INTRODUCTION

In Mexico, Bahía de Los Ángeles (BLA) is an important protected area for ecological conservation and tourism purposes in the state of Baja California, Mexico. Benthic studies in BLA began in the 1960s with the sampling campaigns of the Beaudette Foundation and the Scripps Institute of Oceanography (^{Barnard and Grady 1968}). The collected samples were analyzed by ^{Coan (1968)}, ^{Reish (1968)}, ^{Barnard (1969)}, and ^{Donath-Hernández (1993)}. However, these studies were time-, site-, or taxon- specific and lacked statistical analyses. This study thus aimed to update the records and characterize general benthic coastal macrofauna in BLA at the family level. We also provide macrofaunal comparisons between 2 seasonal surveys. The results from this work could be useful for environmental assessment and conservation studies since benthic organisms respond quickly to disturbances (^{Díaz-Castañeda and Reish 2009}).

MATERIALS AND METHODS

Six coastal stations were sampled in BLA between 10 and 15 m depth in September 2013 (summer) and February 2014 (winter). Whenever possible, sampling stations were set equidistant to cover the entire coastal strip of the bay. At each station, 4 samples were collected using a Petite Ponar grab and sea surface temperature (SST) and salinity (SSS) measurements were made using a YSI model 2030 probe. Samples were sieved using a 1 mm mesh (^{Couto et al. 2010}) and fixed in a 5% formaldehyde solution. Additional samples were taken to determine organic matter (OM) content (^{Dean 1974}).

In the laboratory, samples were washed using a 500 µm mesh screen, and the macrofauna were preserved in 70% ethanol. Organisms were separated into major taxonomic groups (polychaetes, crustaceans, mollusks, echinoderms, and miscellaneous taxa), quantified, and identified at the family level. A redundancy analysis (RDA) was performed to analyze family composition and benthic groups and their relationships with environmental variables (SST, SSS, and OM). Abundance data was treated with a Hellinger transformation (^{Legendre and Gallagher 2001}). For the family composition analysis, only the most representative families were used (>20 organisms). A similarity percentages analysis (SIMPER) was performed to further describe the contribution of families (%) to the dissimilarity between seasons. All analyses were done in R 4.0.0 (^{R Core Team 2020}) using the “vegan” library (^{Oksanen et al. 2019}).

RESULTS

SST ranged from ~29 ºC in summer to ~15 ºC in winter. Conversely, SSS was lower in summer (~32) compared to winter (~34). We report OM concentrations between 1.00%-2.22% in summer and 1.28%-2.70% in winter (Table 1). A total of 18,403 invertebrates representing 6 phyla and 110 families were collected (7,880 in summer and 10,523 in winter). This work reports new family records for BLA: 2 Crustacea, 4 Mollusca, 1 Echinodermata, 1 Polychaeta, 1 Cnidaria, and 1 Chordata (Table S1). Six feeding guilds were reported: carnivores, herbivores, omnivores, filter feeders, deposit feeders, and scavengers, with carnivores being more abundant, followed by deposit and filter feeders. Mollusks dominated the coasts of BLA, mainly the carnivore Cylichnidae and the filter feeder Vermetidae. The Spionidae were abundant during summer and winter. The filter feeder Sabellidae, the deposit feeder Cirratulidae (polychaetes), and the burrowing Phoxocephalidae dominated in summer, while Corophiidae (detritivorous and omnivores) accounted for most of the crustacean abundance in winter.

Overall, mollusks were the dominant group in summer and winter, followed by polychaetes and crustaceans. Average densities per sampling date for most taxa were higher in winter than in summer, except for mollusks (Table 1). Many juvenile vermetids appeared brooding several capsules containing more than 300 embryos each. That is why small vermetid juvenile data were considered outliers and, therefore, omitted from statistical analysis. The RDA was significant (P < 0.05), showing that some families were associated with summer (i.e., Lascidae, Dentallidae, Collumbellidae) or winter (Sabellidae, Nereididae) conditions; however, other families, like Diadumenidae and Corophiidae, did not show such clear associations. Mollusks seemed to prefer summer conditions, while polychaetes thrived in winter. The relevance of OM was notably diminished by reducing the taxonomic resolution (Fig. 1). The summer and winter stations were separated because of the particular environmental conditions; however, station 6 was notably different. Finally, the SIMPER analysis showed that the families contributing about 50% of the differences observed between seasons were those belonging to the mollusks Cylinchnidae, Cerithiidae, Ovulidae, and Collumbellidae, and the Spionidae polychaetes (Table S2).

Figure 1 Redundancy analysis (RDA) triplots. Left: families, stations, and environmental variables. Right: orders, stations, and environmental variables. S, summer; W, winter. 

DISCUSSION

Overall, deposit feeders, filter feeders, and carnivores predominated in summer. In contrast, carnivores and deposit feeders were more abundant in winter. We must emphasize that BLA is characterized by oceanographic processes that keep the water column mixed and favor primary productivity (^{Muñoz-Barbosa et al. 1991}). These processes favor the development of deposit and filter feeders, which in turn are prey to carnivores and scavengers.

We also report the strong seasonality in SST and SSS in BLA. The trend has been noted for the Gulf of California (^{Brusca 1980}) and BLA (^{Barnard and Grady 1968}). The decrease in polychaete and crustacean fauna observed in the summer is consistent with the works of ^{Coan (1968)}, ^{Reish (1968)}, and ^{Barnard (1969)}. Temperature has been hypothesized to possibly play an important role in determining the faunal composition of macrobenthic communities in BLA. Although no study has directly linked such association in this bay, increased macrofaunal polychaete and crustacean mortality in the Gulf of California is known to occur because of temperature seasonality (^{Brusca 1980}). This study also provides the first description of gastropods in this region. Unlike polychaetes and crustaceans, mollusks, mainly gastropods, seem to have greater affinity for summer conditions. However, further studies are required to confirm this trend since no literature exists to contrast our results.

The RDA represent the first direct association between SST and SSS and macrobenthic fauna in BLA. Results suggest that SST and SSS may act synergistically on benthic populations. The influence of SST and SSS on faunal structure is not surprising since both control fitness at the organism, population, community, and ecosystem levels (^{Re et al. 2005}, ^{Angilletta 2009}). Although OM seems to be an essential variable controlling faunal composition, the reduction of the resolution of the evaluated taxa weakens this association. The effect of OM is probably more evident when analyzed at the family level since different feeding families may be more strongly associated, directly or indirectly, with OM.

Regardless of these generalizations, the association of SST and SSS was weaker for crustaceans than for polychaetes, suggesting that other factors not considered here could be influencing faunal composition too. For example, in winter, the families Corophiidae (the most abundant family of crustacean) and Diadumenidae (anthozoan) were more abundant at station 6, which was associated with macroalgae (^{Schmidt 1972}, ^{Appadoo et al. 2002}). This pattern could be related to the vicinity of the La Mona estuary that flows into BLA and periodically provides OM. In fact, a small increase in OM was observed; however, further analysis is required to establish this trend. Regarding vermetids, the collected organisms seemed to correspond to a specific recruitment event (all organisms were small and of similar size) and were also associated with the presence of macroalgae.

In this study, the proximity of the sampling sites to the coast and the shallow depths may have influenced the diversity results. The characterization of BLA benthic assemblages will require covering the entire bay with a network of stations. The last evaluation of benthic organisms (cumaceans) was published by ^{Donath-Hernández (1993)} from samplings conducted by the Beaudette Foundation and the Scripps Institute of Oceanography, and the present study updates the knowledge of benthic biodiversity in this bay.