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RESTORATION EXPERIMENT OF Zostera marina L. IN A SUBTROPICAL COASTAL LAGOON

PAOLA RODRÍGUEZ‐SALINAS, RAFAEL RIOSMENA‐RODRÍGUEZ GUSTAVO HINOJOSA‐ARANGO, RAQUEL MUÑIZ‐SALAZAR

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Ecological Engineering 36 (2010) 12–18

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Restoration experiment of Zostera marina L. in a subtropical coastal lagoon Paola Rodríguez-Salinas a , Rafael Riosmena-Rodríguez a,b,c,∗ , c ˜ Gustavo Hinojosa-Arango b , Raquel Muniz-Salazar a Programa de Investigación en Botánica Marina, Departamento de Biología Marina, Universidad Autónoma de Baja California Sur, Km 5.5 Carretera al Sur, La Paz, BCS, Mexico b The School for Field Studies, San Carlos, BCS, Mexico c Universidad Autónoma del Estado de Baja California, Unidad Valle Dorado, Ensenada, BC 22800, Mexico

a r t i c l e

i n f o

Article history: Received 9 March 2009 Received in revised form 24 July 2009 Accepted 13 September 2009

Keywords: Zostera marina Transplants Survival Nutrients Subtropical

a b s t r a c t Zostera marina is the dominant seagrass species in coastal lagoons on the western coast of Baja California Peninsula, and due to its coastal location it is threatened by natural and anthropogenic factors, as is happening in Puerto San Carlos, B.C.S., where a fish cannery unloads its wastewater to the beach. Apparently an extensive intertidal meadow replacement was established by great amounts of green macroalgae. We evaluated the possibility to mitigate the impacts of this cannery with transplants of Z. marina meadow using adult plants. The transplant experiment was made in two different seasons for which two undisturbed donor meadows were chosen: El Cuervo and San Carlitos. The winter one obtained a 30% and in San Carlitos 90% after 13 months and the autumn transplant in San Carlos obtained a 0% of survival after 3 months. The results of these transplant activities were reflected in the shoot density at the end of the experiment (San Carlos was of 482 shoots/m2 and San Carlitos of 818 shoots/m2 s and agree with the density of the natural meadows. This experiment shows that it is possible to develop a small-scale seagrass restoration as mitigation for Baja California coastal lagoons which are under severe threat for coastal development. © 2009 Elsevier B.V. All rights reserved.

1. Introduction Seagrasses, like other wetlands on the coastal zone, are susceptible to the effects of human activities like pollution, which modifies the sediment condition besides contributing to nutrient excess (Mann, 1982). Pollution could decrease meadows’ vitality since the excessive contribution of nitrogen and ammonium in the water column can inhibit growth, productivity and survival.

In these cases the effects can be amplified by elevated temperatures and salinities (Short, 1983; Taylor et al., 1995; van Katwijk et al., 1997; Touchette et al., 2002). The result of adverse conditions might increase the cover of epiphytes, reducing the availability of light and nutrients on the leaves, which could affect photosynthesis and therefore oxygen concentration in sediment and increase sulfide, causing their deterioration and death of seagrass in short or long term (Carlson et al., 1994; Pedersen et al., 2004).

When anthropogenic activities cause damages, there are two possible ways of action: restoration to “return to a previously exist-

∗ Corresponding author at: Programa de Investigación en Botánica Marina, Departamento de Biología Marina, Universidad Autónoma de Baja California Sur, Km 5.5 Carretera al Sur, La Paz, BCS, Mexico. Tel.: +52 612 1238800.

E-mail address: riosmena@uabcs.mx (R. Riosmena-Rodríguez).

0925-8574/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.ecoleng.2009.09.004

ing natural or altered condition from a disturbed or totally altered condition by some action”, or mitigation that involves “restoration, creation or enhancement of the system to compensate for permitted wetland losses” (Fonseca et al., 1998), which is an action to prevent or diminish a damage and is required generally by the federal governments of some countries (Clark, 1996). However, limited information on subtropical areas is available.

Large-scale restoration of seagrass systems has occurred mainly in developed countries, such as the United States (Fonseca et al., 1996; Orth et al., 1999; Gayaldo et al., 2001), Australia (Kirkman, 1999; Meehan and West, 2002) and the Netherlands (Bos et al., 2005). Some of these methods are still at an experimental level because they are continually tested for different seagrass species, and their success level depends mainly on each site characteristics (Hawkins et al., 1999). In Mexico seagrass restoration experience is limited to a few trials in Baja California and the Caribbean, where only the first one was done as a restoration experiment (CabelloPasini, 1984; van Tussenbroek, 1996).

Although the importance of the protection of wetlands has been recognized, Mexico does not have any law or norm that protects these ecosystems and establishes clearly how restoration activities must be made, with the exception of the NOM-022-SEMARNAT2003 that protects mangroves and wetlands (in which seagrasses and macroalgae are briefly mentioned).

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Carrera-González and De la Fuente (2003) suggest that large extensions of Zostera marina that exist in Bahía Magdalena (approx.

14,000 ha), mainly are intertidal beds. Even so, in the intertidal zone towards the south of Puerto San Carlos, an ample Z. marina bed existed and has been disappearing in the last 10 years (RiosmenaRodriguez, personal observation, October 1989). This area is right on the influence zone of the residual water pen unloading from the fish cannery of the port (Boudrias, personal communication).

In spite of this, there exist no historical registries of populations of this zone, water quality and its importance in recruitment of commercially important species (like mollusks and fish that are widely exploited).

Therefore the goal of this paper is determined if Z. marina populations can be restored in a subtropical area by transplanting adults.

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connects to the sea by a brief channel (Félix-Pico, 1993). The system is generally shallow; depth at most channels is around 3 m and in the main channel it is about 10 m. This anti-estuarine system is characterized by elevated temperatures and salinities due to high evaporation rates mainly in the shallower zones in the bay (LluchBelda et al., 2000). This work was done in the boundary between the Santo Domingo and the Magdalena Bay zones (Fig. 1).

Puerto San Carlos is the principal population center in this bay area, where there are two industrial fishing plants. In these plants, sardine and tuna are canned (mainly in tomato sauce or oil), frozen and in a smaller degree, fish flour is prepared (Guzmán-Vizcarra, 2000). In spite of having a treatment plant for residual water, this company frequently throws out the wastewater of fish processing, creating an impact on the near beach and sea (personal observation).

1.1. Study area 2. Methods The Magdalena-Almejas lagoon complex is on the western coast of Baja California Sur, Mexico. This complex covers an area of 114,600 ha and it is divided into three zones: the northwest, composed by estuaries and channels like Santo Domingo, the central zone called Magdalena Bay which is connected with the sea by a mouth of deep channel and the south zone, Almejas Bay, which

Transplants were carried out in two different seasons (autumn 2005 and winter 2006) and two donor meadows were chosen: (1) located at north of the Santo Domingo Channel (El Cuervo, EC 24◦ 55# N, 112◦ 09# W) and (2) San Carlitos (SCa) located at the entrance of the same name estuary (24◦ 48# 58## N, 112◦ 09# 08## W).

Fig. 1. Location of the transplants sites in the northwest zone of Magdalena Bay.

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The donor plants for the autumn transplant were taken from EC and planted in San Carlos (SC 1), while the winter donor plants were from SCa and planted in SC 2 (about 200 m south SC 1) (Fig. 1).

We followed the core methodology described by Fonseca et al.

(1998) adapted to fulfill our aims (Fig. 2). The planting units (PU) measured 10 cm in diameter by 10 cm deep. Once extracted its content was placed in plastic containers of the same diameter and for each one the number of shoots was counted. Planting units for the experiment were transported by boat to the School for Field Studies in San Carlos and stayed in water until the moment of their plantation.

In each one of the donor locations a control transplant was made and other PU were extracted to be planted in San Carlos. In SCa another experiment was done, besides the control one. Each transplant was separated by 50 m and consisted of two groups of 10 PU. There was a distance of 50 cm between each planting units. These three sites are in intertidal zones within the area of channels to the northwest of the bay, but EC and SCa are apparently pristine areas.

Monitoring was done seven times from October 2005 to March 2007 and consisted of the evaluation of survival percentage by enumeration of live PU (defined as the presence of green leaves), the number of shoots and area of each PU. Natural density was evaluated by counting the number of shoots in five quadrants of 25 cm × 25 cm placed each 10 m in three transects of 50 m, perpendicular to the coast.

Column and pore water samples were taken to determine nutrients concentration in these three sites (San Carlos, SC; San Carlitos, SCa; and El Cuervo, EC, we will follow the same format for the rest of the document) and were placed in a refrigerator to keep them cold until processed in the laboratory. Pore water samples were

obtained at low tide in each site by making a hole in the sediment with a shovel, waiting for it to be water-filled and later a dark BOD bottle was introduced.

Nitrate (NO3 ), nitrite (NO2 ), ammonium (NH3 ), and phosphates (PO4 ) concentration were determined for column water samples, and for pore water in addition to these sulfide (H2 S) content was also analyzed. Temperature and salinity were determined at the same time of sampling with a thermometer and a refractometer.

The analyses were based on methods of Bendschneides and Robinson, Morris and Riley, Solórzano, and Murphy and Riley for the first four (Strickland and Parsons, 1972) and the methylene blue method for the last one (Cline, 1969).

Time needed to transplant each PU was estimated to calculate the effort needed to restore a damaged seagrass bed in this area; this was the mean of collection, preparation and planting time for each PU. 2.1. Statistical analyses Density data were extrapolated to 1 m and grouped in seasons for further comparisons. Kruskal–Wallis analysis was applied to experimental transplants density and the calculated area data for all sites. Two-way ANOVA was applied to determine differences between natural and experimental density.

Mean number of shoots was compared by a two-way ANOVA only for SC 2 and SCa sites because we considered analyzing only the same date transplants and also because first transplant (SC 1) failed.

Multiple regression analyses were done for nutrient factors from column and pore water and density data to determine if these

Fig. 2. Core transplant method with soda bottles. (a) Bottle insertion on sediment; (b) placement of core on same diameter containers; (c) numeration and counting of shoots for each PU; (d) marks placement to identify each PU; (e) recent transplant view.

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Table 1 ANOVAs comparing density from natural and experimental transplants; ˛ = 0.05.

Fig. 3. Survival of experiment and control transplants on different seasons. On San Carlos two transplants were done, the first one on 2005 Autumn (SC 1) and the second on 2006 Winter (SC 2). (c) Means control transplants.

concentrations affected the fate of transplants. Data analyses need to be explained better.

3. Results At the end of the experiment major survival was high in SCa (100%), mid in SC 2 (50%) and low in EC (5%) which experienced a drastic decrease in the first months after transplant. After 4 months in SCa and SC 2, survival became stabilized and in EC after 6 months (although on the last date only one PU survived). In the San Carlitos (control) transplant, the observed “decrease” was due to the loss of some of the marks that identified each PU. Last date increase in SC 2 and SCa (Fig. 3) was due to shoots growth in some PU where no shoots were seen on the last monitoring date. In addition, the first transplant experiment (SC 1) the PU did not survive longer than 3 months. Some PU joined to the adjacent patches, especially in SCa; therefore, they were still considered for density analysis but not for survival.

The area used by experimental controls on EC showed little increase along the 17-month experiment (0.14 ± 0.07 m2 SD) and finalized with a loss of 0.15 m2 with respect to the initial area that was 0.17 m2 for all cases (Fig. 4). However, San Carlos and San Carlitos experiments displayed an increase of 0.36 m2 in the first case and in the second of approximately 0.6 m2 . Kruskal–Wallis analysis showed significant differences between the sizes of experiments in San Carlos and San Carlitos with El Cuervo (H (2, N = 156) = 9.107672; p = 0.0105).

Mean shoot number by m2 on all transplant sites varied seasonally, and in EC increased considerably in the 2006 summer (Fig. 5).

Fig. 4. Transplants occupied area in the different sites throughout 17 months.

Site

Variable

SS

El Cuervo San Carlos San Carlitos

Exp/Nat Exp/Nat Exp/Nat

0.63569 0.01369 0.05903

df

F

p

1

1.498588 0.025500 0.130769

0.225838 0.873521 0.718262

The densities obtained in SC 2 and those of SCa did not present significant differences (F1,2 = 0.32, p = 0.57). When comparing natural meadows against experimental density, no significant differences were observed for any of the three sites, so we can assume that transplants were successful since the variability of its density was like that seen in natural environments (Table 1).

Nutrients in the column water displayed variations between months in sites; nevertheless, it was observed that NO2 + NO3 at EC and SCa had the lowest values from May to October and the highest in October of the 2006, unlike SC 2 that showed a slight increase from January 2006 to March 2007, in spite of showing higher concentrations (13.4 !M) in March 2006.

Ammonium in SC 2 had a considerable increase in 2006 March (11.62 !M), and later decreased in 2006 December and 2007 May (4,03 !M). This site showed higher values than other sites. Phosphate in SC 2 was clearly greater than the other sites, although they showed two peaks, one at the end of the winter and other at the beginning of summer.

On pore water the NO2 + NO3 concentration presented the highest values in 2006 March, decreasing in 2006 October and 2007 March in all sites. In SCa no temporal pattern was observed but the lower concentrations were recorded in 2006 August and the highest in 2006 October. Phosphate in all sites displayed a tendency towards the increase in 2006 October. Sulfides in this same site had a significant increase from August to October 2006 (8.42–27.15 !M, respectively) (Table 2).

Multiple regression analysis between experiments density and nutrients concentration did not show significant relationships.

Temperature ranged from 21.5 to 31 ◦ C. The lowest values were between January and March and the highest in October. This pattern is similar to the one reported by Álvarez-Borrego et al. (1975) and Rosales-Villa (2004) with lower temperatures in winter and increases in summer in almost all the bay. Salinity values varied from 35 to 43 ppm and unlike the temperature pattern, greater values were in the months from January to March and the minors in August and October.

4. Discussion Core technique was used in this experiment, and although a different tool was used to do it (plastic bottles instead of PVC tubes, tins or shovels; Davis and Short, 1997) our results were similar to those of other studies using the same technique (Gayaldo et al., 2001; Orth et al., 2003).

The cost and transplanting effort estimation is important since they give us an idea of the method’s efficiency. Therefore its assessment in experimental or pilot projects would let us decide if it is possible to apply them on greater scales (Fonseca et al., 1998). In this case the effort (time needed to make the transplant) turned out to be shorter than that in other works, which could be because we tried to make the field work faster because of the short time that the low tide allowed us to work in the zones of transplant. Our results confirmed that survival and initial density of transplants diminishes logarithmically (even until its disappearance) (Campbell and Paling, 2003), followed by the stabilization of the density after some time (Bos and van Katwijk, 2007). Two trends were observed, one in each locality: the transplant in San Carlos disappeared completely

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Fig. 5. Mean number of shoots/m2 in each site on the different seasons.

Table 2 Common nutrient concentration on water column and pore water on seagrass areas, maximum levels for toxicity and this work values.

Water column

NO2 + NO3

Common concentrations (!M)

Threshold (!M)

Water column

Water column

<3a 0.05–8b

NH4

<3a 0–3.2b

PO4

<2a 0.1–1.7b

a b c d e f g h

Pore water

This work (!M) Pore water

Water column EC Mean ± SD

2–10b <20–1000a 1–180b 10–300d <20a 0.3–20b <10 mMg

3.5–7 (NO3 )b 8 (NO3 )c 100f d

25–125

SC Mean ± SD

SCa Mean ± SD

EC Mean ± SD

SC Mean ± SD

SCa Mean ± SD

2.5 ± 4.73

2.9 ± 4.85

0.8 ± 0.68

1.8 ± 1.35

1.4 ± 0.50

5.2 ± 5.64

0.6 ± 0.23

5.8 ± 4.96

0.9 ± 0.65

41.9 ± 16.40

39.3 ± 7.54

34.3 ± 6.68

1.42 ± 1.40

0.8 ± 0.56

4.5 ± 2.19

6.3 ± 3.19

7.4 ± 5.72

12.7 ± 9.08

8.7 ± 6.68

11.7 ± 11.04

d

<250

0.57 ± 0.56 100–1000e

Pore water

>1000h

Lee et al. (2007).

Touchette and Burkholder (2000).

Touchette et al. (2003). van Katwijk et al. (1997).

Holmer and Bondgaard (2001).

Short (1983) and Dennison et al. (1987) in Lee et al. (2007).

Carlson et al. (2002). www.vacadsci.org.

after 3 months, while the other in El Cuervo diminished to a 20% and were the same during the following months.

Even further experiments should be done at longer time periods, the seasonal element seemed to be an important factor for survival: the 2006 winter one performed better than the one of 2005 fall. In both cases donor meadows were intertidal. Seagrass developed in this zone is adapted morphologically (Tanaka and Nakaoka, 2004) and physiologically (Ensminger et al., 2001) to drastic changes such as long drying periods and high levels (high, médium, low) of expostion to light that could inhibit the photosynthetic activity, the reason why this factor could not have affected the experiments.

Also, changes in shoot density were observed, showing an increase from the spring to the summer and diminishing in autumn and winter. This agrees with air exhibition time, since it is mainly in winter when the amplitude of the tides rises especially during day time. Similar results have been observed in transplant experiments

with other seagrass species like Thalassia hemprichii, Cymodocea rotundata, C. serrulata (Tanaka and Nakaoka, 2004), Enhaulus acroides and Phyllospadix iwatensis (Erftemeijer and Herman, 1994; Yabe et al., 1995).

When there is sufficient light available and temperatures are low (characteristics present in winter–spring), a positive carbon balance (C) is reached (Lee et al., 2007). Therefore, probably the February transplant performed better, due to favorable environmental conditions (before and after the transplant) that promoted energetic reserves production.

Experimental and natural density did not present significant differences, even between the three sites the same pattern of increase was displayed in summer/fall and diminution in winter/spring. On the other hand, transplant area increased until joining to adjacent patches due to clonal growth and not by sexual reproduction, even though it remained until the following reproductive cycle near a

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small natural meadow that already presented flowers and seeds in 2007 March.

Natural density observed during this work follows the same temporal variation pattern as that for intertidal meadows on Baja California Sur coastal lagoons, being greater in the beginning of summer and decreasing in autumn (Santamaría-Gallegos et al., 2001, 2007), which suggests that high temperatures are the principal limiting factor for its development in this area. Also we found greater densities on San Carlos, San Carlitos and El Cuervo meadows in 2006 March than that in 2007 March, coinciding with the diminution of 3–4◦ from 2006 to 2007 on the same dates. Because of this we could infer that the best season of the year to perform some transplant effort in Bahía Magdalena is at the end of winter or earlier spring.

Nutrient effects: Water column and sediment nutrient concentration are the most important features for water quality (Kaldy, 2006) and therefore seagrass systems health, because high concentrations imply the outbreak of negative events for marine phanerogams communities (Fourqurean et al., 2003).

In this study water column nitrites ranged between 0.11 and 0.48 !M, nitrates between < 0.1 and 13.3 !M and phosphates between < 0.1 and 3.64 !M, which resembles the values found in Bahía Magdalena by Rosales-Villa (2004) (<0.01–0.623 !M; <0.05–12.35 !M and 0.21–2.6 !M, respectively). Our results were slightly higher than those of this author probably because samples were not taken in the channels area but on shallow zones where tides’ influence is reduced (Rosales-Villa, 2004). Also, according to data of different authors, nutrient concentration on pore and column water of the three sites would be within the “normally found” intervals, or were much smaller than that which would be considered toxic levels (Table 2), the reason we could not affirm that these had some influence on poor survival and density of San Carlos’ transplants (SC 1 and SC 2).

Also regressions were not conclusive as far as the relation of experiments’ density and nutrient concentration on water is concerned, because we expected that in San Carlos we would find greater values than that in the other two sites due to the constant nutrients contribution from the cannery (Chaffee, 1998; Padilla˜ 2001).

Gamino, Therefore, the low survival of both San Carlos transplants, as well as the natural meadow diminution, could be caused indirectly by the cannery nutrients loading, which means nutrients could have favored the proliferation of laminar green macroalgae (up to 10 cm of thickness) that reduces light (the major seagrass limiting factor) (McGlathery et al., 2001) and increases the production of organic matter, promoting the subsequent dissolved oxygen diminution, avoiding gaseous interchange of sediment and water column and causing prolonged anoxic conditions in hipogean tissues (Greve et al., 2003).

These macroalgae are present all year, increasing at the end of the summer and autumn, but remaining in great amounts until the following winter and spring. Is until the next summer when its density diminishes remarkably (personal observation) because of the high temperatures and tides, whose influence in the shallow zones of the bay is much smaller than in the channels (RosalesVilla, 2004; Morales-Zárate et al., 2006). Therefore if this is what has been occurring for several years in San Carlos because of the cannery wastewater, it is probably the origin of the natural meadow disappearance, because if macroalgae remain in systems like this one and persist by several years, seagrass cannot return to settle in (Hauxwell et al., 2001). Hence the principal action to be taken in this place should be the adequate treatment of the cannery wastewater.

Although seagrass populations in the bay are in general in good health (Santamaría-Gallegos et al., 2007) throughout this lagunar

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complex. We have found few and small population centers (San Carlos Port and López Mateos Port) that could influence them by their industrial and residential residual waters. The increase of nutrients, salinity and temperature because of the anthropogenic activities as well as the climatic change (Orth et al., 2006a), which as a whole may represent a serious threat for seagrasses in this area. This experiment shows that is possible to develop a smallscale seagrass restoration as mitigation for Baja California Coastal lagoons that are under severe threat for coastal development.

Acknowledgments The research was carried out in the scope of the research project Seagrass restoration in Bahia Magdalena funded by the Packard Foundation in collaboration with the School for Field Studies (SFS).

We are thankful to the many individuals who assisted us in the field like the Marine Botany Research Program from the UABCS members and all the SFS staff. Also we thank Darren Sage who helped us with the English edition. The authors gratefully acknowledge the key financial and logistical and support provided by The School for Field Studies (SFS) Center for Coastal Ecology.

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