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In: Estuaries: Types, Movement Patterns… ISBN: 978-1-60876-859-2 Editors: J. R. Crane, A. E. Solomon, pp. 201-223 © 2010 Nova Science Publishers, Inc. Chapter 5 PHYSICO-CHEMICAL CHARACTERISTICS OF NEGATIVE ESTUARIES IN THE NORTHERN GULF OF CALIFORNIA, MEXICO Hem Nalini Morzaria-Luna 1 , Abigail Iris-Maldonado 2 and Paloma Valdivia-Jiménez. Centro Intercultural de Estudios de Desiertos y Océanos, A.C. Edif. Agustín Cortés s/n. C.P. 83550 Puerto Peñasco. Sonora, México. 2 Current address: Posgrado en Ecología Marina. Centro de Investigación Científica y de Educación Superior de Ensenada, BC. Km. 107 Carretera Tijuana - Ensenada C.P. 22860, Ensenada, B.C. México. ABSTRACT We describe water quality in two hypersaline negative estuaries in the Northern Gulf of California, along the coast of Sonora, Mexico, over a two-year period. In the Northern Gulf, non-mangrove salt marshes known as esteros (negative estuaries) cover 134, 623 ha. Esteros are characterized by an extreme tidal range, higher salinity at their head than at their mouth due to high evaporation, limited freshwater input and a mixed semi-diurnal tidal regime. Between 2005 and 2007, we sampled surface temperature, dissolved oxygen, salinity, pH, depth, chlorophyll, nutrients (NH +4 , NO , NO , and PO 4 ), and total suspended solids across one wetland, Estero Morúa. We also led a participatory monitoring effort, where oyster farmers took daily measurements of surface temperature, salinity, pH, and dissolved oxygen in both Estero Morúa (31°17´09” N; 113° 26´19” W) and Estero Almejas (31°10´15” N; 113°03´53” W). These sites allow comparisons between distinct habitats and levels of oceanic influence. Estero Morúa is a high energy lagoon with a narrow mouth and a prominent permanent channel restricted by spits, while Almejas is an open bay with a large intertidal mudflat. Among the main findings are 1) Surface temperatures follow a seasonal pattern, with highest temperatures in June to September and lowest from December to February. 2) Low rainfall and runoff together with high seawater input and evaporative loss results in high salinities. 3) High dissolved oxygen concentrations and low nutrient levels are indicative of the recharge rate between the wetlands and the sea, and are characteristic of oligotrophic systems. It is likely that The exclusive license for this PDF is limited to personal printing only. No part of this digital document may be reproduced, stored in a retrieval system or transmitted commercially in any form or by any means. The publisher has taken reasonable care in the preparation of this digital document, but makes no expressed or implied warranty of any kind and assumes no responsibility for any errors or omissions. No liability is assumed for incidental or consequential damages in connection with or arising out of information contained herein. This digital document is sold with the clear understanding that the publisher is not engaged in rendering legal, medical or any other professional services.

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In: Estuaries: Types, Movement Patterns… ISBN: 978-1-60876-859-2

Editors: J. R. Crane, A. E. Solomon, pp. 201-223 © 2010 Nova Science Publishers, Inc.

Chapter 5

PHYSICO-CHEMICAL CHARACTERISTICS OF

NEGATIVE ESTUARIES IN THE NORTHERN GULF OF

CALIFORNIA, MEXICO

Hem Nalini Morzaria-Luna1, Abigail Iris-Maldonado

2 and

Paloma Valdivia-Jiménez. Centro Intercultural de Estudios de Desiertos y Océanos, A.C. Edif. Agustín Cortés s/n.

C.P. 83550 Puerto Peñasco. Sonora, México. 2 Current address: Posgrado en Ecología Marina. Centro de Investigación Científica y de

Educación Superior de Ensenada, BC. Km. 107 Carretera Tijuana - Ensenada

C.P. 22860, Ensenada, B.C. México.

ABSTRACT

We describe water quality in two hypersaline negative estuaries in the Northern Gulf

of California, along the coast of Sonora, Mexico, over a two-year period. In the Northern

Gulf, non-mangrove salt marshes known as esteros (negative estuaries) cover 134, 623

ha. Esteros are characterized by an extreme tidal range, higher salinity at their head than

at their mouth due to high evaporation, limited freshwater input and a mixed semi-diurnal

tidal regime. Between 2005 and 2007, we sampled surface temperature, dissolved

oxygen, salinity, pH, depth, chlorophyll, nutrients (NH+4, NO3¯, NO2¯, and PO4), and total

suspended solids across one wetland, Estero Morúa. We also led a participatory

monitoring effort, where oyster farmers took daily measurements of surface temperature,

salinity, pH, and dissolved oxygen in both Estero Morúa (31°17´09” N; 113° 26´19” W)

and Estero Almejas (31°10´15” N; 113°03´53” W). These sites allow comparisons

between distinct habitats and levels of oceanic influence. Estero Morúa is a high energy

lagoon with a narrow mouth and a prominent permanent channel restricted by spits, while

Almejas is an open bay with a large intertidal mudflat. Among the main findings are 1)

Surface temperatures follow a seasonal pattern, with highest temperatures in June to

September and lowest from December to February. 2) Low rainfall and runoff together

with high seawater input and evaporative loss results in high salinities. 3) High dissolved

oxygen concentrations and low nutrient levels are indicative of the recharge rate between

the wetlands and the sea, and are characteristic of oligotrophic systems. It is likely that

The exclusive license for this PDF is limited to personal printing only. No part of this digital document may be reproduced, stored in a retrieval system or transmitted commercially in any form or by any means. The publisher has taken reasonable care in the preparation of this digital document, but makes no expressed or implied warranty of any kind and assumes no responsibility for any errors or omissions. No liability is assumed for incidental or consequential damages in connection with or arising out of information contained herein. This digital document is sold with the clear understanding that the publisher is not engaged in rendering legal, medical or any other professional services.

Hem Nalini Morzaria-Luna, Abigail Iris-Maldonado and Paloma Valdivia-Jiménez. 202

residence time and tidal dynamics are the main factors dictating the physicochemical

dynamics of these systems.

INTRODUCTION

Negative or inverse estuaries are those where seawater is concentrated by the removal of

fresh water, either by evaporation that exceeds precipitation, or by freezing and the

occurrence of sea ice [1,2]. The former type is usually associated with arid climates and

occurs in both hemispheres including in the Red Sea, the Gulf of Suez, the Mediterranean

Sea, the Adriatic Sea, the Arabian Gulf, South Australia, and the Gulf of California [2].

Negative estuaries can be permanent or can be negative only during part of the year where

rainfall is strongly seasonal [3].

According to Miller et al. [4], salinity in negative estuaries can increase as one moves

horizontally from the mouth of the estuary to the head, especially in the bottom layers.

Gravitational circulation can lead to the export of high density lagoonal water, at the same

time that ocean water fills into the lagoon as a low-density surface layer. The water exchange

between the lagoon and the ocean is enhanced in the flood and ebb cycles. The physical and

chemical characteristics of water within estuaries are heavily influenced by meteorological

conditions [5], the amount of freshwater runoff [6] and tidal hydrology [7]. The interaction

among tidal hydraulics, open water, benthic and marsh surface processes yields unique water

chemistry profiles [7].

In Mexico, negative estuaries are hypersaline salt marshes where salinities may exceed >

40, pH ~ 9, oxygen is close to saturation and total nitrogen is low [8]. These wetlands are

found in both the Gulf of Mexico and Pacific coasts of the country, and are common in the

states of Baja California, Sonora and Oaxaca [9]. Negative estuaries in the Northern Gulf of

California, above 29 °N, are non-mangrove salt marshes locally known as esteros [10] that

connect to the open gulf by channels or inlets. The Northern Gulf is very arid, with mean

annual rainfall < 125 mm and mean maximum annual temperature of 22 - 26 °C [11]. There

are no perennial rivers [12], and the lack of freshwater input and excess evaporation result in

an increasing salinity gradient towards the head of wetlands [13]. Tidal range in the Northern

Gulf may exceed 8 m [14], so the wetlands empty out during low tides and at high tides the

water floods the marsh surface, resulting in varied areas of open water habitat, exposed

mudflat, and shallow water available daily [15]. Thus, tidal hydrology plays an important role

in connecting different areas of the marsh that remain isolated during most of the tidal period.

Environmental conditions can be challenging for the organisms that inhabit esteros.

Many species use negative estuaries opportunistically, entering only during high tides to rest,

feed and reproduce [3]. Other species are residents with special adaptations to withstand the

harsh environmental conditions. Esteros represent one of the hottest zones occupied by fish

[16]; eurythermal species such as the gobies Gillichthys miriabilis, the longjaw mudsucker

and the endemic Gillichthys seta, the shortjaw mudsucker are some of the most abundant

residents [17,18]. These fish can withstand the daily temperature fluctuations in the wetlands

that can range from 5° to 7° C seasonally [19]. Other species, such as the halophyte marsh

plants Sarcocornia pacifica, Mönantochloe littoralis, and the endemic Distichlis palmeri, use

the controlled uptake of Na+ into cell vacuoles to drive water into the plant tissues against a

low external water potential.

Physico-Chemical Characteristics of Negative Estuaries… 203

The description of water quality in negative estuaries can be useful to understand the

ecology of species that inhabit them and represents important background information on the

dynamics of physical and chemical parameters. We evaluated seasonal variability of water

quality in Estero Morúa and Estero Almejas in the state of Sonora, Mexico as part of a project

to determine the causes of oyster mortality [21]. We recorded monthly measurements in

Estero Morúa, as well as daily measurements in Estero Morúa and Estero Almejas as part of

participatory monitoring, where members of local oyster cooperatives measured key

parameters in their farms.

METHODS

Survey Location

We surveyed water quality in Estero Morúa (31°17´09” N; 113° 26´19” W; Figure 1) and

Estero Almejas (31°10´15” N; 113°03´53” W; Figure 1). Estero Almejas and Morúa are

negative estuaries with a higher salinity at the head than at the mouth [1]. These sites are

located in the Northern Gulf of California, in the state of Sonora in Northwestern Mexico.

Estero Morúa and Estero Almejas are within the municipality of Puerto Peñasco; the main

city in the area is Puerto Peñasco (Pop. 44,875, [22].

The Northern Gulf of California is characterized by climatic conditions of a low-altitude

coastal desert (Foster 1975), with scarce rain during the summer averaging 70 – 90 mm

[24,10]. The annual temperature average is 20.1°C, fluctuating between 11.3°C in January

and 30°C in August [10]. High evaporation rates, coupled with the lack of freshwater input,

results in the increasing salinity gradient inside the estuaries [12]. The Sonoran coast

experiences prevailing northerly and northwesterly winds in the winter, and southern and

southeasterly winds in the summer. During the winter, offshore winds predominate and in the

summer onshore winds are dominant [24]. Maximum wind speeds vary from 43 km h-1

(maximum one-day mean) in winter to maximum 21.6 km h-1 in summer, with occasional

gusts reaching 118 km h-1 [25].

Estero Morúa (Figure 2) extends over 1,097 ha [13], and is of deltaic origin; it formed as

part of an estuarine system fed by the Sonoyta river, although the flow is now diverted for

agriculture and no longer reaches the sea [26]. In the northeastern side of the wetland,

remnant riparian vegetation remains in the dry river bed maintained by subsurface flow [13].

Estero Morúa is a high energy embayment with a narrow mouth and a central channel

restricted by spits [27] that measures 11.58 km in length with a mouth 0.5 km wide. Rock

outcroppings protrude through the sand at the mouth of the estero. Sediment grain at the

mouth is coarse sand (0.5 mm) and particle size decreases inwards to fine sand in the side

channels and silt in the upper reaches at the head [27]. The main lagoon is separated from the

Gulf by barrier dunes that used to reached heights of ~100 feet [28], but have been partially

been flattened during the construction of the surrounding residential developments. Estero

Morúa houses four aquaculture cooperatives that farm Japanese oysters (Cassostrea

virginica) along the main tidal channel.

Hem Nalini Morzaria-Luna, Abigail Iris-Maldonado and Paloma Valdivia-Jiménez. 204

Figure 1. Location of Estero Morúa and Estero Almejas, hypersaline negative estuaries in the state of

Sonora, northwestern Mexico and (●) oyster cooperatives, where the participatory water quality

monitoring program was implemented.

Figure 2. Estero Morúa, Sonora, México at neap tide, July 2009. Photo: Alejandro Castillo. CEDO

Intercultural.

Physico-Chemical Characteristics of Negative Estuaries… 205

Figure 3. Estero Almejas, Sonora, México at neap tide, July 2009. Photo: Alejandro Castillo. CEDO

Intercultural.

Estero Almejas (Figure 3; also known as Bahía Salina) is located in Bahía San Jorge, and

extends over 2,286.02 ha [10]. The wetland is a semi-open embayment with a sand bar to the

north composed of consolidated dunes. When the tide recedes, it exposes extensive mudflats.

The landward area is covered in salt flats, where salt was harvested in evaporative lagoons

(Salinera del Desierto Rojo). The coastal beaches and mudflats of Estero Almejas formed

during the Holocene, ~ 5,000 BP, when sea level reached its maximum. The beaches and

mudflats were formed by wind-blown sediments and silt deposited by the tides and currents

[13]. Estero Almejas has one oyster farm and a fishing camp in the vicinity (Pop. 41) [22]

which sustains important artisanal fisheries for blue crab (Callinectes arcuatus and

Callinectes bellicosus), rays, and pelagic fish [23]

In both Estero Morúa and Almejas, the wetland channels are surrounded by salt marsh

vegetated with halophytes that rarely grow beyond 50-60 cm [29]. The immediate wetland

margin is covered by low shrubs including Palmer's frankenia (Frankenia palmeri), white bur

sage (Ambrosia dumosa), creosote bush (Larrea tridentata), salt bush (Atriplex polycarpa,

Atriplex canescens), and desert thorn (Lycium spp.) [30]. Beyond, we find vegetation of the

Sonoran Desert - Lower Colorado River Valley subdivision [29].

The tidal regime in the Northern Gulf is mixed semidiurnal (two high and two low tides

of different elevations in 24 hours), with tidal amplitudes of 5-10 m [31]. In the Puerto

Peñasco region tidal amplitude is 7.04 m, with lowest tides in April and highest in October

[21]. During the highest spring tide the marshes flood completely, and at the lowest neap tide

the wetlands empty, uncovering extensive mudflats where some water remains forming pools

[15].

We describe sample collection and analysis for the monitoring program in Estero Morúa,

where data were collected monthly during neap tide. We then describe the participatory

monitoring program in Esteros Morúa and Almejas, for which data were collected daily.

Hem Nalini Morzaria-Luna, Abigail Iris-Maldonado and Paloma Valdivia-Jiménez. 206

Monitoring Program in Estero Morúa

Sample collection – In Estero Morúa, samples were collected between 2005 and 2007.

We used a stratified random sampling design, to account for the difference in channel and

creek area across the marsh. Starting in August 2005, for each month we selected ten random

points across six sections. Each such set of ten points is referred to hereafter as a “survey”. In

total, we sampled 220 points throughout 22 months (Figure 4). Samples were collected at the

lowest tide of the neap tide, to minimize oceanic influence. Thus, collection times varied

monthly. Sampling points were visited in 1-2 days. The time for sampling was selected using

tidal prediction software (WXTide 32 Versión 4.7; http:\\wxtide32.com).

At each point we took three replicate measurements of each parameter: water

temperature, dissolved oxygen (D.O.), salinity, and pH (Figure 3). We also recorded water

depth, time and location. Dissolved oxygen, water temperature, and pH were measured with

an Oakton multimeter 300 (Oakton Instruments, Vernon Hills, Il. EUA). Sensors were

immersed in the water column until a constant value was obtained (Figure 5). Dissolved

oxygen is expressed in mg/L and temperature in °C. Oxygen measurements were

compensated by temperature but not for salinity, as salinity values were routinely higher than

the instrument's compensation limits. A pipette was used to collect 2-3 drops of water, which

were placed on a Vista refractometer to measure salinity on a 0-100 scale. Location was

recorded with an eTrex Garmin GPS (Garmin Ltd., Olathe, KS, EUA), in the WSG1984

coordinate system.

Figure 4. Sampling locations in Estero Morúa, Sonora, México where seawater samples were collected

in 2005 (●), 2006 (■), and 2007 (▲). Dashed lines indicate the six sections where random points were

selected monthly using a stratified random sampling design. Figure also shows habitat types.

Physico-Chemical Characteristics of Negative Estuaries… 207

Figure 5. Data collection in Estero Morúa, Sonora, México. Photo: Alejandro Castillo. CEDO

Intercultural.

Starting in September 2005, we also collected 4 liters of water at six alternate points

(usually points 1, 3, 5, 6, 8 and 10) for determination of dissolved nutrients (NO2¯, NO3¯,

NH+4 and PO4) and particulate compounds (total suspended solids, TSS, chlorophyll a, b and

c). Samples for TSS collected in September and October were lost, so data are only available

for this parameter from November 2005 to May 2007.

We also measured sea surface temperature on the open coast and ambient air temperature.

Sea surface temperature was measured daily at approximately 9 am outside of Estero Morúa,

at 31°17´21” N; 113°29´47” W. Between August 2005 and April 2006 temperature was

measured using a partial immersion mercury thermometer. After this date temperature was

measured using an electronic VWR waterproof remote probe thermometer with ± 0.1 °C

precision (VWR International LLC, Batavia IL, USA). Ambient air temperature was recorded

at CEDO's field station, ~ 0.6 km from Estero Morúa, using a Weather Monitor II station

(Davis Instruments, Haywood, CA, USA). We report monthly averages based on hourly data.

Sample analysis - We analyzed TSS using the gravimetric method [32]. We filtered

700ml of seawater or less, as necessary to saturate an ash-free Whatman GF/C filter of known

Hem Nalini Morzaria-Luna, Abigail Iris-Maldonado and Paloma Valdivia-Jiménez. 208

weight (previously burned at 400 °C for four hours). The filters were then dried at 60 °C until

of constant weight. The filters were re-weighed and the total solids were reported as the

weight difference between the two weights adjusted for volume filtered in mg/L.

Chlorophylls were analyzed following Arar [33]. We analyzed 700 ml of seawater or

less, as necessary to saturate a Whatman GF/C filter. We saved 20 ml of the filtered water for

nutrient analysis; these samples were frozen until analysis. While filtering the last 10 ml of

water we added 1 ml of saturated MgCO3 suspension. The filters were wrapped in aluminum

foil and frozen until analysis. For chlorophyll extraction, the filters were ground with 12 ml of

acetone with a glass rod and incubated for 4 h in the dark (shaking every hour), and

centrifuged at 1000 g for 5 min. The supernatant was read in a spectrophotometer at 750, 664,

647 and 630 nm. Concentrations of chlorophylls a, b and c were determined based on the

trichromatic equations of Jeffrey & Humphrey [34] and expressed as mg/m3.

The nutrient analysis was carried out in the Centro de Investigaciones Biológicas del

Noroeste, in Hermosillo, Sonora. Water samples were thawed and analyzed using the

microplate technique described by Hernández-López & Vargas-Albores [35]. This method is

based on the formation of colored complexes in 96-well plates that are then measured by

spectrophotometry, reducing costs while maintaining precision. Nutrient concentrations are

presented in μM.

Figure 6. Water temperature (means ± SE) between August 2005 and May 2007. a. Monthly

measurements in Estero Morúa (n = 30); b. Participatory monitoring in Estero Morúa, daily readings. c.

Participatory monitoring in Estero Almejas, daily readings.

Physico-Chemical Characteristics of Negative Estuaries… 209

Participatory monitoring

Sample collection - The participatory monitoring program collected daily data but had no

spatial replication, as all samples were taken in a single point across time. Measurements

were recorded between August 14, 2005 and May 15, 2007. In Estero Almejas, the Sociedad

Cooperativa de Producción Pesquera y Acuícola (SCPPA) La Cinita collected data

throughout the study period. In Estero Morúa, the SCPPA Unica de Mujeres collected data

between August and November 2005, after this time it was replaced by the SCPPA Aquamar.

Members of the cooperatives received a pH meter, a D.O. meter, and a refractometer from the

Aquaculture Institute of the State of Sonora. We prepared a manual and training course on

water quality monitoring, that were offered to members of each cooperative prior to the start

of the project. We also assisted the cooperatives with equipment maintenance and calibration

and maintained the database for the duration of the program.

Each day, a member of the cooperative registered near their oyster trays sea surface

temperature, D.O., salinity and pH. Oxygen measurements were compensated for temperature

but not for salinity, as salinity readings were routinely higher than the instrument's

compensation limits. We requested that measurements be carried out at or near the same time

every day. In Estero Almejas, the measurements generally occurred between 6-8 am, and

were recorded by 13 people who alternated. Readings were recorded on 95% of the days of

the study period. In Estero Morúa, one person was routinely responsible for data collection,

parameters were measured at variable times and compliance was only 77 %. Several problems

occurred during the participatory monitoring program, including equipment breakdown and

errors while measuring and recording data. Thus, the quantity of data available by parameter

and site is variable.

Data Analysis

We used linear regression to study the relationship between temperature, salinity, D.O.,

pH, total suspended solids, chlorophylls (a, b and c), and nutrients (NO-2, NO-3, NH+4 and

PO4) across the months surveyed. When negative values were present for parameters that

conceptually can only be ≥0, such as nutrients and chlorophylls, we corrected the data by

substituting negative values for 0. The Akaike Information Criterion (AIC) was used on the

linear models to select the variables that best explained the structure of the data [36]. Data

summarized in tables and graphs is untransformed. Data analysis was carried out in the R

Open Source system (R Development Core Team).

RESULTS AND DISCUSSION

Temperature, Salinity, pH and Dissolved Oxygen

Mean water temperature in Estero Morúa throughout the study period was 19.8 ± 0.2 °C

(Table 1). Temperature followed a seasonal pattern with highest temperatures in summer

(30.3 ± 0.3 °C in August 2005) and lowest in winter (9.4 ± 0.3 °C in January 2006; F =

362.27, P < 0.001; Figure 6). Previous studies in Estero Morúa found similar temperature

Hem Nalini Morzaria-Luna, Abigail Iris-Maldonado and Paloma Valdivia-Jiménez. 210

intervals. Place & Hofmann [37] found that on average water temperature in the estuary

ranged from 5° to 30°C during tidal cycles in winter and from 18° to 36°C during tidal cycles

in summer. Buckley & Hofmann [19] recorded temperature in the water column of Estero

Morúa between January and June 2001, and found a range from < 5°C in early January to

higher than 33 °C in June. We also found significant variability in water temperature between

sampling locations (F = 12.7, P < 0.001). Spatial variations in temperature in the wetland

result from differences in water depth, tidal exchange and bottom sediments, which may play

a role in the absorption or transfer of heat to overlaying waters [38].

Water temperatures from the participatory monitoring program were in agreement with

monthly data, although the latter average measurements throughout the tidal cycle. Mean

temperature was 22.2 ± 0.3 °C in Estero Morúa, and there was variation between surveys (F =

95.39, P < 0.001), with the highest mean in September 2005, 33 ± 0.4 °C, and lowest in

November 2006, 13.3 ± 1 °C. In Estero Almejas, temperature varied between 33 ± 1.2 °C in

August 2005, to 12.5 ± 1 °C in December 2005 (Figure 6), and there was significant variation

amongst surveys (F = 61.36, P < 0.001). Water temperature in both wetlands follows the

general patterns of sea surface and ambient temperature measured outside Estero Morúa

(Figure 7). The main exception is in winter, when water temperatures in the estuary are lower

because tidal areas are shallow and lack sufficient heat storage capacity. The pattern of

variation in water temperature is the result of variations of solar heating, which is extreme in

the desert climate of Northwest Mexico [1] and can also be related to seasonal changes in

water masses [39].

Table 1. Physical and chemical parameters of water in two coastal wetlands of the

Northern Gulf of California, measured between August 2005 and May 2007

Model Estero Morúa Participatory monitoring

Estero Morúa Estero Almejas

Mean Max Min Mean Max Min Mean Max Min

Temp. (°C) 19.77 ± 0.24 33.1 6 19.53 ±

0.28

39.6 10 22.19 ±

0.31

37.7 8.05

Sal. 46.13 ± 0.38 > 100 31 43.83 ±

0.16

54 34 47.12 ± 0.16 60 38

pH 8.06 ± 0.02 10.25 5.09 7.88 ± 0.02 8.98 6.08 7.91 ± 0.19 9.62 4.73

D.O.

(mg/L)

8.68 ± 0.07 16.12 3.81 8.31 ± 0.07 14.64 6.01 8.14 ± 0.06 12.14 5.25

NO3¯ (μM) 2.92 ± 0.16 6.52 0

NO2¯ (μM) 0.001 ±

0.0002

0.01 0

NH4+ (μM) 0.006 ±

0.0006

0.02 0

PO4 (μM) 0.002 ±

0.0004

0.04 0

TSS (mg/L) 18 ± 0.45 40.95 7.52

Chl a

(mg/m3)

0.13 ± 0.02 0 0.02

Chl b

(mg/m3)

0. 03 ± 0.01 2.54 0

Chl c

(mg/m3)

0.07 ± 0.02 2.92 0

Physico-Chemical Characteristics of Negative Estuaries… 211

Figure 7. Ambient and sea surface temperature (b.) measured in the CEDO field station and outside of

Estero Morúa during the study period (means ± SE).

Salinity values were high in Estero Morúa, overall 46.2 ± 0.4 (Table 1), and varied

between 53.2 ± 3.2 in April 2006 to 41.1 ± 0.45 in May 2007 (Figure 8). These hypersaline

values are likely due to excess evaporation and lack of freshwater input. The Puerto Peñasco

region receives < 100 mm of rain per year [24]. Although there was variation among surveys

(F = 10.15, P < 0.001) there was no seasonal pattern. We also found significant variation

between sampling locations (F = 83.8, P < 0.001), a product of the spatial variability in

salinity, with higher values at the head of the estuary compared to the mouth, where there is

more water exchange with the Gulf. Salinity increases in the inner arms of bays and lagoons

are typical in regions where evaporation exceeds river flow and precipitation [8]; in the

Northern Gulf evaporation exceeds precipitation by 250 cm/yr-1 [1].

In the participatory monitoring program, daily salinity readings in Estero Morúa (43.8 ±

0.2; 45.21 ± 0.56 April 2006 – 38.9 ± 0.5 August 2005) and Estero Almejas (47 ± 0.2; 49.7 ±

0.7 May 2006 – 42.4 ± 0.5 August 2005) were equivalent to monthly data. At both sites,

salinity varied among surveys (Estero Morúa: F = 6.44, P < 0.001; Estero Almejas: F = 20.24,

P < 0.001; Figure 8). Salinity values recorded in both Estero Morúa and Almejas are similar

to those reported for other inverse estuaries. In Bahía San Quintin, on the Pacific Coast of the

Baja California Península, México, average salinities range from 34.7 in summer to 33.8 in

winter [40]; while in Estero La Cruz, in the central Gulf of California, salinity averages 36.8

Hem Nalini Morzaria-Luna, Abigail Iris-Maldonado and Paloma Valdivia-Jiménez. 212

[41]. We found water salinity values as low as 31 in October 2005 and as high as >100 in

June 2006. These extreme values are common in negative estuaries. Valenzuela-Siu et al. [42]

found salinity varied between 35 – 42 in summer and 37 – 39 in winter at Estero Lobos.

pH values in Estero Morúa were on average 8.4 ± 0.2 (Table 1), with a high of 9.1 ± 0.1

in February 2006 and a low of 7.4 ± 0.2 in September 2006. The overall mean is slightly

higher than pH values for seawater in equilibrium with atmospheric CO2 (8.1-8.3) [38]. There

was no significant variation in pH values among sample locations or surveys (Figure 9). We

found that pH readings were very sensitive to small changes in how measurements are

collected, which could explain some of the high values. It is unlikely that high pH values are

related to plant growth which reduces CO2 content, as we did not sample the marsh surface.

pH data from the participatory monitoring program showed less variation than monthly data

(Figure 9). pH values in Estero Morúa varied between 8.1 ± 0.02 in November 2005 to 7.6 ±

0.03 February 2007 (7.9 ± 0.02 overall). In Estero Almejas, mean pH during the study period

was 7.9 ± 0.02, and varied from 8.2 ± 0.1 November 2005 to 7.4 ± 0.1 in October 2006

(Figure 9). Lower pH values, especially in the summer, could reflect the production of CO2

by the decay of organic matter in bottom muds [8].

Figure 8. Water salinity (means ± SE) between August 2005 and May 2007. a. Monthly measurements

in Estero Morúa (n = 30); b. Participatory monitoring in Estero Morúa, daily readings. c. Participatory

monitoring in Estero Almejas, daily readings.

Physico-Chemical Characteristics of Negative Estuaries… 213

Figure 9. pH (means ± SE) between August 2005 and May 2007. a. Monthly measurements in Estero

Morúa (n = 30); b. Participatory monitoring in Estero Morúa, daily readings. c. Participatory

monitoring in Estero Almejas, daily readings.

Dissolved oxygen concentrations in Estero Morúa were high (8.68 ± 0.07 mg/L), and

varied between 11.34 ± 0.18 mg/L in July 2006 to 6.21 ± 0.22 mg/L in August 2005

(Figure 10). We found that D.O. values varied with location (F = 2.46, P < 0.001) and survey

(F = 64.5, P < 0.001), with a general pattern of increasing concentrations in warmer months,

but no definite seasonal pattern (Figure 10). In other coastal lagoons, such as Estero La Cruz,

Sonora, D.O. shows a clear seasonal pattern with higher values in winter (8.58 ml/L) to (2.58

ml/l) in spring and summer [41].

The D.O. values we found are within the intervals previously reported in other coastal

lagoons in the Gulf of California [40]. Dissolved oxygen in Estero Almejas and Estero Morúa

measured during the participatory monitoring showed a similar pattern, with low values of 6.1

± 0.08 and 6.09 ± 0.08 mg/L respectively in August 2005, to highs of 10.91 ± 0.22 mg/L on

April 2007 in Morúa and 10.61 ± 0.11 mg/L on December 2006 in Almejas (Figure 10). The

high D.O. concentrations can be attributed to the high exchange rate between the wetland and

Hem Nalini Morzaria-Luna, Abigail Iris-Maldonado and Paloma Valdivia-Jiménez. 214

the sea, and the low depth of the water column during sampling, while high values in winter

are related to increased solubility at low temperatures [41].

Figure 10. Dissolved oxygen (means ± SE) between August 2005 and May 2007. a. Monthly

measurements in Estero Morúa (n = 30); b. Participatory monitoring in Estero Morúa, daily readings. c.

Participatory monitoring in Estero Almejas, daily readings.

Dissolved Nutrients

We found that nutrient concentrations in Estero Morúa were low, likely a result of low

precipitation and runoff. Figure 11 shows the fluctuations of the various forms of nitrogen

and of phosphate in water throughout the study period. Nitrate was the main inorganic N form

in Estero Morúa, with concentrations of 3.17 ± 0.15 μM (Table 1). The other nutrients were

present in lower concentrations, NO2¯, 0.001 ± 0.0003 μM, PO4, 0.002 ± 0.0004 μM, and

NH4+, 0.006 ± 0.0006 μM. Nitrogen concentrations are lower than values reported for other

hypersaline wetlands in the Northern Gulf. In Estero Lobos, NO2¯ + NO3¯ ranged from 1.2 –

1.1 μM seasonally and NH4+ increased from 0.6 μM in summer to 1.2 μM in winter [42]. The

dynamics of biophilic elements, such as nitrogen and phosphorus, in tidal estuaries are

strongly related to the variation in tidal cycle [43]. These changes are strongly dependent on

the spring-neap stage or amplitude [7], current velocity [44] winds [45] and precipitation rate,

Physico-Chemical Characteristics of Negative Estuaries… 215

which affect runoff [6]. The nutrients found in Estero Morua probably stem from internal

recycling and wind; desert dust may provide nutrient inputs to wetlands in arid areas [46].

Runoff during rain is most certainly an insignificant factor, as in 2006, Puerto Peñasco

received only 2.27 cm of rain and between January and June 2007 only 0.13 cm (Data: CEDO

Intercultural). In Northwest Sonora, there are no other nutrient sources, such as rivers or the

shrimp aquaculture farms that are present in coastal lagoons in the southern part of the state

[47]. The observed increase in NH4+ and NO2¯ during 2007 (Figure 11) could be related to

upwelling frequently present on the eastern coast of the Gulf of California during winter-

spring [48].

The low nutrient levels observed in Estero Morúa be an artifact from collecting samples

at low tide in wetlands nutrients can be rapidly sequestered by microbial activity in benthic

surfaces, in which case water column monitoring such as ours can result in an

underestimation of nutrient availability [50].

NO2¯and NH4+ concentrations were higher in winter and spring 2007 (Figure 11) relative

to other surveys (F = 11.28, P < 0.001; F = 34.72, P < 0.001), while PO4 showed few

differences between surveys (Figure 11). Nitrate concentrations were higher, 3.17 ± 0.15 μM,

than for other nutrients and showed high variability as a function of sampling location (F =

2.76, P = 0.02) and survey (F = 11.03, P < 0.0001), but there is no clear monthly or yearly

pattern. Patterns in the variability of total dissolved N (NO3¯ + NO2¯ + NH4+) in Estero Morúa

will reflect the concentrations of NO3¯, since levels of the other forms of nitrogen were so

low.

Figure 11. Nutrient concentrations (means ± SE) between August 2005 and May 2007 in Estero Morúa

(n = 6).

Hem Nalini Morzaria-Luna, Abigail Iris-Maldonado and Paloma Valdivia-Jiménez. 216

Figure 12. Total dissolved solids (means ± SE, n=12) measured monthly in Estero Morúa between

October 2005 and May 2007.

Particulate Compounds

The average TSS concentration was 18.06 ± 0.45 mg/L (Table 1). We sampled in low

tide where water depth during the study period was 15.26 ± 0.43 cm. In shallow areas, light

can penetrate to the entire water column and hydrodynamics are affected by bottom

morphology and wind, which promote the resuspension of materials, nutrients and small biota

from the bottom surface into the water column [50]. TSS is also influenced by the type of

vegetation, land cover and land use surrounding the site. Estero Morúa is surrounded by

Sonoran Desert, with low lying, scarce vegetation [29], and nearby residential developments

(Figure 2) have contributed to erosion by destroying vegetation and flattening the dunes that

surrounded the site on the seaward edge [28].

We found that TSS concentration varied between survey (F = 6.77, P < 0.001; Figure 12)

and sampling location (F = 4.36, P < 0.001). A high TSS concentration was present in May

2006 (27.75 ± 1.33 mg/L) and some summer months (Figure 12), but there was no clear

seasonal pattern. In estuaries, the cycling of suspended particles depends on processes such as

re-suspension and settling, mudflat processes and particle-particle interactions (i.e. Brownian

motion, differential settling and coagulation), which are driven by river flow, tidal energy and

storms and tend to be accentuated in shallow environments [51]. In Estero Morúa, the

variation in TSS is likely driven by wind and the tidal regime, as river flow and runoff are not

important factors in the region [10].

Chlorophylls

The chlorophyll a (Chl a) concentrations observed in Estero Morúa indicate a system

with low primary productivity. Although the Gulf of California is very productive [13]. The

Northern Gulf exhibits patches of high Chl (up to > 2 mg/m3) even during summer due to

Physico-Chemical Characteristics of Negative Estuaries… 217

tidal mixing which carries cold and nutrient rich waters to the surface, throughout the year

[52].

In esteros of the Northern Gulf, the oceanic influence is strong, resulting from the

exchange of water during high tides [41]. A stable isotope analysis of trophic food webs in

Estero Morúa found that marine derived phytoplankton contributes the most carbon to the

system [53]. Mean Chl a concentrations were on average 0.13 ± 0.02 mg/m3 for the study

period (Table 1). Chl a concentrations showed a significant variability between sampling

locations (F= 2.96; P = 0.009) and surveys (F= 2.26; P = 0.004; Figure 13). The highest

concentration was found in June 2006 (0.50 ± 0.32 mg/m3; Figure 13) but there was no

seasonal pattern. The average Chl a concentrations in Estero Morúa are on the low range of

previously reported values for other arid wetlands. Gilmartin and Relevante [49] found values

between 0.2 – 19.9 mg/m3 in 12 coastal lagoons of the Gulf of California. Negative estuaries

in the Northern Gulf are usually less productive than positive estuaries because of the scarcity

of organic matter, especially at their head waters [1].

The concentrations of chlorophyll b (Chl b) and chlorophyll c (Chl c), were low (0.03 ±

0.01 and 0.07 ± 0.02 mg/m3 respectively). These parameters were only detected in a few

surveys. Both were found in January, February, and June 2006. Chlorophyll b was also found

in April 2007 and Chl c was detected in August 2006, and January and March 2007.

Relationship between Parameters

Explanatory linear models for the variables measured are found in Table 2. We found a

significant negative relationship between temperature and dissolved oxygen, likely due to the

relationship between water temperature and gas saturation that results in less oxygen being

available at higher temperatures [41]. We also found a negative relation of temperature with

pH, and a positive response in relation to depth. There was a positive relationship between

variability of NO2¯ and NO3¯ , and a negative relation between NO3¯ and NH4+, as expected

since NH4+ is sequentially oxidated to NO2¯ and then to NO3¯ during bacterial

denitrification [54]. In some cases these nitrogen forms were also related to D.O., pH,

temperature, depth, salinity. Strong positive relationships were found between PO4, salinity,

D.O. and NO3¯. Phosphate concentrations and dissolved oxygen are linked and controlled by

the rate of water exchange and biological processes [55]. Lower TSS values were associated

with lower depths, salinity, temperature, and Chl a. Finally, Chl a concentrations showed a

negative relation with TSS and were a positive function of PO4, water temperature, depth, and

salinity, underscoring the fact that microalgal biomass is sensitive to changes in

environmental conditions [43], and is regulated by light [41].

CONCLUSIONS

Estero Morúa and Almejas are hypersaline systems, where temperature, dissolved oxygen

concentrations, pH, and salinity are highly dependent on depth, tidal circulation, and solar

heating. The hypersaline conditions are prevalent year-round because of the low precipitation

and high evaporation present in the region [1]. We found that environmental conditions

Hem Nalini Morzaria-Luna, Abigail Iris-Maldonado and Paloma Valdivia-Jiménez. 218

resulting from physical and chemical factors can be extreme: temperatures ranged between 6°

and ~40 °C and salinity reached > 100. Overall levels of dissolved oxygen were high > 8

mg/L and nutrient concentrations were low, except for nitrate, particularly in summer and

autumn, resulting in oligotrophic conditions. The complex interactions between biological,

physical and chemical parameters of water in these estuaries can exert stress in the organisms

found in different environments in the marsh, many of which are important commercial

species in the region.

Table 2. Linear models for the selected physical and chemical variables in Estero

Morúa, Sonora. Asterisks indicate explanatory variables (ANOVA, ns: not significant, .

P < 0.1, * P < 0.05, ** P < 0.01, ***: P < 0.001). Models with lowest AIC values were

selected. Negative relationships are underlined.

Model Temp. Sal. pH Depth D.O. NO3¯ NO2¯ NH4+ PO4 TSS Chl a

Temp. . *** *** ***

Sal.

pH ***

D.O. ***

NO3¯ ns *** *** ***

NO2¯ ns ns ** *** ***

NH4+ ns *** *** *** ***

PO4 *** *** *** * .

TSS *** * ** *

Chl a * *** * ns ns ns * *

We found that seasonal cycles clearly determine physicochemical variables such as

temperature and salinity, but the seasonal effect was not as clear for other variables such as

TSS (Figure 12) and Chlorophylls (Figure 13). These variables might experience higher

spatial variability or be influenced by the spring-neap variations in tidal cycle [41]. On a time

scale of hours, the entry of sea water could be responsible for changes in salinity, nutrient

concentrations, and suspended solid content [43]. Mixing and strong currents due to the

macrotidal regime likely preclude the formation of vertical gradients during high tide [42].

Current velocities in the mouth of Estero Morúa can reach 50 cm/s and decrease to 10 cm/s in

the arms of the wetland and residence time is only 6 hours [21]. As a result, during high tides,

physicochemical parameters likely approximate seawater. For example, water salinity during

spring tides in Estero Morúa is closer to sea water, 38.2 ± 0.4 (A. Iris Maldonado,

unpublished data).

Our study is a first step in describing the environmental conditions of negative estuaries

in northwest Sonora. Further studies are needed that consider the spring-neap tide, depth

profile variations and fluxes of nutrients and net metabolism [i.e. 42] to evaluate changes in

the system and the effect of human activities. Coastal wetlands in the Gulf of California, like

Esteros Morúa and Almejas, are under increasing stress from coastal zone development [56]

and other human activities that cause changes in tidal hydrology, increased pollution, and

changes in flora and fauna [57]. Particular attention should be placed on waterborne health

risks, since estuaries in the region contribute to the local economy through fisheries

production and oyster culture [23]. Our sampling did not reveal the high levels of nutrients

common in other wetlands in Sonora, that have been impacted by the shrimp farms or other

Physico-Chemical Characteristics of Negative Estuaries… 219

human activities [47], but erosion of coastal dunes surrounding Estero Morúa and other local

wetlands could increase sediment deposition. In Estero Morúa and Almejas, a state water

quality monitoring program continues to ensure that farmed oysters are safe for human

consumption (more information available at ttp://www.cosaes.com).

Figure 13. Chlorophyll a, b, and c concentrations (means ± SE, n=12) measured monthly in Estero

Morúa between October 2005 and May 2007.

ACKNOWLEDGMENTS

This study was funded by The David and Lucile Packard Foundation grants 2004-26759

and 2006-30328 to CEDO Intercultural and by the Secretaría de Agricultura, Ganadería,

Desarrollo Rural y Pesca - Comisión Nacional de Acuacultura y Pesca - Instituto de

Acuacultura del Estado de Sonora, O.P.D. through the Grupo Interinstitucional de

Investigación en Moluscos Bivalvos and the project “Determinación de agentes causales de

alta mortalidad en los cultivos del Ostión Japonés, Crassostrea gigas, de las costas de

Sonora”. A. Castillo López, R. Fraser, A. García Sanchez, S. López Alvirde, S. Mason, S.

Reyes Fiol, and A. Rosemartin participated in sample collection. J. Hernández-López at

Hem Nalini Morzaria-Luna, Abigail Iris-Maldonado and Paloma Valdivia-Jiménez. 220

CIBNOR facilitated the analysis of nutrient samples. I.C. Kaplan provided valuable

comments to the manuscript. We would specially like to thank the members of the oyster

farm cooperatives for patiently collecting daily data, at La Cinita: I. Zepeda, G. Hernández P.,

S. Álvarez P., J. Curiel, J.Villalobos, E. Duarte O., V. Rodríguez G., F. Núñez R., E. López

B., J. Bernal, R. Porra, G. Curiel, and H. Bernal. Unica de Mujeres: M. Esther, X. Tanori, M.

del R. Luna, J.R. Luna, Ma. C. García S., and I. Cervantes. Aquamar: C. Castañeda and Don

Carlos.

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