Journal Pre-proof

Environmental assessment of three different sites in shallow environments

of La Paz Bay (Gulf of California) using the TRIX index and macroalgae
biomass, Part I

Jaime Antonio-Robles, Alejandra Piñón-Gimate, Alberto Sánchez,

Rafael Cervantes-Duarte, José Alfredo Arreola-Lizárraga,
Margarita Casas-Valdez

PII: S2352-4855(21)00433-3
DOI: https://doi.org/10.1016/j.rsma.2021.102041
Reference: RSMA 102041

To appear in: Regional Studies in Marine Science

Received date : 9 July 2021

Revised date : 26 September 2021
Accepted date : 5 October 2021

Please cite this article as: J. Antonio-Robles, A. Piñón-Gimate, A. Sánchez et al., Environmental
assessment of three different sites in shallow environments of La Paz Bay (Gulf of California)
using the TRIX index and macroalgae biomass, Part I. Regional Studies in Marine Science (2021),
doi: https://doi.org/10.1016/j.rsma.2021.102041.

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Highlights Journal Pre-proof

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4 The TRIX index showed that mesotrophic conditions prevailed trough warmer
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6 months.
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8 Oligotrophic conditions were met in the colder months.
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Biomass of Ulva spp. and Spyridia filamentosa was the highest, followed by

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11 Acanthophora spicifera.
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13 Macroalgae biomass of Ulva, Hypnea and Gracilaria was related to nutrients, the
14 N:P ratio and TRIX.

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4 Environmental Assessment of Three Different Sites in Shallow Environments of La Paz
5
6 Bay (Gulf of California) Using the TRIX Index and Macroalgae Biomass. PART I
7
8
9 Antonio-Robles Jaime1, Piñón-Gimate Alejandra1*, Sánchez Alberto1, Cervantes-

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Duarte Rafael1, Arreola-Lizárraga José Alfredo2, Casas-Valdez Margarita1.
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13 1Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas (IPN-
14
CICIMAR). Av. Instituto Politécnico Nacional s/n, Col. Playa Palo de Santa Rita, La

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17 Paz, Baja California Sur, C.P. 23096, México.
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19 2Centro de Investigaciones Biológicas del Noroeste, S.C. CIBNOR. Unidad Sonora
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21 Carr. a Las Tinajas km 2.3 Predio El Tular, A.P. 349, C.P. 85454, Guaymas, Sonora,
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23 México.
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27
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*Corresponding author: ale_pinion@hotmail.com

28 Abstract
29
30
31 Coastal areas are of particular ecological and economic importance as they provide
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32 direct and indirect goods and services to society, both biological indicators and water
33 quality assessment are of importance when monitoring these environments.
34 Hydrographical parameters, nutrients, chlorophyll-a, and macroalgae biomass were
35
measured, and the TRIX index was obtained, at three sites of La Paz Bay subjected to
36
37 different types of anthropogenic influence: San Juan de la Costa (SJC), Casa del
38 Marino (CM), and El Tecolote (TE), during two months of 2017 and four months of
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39 2018. Also, macroalgae blooms at these sites were monitored by sampling the biomass
40 of key species. Temperature showed the typical seasonal variation, from 21°C in winter
41
42
to 28°C in summer, while salinity showed little variation (35–37 psu). Chlorophyll-a
43 varied in parallel with changes in water temperature (0.3–2.4 µg L-1), while nutrients
44 varied depending on the season and site. The TRIX index showed significant
45 differences between seasons, with the highest values in the warmer months (6.0) and
46 the lowest in November (2.7); the sites studied ranged from mesotrophic to oligotrophic.
47
Four macroalgae species accounted for over 60% of the biomass during the sampling
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49 period: Ulva ohnoi (16.1 kg), Spyridia filamentosa (6.5 kg), Acanthophora spicifera (4.2
50 kg), and Ulva sp. 1 (2.7 kg). Ulva, Gracilaria, and Hypnea species showed a positive
51 significant correlation with nutrients and the TRIX index. A high macroalgae biomass
52
53
may be related to a mesotrophic state, showing its value for determining the health
54 status of coastal ecosystems and issuing proper management recommendations.
55
56 Key words
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59 TRIX index, La Paz Bay, water quality, nutrients, chlorophyll-a, macoalgae biomass.
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7 1. Introduction
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9

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11 Coastal areas are of ecological and economic importance as they supply direct and
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13 indirect goods and services to society, especially those related to productive activities
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like fishing, tourism, and aquaculture. It is therefore important to set ecological values
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18 for coastal ecosystems aiming to maintain the desired environmental conditions
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20 (Wulff et al. 2001). Shallow coastal bays and lagoons are particularly vulnerable to
21
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23 changes in human population density and land use in coastal areas (Nixon et al.
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2001; McGlathery et al. 2007).
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Nutrient enrichment is considered one of the major anthropogenic disturbances to
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30 ecosystems worldwide. Eutrophication and the increase rate of organic matter
31
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production due to nutrient enrichment contribute significantly to habitat degradation
34
35 and changes in community composition in marine ecosystems (Nixon 1995, Thomsen
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37 et al. 2012), and also promote high chlorophyll-a levels (Boynton et al. 1982) and
38
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40 overgrowth of seaweeds and epiphytes (Ferreira et al. 2007). Excessive nutrient
41
42 enrichment affects ecosystem health, leading to eutrophication processes and
43
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45 impacting economic activities (tourism, aquaculture, and fisheries) in coastal regions
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47 (Andersen et al. 2006).
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50 An array of indices (Bricker et al. 2003; Neto et al. 2013), thresholds (Bell et al. 2014),
51
52 frameworks (Scanlan et al. 2007), and quantitative nutrient criteria (Green et al. 2014)
53
54
have been proposed and implemented to evaluate water quality in estuarine and
55
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57 marine environments (Green et al. 2015). The TRIX index has been particularly useful
58
59 for the interpretation of water quality since it includes a biological variable that
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4 responds to nutrient enrichment (Barraza-Guardado et al. 2014). Macroalgae blooms
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7 are of particular interest because they have been related to nutrient enrichment in
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9 coastal areas (Piñón-Gimate et al. 2008). It has been shown that one or two species,

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12 particularly ephemeral species with high growth rates, commonly dominate
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14 macroalgae blooms in both cover and biomass. Usually, high biomass of macroalgae

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species occur in areas with nutrient enrichment from anthropogenic sources (Valiela
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19 et al. 1997).
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21 In the Gulf of California, Mexico, different indices have been applied to monitor water
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24 quality in different bays in Sonora and Baja California (e.g., Vargas-González et al.
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26 2014; Arreola-Lizárraga et al. 2016). Ruiz-Ruiz et al. (2016) also included macroalgae
27
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29 biomass in their study and concluded that the Lobos Lagoon, Sonora, showed a good
30
31 environmental condition; however, signs of eutrophication were identified in the zone
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where untreated urban and agricultural wastewater is discharged. High biomass of
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36 macroalgae species such as Gracilaria lameneiformes and Ulva ohnoi (as Ulva
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38 lactuca) was indicative of nutrient enrichment derived from anthropogenic activities.
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41 To the best of our knowledge, no studies addressing water quality in La Paz Bay have
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43 included macroalgae biomass. However, some studies conducted in the region have
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46 concluded that the presence of some macroalgae species may be related to nutrient
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48 enrichment, depending on the site and season of the year (Águila-Ramírez et al.
49
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51 2005; Chávez-Sánchez et al. 2017, 2018).
52
53 There is evidence showing differences in the marine environmental conditions in
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different sites due to differences in nutrient inputs from anthropogenic sources by
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58 adjacent land uses (Carlson et al. 2019; Raateoja and Kauppila 2019). We examined
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60 the prevailing environmental conditions using the trophic state with the TRIX index
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4 and macroalgae biomass as a biological indicator on three sites with macroalgae
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7 blooms. Our objectives were (1) to determine the relationship between trophic state
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9 and the presence and abundance of macroalgae, and (2) to determine the influence

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12 of wastewater discharges evidenced by macroalgae biomass as an indicator of the
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14 environmental conditions of La Paz Bay, Mexico.

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2. Material and Methods
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19 The study was carried out at La Paz Bay, a semi-protected water body in the western
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21 littoral area of the Gulf of California located at coordinates 24º06’–24º47’ N and
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24 110º18’ W–110º45’ W. The climate in the region is warm dry (BWh) with the rainy
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26 season from July to October; September is the rainiest month of the year (approx. 80
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29 mm), declining abruptly in October (less than 5 mm) (INEGI 2017).
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31 Three sampling locations were selected based on previous studies addressing
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macroalgae blooms in the area (Chávez-Sánchez et al. 2017, 2018): 1) San Juan de
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36 la Costa (SJC), with mining operations near the coast (24°22’30’’ N, 110°42’00’’ W),
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38 2) Casa del Marino (CM), influenced by urban development (24°10’20.8’’ N,
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41 110°18’33.3’’ W), and 3) El Tecolote (TE), a sandy beach with tourism affluence (24°
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43 20´N, 110º 18´ W) (Fig. 1). In September and October 2017, only two sites could be
44
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46 visited (SJC and CM), and in February, May, September, and November 2018, three
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48 sites were monitored (SJC, CM and TE).

49
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51 2.1 Hydrographical parameters, Chlorophyll a, and TRIX
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53 At each site, sea surface temperature, salinity, and dissolved oxygen (DO) across the
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56 water column were measured during low tide using a multi-parameter probe (Horiba
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58 U-50). The probe was calibrated following the manufacturer’s indications. Three
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surface water samples were collected at 0.5 m depth using clean one-litre bottles.
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4 These samples were placed on an ice box (4°C) for transportation to the laboratory
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7 for subsequent analysis. The concentrations of dissolved inorganic nitrogen (DIN, as
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9 the sum of nitrites, nitrates, and ammonia), Total Nitrogen (TN), orthophosphates

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12 (PO43-), and Total Phosphorus (TP) were determined using the techniques described
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14 in Strickland and Parsons (1972). The precision of the methods used for nutrient

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testing within the 0.01–10 μM range was between ±1 and 5% (nitrite ± 0.03; nitrate ±
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19 0.15; ammonia ± 0.01; phosphate ± 0.03; total phosphorus ± 0.013; total nitrogen ±
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21 0.5 µM).
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Chlorophyll-a concentrations were determined from three additional water samples

using the spectrophotometric method proposed by Venrick and Hayward (1984), the
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29 equations of Jeffrey and Humphrey (1975), and following the procedure by Parsons et
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31
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32 al. (1984) after 24 h extraction in 90% acetone in refrigeration. The precision of the
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34 chlorophyll-a method was ± 0.04 mg m-3.
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36
37 The TRIX Index developed by Vollenweider et al. (1998) was calculated with the
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40 following equation:
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43 TRIX = [log10 (DIN ∗ TP ∗ [D%O2] ∗ Chl-a) + a]/b
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45
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47 Where Chl-a represents the chlorophyll-a concentration (in µg Chl-a L−1) and [D%O2]
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49 is the absolute deviation from the dissolved oxygen percent saturation (i.e., [100 –
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52 %DO]). DIN and TP are dissolved inorganic nitrogen (in µg L−1) and total phosphorus
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54 (in µg L−1), respectively. The parameters a = 1.5 and b = 1.2 are scale coefficients used
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57 to set the lower limit value of the index and the length of the related trophic scale from
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59 0 to 10 (Giovanardi and Vollenweider 2004) (Table 1).
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4 2.2 Macroalgae sampling
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7 To obtain macroalgal biomass at each site, three transects were established running
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9 perpendicular to the shoreline according to the length of each bloom mat, with one

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12 transect at each end and the third in the middle of the bloom. Five equidistant points
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14 were defined for each transect with end points at the shoreline and at the far edge of

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17 the bloom. At each point, macroalgae were collected by free diving from four non-
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19 overlapping quadrants (0.25 m-2) placed at random (Piñón-Gimate et al. 2008).
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Samples were washed in the field and sorted into species by hand, labelled, and
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24 weighed in a digital scale (± 0.1 g, wet weight) to determine biomass (mean biomass
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26 g m-2, wet weight). A subsample was fixed with 4% formaldehyde in seawater for
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29 taxonomic identification in the laboratory based on the keys from Abbott and
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31 Hollenberg (1992) and Norris (2010) for the region.
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34 For each of the major species identified and for the general analysis of wet biomass
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36 data, we defined the following terms (modified from Cruz-Ayala et al. 1998):
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i = sampling sites (1 to 3 sampling sites), j = species (1 to n species), k = months of
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41 the year (1 to 6 months).
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43 Site monthly biomass (SB): sum of the biomass of species j in one of the three
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46 locations in month k.
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𝑘=1
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49 𝑆𝐵 = ∑ 𝑀𝐵𝑖𝑗𝑘
50 𝑖=1
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52 Where MB is mean biomass of species j in site i during month k.
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4 Monthly relative contribution (MRC) is the sum of the monthly biomass of species j in
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7 site i in month k, divided by total monthly biomass (TMB = sum of the biomass for the
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9 n species) in month k.

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𝑆𝐵𝐽
12 𝑀𝑅𝐶𝑗𝑘 = 𝑥100
13 𝑇𝑀𝐵𝑘
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17 At each site and month, mean biomass was calculated as the sum of the biomass per
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19 square meter and divided by the number of points sampled.
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2.3 Statistical analyses
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24 The mean of the hydrographic parameters, nutrients, chlorophyll-a, biomass, and the
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26 TRIX index were analysed using a one-way analysis of variance. Data were tested for
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29 normality (Kolmogorov-Smirnov test) and homogeneity of variances (Cochran’s test).
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31 Pairwise comparisons of means were conducted using Tukey’s test only when there
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34 was a significant effect of the interaction (p < 0.05; Zar 1984). A Kruskal-Wallis
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36 ANOVA by Ranks and Median Test for nonparametric data was conducted to
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compare biomass data between sites.
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41 A Principal Components Analysis (PCA) was performed to identify significant
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relationships of hydrographic variables and the TRIX index with the biomass of
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46 macroalgae species. The significance criterion for each component was the
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48 eigenvalue (>1), and the greatest absolute values were selected from the correlation
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51 matrix. Two or more values in the same column indicate a correlation; if the signs are
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53 the same, there is a direct relation, and if the signs are different, there is an inverse
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56 association (Santamaría-del-Angel et al. 1992; Piñón-Gimate et al. 2008). All
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58 analyses were carried out using the program STATISTICA 7.0 (StatSoft Inc. 2004).
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4 3. Results
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7 3.1 Environmental Parameters
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9 Temperature showed a seasonal pattern, with peak values in September 2017 (mean

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12 28°C) and August 2018 (mean 28°C); by contrast, February 2018 (mean 20.9°C)
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14 showed the lowest values (Fig. 2a). Salinity showed little variation, but significant

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17 differences (p < 0.05) were recorded in some cases. The lowest salinity (35.3 psu)
18
19 was observed at SJC in October 2017; low values were also recorded in February
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and May 2018 at TE (35.8 and 35.7 psu, respectively) while the highest values were
22
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24 found in November 2018 at CM and TE (37 and 37.1 psu, respectively) (Fig. 2b).
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26 Dissolved oxygen showed significant differences (p < 0.05), with higher values in
27
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29 October 2017 at SJC and in February 2018 at the three sites (12.8–14.7 mg L-1). In
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31 general, low values were recorded at CM, with the lowest in May 2018 (2.8 mg L-1)
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34 (Fig. 2c).
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36 3.2 Chlorophyll-a
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Chlorophyll-a showed significant differences (p < 0.05); the lowest values were
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41 observed at SJC in 2017 (1.0 and 0.6 µg L-1, respectively), and in August and
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43 November 2018 (0.3–0.7 µg L-1), in relation to CM 2017 and February 2018 (Fig. 2d).
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46 3.3 Nutrients
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48 For total nitrogen, the highest value (p < 0.05) was found at SJC in May 2018
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51 (41.5 µM), followed by CM in October 2017 and May 2018 (35.4 and 31.6 µM,
52
53 respectively) (Fig. 3a). For total phosphorus, the highest value was observed at SJC
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56 in August 2018 (57.7 µM), followed by May and November 2018 at the same site
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58 (14.3 and 4.9 µM, respectively) (Fig. 3b). Dissolved inorganic nitrogen (DIN) also
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60 showed significant differences (p < 0.05). DIN concentrations were high at SJC in
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4 May and August 2018 (21.6 and 12.0 µM, respectively) and at CM in February and
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7 May 2018 (9.0 and 11.6 µM, respectively) (Fig. 3c). For orthophosphates, the highest
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9 value was observed at SJC in August 2018 (22.0 µM); the remaining values ranged

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12 between 0.5 and 1.5 µM (Fig. 3d). The N:P ratio was high at CM in February and May
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14 2018 (11.6 and 35.0, respectively), and at SJC in May 2018 (14.1) (Fig. 3e).

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3.4 TRIX Index
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19 The TRIX index showed significant differences (p < 0.05), with the lowest values in
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21 November 2018 at the three sites (3.0, 2.5 and 2.5, respectively), corresponding to an
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24 oligotrophic state. In September–October 2017 and from February to August 2018,
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26 the TRIX index ranged between 4 and 6, indicating a mesotrophic state (Fig. 3f).
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29 3.5 Relative contribution and biomass of macroalgae species
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31 In the macroalgae blooms of 2017 and 2018, 21 species contributed more than
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1 g m-2 each and were considered important. Of these, 14 species belonged to the
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36 Rhodophyta, 4 to the Chlorophyta, and 1 to the Ochrophyta; the remaining
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38 unidentified species were grouped together. The green species Ulva ohnoi accounted
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41 for 40% of the total biomass collected, followed by Spyridia filamentosa (16.2%),
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43 Acanthophora spicifera (10.5%), and Ulva sp.1 (6.9%); the remaining species
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46 contributed lower volumes of biomass (Table 2). The relative contribution and
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48 biomass varied according to the month and site. The species in the genera Gracilaria,
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51 Hypnea, and Ulva were grouped together in each genus to facilitate the interpretation
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53 of the results. In 2017, the macroalgae blooms sampled involved a lower number of
54
55
species, with six species present. Caulerpa sertularioides contributed more than 40%
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58 to biomass in September 2017 at SJC and CM; in October 2017, S. filamentosa
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60 accounted for more than 50% of the biomass at SJC and CM. A shift in species
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4 composition was observed in 2018 since Ulva species contributed the higher
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7 percentages to biomass in February and May 2018 at SJC, CM, and TE. At the end of
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9 the year, S. filamentosa contributed the highest relative biomass (Fig. 4a).

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12 In regards of biomass, during 2017, the highest biomass occurred at CM and mostly
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14 involved C. sertularioides, Ulva spp., A. spicifera, and Gracilaria spp. (22.7, 8.6, 16.8

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and 11.1 g m-2, respectively). In May 2018, the highest biomass was recorded at CM
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19 and TE, corresponding to Ulva species (163.8 and 181.4 g m-2, respectively), followed
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21 by February 2018 at the same sites, also with Ulva spp. (45.2 and 44.8 g m-2). In
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24 August 2018, the highest biomass was found at CM with A. spicifera contributing the
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26 highest biomass (43.1 g m-2) and in November at TE with S. filamentosa (114.1 g m-2)
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28
29 (Fig. 4b).
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31 The Kruskal-Wallis ANOVA test showed that, overall, SJC had the lowest biomass,
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34
with significant differences versus CM and TE (p = 0.008), but not between the latter
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36 (Fig. 5).
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38 3.6 PCA
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41 Components 1 and 2 of the PCA accounted for 66% (eigenvalues were significant at
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43 3.1 and 2.1, respectively) of the relationship of hydrographic parameters, nutrients
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46 and the TRIX index with macroalgae biomass of the most important genus (Table 3).
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48 Component 1 (39.8%) showed that the biomass of Gracilaria spp. and Hypnea spp.
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51 was positively correlated with the TRIX index, nutrients, and the N:P ratio. On
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53 Component 2 (26.6%), also Gracilaria spp., Hypnea spp. and Ulva spp. were related
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55
to Nitrogen and the N:P ratio (Fig. 6a). The PCA plot of components shows a blue
56
57
58 circle grouping together May 2018 for SJC and CM closely related to Nitrogen and the
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60 N:P ratio with the biomass of Ulva, Gracilaria, and Hypnea. The red circle grouped
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4 together September, and October 2017 and August 2018, for the three sites CM, SJC
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7 and TE, closely influenced by PO4 and TP, and temperature related with the presence
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9 of A. spicifera, S. filamentosa and C. sertularioides. Last, the black circle grouped

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12 together November, where the biomass of Spyridia filamentosa was related to DO
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14 and low temperatures, and the green circle grouped together February and May

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2018, with the biomass of Ceramium sp. related to DO (Fig. 6b).
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21 4. Discussion
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24 The periods with maximum and minimum temperatures are consistent with the
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26 seasonality described by Cruz-Ayala et al. (1998), Chávez-Sánchez et al. (2017), and
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29 Cervantes-Duarte et al. (2021a). The interannual variation of sea surface temperature
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31 (SST) in La Paz Bay includes normal conditions and El Niño and La Niña events. The
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34 El Niño/Southern Oscillation (ENSO) is notably associated with SST anomalies
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36 originating from the equatorial region, and its index fluctuates from positive warm (El
37
38
Niño) to negative cold phases (La Niña) (Duque-Herrera et al. 2020). In this regard, a
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41 shift of regime was described by Cervantes-Duarte et al. (2021a) for the period 2002-
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43 2020, including negative anomalies between 2002 and 2013, followed by positive
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46 anomalies from 2014 to 2020. El Niño conditions are described with the multivariate
47
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48 ENSO index (MEI). Considering the values for strong El Niño (MEI > 1) and La Niña
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51 (MEI < −1) events, our results indicate that the study period from September 2017 to
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53 November 2018 correspond to a regime of positive anomalies and may be considered
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56 within normal conditions.
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58 Seasonal changes in temperature, dissolved oxygen, and chlorophyll-a observed for
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La Paz Bay are typical of the annual variations in the Gulf of California (Valdez-
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1
2
3
4 Holguín 1994). These changes, along with the little variability in salinity throughout
5
6
7 the year, evidence the semi-arid subtropical nature of coastal zones in this region.
8
9 Some broad ranges in salinity were observed, particularly at SJC, which may be

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12 explained as associated with wastewater discharges from mining operations in close
13
14 proximity of the sampling site (Piñón-Gimate et al. 2017). Chlorophyll-a also showed

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the broadest variation at SJC. Seasonal patterns in chlorophyll-a concentration have
18
19 been previously observed in this area, with peak levels in March and minimum levels
20
21 in August (Robles et al. 2020), which are consistent with the values recorded in 2018.
22
23
24 Much higher chlorophyll-a concentrations have been observed in the deep zone of La
re-
25
26 Paz Bay, particularly in the Alfonso Basin, where nutrient concentrations are higher
27
28
29 because of the cyclonic circulation in the bay (Coria-Monter et al. 2017). At San Juan
30
31 de la Costa, phosphate mining activities take place and upwelling events are
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34
produced frequently when water currents flow into abrupt topographies (Genin 2004),
35
36 resulting in high nutrient concentrations that boost local biological production. These
37
38 variations in nutrient concentrations had been observed previously at the sampling
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41 sites and were attributed to nutrient-rich sources from La Paz City (CM) and mining
42
43 operations at SJC, respectively (Chávez-Sánchez et al. 2019). Phosphorus
44
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46 concentrations lower than 1.32 µM are thought to be of natural origin (Ketchum 1969),
47
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48 in the TE area and coastal upwellings are a likely source of phosphorus; in CM and
49
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51 SJC, high phosphate values may indicate wastewater discharges from urban sources
52
53 and mining activities.
54
55
The Redfield ratio (N:P) showed a wide range (0.5 to 35), indicating that P is not a
56
57
58 limiting factor for primary productivity in our sampling sites (Cervantes-Duarte et al.
59
60 2012). These values were high and more variable compared to other studies in the
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1
2
3
4 coastal region; for example, in a lagoon on the Pacific coast, N:P values varied
5
6
7 between 2.9 and 4.4 and P was not considered to be a limiting nutrient (Cervantes-
8
9 Duarte et al. 2021b).

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12 The TRIX index also showed differences, being higher in 2017 and February, May,
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14 and August 2018, relative to November 2018. Seasonal variations in water quality

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throughout an annual cycle based on the TRIX index have been previously reported
18
19 for other water bodies (e.g. Barraza-Guardado et al. 2014; Ruiz-Ruiz et al. 2017). In
20
21 Magdalena Bay, in the Pacific Coast of BCS, monthly average TRIX values rose
22
23
24 towards the warmer months (with peak values observed in May and June) and
re-
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26 decreased in the colder months, with some variations between years (Cervantes-
27
28
29 Duarte et al. 2021b); in the present study, May and August 2018 were warmer than
30
31 November 2018.
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Higher TRIX index values were observed particularly at CM and SJC. Differences in
35
36 the TRIX index for SJC were expected because of the mining and aquaculture
37
38 activities nearby. The high values observed at CM could be attributed to nutrient
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41 inputs from diffuse sources in the city of La Paz, as previously reported by Piñón-
42
43 Gimate et al. (2017).
44
45
46 Macroalgae blooms in the study sites showed variations in relative contributions,
47
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48 biomass, and composition, depending on the site and sampling month. Dominance
49
50
51 patterns have been previously observed for macroalgae blooms (Valiela et al. 1997;
52
53 Lapointe et al. 2005). In our study sites, green macroalgae were dominant over red
54
55
algae during the warmer months, subsequently shifting to red macroalgae during the
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58 colder months. Changes in the composition of macroalgae blooms have been
59
60 observed elsewhere. For example, in the coastal lagoons of Sinaloa, changes in the
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2
3
4 composition and abundance of macroalgae blooms have been reported, with C.
5
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7 sertulariodes present in the dry season with a lower abundance than the red species
8
9 Hypnea spinella and Spyridia filamentosa; however, in the cold season, C.

of
10
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12 sertularioides attained de highest biomass at Ohuira. Other sites have also
13
14 experienced shifts in biomass dominance from Gracilaria vermiculophylla to S.

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filamentosa or H. spinella (Piñón-Gimate et al. 2008), showing that macroalgae
18
19 blooms may involve different species composition, as observed in the present study.
20
21 These differences in macroalgae composition have been reported extensively
22
23
24 because they depend on the season where optimal conditions for the development of
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25
26 particular species occur (Lotze and Shramm 2000; Chávez-Sánchez et al. 2017).
27
28
29 Over the study period, macroalgae biomass was well below the values reported for
30
31 other water bodies with nutrient enrichment from anthropogenic activities in the Gulf
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34
of California (Table 3). Some studies in La Paz Bay have shown that Ulva may attain
35
36 high biomass levels, particularly along the shore of the waterfront of the city of La Paz
37
38 (Águila-Ramírez et al. 2005), while Chávez-Sánchez et al. (2018) reported that the
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41 biomass of attached Ulva species was not as high, similar to our findings for La Paz
42
43 Bay in the present study. The distribution and abundance of macroalgae are closely
44
45
46 related to light, nutrients, and substratum availability. For this reason, alterations of
47
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48 the substratum within the bay due to activities such as dredging are likely to affect
49
50
51 macroalgae composition and abundance, particularly near the channel of the
52
53 Ensenada La Paz, making this a limiting factor for the presence and abundance of
54
55
macroalgae. However, mean biomass and total biomass were higher than the levels
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57
58 reported in a study of macroalgae assemblages on the bay, where the highest total
59
60 biomass was 78 g m-2 in the winter (Cruz-Ayala et al. 1998); by contrast, we found a
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2
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4 mean biomass up to 160 g m-2 for Ulva species in May at CM and higher than
5
6
7 180 g m-2 at TE. The species composition found in our study was similar to the
8
9 composition found by Cruz-Ayala et al. (1998), which included benthic Sargassum

of
10
11
12 species, Spyridia filamentosa, Caulerpa sertularioides, Padina durvallaei, and
13
14 Hydroclathus clathratus. The presence and abundance of these species has been

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17
associated with nutrient enrichment from anthropogenic sources (Piñón-Gimate et al.
18
19 2008; Abreu et al. 2011; Melton III et al. 2016). However, the number of species and
20
21 the change in species composition throughout the year indicate that the macroalgae
22
23
24 community is still diverse. Therefore, attention must be paid if macroalgae blooms or
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26 the macroalgae community progress towards the dominance of one species over the
27
28
29 others, as these are signs of nutrient enrichment towards eutrophic waters (Valiela et
30
31 al. 1997).
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34
The PCA showed that the biomass of Gracilaria, Hypnea and Ulva species was
35
36 positively correlated with nutrient concentrations, the TRIX index, and the N:P ratio,
37
38 while Caulerpa sertularioides and Acanthophora spicifera biomass was related to TP
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39
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41 and temperature. This is consistent with other studies reporting that macroalgae
42
43 biomass increases in response to nutrient levels (Valiela et al. 1997; Teichberg et al.
44
45
46 2010; Melton III et al. 2016). Piñón-Gimate et al. (2008) found, in coastal lagoons of
47
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48 Sinaloa, a correlation of some species (e.g., Caulerpa sertularioides) with nutrient

49
50
51 levels and with the N:P ratio. We found that biomass values of the some of the major
52
53 species are related to sites with anthropogenic influence, evidenced by the grouping
54
55
of CM and SJC associated with high TRIX index values, but also with temperature
56
57
58 values during May where high Ulva biomass was observed at CM and TE as well as a
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60 mesotrophic TRIX index. On the other hand, we observed that at TE, where higher
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2
3
4 biomasses were found according to the Kruskal-Wallis test, little influence from
5
6
7 anthropogenic sources have been reported; however, this site has been previously
8
9 reported as with influence from nutrient rich water masses (Piñón-Gimate et al. 2017),

of
10
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12 that in turn could be favourable for the presence and abundance of the species Ulva
13
14 and Spyridia filamentosa present during the year, as mentioned earlier, a steady

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17
substrate could also be an advantage for macroalgae to attach.
18
19 Ruiz-Ruiz et al. (2017) found that the presence and abundance of Gracilaria
20
21 lameneiformis and Ulva lactuca was related to higher values of the water quality
22
23
24 index; the total biomass for these species was very high at sites directly affected by
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26 wastewater discharges, with biomass values of 20 216 and 1 264 g m-2 dry weight,
27
28
29 respectively.
30
31 To note, the biomass sampled in the present study is lower than the biomass
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34
sampled in other studies (Table 3); however, studies addressing biomass variability
35
36 are important since rapidly growing human populations may boost eutrophication
37
38 processes and increase the frequency and abundance of macroalgae blooms. Also,
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41 the changes in temperature patterns throughout the year observed in La Paz Bay
42
43 (Cervantes-Duarte et al. 2021b) may affect the presence and abundance of
44
45
46 macroalgae blooms, hence the importance of establishing monitoring programs in
47
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48 coastal lagoons.
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51 Coastal regions are complex ecological systems and water quality should be studied
52
53 through indices and biological variables, as recommended by other authors (Muciño-
54
55
Márquez et al. 2017). Despite its undeniable ecological value, the coastal zone
56
57
58 receives a variety of pollutants, including those from industrial (Dell’anno et al. 2002),
59
60 agricultural (Noriega and Araujo 2009), urban (Mearns 1981), and aquacultural
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1
2
3
4 (Primavera 2006, Kern 2011) sources. Many coastal areas worldwide are currently
5
6
7 experiencing eutrophication and/or hypernutrification, with adverse consequences for
8
9 the health of ecosystems (Barraza-Guardado et al. 2014). However, the TRIX index

of
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12 shows that La Paz Bay is mostly oligotrophic, with some months trending towards a
13
14 mesotrophic state.

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In the city of La Paz, the number of inhabitants increased by 36 thousand persons
18
19 from 1990 to 2000 and by 76 thousand from 2000 to 2015 (from 140 thousand in
20
21 1990 to 273 thousand in 2015), the latter being the highest growth rate recorded for
22
23
24 La Paz in recent times (INEGI 2017). This has led to a growing demand for goods
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26 and services for the population, and also for recreational activities like tourism.
27
28
29 Therefore, the use of water quality indices such as TRIX and long-term monitoring
30
31 series of hydrological and biological variables such as macroalgae are recommended
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to set water quality standards for coastal zones.
35
36 5. Conclusion
37
38 Coastal regions provide ecologically important goods and services to the local human
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41 populations. The establishment of water quality standards and biological indicators of
42
43 ecosystem health are valuable for environmental monitoring. The TRIX index showed
44
45
46 that coastal water in the region may transition to a mesotrophic state, but that
47
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48 oligotrophic conditions also occur. The PCA analysis evidenced that macroalgae
49
50
51 biomass of species in the genera Ulva, Hypnea, and Gracilaria was related to nutrient
52
53 variability, the TRIX index, and the N:P ratio, showing that biological indicators are
54
55
also valuable to indicate environmental conditions. Besides, the presence,
56
57
58 distribution, and abundance of macroalgae as indicators of the health status of
59
60 coastal areas are relevant because the species composition and biomass of
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4 macroalgae blooms readily change in response to nutrient enrichment from the
5
6
7 increasing anthropogenic activities in adjacent coastal regions. The increase in
8
9 human populations and economic activities impacts environmental conditions, hence

of
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12 the importance of implementing regular monitoring through water quality indices and
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14 macroalgae species and biomass.

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Acknowledgments
18
19 We would like to thank Efraín López Montaño Tonatiuh Chávez-Sánchez, (TCHS),
20
21 and Betsabé Cañedo Castro (BCC) for their assistance in field sample collection. To
22
23
24 the project Instituto Politécnico Nacional (IPN)-SIP20172269 for funding and granting
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26 the Beca de Estímulo Institucional de Formación de Investigadores (BEIFI) to TCHS,
27
28
29 BCC, and Jaime Antonio Robles, who also was awarded a CONACYT grant.
30
31 Alejandra Piñón-Gimate received economic support from Estímulo al Desempeño de
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la Investigación (EDI-IPN), and Margarita Casas-Valdez, Alberto Sánchez and Rafael
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36 Cervantes-Duarte, from EDI-IPN and Comisión de Fomento a las Actividades
37
38 Académicas (COFAA-IPN). María Elena Sánchez-Salazar edited the English
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41 manuscript.
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ecosystem consequences. Limnol. Oceanogr. 42, 1105-1118.
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41 Rodríguez, L.C., Lechuga-Deveze, C.H., Padilla-Arredondo, G., Córdoba-Matson, M.,
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43 2014. Effects of sewage discharge on trophic state and water quality in a coastal
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48 https://doi.org/10.1155/2014/618054
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51 Venrick, E.L., Hayward, T.L., 1984. Determining chlorophyll on the 1984 CalCOFI
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4 index. Environmetrics 9, 329-357.
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16 Zar, J.H., 1984. Biostatistical analysis. 2nd ed. Prentice Hall, Inc., Englewood Cliffs,
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19 NJ.pp. 718.
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4 Table 1. Trophic level and water quality associated with the TRIX index (Vollenweider
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et al. 1998).
7
Trix index Water Characteristics of the
8 Trophic state
9 value quality water column

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11 Low productive waters, low
0–4 Oligotrophic High
12 trophic level
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14 Moderately productive

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15 4–6 Mesotrophic Good waters, medium trophic
16 level
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18 Moderately to highly
19 6–8 Eutrophic Bad productive waters, high
20
21 trophic level
22
Highly productive waters,
23 8–10 Hypertrophic Poor
highest trophic level
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27
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29 Table 2. Total macroalgae species biomass (g, wet weight).
30
31 Species Species abundance Relative abundance
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32 (g) (%)
33 Rhodophyta
34
35
Acanthophora spicifera 4214.4 10.52
36 Ceramium sp. 164.3 0.4
37 Gracilaria crispata 423.1 1.05
38 G. paquidermatica 143.5 0.35
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39 G. pinnata 1757.2 4.4

40
41 G. spinifera 93.8 0.23
42 G. subsecundata 1049.6 2.6
43 Hypnea johnstonii 125 0.3
44 H. spinella 182.4 0.45
45
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Hypnea sp. 316 0.8
47 H. valentiae 44.5 0.11
Laurencia sp. 406.1 1.01
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49 Rosenvingea intrincata 950.5 2.4
50 Spyridia filamentosa 6501.8 16.2
51
52
53 Chlorophyta
54 C. sertularioides 1986.6 4.9
55 Ulva sp1 2758.9 6.9
56
57
U. ohnoi 16072.6 40.1
58 U. tepida 21.9 0.05
59 U. torta 2055.32 5.1
60
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4 Ochrophyta
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6 Padina spp. 84.6 0.2
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8 Other species 684.8 1.71
9 Total biomass 40037.32 100

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13 Table 3. Values of the component coordinates of variables based on PCA
14 correlations. TRIX index, °C = Temperature, DO = Dissolved oxygen, PO4 =

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15 Ortophosphates, TP = Total phosphorus, DIN = Dissolved Inorganic Nitrogen, TN =
16
17 Total Nitrogen, N:P = Nitrogen Phosphorus ratio, Cs = Caulerpa sertularioides, Ul =
18 Ulva spp., As = Acantophora spicifera, Gr = Gracilaria spp., Hy = Hypnea spp., Sf =
19 Spyridia filamentosa, and Ce = Ceramium sp. Bold letters indicate a significant
20 correlation between variables.
21
22 Variables Component 1 Component 2
23
Eigenvalue 3.2 2.1
24
25
26
27
%
TRIX
°C
re-
39.7
-0.8
0.14
26.6
0.50
0.69
28
OD 0.28 0.20
29
30 PO4 -0.58 0.77
31 TP -0.65 0.69
lP
32 DIN -0.86 -0.22
33 TN -0.77 -0.46
34
35
N:P -0.55 -0.69
36 Cs 0.02 0.18
37 Ul -0.19 -0.47
38 As 0.02 0.00
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39 Gr -0.49 -0.47
40
41 Hy -0.41 -0.45
42 Sf 0.37 0.02
43 Ce 0.11 -0.11
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22 Table 4. Nutrient concentrations (µg L-1), Chlorophyll-a (mg m-3), TRIX index and macroalgae biomass (g m-2 dry weight)
23
24
from other studies. Some values were transformed from their original source for comparative purposes; therefore, they are
25 approximations. Ag = Agriculture, Aq = Aquaculture, AP = Atmospheric pollution, Fr = Farming, FW = Fish and shellfish
26 processing, IW = Industrial waste, Lv = Livestock, Mn = Mining, NHI = No human impact, Se = Sewage, Oc = Oceanic
27 influence, Rd = River discharges, SF = Shrimp farm, Upw = Upwelling influence, T = Tourism.
28
29 Site Type of DIN TN PO4 TP N:P Chl a TRIX Macroalgae Reference
30
31
32
33
34
Lagoon
influence
Mediterranean Sea
Bizerte Ag, Aq, Lv,
Fr, Se, Iw,
AP
3.20-11.5 NM
re-
0.58-1.58 NM 7.2 max 5.18-6.12
biomass

NM Béjaoui et al.
(2016)

35 Mexico
36 Gulf of Mexico
37 Veracruz, Términos Lagoon
38 Pom Rd, Se 0.1-5.6 NM 7.1 max NM 0.1-43 0.0-3.9 NM Muciño-
39 Atasta Márquez et al.
lP
40 system (2017)
41 Palizada Rd, Se 0.1-7.2 NM 7.1 max NM 0.1-37.9
del Este
42
system
43
Gulf of California
44 Sonora
45 Kino Bay NHI 0.8-2.3 28.6 2.7-3.3 4.3-8.7 1.1-3.00 2.2-2.9 NM Barraza-
46 SF 0.9-6.2 47.1-100 2-5.3 4.3-8.7 2.4-5.8 2.4-3.7 NM Guardado et al.
47 (2014)
48 La Salada Se 0.1-24.1 NM 0.32-22 NM 0-16.9 2-3.5 NM Vargas-
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49 Cove González et al.

50 (2014)
51 El Rancho SF, Upw 0.1-17.7 NM 0.4-4.6 NM 0.02-7.7 2-3.8 Arreola-
52 (System Lizarraga et al.
53 lagoon) (2016)
54 Empalme OI, Upw 0.04-19.9 NM 0.2-3.0 NM 0-6.51 1.5-3.5
55 (System
lagoon)
56
Lobos Ag, Se 2.8-428.4 NM 12-72 NM 0.04-14 0.5-4.5 20,216.1 Ruiz-Ruiz et al.
57 Lagoon (Gracilaria (2017)
58 OI 1.4-236.6 NM 9-42 NM 0.0-8.3 0.5-4.5 lameneiformis);
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20 1264.5 (Ulva
21 lactuca)
22 Sinaloa
23 Urías FW, Se, IW 23.3 ± 8.1 NM NM 1.8 ± 0.8 10.4-35.2 NM NM 57.1 ++ (G. Ochoa-Izaguirre
24 vermiculophylla, U. et al. (2017)
expansa)
25
26
27 Ensenada RI, Se, IW, 18.1 ± NM NM 4.4± 2.5 1.1-30.9 NM NM 27.8 ++ (Caulerpa
28 Pabellón SF, Ag 20.2 sertularioides and
29 G. vermiculophylla)
30
31
32
33
34
Altata Se, IW, SF,
Ag

Baja California Sur

La Paz Bay
2.5 ± 1.5 NM NM re- 0.1 ± 0.0 15.4-
294.3
48.6 ++ (C.
sertularioides and
G. vermiculophylla)

35 Portugués NHI 1.2-5.1 6.0-33.1 0.4-1.5 0.7-3.1 8.6-10.7 NM NM 0.313 (U. flexuosa) Chávez-
San Juan Mn, FW 2.8-61 4.8-98.8 0.2-5.3 0.9-12.3 5.3-35.3 NM NM 1.319 ++ (U. rigida Sánchez et al.
36
de La and U. (2018)
37 Costa acanthophora)
38 Casa del FW, T 1.2-12.7 15.5-53.8 0.5-2.1 0.9-2.8 17.2-19.2 NM NM 0.641 ++ (U. rigida
39
lP
Marino and U.
40 acanthophora)
41 El NHI, T 0.9-5.5 8.8-31.5 0.3-1.2 0.9-2.2 9.8-14.3 NM NM 0.968 ++ (U. rigida
42 Tecolote and U.
43 acanthophora)
44 La Paz Bay (2017)
45 San Juan Mn, FW 1.3-2.4 6.8-20 0.9-1.1 1.2-1.6 13.5-14.4 0.6-1.1 4.7-4.8 1.2 C. This study
46 de La sertularioides
Costa 0.44 U. rigida
47
0.9 A. spicifera
48
rna

0.81 Gracilaria spp.

49 0.43 Red
50 filamentous group
51 Casa del FW, T 1.1-3 14.8-35.4 1.1 2.5-2.6 8.4-12.2 1.6-2.3 4.8-4.9 0.12 C.
52 Marino sertularioides
53 0.01 Gracilaria spp.
54 0.20 Red
55 filamentous group
56
57 ++ sum of various macroalgae species; the species that represent bulk biomass are mentioned.
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4 List of figures
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7 Figure 1. Study area (La Paz Bay) showing the sampling sites: SJC = San Juan de la
8 Costa, CM = Casa del Marino, TE = El Tecolote.
9

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11 Figure 2. Mean (± SD) of a) Temperature, b) Salinity, c) Dissolved oxygen, and d)
12
13 Chlorophyll a. Sept = September, Oct = October, Feb = February, Aug = August, Nov
14

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15 = November. SJC = San Juan de la Costa, CM = Casa del Marino, TE = El Tecolote.
16
17
18 Figure 3. Mean (± SD) of a) Total Nitrogen, b) Total Phosphorus, c) Dissolved
19
20 Inorganic Nitrogen, d) PO4, e) N:P ratio, and f) TRIX index. Sept = September, Oct =
21
22
October, Feb = February, Aug = August, Nov = November. SJC = San Juan de la
23 Costa, CM = Casa del Marino, TE = El Tecolote.
24
25
26
27
re-
Figure 4. a) Relative biomass (%) of macroalgae biomass for each species, site, and
month. b) Mean (± SD) macroalgae biomass (g m-2 wet weight) for each species, site,
28
29
30
and month. Sept = September, Oct = October, Feb = February, Aug = August, Nov =
31 November. SJC = San Juan de la Costa, CM = Casa del Marino, TE = El Tecolote.
lP
32
33
34 Figure 5. Box and Whisker Plot representation of the Kruskal-Wallis ANOVA test for
35
36 site biomass at SJC, CM, and TE.
37
38 Figure 6. a) Principal Components Analysis (PCA) for the correlation between
rna

39
40 macroalgae biomass and: TRIX index, °C = Temperature, DO = Dissolved oxygen, PO4
41
42 = Ortophosphates, TP = Total phosphorus, DIN = Dissolved Inorganic Nitrogen, TN =
43
44 Total Nitrogen, N:P = Nitrogen Phosphorus ratio. Cs = Caulerpa sertularioides, Ul =
45
46
Ulva spp., Sp = Spyridia filamentosa, As = Acanthophora spcifera, Ce = Ceramium sp.,
47 Gr = Gracilaria spp., Hy = Hypnea spp. b) Plot of coordinates for sites. Bold symbols
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49 correspond to the year 2018.
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Figure 5 Click here to access/download;Figure;Figure 5 Kruskal Wallis.jpg

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Figure 6 Click here to access/download;Figure;Figure 6 PCA Final Version.jpg

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Author Statement Journal Pre-proof

CRedit author statement

Antonio-Robles Jaime: Conceptualization, Methodology, Formal analysis,
Investigation, writing-Original Draft, Visualization.

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Piñón-Gimate Alejandra: Conceptualization, Methodology, Formal análisis,
Investigation, Resources, Writing Original Draft, Visualization, Project
administration, Supervision, Funding acquisition.

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Sánchez-González Alberto: Conceptualization, Methodology, Formal analysis,
Investigation, writing-Original Draft, Visualization.

Cervantes-Duarte Rafael: Conceptualization, Methodology, Formal analysis,

Investigation, writing-Original Draft, Visualization.
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Arreola-Lizárraga José Alfredo: Conceptualization, Methodology, Formal analysis,
Investigation, writing-Original Draft, Visualization.

Casas-Valdez Margarita: Conceptualization, Methodology, Formal analysis,

lP
Investigation, writing-Original Draft, Visualization.
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 Journal Pre-proof

Declaration of interests

☒ The authors declare that they have no known competng fnancial interests or personal relatonships
that could have appeared to influence the work reported in this paper.

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☐ The authors declare the following fnancial interests/personal relatonships which may be considered
as potental competng interests:

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