in 1988–1992, as more than 70% of the community was composed by a single species (Table 2), and increased in 2004–2006 and 2010–2012, which presented similar values. Functional richness followed a similar pattern to species richness, with a decrease during the study period. As traits are categorical, functional richness refers to the number of unique trait combinations in a community (Erõs et al., 2009). Still, functional richness was lower than species richness, particularly in 1988–1992 (Fig. 3). Rao’s quadratic entropy varied within similar values in the whole study period, being slightly higher in 2010–2012 and lower in 2004–2006; it was considerably lower than Simpson index values (Fig. 3). The 15 top species regarding biomass in each period represented 98.8% of the total biomass in 1988/1992, 97.6% in 2004/2006, and 99.1% in 2010/2012, and changed considerably
16 14 12
8
2006
2010
2011
2012
2006
2010
2011
2012
40
2005
2004
1992
B
1991
6
Year
30
Salinity
20
10
2005
2004
1992
180
700000
Precipitation
160
600000
140 500000
120 100
400000
80
300000
60
3)
C
1991
1988
0
Precipitation (mm)
200000
40
100000
20 0 Winter 10 Spring 10 Summer 10 Autumn 10 Winter 11 Spring 11 Summer 11 Autumn 11 Winter 12 Spring 12 Summer 12 Autumn 12
Winter 04 Spring 04 Summer 04 Autumn 04 Winter 05 Spring 05 Summer 05 Autumn 05 Winter 06 Spring 06 Summer 06 Autumn 06
Winter 91 Spring 91 Summer 91 Autumn 91 Winter 92 Spring 92 Summer 92 Autumn 92
0 Winter 88 Spring 88 Summer 88 Autumn 88
From this point onwards, the three periods will be color coded, for an easier understanding of the changes in environmental and fish components: 1988/1992 – white, 2004/2006 – dark gray, 2010/2012 – light gray. Surface seawater temperature remained similar throughout the study period (16.2–16.7 °C, p = 0.751), with seasonal variations typical of temperate ecosystems (10–14 °C during winter and 20–22 °C in summer periods, Fig. 2A). During the period of 1988/1992, a statistically significant lower mean estuarine salinity was observed compared to the other periods (3-year mean value of 11.3 compared to 25.0 and 22.2 for 2004/2006 and 2010/2012, p =
