Marine Environmental Research 98 (2014) 39e48
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Recovery trends of Scrobicularia plana populations after restoration measures, affected by extreme climate events T. Verdelhos a, *, P.G. Cardoso a, M. Dolbeth b, c, M.A. Pardal c a
IMAR e CMA Marine and Environmental Research Centre, Department of Life Sciences, University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal CESAM & Biology Department, University of Aveiro, Campus de Santiago, 3810-193 Aveiro, Portugal c CFE e Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 12 December 2013 Received in revised form 6 March 2014 Accepted 7 March 2014
The Mondego estuary (Portugal) went through different ecological scenarios over the last decades. An eutrophication process led to a decline in the ecosystem quality. The ensuing restoration plan resulted into a gradual ecological recovery, which was impaired by the occurrence of successive extreme climate events that affected dynamics and productivity of key species. In this study we assess the response of the bivalve Scrobicularia plana to the impacts of these events in a recovery scenario, by comparing populations in two different intertidal habitats: a seagrass bed and a sandflat area. As a general tendency, S. plana, which was negatively affected by eutrophication, responded positively to restoration. However, the occurrence of extreme climate events seemed to affect recruitment success, biomass and production, impairing the recovery process. In the seagrass bed, S. plana maintained a stable and structured population, while in the sandflat area recovery clearly reverted into a decline, mainly concerning biomass and production values. This sequence of multiple stressors might have reduced S. plana resilience to further impacts and therefore, understanding the behavior of biological populations following restoration initiatives requires acknowledgement that some changes may not be easily reversible. Ó 2014 Elsevier Ltd. All rights reserved.
Keywords: Extreme climate events Scrobicularia plana Restoration Resilience Seagrass Sandflat
1. Introduction Estuaries are among the Earth’s most important ecosystems both ecologically and socio-economically, with an estimated value of wUS$ 4100 (109) per km2 per year (Martínez et al., 2007). On the one hand, they are highly productive and provide essential ecological functions and services such as habitat, protection and food for resident and migratory species (Kennish, 2002; Paerl, 2006; Dolbeth et al., 2011). On the other, they are a valuable and widely explored resource for agriculture and fisheries, and for industrial and urban development (Kennish, 2002; Paerl, 2006; Fujii, 2012; Wetz and Yoskowitz, 2013). As such, estuaries are usually subjected to a wide variety of anthropogenic stressors (Paerl, 2006; Doney et al., 2012; Fujii, 2012; Wetz and Yoskowitz, 2013). In addition, ongoing global warming impacts these areas, through extreme weather episodes and the combined effects of these stressors are complex and difficult to predict (Vinebrooke et al., 2004; Doney et al., 2012; Fujii, 2012; Wetz and Yoskowitz, 2013).
* Corresponding author. E-mail address: [email protected] (T. Verdelhos). http://dx.doi.org/10.1016/j.marenvres.2014.03.004 0141-1136/Ó 2014 Elsevier Ltd. All rights reserved.
Recent climate models forecast an increase on the frequency and severity of extreme weather events (IPCC, 2007, 2013). This may amplify the risk of abrupt and non-linear changes in many ecosystems, which may render them incapable of compensating for the loss of biodiversity, thereby reducing their resilience to environmental change (Vinebrooke et al., 2004; Doney et al., 2012; Fujii, 2012; Wetz and Yoskowitz, 2013). Distinguishing and integrating the effects of natural and anthropogenic stressors is a challenge for understanding and managing coastal biotic resources in order to mitigate a foreseeable “extreme future” (Paerl, 2006; Doney et al., 2012; Fujii, 2012; Wetz and Yoskowitz, 2013). Seagrass beds are one of the richest and most productive coastal habitats, with a worldwide economic value estimated at US$ 299 (109) per km2 per year (Martínez et al., 2007), through a wide variety of ecosystem services. Seagrasses have high primary productivity and operate as the basis of the food web (Waycott et al., 2009; Short et al., 2011). They play an important role in nutrient cycling, sediment stabilization and clearing the water from suspended sediments (Orth et al., 2006; Waycott et al., 2009; Short et al., 2011). Furthermore, seagrasses contribute globally to carbon sequestration and storage (Duarte et al., 2005). These habitats and their valuable services have been threatened by the impacts of
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anthropogenic activities and climatic events (Orth et al., 2006; Waycott et al., 2009; Short et al., 2011), and are declining worldwide. The Mondego estuary, Portugal, has been well documented over the last decades, during which it went through different ecological scenarios. Eutrophication led to water quality degradation and increased turbidity, seagrass beds decline and a general decay of the overall environmental quality (Cardoso et al., 2005, 2007; Verdelhos et al., 2005; Dolbeth et al., 2007). In order to mitigate eutrophication and recover seagrass beds a management plan was implemented in 1998, which resulted in a gradual ecological recovery (Cardoso et al., 2007, 2010; Lillebø et al., 2005; Verdelhos et al., 2005; Dolbeth et al., 2011). Finally, the occurrence of extreme climate events over the last decade affected the estuarine gradual recovery (Cardoso et al., 2010; Dolbeth et al., 2011; Grilo et al., 2011 and references therein). The existing seagrass has then become confined to the outer reach of the estuary, due to extensive eutrophication (Lillebø et al., 2005; Verdelhos et al., 2005; Cardoso et al., 2008a,b). Differences in macrofaunal assemblage were registered between seagrass beds and the inner unvegetated sandflats. Seagrass habitat showed higher diversity, productivity, functional organization and sustained longer and more complex food webs (Dolbeth et al., 2007, 2011, 2013, 2014; Baeta et al., 2009; Cardoso et al., 2010). These intertidal areas have great economic importance to local human populations, due to their valuable biological resources, such as the bivalve Scrobicularia plana. Bivalves are an essential link between the primary producers and epibenthic consumers, filtering organic matter, purifying the water column and influencing the energy flow on the entire community (Dolbeth et al., 2007, 2011; Dumbauld et al., 2009; Beukema et al., 2010; Parada et al., 2011; Santos et al., 2011). They are also one of the most productive groups of infaunal organisms and represent a major food provisioning service of estuaries (Dumbauld et al., 2009; Beukema et al., 2010; Parada et al., 2011; Santos et al., 2011). S. plana has been the subject of a previous study in this system, which evaluated the impacts of eutrophication and subsequent restoration effects (Verdelhos et al., 2005). On the one hand, eutrophication seemed to impact S. plana abundance, biomass and annual production. On the other, this species responded positively to the mitigation measures, which led to a more structured and stable population, with biomass and production increments. In this study we evaluate the response of the population in the ensuing scenario e an ongoing recovery ecosystem subjected to successive extreme weather events. Therefore, the main goals of this study were: a) to assess the impacts of weather extremes on the dynamics, structure and production of S. plana; b) to evaluate the long-term effectiveness of management; c) to compare the response of S. plana in two different intertidal existing habitats e seagrass bed vs. sandflat area.
Fig. 1. The Mondego estuary and sampling stations.
2. Materials and methods
the southern arm. Thus, the system has been under environmental stress by eutrophication processes (Lillebø et al., 2005). Following a restoration intervention in 1998, water circulation and transparency improved, nutrient loading decreased and the eutrophication effects were mitigated, leading to a gradual ecosystem recovery (Cardoso et al., 2007, 2010; Lillebø et al., 2005; Verdelhos et al., 2005; Dolbeth et al., 2011). The implemented measures included: (1) the re-establishment of the South arm riverhead connection, improving the hydraulic regime; (2) most of the nutrient enriched Pranto freshwater is diverted to the Northern arm by another sluice located further upstream, leading to nutrient loading reduction (Lillebø et al., 2005); (3) seagrass bed protection from human disturbance; and (4) public education of the ecological importance of intertidal vegetation for health and related socioeconomic activities of the estuary. Over the last 30 years the climate of Portugal has suffered changes when compared to the patterns for period 1931e1990 (Santos et al., 2002; Miranda et al., 2006): a) the frequency of flood events (precipitation in excess of 50% of the winter mean) has clearly increased; b) the frequency and intensity of dry years has also increased, compared to the period 1940e1970; c) the occurrence of heat waves has become more frequent. In fact, during the study period (from 1999 to 2005) several events occurred: heavy winter precipitation in 2000/01 and 2000/02; heat waves in 2003 and 2005 summers; drought periods in 2002 (dry year), 2004 (extremely dry year) and 2005 (very dry year) (Cardoso et al., 2008b). Therefore, in a post e eutrophication scenario, climatic conditions, particularly extremes of precipitation and temperature, became the major impacts acting on the estuary.
2.1. Study site and ecological scenarios
2.2. Sampling, laboratory procedures and climate data
The Mondego estuary, located on the Atlantic coast of Portugal (40 080 N, 8 500 W) is a small estuary of 8.6 km2, comprising two arms, North and South, separated by the Murraceira island (Fig. 1). Until 1998, the South arm was almost silted up in the innermost areas, and the river outflow occurred mainly via the North arm. Water circulation was therefore mostly dependent on the tides and on the freshwater input from the Pranto River. The discharge from this tributary is controlled by a sluice and is regulated according to the irrigation needs in rice fields in the Mondego Valley. This freshwater input represented an important source of nutrients into
Sampling was carried out monthly from January 1999 to December 2005. Two different areas were sampled (Fig. 1): (1) a seagrass bed, characterized by muddy sediments covered with Zostera noltii, higher organic matter content (mean 6.2% 1.76) and higher water-flow velocity (1.2e1.4 m s1) (Dolbeth et al., 2011); (2) a sandflat area, composed by sandy-muddy-sediments with lower organic matter content (mean 3.0% 1.14), characterized by lower water flows (0.8e1.2 m s1) (Dolbeth et al., 2011), which has not supported rooted macrophytes for decades and has been covered seasonally by green macroalgae.
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On each occasion 5e10 cores corresponding to a total area of 0.0705 m2e0.1410 m2 were randomly taken to a depth of 25 cm. Each sample was sieved through a 500 mm mesh using estuarine water and then preserved in 4% buffered formalin. At each sampling station, water temperature and salinity were measured directly in situ (in low water pools), and sediment was collected. The collected sediment was dried (for 72 h at 60 C) and the organic matter content assessed after combustion of samples for 8 h at 450 C. Sediment grain size was analyzed from combusted sediment, sieving on a series of sieves (38, 63, 125, 250, 500, 1000, and 2000 mm, converted into F scale for the analyses) and grain size distributions were determined by GRADISTAT Version 4.0 (Blott and Pye, 2001) using logarithmic Folk and Ward method, as Median Grain Size (Md) and % of the different sediment fractions. Plant material was sorted and subsequently dried (for 72 h at 60 C) and ash-free dry weight (AFDW) assessed after combustion of samples for 8 h at 450 C. S. plana individuals were counted, their total length was measured and lengtheweight relationships determined for production estimates, using the regression equation AFDW ¼ 0.00000991 Total length 2.68809 (r2 ¼ 0.97, N ¼ 152, Verdelhos et al., 2005). Preliminary ANOVA of length AFDW relationships indicated no significant seasonal differences (Verdelhos et al., 2005). The secondary production of S. plana was computed using the mass-specific growth rate method, adjusted for a von Bertalanffy growth function (VBGF e Equation (1)), after recommendation of Cusson et al. (2006) and using VBGF parameters (Equation (2)) determined by Verdelhos et al. (2011). This method enables to estimate production without the recognition of cohorts, which could not be distinguished per area for all the population (Verdelhos et al., 2005).
P ¼ K
K1 X k¼1
0 L L Iðk þ 1Þ Bk a0 a0 k log max L0max IðkÞ IðkÞ
(1)
where P is growth production of the population, K is the number of size classes, Bk, population biomass for k size class, Lk is the length of the kth size class, I(k) was determined by I(k) ¼ (Lk þ Lkþ1)/2, L0max was obtained by fitting a VBGF:
0 LðTÞ ¼ L0max 1 exp l T T00
(2)
and a0 results from adjusting the linear regression curve:
logðWÞ ¼ a0 logðLÞ þ b0
(3)
where W is the individual weight and L the length. Finally, the rainfall data were collected from the Source forecast station (INAG e Portuguese Water Institute, http://snirh.inag.pt/), as total cumulative per month and climate normal for the period 1971e2000. Air temperature data were obtained from Coimbra station (Portuguese Institute of Sea and Atmosphere e IPMA, http://www.ipma.pt/en/), and displayed as monthly means, absolute maximum value registered and climate normal for the period 1971e2000.
3. Results 3.1. The mondego estuary e climate and intertidal habitats Over the study period, precipitation and air temperature generally followed a seasonal pattern, typical of temperate regions e pluvious and cold winter, with precipitation decreasing and temperature increasing towards summer. However, several unusual
41
weather phenomena occurred in comparison with the climate normal of 1971e2000 (Fig. 2 A, B). In 2000/01 and 2002/03 heavy winter precipitation was registered (Fig. 2 A), originating an unprecedented flood in 2000/01, considered the major flood of the last century. In contrast, 2004 and 2005 showed extremely lower rainfall and were considered extremely dry and very dry years, respectively (Fig. 2 A). The lowest annual precipitation was observed in 2005 (486.1 mm against 905.1 mm for 1971e2000 mean), with below mean precipitation periods quite evident practically during all the year. On the other hand, in spring and summer of 2003 and 2005, higher mean monthly temperatures were recorded (Fig. 2 B) when the maximum temperature was above 40 C on several occasions. In fact, in most of the Portuguese territory, heat waves were recorded in July/August 2003 (16e17 days) and in June 2005 (8e12 days). A heat wave occurs when the maximum air temperature increases by 5 C relative to the mean daily value of the reference period for at least 6 consecutive days (according to IPMA). Salinity and water temperature values followed precipitation and air temperature patterns, respectively, and responded to extreme weather phenomena (Fig 2 C, D). During heavy rainfall, salinity decreased considerably to values 50 g AFDW m2), decreasing progressively in the subsequent years (2001e2003: w10 to >30 g AFDW m2; 2004e2005: 10 mm (ind m2) P (g AFDW m2 y1) B (g AFDW m2) w (mg AFDW) P: B (y1)
Seagrass bed
Sandflat area
ManneWhitney
X
Range
X
Range
578.64 15.94 351.15 235.35 10.36 15.88 0.034 0.72
93.15e5183.83 3.13e30.01 11.64e5044.10 58.22e442.47 9.13e11.86 14.30e17.74 0.012e0.051 0.54e0.72
2620.99 19.71 2590.94 126.86 8.30 20.79 0.009 0.46
116.44e10451.49 0.03e57.63 11.64e10158.07 0.00e447.12 3.86e15.12 5.97e38.91 0.002e0.019 0.30e0.81
The parameters that show statistically significant differences between the two areas were given in bold.
T T T T T T T T
¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼
7825.5 6049.0 8071.5 4051.5 63.0 48.0 74.0 67.0
P £ 0.001 P ¼ 0.567 P £ 0.001 P £ 0.001 P ¼ 0.209 P ¼ 0.620 P £ 0.001 P £ 0.001
s s s
s s
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Verdelhos, T., Cardoso, P.G., Dolbeth, M., Pardal, M.A., 2011. Latitudinal gradients in Scrobicularia plana reproduction patterns, population dynamics, growth, and secondary production. Mar. Ecol. Prog. Ser. 442, 271e283. Vinebrooke, R.D., Cottingham, K.L., Norberg, J., Scheffer, M., Dodson, S.I., Maberly, S.C., Sommer, U., 2004. Impacts of multiple stressors on biodiversity and ecosystem functioning: the role of species cotolerance. Oikos 104, 451e457. Waycott, M., Duarte, C.M., Carruthers, T.J.B., Orth, R.J., Dennison, W.C., Olyarnik, S., Calladine, A., Fourqurean, J.W., Heck, K.L., Hughes, A.R., Kendrick, G.A.,
Kenworthy, W.J., Short, F.T., Williams, S.W., 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc. Natl. Acad. Sci. 106, 12377e 12381. Wetz, M.S., Yoskowitz, D.W., 2013. An ‘extreme’ future for estuaries? Effects of extreme climatic events on estuarine water quality and ecology. Mar. Pollut. Bull. 69, 7e18.
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Recovery trends of Scrobicularia plana populations after restoration measures, affected by extreme climate events T. Verdelhos a, *, P.G. Cardoso a, M. Dolbeth b, c, M.A. Pardal c a
IMAR e CMA Marine and Environmental Research Centre, Department of Life Sciences, University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal CESAM & Biology Department, University of Aveiro, Campus de Santiago, 3810-193 Aveiro, Portugal c CFE e Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, PO Box 3046, 3001-401 Coimbra, Portugal b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 12 December 2013 Received in revised form 6 March 2014 Accepted 7 March 2014
The Mondego estuary (Portugal) went through different ecological scenarios over the last decades. An eutrophication process led to a decline in the ecosystem quality. The ensuing restoration plan resulted into a gradual ecological recovery, which was impaired by the occurrence of successive extreme climate events that affected dynamics and productivity of key species. In this study we assess the response of the bivalve Scrobicularia plana to the impacts of these events in a recovery scenario, by comparing populations in two different intertidal habitats: a seagrass bed and a sandflat area. As a general tendency, S. plana, which was negatively affected by eutrophication, responded positively to restoration. However, the occurrence of extreme climate events seemed to affect recruitment success, biomass and production, impairing the recovery process. In the seagrass bed, S. plana maintained a stable and structured population, while in the sandflat area recovery clearly reverted into a decline, mainly concerning biomass and production values. This sequence of multiple stressors might have reduced S. plana resilience to further impacts and therefore, understanding the behavior of biological populations following restoration initiatives requires acknowledgement that some changes may not be easily reversible. Ó 2014 Elsevier Ltd. All rights reserved.
Keywords: Extreme climate events Scrobicularia plana Restoration Resilience Seagrass Sandflat
1. Introduction Estuaries are among the Earth’s most important ecosystems both ecologically and socio-economically, with an estimated value of wUS$ 4100 (109) per km2 per year (Martínez et al., 2007). On the one hand, they are highly productive and provide essential ecological functions and services such as habitat, protection and food for resident and migratory species (Kennish, 2002; Paerl, 2006; Dolbeth et al., 2011). On the other, they are a valuable and widely explored resource for agriculture and fisheries, and for industrial and urban development (Kennish, 2002; Paerl, 2006; Fujii, 2012; Wetz and Yoskowitz, 2013). As such, estuaries are usually subjected to a wide variety of anthropogenic stressors (Paerl, 2006; Doney et al., 2012; Fujii, 2012; Wetz and Yoskowitz, 2013). In addition, ongoing global warming impacts these areas, through extreme weather episodes and the combined effects of these stressors are complex and difficult to predict (Vinebrooke et al., 2004; Doney et al., 2012; Fujii, 2012; Wetz and Yoskowitz, 2013).
* Corresponding author. E-mail address: [email protected] (T. Verdelhos). http://dx.doi.org/10.1016/j.marenvres.2014.03.004 0141-1136/Ó 2014 Elsevier Ltd. All rights reserved.
Recent climate models forecast an increase on the frequency and severity of extreme weather events (IPCC, 2007, 2013). This may amplify the risk of abrupt and non-linear changes in many ecosystems, which may render them incapable of compensating for the loss of biodiversity, thereby reducing their resilience to environmental change (Vinebrooke et al., 2004; Doney et al., 2012; Fujii, 2012; Wetz and Yoskowitz, 2013). Distinguishing and integrating the effects of natural and anthropogenic stressors is a challenge for understanding and managing coastal biotic resources in order to mitigate a foreseeable “extreme future” (Paerl, 2006; Doney et al., 2012; Fujii, 2012; Wetz and Yoskowitz, 2013). Seagrass beds are one of the richest and most productive coastal habitats, with a worldwide economic value estimated at US$ 299 (109) per km2 per year (Martínez et al., 2007), through a wide variety of ecosystem services. Seagrasses have high primary productivity and operate as the basis of the food web (Waycott et al., 2009; Short et al., 2011). They play an important role in nutrient cycling, sediment stabilization and clearing the water from suspended sediments (Orth et al., 2006; Waycott et al., 2009; Short et al., 2011). Furthermore, seagrasses contribute globally to carbon sequestration and storage (Duarte et al., 2005). These habitats and their valuable services have been threatened by the impacts of
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anthropogenic activities and climatic events (Orth et al., 2006; Waycott et al., 2009; Short et al., 2011), and are declining worldwide. The Mondego estuary, Portugal, has been well documented over the last decades, during which it went through different ecological scenarios. Eutrophication led to water quality degradation and increased turbidity, seagrass beds decline and a general decay of the overall environmental quality (Cardoso et al., 2005, 2007; Verdelhos et al., 2005; Dolbeth et al., 2007). In order to mitigate eutrophication and recover seagrass beds a management plan was implemented in 1998, which resulted in a gradual ecological recovery (Cardoso et al., 2007, 2010; Lillebø et al., 2005; Verdelhos et al., 2005; Dolbeth et al., 2011). Finally, the occurrence of extreme climate events over the last decade affected the estuarine gradual recovery (Cardoso et al., 2010; Dolbeth et al., 2011; Grilo et al., 2011 and references therein). The existing seagrass has then become confined to the outer reach of the estuary, due to extensive eutrophication (Lillebø et al., 2005; Verdelhos et al., 2005; Cardoso et al., 2008a,b). Differences in macrofaunal assemblage were registered between seagrass beds and the inner unvegetated sandflats. Seagrass habitat showed higher diversity, productivity, functional organization and sustained longer and more complex food webs (Dolbeth et al., 2007, 2011, 2013, 2014; Baeta et al., 2009; Cardoso et al., 2010). These intertidal areas have great economic importance to local human populations, due to their valuable biological resources, such as the bivalve Scrobicularia plana. Bivalves are an essential link between the primary producers and epibenthic consumers, filtering organic matter, purifying the water column and influencing the energy flow on the entire community (Dolbeth et al., 2007, 2011; Dumbauld et al., 2009; Beukema et al., 2010; Parada et al., 2011; Santos et al., 2011). They are also one of the most productive groups of infaunal organisms and represent a major food provisioning service of estuaries (Dumbauld et al., 2009; Beukema et al., 2010; Parada et al., 2011; Santos et al., 2011). S. plana has been the subject of a previous study in this system, which evaluated the impacts of eutrophication and subsequent restoration effects (Verdelhos et al., 2005). On the one hand, eutrophication seemed to impact S. plana abundance, biomass and annual production. On the other, this species responded positively to the mitigation measures, which led to a more structured and stable population, with biomass and production increments. In this study we evaluate the response of the population in the ensuing scenario e an ongoing recovery ecosystem subjected to successive extreme weather events. Therefore, the main goals of this study were: a) to assess the impacts of weather extremes on the dynamics, structure and production of S. plana; b) to evaluate the long-term effectiveness of management; c) to compare the response of S. plana in two different intertidal existing habitats e seagrass bed vs. sandflat area.
Fig. 1. The Mondego estuary and sampling stations.
2. Materials and methods
the southern arm. Thus, the system has been under environmental stress by eutrophication processes (Lillebø et al., 2005). Following a restoration intervention in 1998, water circulation and transparency improved, nutrient loading decreased and the eutrophication effects were mitigated, leading to a gradual ecosystem recovery (Cardoso et al., 2007, 2010; Lillebø et al., 2005; Verdelhos et al., 2005; Dolbeth et al., 2011). The implemented measures included: (1) the re-establishment of the South arm riverhead connection, improving the hydraulic regime; (2) most of the nutrient enriched Pranto freshwater is diverted to the Northern arm by another sluice located further upstream, leading to nutrient loading reduction (Lillebø et al., 2005); (3) seagrass bed protection from human disturbance; and (4) public education of the ecological importance of intertidal vegetation for health and related socioeconomic activities of the estuary. Over the last 30 years the climate of Portugal has suffered changes when compared to the patterns for period 1931e1990 (Santos et al., 2002; Miranda et al., 2006): a) the frequency of flood events (precipitation in excess of 50% of the winter mean) has clearly increased; b) the frequency and intensity of dry years has also increased, compared to the period 1940e1970; c) the occurrence of heat waves has become more frequent. In fact, during the study period (from 1999 to 2005) several events occurred: heavy winter precipitation in 2000/01 and 2000/02; heat waves in 2003 and 2005 summers; drought periods in 2002 (dry year), 2004 (extremely dry year) and 2005 (very dry year) (Cardoso et al., 2008b). Therefore, in a post e eutrophication scenario, climatic conditions, particularly extremes of precipitation and temperature, became the major impacts acting on the estuary.
2.1. Study site and ecological scenarios
2.2. Sampling, laboratory procedures and climate data
The Mondego estuary, located on the Atlantic coast of Portugal (40 080 N, 8 500 W) is a small estuary of 8.6 km2, comprising two arms, North and South, separated by the Murraceira island (Fig. 1). Until 1998, the South arm was almost silted up in the innermost areas, and the river outflow occurred mainly via the North arm. Water circulation was therefore mostly dependent on the tides and on the freshwater input from the Pranto River. The discharge from this tributary is controlled by a sluice and is regulated according to the irrigation needs in rice fields in the Mondego Valley. This freshwater input represented an important source of nutrients into
Sampling was carried out monthly from January 1999 to December 2005. Two different areas were sampled (Fig. 1): (1) a seagrass bed, characterized by muddy sediments covered with Zostera noltii, higher organic matter content (mean 6.2% 1.76) and higher water-flow velocity (1.2e1.4 m s1) (Dolbeth et al., 2011); (2) a sandflat area, composed by sandy-muddy-sediments with lower organic matter content (mean 3.0% 1.14), characterized by lower water flows (0.8e1.2 m s1) (Dolbeth et al., 2011), which has not supported rooted macrophytes for decades and has been covered seasonally by green macroalgae.
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On each occasion 5e10 cores corresponding to a total area of 0.0705 m2e0.1410 m2 were randomly taken to a depth of 25 cm. Each sample was sieved through a 500 mm mesh using estuarine water and then preserved in 4% buffered formalin. At each sampling station, water temperature and salinity were measured directly in situ (in low water pools), and sediment was collected. The collected sediment was dried (for 72 h at 60 C) and the organic matter content assessed after combustion of samples for 8 h at 450 C. Sediment grain size was analyzed from combusted sediment, sieving on a series of sieves (38, 63, 125, 250, 500, 1000, and 2000 mm, converted into F scale for the analyses) and grain size distributions were determined by GRADISTAT Version 4.0 (Blott and Pye, 2001) using logarithmic Folk and Ward method, as Median Grain Size (Md) and % of the different sediment fractions. Plant material was sorted and subsequently dried (for 72 h at 60 C) and ash-free dry weight (AFDW) assessed after combustion of samples for 8 h at 450 C. S. plana individuals were counted, their total length was measured and lengtheweight relationships determined for production estimates, using the regression equation AFDW ¼ 0.00000991 Total length 2.68809 (r2 ¼ 0.97, N ¼ 152, Verdelhos et al., 2005). Preliminary ANOVA of length AFDW relationships indicated no significant seasonal differences (Verdelhos et al., 2005). The secondary production of S. plana was computed using the mass-specific growth rate method, adjusted for a von Bertalanffy growth function (VBGF e Equation (1)), after recommendation of Cusson et al. (2006) and using VBGF parameters (Equation (2)) determined by Verdelhos et al. (2011). This method enables to estimate production without the recognition of cohorts, which could not be distinguished per area for all the population (Verdelhos et al., 2005).
P ¼ K
K1 X k¼1
0 L L Iðk þ 1Þ Bk a0 a0 k log max L0max IðkÞ IðkÞ
(1)
where P is growth production of the population, K is the number of size classes, Bk, population biomass for k size class, Lk is the length of the kth size class, I(k) was determined by I(k) ¼ (Lk þ Lkþ1)/2, L0max was obtained by fitting a VBGF:
0 LðTÞ ¼ L0max 1 exp l T T00
(2)
and a0 results from adjusting the linear regression curve:
logðWÞ ¼ a0 logðLÞ þ b0
(3)
where W is the individual weight and L the length. Finally, the rainfall data were collected from the Source forecast station (INAG e Portuguese Water Institute, http://snirh.inag.pt/), as total cumulative per month and climate normal for the period 1971e2000. Air temperature data were obtained from Coimbra station (Portuguese Institute of Sea and Atmosphere e IPMA, http://www.ipma.pt/en/), and displayed as monthly means, absolute maximum value registered and climate normal for the period 1971e2000.
3. Results 3.1. The mondego estuary e climate and intertidal habitats Over the study period, precipitation and air temperature generally followed a seasonal pattern, typical of temperate regions e pluvious and cold winter, with precipitation decreasing and temperature increasing towards summer. However, several unusual
41
weather phenomena occurred in comparison with the climate normal of 1971e2000 (Fig. 2 A, B). In 2000/01 and 2002/03 heavy winter precipitation was registered (Fig. 2 A), originating an unprecedented flood in 2000/01, considered the major flood of the last century. In contrast, 2004 and 2005 showed extremely lower rainfall and were considered extremely dry and very dry years, respectively (Fig. 2 A). The lowest annual precipitation was observed in 2005 (486.1 mm against 905.1 mm for 1971e2000 mean), with below mean precipitation periods quite evident practically during all the year. On the other hand, in spring and summer of 2003 and 2005, higher mean monthly temperatures were recorded (Fig. 2 B) when the maximum temperature was above 40 C on several occasions. In fact, in most of the Portuguese territory, heat waves were recorded in July/August 2003 (16e17 days) and in June 2005 (8e12 days). A heat wave occurs when the maximum air temperature increases by 5 C relative to the mean daily value of the reference period for at least 6 consecutive days (according to IPMA). Salinity and water temperature values followed precipitation and air temperature patterns, respectively, and responded to extreme weather phenomena (Fig 2 C, D). During heavy rainfall, salinity decreased considerably to values 50 g AFDW m2), decreasing progressively in the subsequent years (2001e2003: w10 to >30 g AFDW m2; 2004e2005: 10 mm (ind m2) P (g AFDW m2 y1) B (g AFDW m2) w (mg AFDW) P: B (y1)
Seagrass bed
Sandflat area
ManneWhitney
X
Range
X
Range
578.64 15.94 351.15 235.35 10.36 15.88 0.034 0.72
93.15e5183.83 3.13e30.01 11.64e5044.10 58.22e442.47 9.13e11.86 14.30e17.74 0.012e0.051 0.54e0.72
2620.99 19.71 2590.94 126.86 8.30 20.79 0.009 0.46
116.44e10451.49 0.03e57.63 11.64e10158.07 0.00e447.12 3.86e15.12 5.97e38.91 0.002e0.019 0.30e0.81
The parameters that show statistically significant differences between the two areas were given in bold.
T T T T T T T T
¼ ¼ ¼ ¼ ¼ ¼ ¼ ¼
7825.5 6049.0 8071.5 4051.5 63.0 48.0 74.0 67.0
P £ 0.001 P ¼ 0.567 P £ 0.001 P £ 0.001 P ¼ 0.209 P ¼ 0.620 P £ 0.001 P £ 0.001
s s s
s s
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